Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 7454031, 20 pages
https://doi.org/10.1155/2017/7454031
Review Article

Caveolin-1: An Oxidative Stress-Related Target for Cancer Prevention

1Department of Mammary Disease, Discipline of Integrated Chinese and Western Medicine in Guangzhou University of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, Guangdong, China
2The Research Center for Integrative Medicine, Guangzhou University of Chinese Medicine, Guangzhou, Guangdong, China
3Post-Doctoral Research Center, Guangzhou University of Chinese Medicine, Guangzhou, Guangdong, China
4Department of Breast Oncology, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, Guangdong, China

Correspondence should be addressed to Zhiyu Wang; moc.621@679uyihzgnaw

Received 6 November 2016; Revised 23 January 2017; Accepted 7 March 2017; Published 4 May 2017

Academic Editor: Ilaria Peluso

Copyright © 2017 Shengqi Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. K. Gupta, A. K. Patel, N. Shah et al., “Oxidative stress and antioxidants in disease and cancer: a review,” Asian Pacific Journal of Cancer Prevention : APJCP, vol. 15, no. 11, pp. 4405–4409, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Klaunig, L. M. Kamendulis, and B. A. Hocevar, “Oxidative stress and oxidative damage in carcinogenesis,” Toxicologic Pathology, vol. 38, no. 1, pp. 96–109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. B. Kryston, A. B. Georgiev, P. Pissis, and A. G. Georgakilas, “Role of oxidative stress and DNA damage in human carcinogenesis,” Mutation Research, vol. 711, no. 1-2, pp. 193–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. J. E. Klaunig, Z. Wang, X. Pu, and S. Zhou, “Oxidative stress and oxidative damage in chemical carcinogenesis,” Toxicology and Applied Pharmacology, vol. 254, no. 2, pp. 86–99, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Finkel, “Signal transduction by reactive oxygen species,” The Journal of Cell Biology, vol. 194, no. 1, pp. 7–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Yang, S. Karakhanova, W. Hartwig et al., “Mitochondria and mitochondrial ROS in cancer: novel targets for anticancer therapy,” Journal of Cellular Physiology, vol. 231, no. 12, pp. 2570–2581, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. R. A. Cairns, I. S. Harris, and T. W. Mak, “Regulation of cancer cell metabolism,” Nature Reviews. Cancer, vol. 11, no. 2, pp. 85–95, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Sundaresan, Z. X. Yu, V. J. Ferrans et al., “Regulation of reactive-oxygen-species generation in fibroblasts by Rac1,” The Biochemical Journal, vol. 318, no. Part 2, pp. 379–382, 1996. View at Google Scholar
  9. V. Nogueira, Y. Park, C. C. Chen et al., “Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis,” Cancer Cell, vol. 14, no. 6, pp. 458–470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Hecht, C. F. Pessoa, L. B. Gentile, D. Rosenthal, D. P. Carvalho, and R. S. Fortunato, “The role of oxidative stress on breast cancer development and therapy,” Tumour Biology, vol. 37, no. 4, pp. 4281–4291, 2016. View at Google Scholar
  11. P. A. Thompson, E. L. Ashbeck, D. J. Roe et al., “Selenium supplementation for prevention of colorectal adenomas and risk of associated type 2 diabetes,” Journal of the National Cancer Institute, vol. 108, no. 12, 2016. View at Publisher · View at Google Scholar
  12. K. N. Prasad, “Simultaneous activation of Nrf2 and elevation of dietary and endogenous antioxidant chemicals for cancer prevention in humans,” Journal of the American College of Nutrition, vol. 35, no. 2, pp. 175–184, 2016. View at Google Scholar
  13. K. C. Rocha, M. L. Vieira, R. L. Beltrame et al., “Impact of selenium supplementation in neutropenia and immunoglobulin production in childhood cancer patients,” Journal of Medicinal Food, vol. 19, no. 6, pp. 560–568, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. N. S. Chandel and D. A. Tuveson, “The promise and perils of antioxidants for cancer patients,” The New England Journal of Medicine, vol. 371, no. 2, pp. 177–178, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. J. X. Chen, G. Li, H. Wang et al., “Dietary tocopherols inhibit PhIP-induced prostate carcinogenesis in CYP1A-humanized mice,” Cancer Letters, vol. 371, no. 1, pp. 71–78, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Gorrini, I. S. Harris, and T. W. Mak, “Modulation of oxidative stress as an anticancer strategy,” Nature Reviews. Drug Discovery, vol. 12, no. 12, pp. 931–947, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Greenlee, D. L. Hershman, and J. S. Jacobson, “Use of antioxidant supplements during breast cancer treatment: a comprehensive review,” Breast Cancer Research and Treatment, vol. 115, no. 3, pp. 437–452, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. P. J. Smith and K. J. Steadman, “Antioxidant supplementation and cancer patients receiving curative-intent chemotherapy,” The Medical Journal of Australia, vol. 204, no. 5, pp. 185–185e1, 2016. View at Publisher · View at Google Scholar
  19. M. K. Chung, D. H. Kim, Y. C. Ahn, J. Y. Choi, E. H. Kim, and Y. I. Son, “Randomized trial of vitamin C/E complex for prevention of radiation-induced xerostomia in patients with head and neck cancer,” Otolaryngology Head and Neck Surgery, vol. 155, no. 3, pp. 423–430, 2016. View at Publisher · View at Google Scholar
  20. J. P. Cheng and B. J. Nichols, “Caveolae: one function or many?” Trends in Cell Biology, vol. 26, no. 3, pp. 177–189, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Sargiacomo, P. E. Scherer, Z. Tang et al., “Oligomeric structure of caveolin: implications for caveolae membrane organization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 20, pp. 9407–9411, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. H. N. Fridolfsson, D. M. Roth, P. A. Insel, and H. H. Patel, “Regulation of intracellular signaling and function by caveolin,” FASEB Journal, vol. 28, no. 9, pp. 3823–3831, 2014. View at Google Scholar
  23. M. Salatino, W. Beguelin, M. G. Peters et al., “Progestin-induced caveolin-1 expression mediates breast cancer cell proliferation,” Oncogene, vol. 25, no. 59, pp. 7723–7739, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Du, L. Chen, H. Zhang et al., “Caveolin-1 limits the contribution of BKCa channel to MCF-7 breast cancer cell proliferation and invasion,” International Journal of Molecular Sciences, vol. 15, no. 11, pp. 20706–20722, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Tang, X. Zeng, F. He, Y. Liao, N. Qian, and M. Toi, “Caveolin-1 is related to invasion, survival, and poor prognosis in hepatocellular cancer,” Medical Oncology, vol. 29, no. 2, pp. 977–984, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. T. C. Thompson, T. L. Timme, L. Li, and A. Goltsov, “Caveolin-1, a metastasis-related gene that promotes cell survival in prostate cancer,” Apoptosis, vol. 4, no. 4, pp. 233–237, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Pongjit and P. Chanvorachote, “Caveolin-1 sensitizes cisplatin-induced lung cancer cell apoptosis via superoxide anion-dependent mechanism,” Molecular and Cellular Biochemistry, vol. 358, no. 1-2, pp. 365–373, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Xu, X. Qu, H. Li et al., “Src/caveolin-1-regulated EGFR activation antagonizes TRAIL-induced apoptosis in gastric cancer cells,” Oncology Reports, vol. 32, no. 1, pp. 318–324, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Wang, Z. Li, H. Guo et al., “Caveolin 1 knockdown inhibits the proliferation, migration and invasion of human breast cancer BT474 cells,” Molecular Medicine Reports, vol. 9, no. 5, pp. 1723–1728, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Miao, X. Xiong, Y. Lin et al., “miR-203 inhibits tumor cell migration and invasion via caveolin-1 in pancreatic cancer cells,” Oncology Letters, vol. 7, no. 3, pp. 658–662, 2014. View at Publisher · View at Google Scholar
  31. M. Joglekar, W. O. Elbazanti, M. D. Weitzman, H. L. Lehman, and K. L. van Golen, “Caveolin-1 mediates inflammatory breast cancer cell invasion via the Akt1 pathway and RhoC GTPase,” Journal of Cellular Biochemistry, vol. 116, no. 6, pp. 923–933, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Yang, L. Guan, S. Li et al., “Mechanosensitive caveolin-1 activation-induced PI3K/Akt/mTOR signaling pathway promotes breast cancer motility, invadopodia formation and metastasis in vivo,” Oncotarget, vol. 7, no. 13, pp. 16227–16247, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Nimri, H. Barak, L. Graeve, and B. Schwartz, “Restoration of caveolin-1 expression suppresses growth, membrane-type-4 metalloproteinase expression and metastasis-associated activities in colon cancer cells,” Molecular Carcinogenesis, vol. 52, no. 11, pp. 859–870, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Shi, S. H. Tan, S. Ng et al., “Critical role of CAV1/caveolin-1 in cell stress responses in human breast cancer cells via modulation of lysosomal function and autophagy,” Autophagy, vol. 11, no. 5, pp. 769–784, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Wang, W. He, Z. Li, W. Chang, Y. Xin, and T. Huang, “Caveolin-1 functions as a key regulator of 17beta-estradiol-mediated autophagy and apoptosis in BT474 breast cancer cells,” International Journal of Molecular Medicine, vol. 34, no. 3, pp. 822–827, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. Z. Xie, X. Zeng, T. Waldman, and R. I. Glazer, “Transformation of mammary epithelial cells by 3-phosphoinositide-dependent protein kinase-1 activates beta-catenin and c-Myc, and down-regulates caveolin-1,” Cancer Research, vol. 63, no. 17, pp. 5370–5375, 2003. View at Google Scholar
  37. P. Chunhacha and P. Chanvorachote, “Roles of caveolin-1 on anoikis resistance in non small cell lung cancer,” International Journal of Physiology Pathophysiology and Pharmacology, vol. 4, no. 3, pp. 149–155, 2012. View at Google Scholar
  38. H. Halim, S. Luanpitpong, and P. Chanvorachote, “Acquisition of anoikis resistance up-regulates caveolin-1 expression in human non-small cell lung cancer cells,” Anticancer Research, vol. 32, no. 5, pp. 1649–1658, 2012. View at Google Scholar
  39. W. Zou, X. Ma, W. Hua, B. Chen, and G. Cai, “Caveolin-1 mediates chemoresistance in cisplatin-resistant ovarian cancer cells by targeting apoptosis through the Notch-1/Akt/NF-kappaB pathway,” Oncology Reports, vol. 34, no. 6, pp. 3256–3263, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. S. C. Sekhar, T. Kasai, A. Satoh et al., “Identification of caveolin-1 as a potential causative factor in the generation of trastuzumab resistance in breast cancer cells,” Journal of Cancer, vol. 4, no. 5, pp. 391–401, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. K. N. Wu, M. Queenan, J. R. Brody et al., “Loss of stromal caveolin-1 expression in malignant melanoma metastases predicts poor survival,” Cell Cycle, vol. 10, no. 24, pp. 4250–4255, 2011. View at Google Scholar
  42. A. K. Witkiewicz, A. Dasgupta, S. Sammons et al., “Loss of stromal caveolin-1 expression predicts poor clinical outcome in triple negative and basal-like breast cancers,” Cancer Biology & Therapy, vol. 10, no. 2, pp. 135–143, 2010. View at Google Scholar
  43. A. K. Witkiewicz, A. Dasgupta, F. Sotgia et al., “An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers,” The American Journal of Pathology, vol. 174, no. 6, pp. 2023–2034, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. Zhao, F. H. Han, S. B. Yang, L. X. Hua, J. H. Wu, and W. H. Zhan, “Loss of stromal caveolin-1 expression in colorectal cancer predicts poor survival,” World Journal of Gastroenterology, vol. 21, no. 4, pp. 1140–1147, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Shan-Wei, X. Kan-Lun, R. Shu-Qin, Z. Li-Li, and C. Li-Rong, “Overexpression of caveolin-1 in cancer-associated fibroblasts predicts good outcome in breast cancer,” Breast Care, vol. 7, no. 6, pp. 477–483, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. K. C. Moon, G. K. Lee, S. H. Yoo et al., “Expression of caveolin-1 in pleomorphic carcinoma of the lung is correlated with a poor prognosis,” Anticancer Research, vol. 25, no. 6C, pp. 4631–4637, 2005. View at Google Scholar
  47. J. A. Karam, Y. Lotan, C. G. Roehrborn, R. Ashfaq, P. I. Karakiewicz, and S. F. Shariat, “Caveolin-1 overexpression is associated with aggressive prostate cancer recurrence,” The Prostate, vol. 67, no. 6, pp. 614–622, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. S. A. Tahir, G. Yang, S. Ebara et al., “Secreted caveolin-1 stimulates cell survival/clonal growth and contributes to metastasis in androgen-insensitive prostate cancer,” Cancer Research, vol. 61, no. 10, pp. 3882–3885, 2001. View at Google Scholar
  49. L. Liu, H. X. Xu, W. Q. Wang et al., “Cavin-1 is essential for the tumor-promoting effect of caveolin-1 and enhances its prognostic potency in pancreatic cancer,” Oncogene, vol. 33, no. 21, pp. 2728–2736, 2014. View at Google Scholar
  50. S. Pavlides, A. Tsirigos, I. Vera et al., “Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the “reverse Warburg effect”: a transcriptional informatics analysis with validation,” Cell Cycle, vol. 9, no. 11, pp. 2201–2219, 2010. View at Google Scholar
  51. T. Songserm, V. Pongrakhananon, and P. Chanvorachote, “Sub-toxic cisplatin mediates anoikis resistance through hydrogen peroxide-induced caveolin-1 up-regulation in non-small cell lung cancer cells,” Anticancer Research, vol. 32, no. 5, pp. 1659–1669, 2012. View at Google Scholar
  52. W. Suchaoin and P. Chanvorachote, “Caveolin-1 attenuates hydrogen peroxide-induced oxidative damage to lung carcinoma cells,” Anticancer Research, vol. 32, no. 2, pp. 483–490, 2012. View at Google Scholar
  53. D. Volonte, K. Zhang, M. P. Lisanti, and F. Galbiati, “Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts,” Molecular Biology of the Cell, vol. 13, no. 7, pp. 2502–2517, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Rungtabnapa, U. Nimmannit, H. Halim, Y. Rojanasakul, and P. Chanvorachote, “Hydrogen peroxide inhibits non-small cell lung cancer cell anoikis through the inhibition of caveolin-1 degradation,” American Journal of Physiology. Cell Physiology, vol. 300, no. 2, pp. C235–C245, 2011. View at Google Scholar
  55. Y. N. Kim, G. J. Wiepz, A. G. Guadarrama, and P. J. Bertics, “Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1. Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status,” The Journal of Biological Chemistry, vol. 275, no. 11, pp. 7481–7491, 2000. View at Publisher · View at Google Scholar
  56. D. Volonte, F. Galbiati, R. G. Pestell, and M. P. Lisanti, “Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress,” The Journal of Biological Chemistry, vol. 276, no. 11, pp. 8094–8103, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. A. R. Sanguinetti and C. C. Mastick, “c-Abl is required for oxidative stress-induced phosphorylation of caveolin-1 on tyrosine 14,” Cellular Signalling, vol. 15, no. 3, pp. 289–298, 2003. View at Publisher · View at Google Scholar
  58. Y. S. Kang, Y. G. Ko, and J. S. Seo, “Caveolin internalization by heat shock or hyperosmotic shock,” Experimental Cell Research, vol. 255, no. 2, pp. 221–228, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Kitano, H. Yoda, K. Tabata et al., “Vitamin K3 analogs induce selective tumor cytotoxicity in neuroblastoma,” Biological & Pharmaceutical Bulletin, vol. 35, no. 4, pp. 617–623, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. U. E. Martinez-Outschoorn, R. M. Balliet, D. B. Rivadeneira et al., “Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution: a new paradigm for understanding tumor metabolism, the field effect and genomic instability in cancer cells,” Cell Cycle, vol. 9, no. 16, pp. 3256–3276, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. B. Salani, S. Maffioli, M. Hamoudane et al., “Caveolin-1 is essential for metformin inhibitory effect on IGF1 action in non-small-cell lung cancer cells,” FASEB Journal, vol. 26, no. 2, pp. 788–798, 2012. View at Google Scholar
  62. U. E. Martinez-Outschoorn, F. Sotgia, and M. P. Lisanti, “Caveolae and signalling in cancer,” Nature Reviews. Cancer, vol. 15, no. 4, pp. 225–237, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. J. R. Glenney Jr. and D. Soppet, “Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 21, pp. 10517–10521, 1992. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Schlegel and M. P. Lisanti, “A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo,” The Journal of Biological Chemistry, vol. 275, no. 28, pp. 21605–21617, 2000. View at Publisher · View at Google Scholar
  65. P. Dupree, R. G. Parton, G. Raposo, T. V. Kurzchalia, and K. Simons, “Caveolae and sorting in the trans-Golgi network of epithelial cells,” The EMBO Journal, vol. 12, no. 4, pp. 1597–1605, 1993. View at Google Scholar
  66. J. Lee and K. J. Glover, “The transmembrane domain of caveolin-1 exhibits a helix-break-helix structure,” Biochimica et Biophysica Acta, vol. 1818, no. 5, pp. 1158–1164, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. P. E. Scherer, Z. Tang, M. Chun, M. Sargiacomo, H. F. Lodish, and M. P. Lisanti, “Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe,” The Journal of Biological Chemistry, vol. 270, no. 27, pp. 16395–16401, 1995. View at Google Scholar
  68. M. Simionescu, N. Simionescu, and G. E. Palade, “Biochemically differentiated microdomains of the cell surface of capillary endothelium,” Annals of the New York Academy of Sciences, vol. 401, no. 1, pp. 9–24, 1982. View at Publisher · View at Google Scholar · View at Scopus
  69. M. P. Lisanti, P. E. Scherer, J. Vidugiriene et al., “Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease,” The Journal of Cell Biology, vol. 126, no. 1, pp. 111–126, 1994. View at Publisher · View at Google Scholar · View at Scopus
  70. H. H. Patel, F. Murray, and P. A. Insel, “Caveolae as organizers of pharmacologically relevant signal transduction molecules,” Annual Review of Pharmacology and Toxicology, vol. 48, pp. 359–391, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Mineo, G. L. James, E. J. Smart, and R. G. Anderson, “Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane,” The Journal of Biological Chemistry, vol. 271, no. 20, pp. 11930–11935, 1996. View at Publisher · View at Google Scholar · View at Scopus
  72. J. Couet, S. Li, T. Okamoto, T. Ikezu, and M. P. Lisanti, “Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins,” The Journal of Biological Chemistry, vol. 272, no. 10, pp. 6525–6533, 1997. View at Google Scholar
  73. M. Yamamoto, Y. Toya, C. Schwencke, M. P. Lisanti, M. G. Myers Jr., and Y. Ishikawa, “Caveolin is an activator of insulin receptor signaling,” The Journal of Biological Chemistry, vol. 273, no. 41, pp. 26962–26968, 1998. View at Publisher · View at Google Scholar · View at Scopus
  74. V. J. Venema, R. Zou, H. Ju, M. B. Marrero, and R. C. Venema, “Caveolin-1 detergent solubility and association with endothelial nitric oxide synthase is modulated by tyrosine phosphorylation,” Biochemical and Biophysical Research Communications, vol. 236, no. 1, pp. 155–161, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Murata, J. Peranen, R. Schreiner, F. Wieland, T. V. Kurzchalia, and K. Simons, “VIP21/caveolin is a cholesterol-binding protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 22, pp. 10339–10343, 1995. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Pol, R. Luetterforst, M. Lindsay, S. Heino, E. Ikonen, and R. G. Parton, “A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance,” The Journal of Cell Biology, vol. 152, no. 5, pp. 1057–1070, 2001. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Tagawa, A. Mezzacasa, A. Hayer, A. Longatti, L. Pelkmans, and A. Helenius, “Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters,” The Journal of Cell Biology, vol. 170, no. 5, pp. 769–779, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. C. Boscher and I. R. Nabi, “Caveolin-1: role in cell signaling,” Advances in Experimental Medicine and Biology, vol. 729, pp. 29–50, 2012. View at Google Scholar
  79. N. Patani, L. A. Martin, J. S. Reis-Filho, and M. Dowsett, “The role of caveolin-1 in human breast cancer,” Breast Cancer Research and Treatment, vol. 131, no. 1, pp. 1–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. J. C. Zenklusen, J. N. Weitzel, H. G. Ball, and C. J. Conti, “Allelic loss at 7q31.1 in human primary ovarian carcinomas suggests the existence of a tumor suppressor gene,” Oncogene, vol. 11, no. 2, pp. 359–363, 1995. View at Google Scholar
  81. J. A. Engelman, X. L. Zhang, and M. P. Lisanti, “Genes encoding human caveolin-1 and -2 are co-localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers,” FEBS Letters, vol. 436, no. 3, pp. 403–410, 1998. View at Publisher · View at Google Scholar
  82. W. Ma, D. D. Wang, L. Li et al., “Caveolin-1 plays a key role in the oleanolic acid-induced apoptosis of HL-60 cells,” Oncology Reports, vol. 32, no. 1, pp. 293–301, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. T. M. Williams and M. P. Lisanti, “Caveolin-1 in oncogenic transformation, cancer, and metastasis,” American Journal of Physiology. Cell Physiology, vol. 288, no. 3, pp. C494–C506, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Caliceti, L. Zambonin, B. Rizzo et al., “Role of plasma membrane caveolae/lipid rafts in VEGF-induced redox signaling in human leukemia cells,” BioMed Research International, vol. 2014, Article ID 857504, p. 13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Zhang, G. Yang, W. Wu et al., “Decreased expression of caveolin-1 and E-cadherin correlates with the clinicopathologic features of gastric cancer and the EMT process,” Recent Patents on Anti-Cancer Drug Discovery, vol. 11, no. 2, pp. 236–244, 2016. View at Publisher · View at Google Scholar · View at Scopus
  86. X. J. Shen, H. Zhang, G. S. Tang et al., “Caveolin-1 is a modulator of fibroblast activation and a potential biomarker for gastric cancer,” International Journal of Biological Sciences, vol. 11, no. 4, pp. 370–379, 2015. View at Publisher · View at Google Scholar · View at Scopus
  87. E. Burgermeister, T. Friedrich, I. Hitkova et al., “The Ras inhibitors caveolin-1 and docking protein 1 activate peroxisome proliferator-activated receptor gamma through spatial relocalization at helix 7 of its ligand-binding domain,” Molecular and Cellular Biology, vol. 31, no. 16, pp. 3497–3510, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Hammarsten, T. Dahl Scherdin, C. Hagglof et al., “High caveolin-1 expression in tumor stroma is associated with a favourable outcome in prostate cancer patients managed by watchful waiting,” PloS One, vol. 11, no. 10, article e0164016, 2016. View at Publisher · View at Google Scholar
  89. J. Huertas-Martinez, S. Rello-Varona, D. Herrero-Martin et al., “Caveolin-1 is down-regulated in alveolar rhabdomyosarcomas and negatively regulates tumor growth,” Oncotarget, vol. 5, no. 20, pp. 9744–9755, 2014. View at Publisher · View at Google Scholar
  90. F. Han and H. G. Zhu, “Caveolin-1 regulating the invasion and expression of matrix metalloproteinase (MMPs) in pancreatic carcinoma cells,” The Journal of Surgical Research, vol. 159, no. 1, pp. 443–450, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. F. Han and H. G. Zhu, “Over-expression of caveolin-1 inhibits proliferation and invasion of pancreatic carcinoma cells in vitro,” Zhonghua Zhong Liu Za Zhi, vol. 31, no. 10, pp. 732–737, 2009. View at Publisher · View at Google Scholar
  92. S. F. Chen, J. Y. Liou, T. Y. Huang et al., “Caveolin-1 facilitates cyclooxygenase-2 protein degradation,” Journal of Cellular Biochemistry, vol. 109, no. 2, pp. 356–362, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Feldman and J. D. Martinez, “Growth suppression by ursodeoxycholic acid involves caveolin-1 enhanced degradation of EGFR,” Biochimica et Biophysica Acta, vol. 1793, no. 8, pp. 1387–1394, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Trimmer, D. Whitaker-Menezes, G. Bonuccelli et al., “CAV1 inhibits metastatic potential in melanomas through suppression of the integrin/Src/FAK signaling pathway,” Cancer Research, vol. 70, no. 19, pp. 7489–7499, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Kang, J. H. Park, H. J. Lee et al., “Caveolin-1 modulates docetaxel-induced cell death in breast cancer cell subtypes through different mechanisms,” Cancer Research and Treatment, vol. 48, no. 2, pp. 715–726, 2016. View at Publisher · View at Google Scholar · View at Scopus
  96. X. Y. Shi, L. X. Xiong, L. Xiao, C. Meng, G. Y. Qi, and W. L. Li, “Downregulation of caveolin1 upregulates the expression of growth factors and regulators in coculture of fibroblasts with cancer cells,” Molecular Medicine Reports, vol. 13, no. 1, pp. 744–752, 2016. View at Publisher · View at Google Scholar · View at Scopus
  97. A. K. Witkiewicz, A. Dasgupta, K. H. Nguyen et al., “Stromal caveolin-1 levels predict early DCIS progression to invasive breast cancer,” Cancer Biology & Therapy, vol. 8, no. 11, pp. 1071–1079, 2009. View at Google Scholar
  98. E. K. Sloan, D. R. Ciocca, N. Pouliot et al., “Stromal cell expression of caveolin-1 predicts outcome in breast cancer,” The American Journal of Pathology, vol. 174, no. 6, pp. 2035–2043, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. J. S. Koo, S. Park, S. I. Kim, S. Lee, and B. W. Park, “The impact of caveolin protein expression in tumor stroma on prognosis of breast cancer,” Tumour Biology, vol. 32, no. 4, pp. 787–799, 2011. View at Google Scholar
  100. N. Qian, T. Ueno, N. Kawaguchi-Sakita et al., “Prognostic significance of tumor/stromal caveolin-1 expression in breast cancer patients,” Cancer Science, vol. 102, no. 8, pp. 1590–1596, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. S. M. El-Gendi, M. F. Mostafa, and A. M. El-Gendi, “Stromal caveolin-1 expression in breast carcinoma. Correlation with early tumor recurrence and clinical outcome,” Pathology Oncology Research: POR, vol. 18, no. 2, pp. 459–469, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. D. Di Vizio, M. Morello, F. Sotgia, R. G. Pestell, M. R. Freeman, and M. P. Lisanti, “An absence of stromal caveolin-1 is associated with advanced prostate cancer, metastatic disease and epithelial Akt activation,” Cell Cycle, vol. 8, no. 15, pp. 2420–2424, 2009. View at Google Scholar
  103. X. Zhao, Y. He, J. Gao et al., “Caveolin-1 expression level in cancer associated fibroblasts predicts outcome in gastric cancer,” PloS One, vol. 8, no. 3, article e59102, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. L. Cantiani, M. C. Manara, C. Zucchini et al., “Caveolin-1 reduces osteosarcoma metastases by inhibiting c-Src activity and met signaling,” Cancer Research, vol. 67, no. 16, pp. 7675–7685, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Shatz and M. Liscovitch, “Caveolin-1 and cancer multidrug resistance: coordinate regulation of pro-survival proteins?” Leukemia Research, vol. 28, no. 9, pp. 907–908, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Pang, W. Y. Au, and Y. L. Kwong, “Caveolin-1 gene is coordinately regulated with the multidrug resistance 1 gene in normal and leukemic bone marrow,” Leukemia Research, vol. 28, no. 9, pp. 973–977, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. M. M. Belanger, M. Gaudreau, E. Roussel, and J. Couet, “Role of caveolin-1 in etoposide resistance development in A549 lung cancer cells,” Cancer Biology & Therapy, vol. 3, no. 10, pp. 954–959, 2004. View at Google Scholar
  108. C. Cai and J. Chen, “Overexpression of caveolin-1 induces alteration of multidrug resistance in Hs578T breast adenocarcinoma cells,” International Journal of Cancer, vol. 111, no. 4, pp. 522–529, 2004. View at Publisher · View at Google Scholar · View at Scopus
  109. D. J. Stewart, “Mechanisms of resistance to cisplatin and carboplatin,” Critical Reviews in Oncology/Hematology, vol. 63, no. 1, pp. 12–31, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. E. M. Bertino, T. M. Williams, S. P. Nana-Sinkam et al., “Stromal caveolin-1 is associated with response and survival in a phase II trial of nab-paclitaxel with carboplatin for advanced NSCLC patients,” Clinical Lung Cancer, vol. 16, no. 6, pp. 466–474, 2015. View at Publisher · View at Google Scholar · View at Scopus
  111. G. Ayala, M. Morello, A. Frolov et al., “Loss of caveolin-1 in prostate cancer stroma correlates with reduced relapse-free survival and is functionally relevant to tumour progression,” The Journal of Pathology, vol. 231, no. 1, pp. 77–87, 2013. View at Publisher · View at Google Scholar · View at Scopus
  112. Y. Jia, N. Wang, J. Wang et al., “Down-regulation of stromal caveolin-1 expression in esophageal squamous cell carcinoma: a potent predictor of lymph node metastases, early tumor recurrence, and poor prognosis,” Annals of Surgical Oncology, vol. 21, no. 1, pp. 329–336, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. S. F. Yang, J. Y. Yang, C. H. Huang et al., “Increased caveolin-1 expression associated with prolonged overall survival rate in hepatocellular carcinoma,” Pathology, vol. 42, no. 5, pp. 438–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. Ye, S. H. Miao, R. Z. Lu, and J. W. Zhou, “Prognostic value of caveolin-1 expression in gastric cancer: a meta-analysis,” Asian Pacific Journal of Cancer Prevention : APJCP, vol. 15, no. 19, pp. 8367–8370, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. M. Shatz and M. Liscovitch, “Caveolin-1: a tumor-promoting role in human cancer,” International Journal of Radiation Biology, vol. 84, no. 3, pp. 177–189, 2008. View at Google Scholar
  116. C. C. Ho, S. H. Kuo, P. H. Huang, H. Y. Huang, C. H. Yang, and P. C. Yang, “Caveolin-1 expression is significantly associated with drug resistance and poor prognosis in advanced non-small cell lung cancer patients treated with gemcitabine-based chemotherapy,” Lung Cancer, vol. 59, no. 1, pp. 105–110, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. E. Selga, C. Morales, V. Noe, M. A. Peinado, and C. J. Ciudad, “Role of caveolin 1, E-cadherin, enolase 2 and PKCalpha on resistance to methotrexate in human HT29 colon cancer cells,” BMC Medical Genomics, vol. 1, no. 1, p. 35, 2008. View at Google Scholar
  118. Z. Wang, N. Wang, W. Li et al., “Caveolin-1 mediates chemoresistance in breast cancer stem cells via beta-catenin/ABCG2 signaling pathway,” Carcinogenesis, vol. 35, no. 10, pp. 2346–2356, 2014. View at Publisher · View at Google Scholar · View at Scopus
  119. Z. Y. Wang, N. Wang, P. X. Liu et al., “Caveolin-1, a stress-related oncotarget, in drug resistance,” Oncotarget, vol. 6, no. 35, pp. 37135–37150, 2015. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Tien Kuo and N. Savaraj, “Roles of reactive oxygen species in hepatocarcinogenesis and drug resistance gene expression in liver cancers,” Molecular Carcinogenesis, vol. 45, no. 9, pp. 701–9, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Kimura, S. Ito, M. Nagino, and K. Isobe, “Inhibition of reactive oxygen species down-regulates protein synthesis in RAW 264.7,” Biochemical and Biophysical Research Communications, vol. 372, no. 1, pp. 272–275, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. A. S. Veskoukis, A. M. Tsatsakis, and D. Kouretas, “Dietary oxidative stress and antioxidant defense with an emphasis on plant extract administration,” Cell Stress & Chaperones, vol. 17, no. 1, pp. 11–21, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. A. Matsui, T. Ikeda, K. Enomoto et al., “Increased formation of oxidative DNA damage, 8-hydroxy-2′-deoxyguanosine, in human breast cancer tissue and its relationship to GSTP1 and COMT genotypes,” Cancer Letters, vol. 151, no. 1, pp. 87–95, 2000. View at Publisher · View at Google Scholar · View at Scopus
  124. A. Abdul-Aziz, D. J. MacEwan, K. M. Bowles, and S. A. Rushworth, “Oxidative stress responses and NRF2 in human leukaemia,” Oxidative Medicine and Cellular Longevity, vol. 2015, p. 454659, 2015. View at Publisher · View at Google Scholar · View at Scopus
  125. J. L. Arbiser, J. Petros, R. Klafter et al., “Reactive oxygen generated by Nox1 triggers the angiogenic switch,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 715–720, 2002. View at Publisher · View at Google Scholar · View at Scopus
  126. C. Polytarchou, M. Hatziapostolou, and E. Papadimitriou, “Hydrogen peroxide stimulates proliferation and migration of human prostate cancer cells through activation of activator protein-1 and up-regulation of the heparin affin regulatory peptide gene,” The Journal of Biological Chemistry, vol. 280, no. 49, pp. 40428–40435, 2005. View at Publisher · View at Google Scholar · View at Scopus
  127. Y. Nakamura, T. D. Gindhart, D. Winterstein, I. Tomita, J. L. Seed, and N. H. Colburn, “Early superoxide dismutase-sensitive event promotes neoplastic transformation in mouse epidermal JB6 cells,” Carcinogenesis, vol. 9, no. 2, pp. 203–207, 1988. View at Publisher · View at Google Scholar · View at Scopus
  128. B. del Bello, A. Paolicchi, M. Comporti, A. Pompella, and E. Maellaro, “Hydrogen peroxide produced during gamma-glutamyl transpeptidase activity is involved in prevention of apoptosis and maintenance of proliferation in U937 cells,” FASEB Journal, vol. 13, no. 1, pp. 69–79, 1999. View at Google Scholar
  129. E. Giannoni, T. Fiaschi, G. Ramponi, and P. Chiarugi, “Redox regulation of anoikis resistance of metastatic prostate cancer cells: key role for Src and EGFR-mediated pro-survival signals,” Oncogene, vol. 28, no. 20, pp. 2074–2086, 2009. View at Publisher · View at Google Scholar · View at Scopus
  130. U. E. Martinez-Outschoorn, C. Trimmer, Z. Lin et al., “Autophagy in cancer associated fibroblasts promotes tumor cell survival: role of hypoxia, HIF1 induction and NF kappa B activation in the tumor stromal microenvironment,” Cell Cycle, vol. 9, no. 17, pp. 3515–3533, 2010. View at Google Scholar
  131. C. Trimmer, F. Sotgia, D. Whitaker-Menezes et al., “Caveolin-1 and mitochondrial SOD2 (MnSOD) function as tumor suppressors in the stromal microenvironment: a new genetically tractable model for human cancer associated fibroblasts,” Cancer Biology & Therapy, vol. 11, no. 4, pp. 383–394, 2011. View at Google Scholar
  132. A. C. Souici, J. Mirkovitch, P. Hausel, L. K. Keefer, and E. Felley-Bosco, “Transition mutation in codon 248 of the p53 tumor suppressor gene induced by reactive oxygen species and a nitric oxide-releasing compound,” Carcinogenesis, vol. 21, no. 2, pp. 281–287, 2000. View at Publisher · View at Google Scholar
  133. J. A. Coulter, H. O. McCarthy, J. Xiang et al., “Nitric oxide - a novel therapeutic for cancer,” Nitric Oxide: Biology Ch, vol. 19, no. 2, pp. 192–198, 2008. View at Publisher · View at Google Scholar · View at Scopus
  134. L. Ying and L. J. Hofseth, “An emerging role for endothelial nitric oxide synthase in chronic inflammation and cancer,” Cancer Research, vol. 67, no. 4, pp. 1407–1410, 2007. View at Publisher · View at Google Scholar · View at Scopus
  135. B. R. Crane, A. S. Arvai, R. Gachhui et al., “The structure of nitric oxide synthase oxygenase domain and inhibitor complexes,” Science, vol. 278, no. 5337, pp. 425–431, 1997. View at Publisher · View at Google Scholar · View at Scopus
  136. Z. L. Chen, F. R. Bakhshi, A. N. Shajahan et al., “Nitric oxide-dependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/caveolin-1 binding and eNOS inhibition,” Molecular Biology of the Cell, vol. 23, no. 7, pp. 1388–1398, 2012. View at Google Scholar
  137. T. M. Williams and M. P. Lisanti, “Caveolin-1 in oncogenic transformation, cancer, and metastasis,” American Journal of Physiology. Cell Physiology, vol. 288, no. 3, pp. C494–C506, 2005. View at Google Scholar
  138. N. B. Janakiram and C. V. Rao, “iNOS-selective inhibitors for cancer prevention: promise and progress,” Future Medicinal Chemistry, vol. 4, no. 17, pp. 2193–2204, 2012. View at Publisher · View at Google Scholar · View at Scopus
  139. C. V. Rao, C. Indranie, B. Simi, P. T. Manning, J. R. Connor, and B. S. Reddy, “Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase-2 inhibitor,” Cancer Research, vol. 62, no. 1, pp. 165–170, 2002. View at Google Scholar
  140. E. J. Smart, G. A. Graf, M. A. McNiven et al., “Caveolins, liquid-ordered domains, and signal transduction,” Molecular and Cellular Biology, vol. 19, no. 11, pp. 7289–7304, 1999. View at Publisher · View at Google Scholar
  141. R. Gniadecki, N. Christoffersen, and H. C. Wulf, “Cholesterol-rich plasma membrane domains (lipid rafts) in keratinocytes: importance in the baseline and UVA-induced generation of reactive oxygen species,” The Journal of Investigative Dermatology, vol. 118, no. 4, pp. 582–588, 2002. View at Publisher · View at Google Scholar · View at Scopus
  142. A. Mougeolle, S. Poussard, M. Decossas, C. Lamaze, O. Lambert, and E. Dargelos, “Oxidative stress induces caveolin 1 degradation and impairs caveolae functions in skeletal muscle cells,” PloS One, vol. 10, no. 3, article e0122654, 2015. View at Publisher · View at Google Scholar · View at Scopus
  143. R. P. Cai, Y. X. Xue, J. Huang et al., “NS1619 regulates the expression of caveolin-1 protein in a time-dependent manner via ROS/PI3K/PKB/FoxO1 signaling pathway in brain tumor microvascular endothelial cells,” Journal of the Neurological Sciences, vol. 369, pp. 109–118, 2016. View at Publisher · View at Google Scholar · View at Scopus
  144. Z. Zhang, K. Yao, and C. Jin, “Apoptosis of lens epithelial cells induced by high concentration of glucose is associated with a decrease in caveolin-1 levels,” Molecular Vision, vol. 15, no. 214, pp. 2008–2017, 2009. View at Google Scholar
  145. S. Luanpitpong, S. J. Talbott, Y. Rojanasakul et al., “Regulation of lung cancer cell migration and invasion by reactive oxygen species and caveolin-1,” The Journal of Biological Chemistry, vol. 285, no. 50, pp. 38832–38840, 2010. View at Publisher · View at Google Scholar · View at Scopus
  146. C. J. Percy, B. K. Pat, H. Healy, D. W. Johnson, and G. C. Gobe, “Phosphorylation of caveolin-1 is anti-apoptotic and promotes cell attachment during oxidative stress of kidney cells,” Pathology, vol. 40, no. 7, pp. 694–701, 2008. View at Publisher · View at Google Scholar · View at Scopus
  147. Y. Zhang, X. Qu, Y. Teng et al., “Cbl-b inhibits P-gp transporter function by preventing its translocation into caveolae in multiple drug-resistant gastric and breast cancers,” Oncotarget, vol. 6, no. 9, pp. 6737–6748, 2015. View at Publisher · View at Google Scholar
  148. J. R. Glenney Jr., “Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus,” The Journal of Biological Chemistry, vol. 264, no. 34, pp. 20163–20166, 1989. View at Google Scholar
  149. C. C. Mastick, M. J. Brady, and A. R. Saltiel, “Insulin stimulates the tyrosine phosphorylation of caveolin,” The Journal of Cell Biology, vol. 129, no. 6, pp. 1523–1531, 1995. View at Publisher · View at Google Scholar · View at Scopus
  150. M. O. Parat, R. Z. Stachowicz, and P. L. Fox, “Oxidative stress inhibits caveolin-1 palmitoylation and trafficking in endothelial cells,” The Biochemical Journal, vol. 361, no. Part 3, pp. 681–688, 2002. View at Publisher · View at Google Scholar · View at Scopus
  151. R. Nomura and T. Fujimoto, “Tyrosine-phosphorylated caveolin-1: immunolocalization and molecular characterization,” Molecular Biology of the Cell, vol. 10, no. 4, pp. 975–986, 1999. View at Publisher · View at Google Scholar
  152. S. Wehinger, R. Ortiz, M. I. Diaz et al., “Phosphorylation of caveolin-1 on tyrosine-14 induced by ROS enhances palmitate-induced death of beta-pancreatic cells,” Biochimica et Biophysica Acta, vol. 1852, no. 5, pp. 693–708, 2015. View at Publisher · View at Google Scholar · View at Scopus
  153. L. N. Sun, X. C. Liu, X. J. Chen, G. J. Guan, and G. Liu, “Curcumin attenuates high glucose-induced podocyte apoptosis by regulating functional connections between caveolin-1 phosphorylation and ROS,” Acta Pharmacologica Sinica, vol. 37, no. 5, pp. 645–655, 2016. View at Publisher · View at Google Scholar
  154. T. Aoki, R. Nomura, and T. Fujimoto, “Tyrosine phosphorylation of caveolin-1 in the endothelium,” Experimental Cell Research, vol. 253, no. 2, pp. 629–636, 1999. View at Publisher · View at Google Scholar · View at Scopus
  155. A. Schlegel, P. Arvan, and M. P. Lisanti, “Caveolin-1 binding to endoplasmic reticulum membranes and entry into the regulated secretory pathway are regulated by serine phosphorylation protein sorting at the level of the endoplasmic reticulum,” The Journal of Biological Chemistry, vol. 276, no. 6, pp. 4398–4408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  156. X. Q. Wang, P. Sun, and A. S. Paller, “Ganglioside induces caveolin-1 redistribution and interaction with the epidermal growth factor receptor,” The Journal of Biological Chemistry, vol. 277, no. 49, pp. 47028–47034, 2002. View at Publisher · View at Google Scholar · View at Scopus
  157. S. Blaskovic, M. Blanc, and F. G. van der Goot, “What does S-palmitoylation do to membrane proteins?” The FEBS Journal, vol. 280, no. 12, pp. 2766–2774, 2013. View at Publisher · View at Google Scholar · View at Scopus
  158. O. Rocks, A. Peyker, M. Kahms et al., “An acylation cycle regulates localization and activity of palmitoylated Ras isoforms,” Science, vol. 307, no. 5716, pp. 1746–1752, 2005. View at Publisher · View at Google Scholar · View at Scopus
  159. D. J. Dietzen, W. R. Hastings, and D. M. Lublin, “Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae,” The Journal of Biological Chemistry, vol. 270, no. 12, pp. 6838–6842, 1995. View at Google Scholar
  160. A. Uittenbogaard and E. J. Smart, “Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae,” The Journal of Biological Chemistry, vol. 275, no. 33, pp. 25595–25599, 2000. View at Publisher · View at Google Scholar · View at Scopus
  161. H. Lee, S. E. Woodman, J. A. Engelman et al., “Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14),” The Journal of Biological Chemistry, vol. 276, no. 37, pp. 35150–35158, 2001. View at Publisher · View at Google Scholar · View at Scopus
  162. E. J. Smart, Y. S. Ying, P. A. Conrad, and R. G. Anderson, “Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation,” The Journal of Cell Biology, vol. 127, no. 5, pp. 1185–1197, 1994. View at Publisher · View at Google Scholar · View at Scopus
  163. A. Blair, P. W. Shaul, I. S. Yuhanna, P. A. Conrad, and E. J. Smart, “Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation,” The Journal of Biological Chemistry, vol. 274, no. 45, pp. 32512–32519, 1999. View at Publisher · View at Google Scholar · View at Scopus
  164. T. Shiroto, N. Romero, T. Sugiyama et al., “Caveolin-1 is a critical determinant of autophagy, metabolic switching, and oxidative stress in vascular endothelium,” PloS One, vol. 9, no. 2, article e87871, 2014. View at Publisher · View at Google Scholar · View at Scopus
  165. H. Wang, A. X. Wang, Z. Liu, W. Chai, and E. J. Barrett, “The trafficking/interaction of eNOS and caveolin-1 induced by insulin modulates endothelial nitric oxide production,” Molecular Endocrinology, vol. 23, no. 10, pp. 1613–1623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  166. J. P. Gratton, M. I. Lin, J. Yu et al., “Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice,” Cancer Cell, vol. 4, no. 1, pp. 31–39, 2003. View at Publisher · View at Google Scholar · View at Scopus
  167. H. L. Yang, W. Q. Chen, X. Cao et al., “Caveolin-1 enhances resveratrol-mediated cytotoxicity and transport in a hepatocellular carcinoma model,” Journal of Translational Medicine, vol. 7, no. 1, p. 22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  168. H. Zhan, F. Huang, W. Ma, Z. Zhao, H. Zhang, and C. Zhang, “Protective effect of ginsenoside Rg1 on bleomycin-induced pulmonary fibrosis in rats: involvement of caveolin-1 and TGF-beta1 signal pathway,” Biological & Pharmaceutical Bulletin, vol. 39, no. 8, pp. 1284–1292, 2016. View at Publisher · View at Google Scholar · View at Scopus
  169. K. Nakaso, N. Tajima, Y. Horikoshi et al., “The estrogen receptor beta-PI3K/Akt pathway mediates the cytoprotective effects of tocotrienol in a cellular Parkinson’s disease model,” Biochimica et Biophysica Acta, vol. 1842, no. 9, pp. 1303–1312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  170. P. Palozza, R. Simone, A. Catalano, N. Parrone, G. Monego, and F. O. Ranelletti, “Lycopene regulation of cholesterol synthesis and efflux in human macrophages,” The Journal of Nutritional Biochemistry, vol. 22, no. 10, pp. 971–978, 2011. View at Publisher · View at Google Scholar · View at Scopus
  171. M. Sanchez, M. Galisteo, R. Vera et al., “Quercetin downregulates NADPH oxidase, increases eNOS activity and prevents endothelial dysfunction in spontaneously hypertensive rats,” Journal of Hypertension, vol. 24, no. 1, pp. 75–84, 2006. View at Publisher · View at Google Scholar
  172. X. Zeng, Y. Cheng, Y. Qu, J. Xu, Z. Han, and T. Zhang, “Curcumin inhibits the proliferation of airway smooth muscle cells in vitro and in vivo,” International Journal of Molecular Medicine, vol. 32, no. 3, pp. 629–636, 2013. View at Publisher · View at Google Scholar · View at Scopus
  173. L. N. Sun, Z. X. Chen, X. C. Liu, H. Y. Liu, G. J. Guan, and G. Liu, “Curcumin ameliorates epithelial-to-mesenchymal transition of podocytes in vivo and in vitro via regulating caveolin-1,” Biomedicine Pharmacotherapy Biochemical Pharmacology, vol. 68, no. 8, pp. 1079–1088, 2014. View at Publisher · View at Google Scholar
  174. L. N. Sun, Z. Y. Yang, S. S. Lv, X. C. Liu, G. J. Guan, and G. Liu, “Curcumin prevents diabetic nephropathy against inflammatory response via reversing caveolin-1 Tyr14 phosphorylation influenced TLR4 activation,” International Immunopharmacology, vol. 23, no. 1, pp. 236–246, 2014. View at Publisher · View at Google Scholar · View at Scopus
  175. H. Y. Yuan, S. Y. Kuang, X. Zheng et al., “Curcumin inhibits cellular cholesterol accumulation by regulating SREBP-1/caveolin-1 signaling pathway in vascular smooth muscle cells,” Acta Pharmacologica Sinica, vol. 29, no. 5, pp. 555–563, 2008. View at Publisher · View at Google Scholar · View at Scopus
  176. O. P. Heinonen, J. K. Huttunen, D. Albanes et al., “The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. The alpha-tocopherol, beta carotene cancer prevention study group,” The New England Journal of Medicine, vol. 330, no. 15, pp. 1029–1035, 1994. View at Publisher · View at Google Scholar · View at Scopus
  177. V. I. Sayin, M. X. Ibrahim, E. Larsson, J. A. Nilsson, P. Lindahl, and M. O. Bergo, “Antioxidants accelerate lung cancer progression in mice,” Science Translational Medicine, vol. 6, no. 221, p. 221ra15, 2014. View at Publisher · View at Google Scholar
  178. S. M. Lippman, P. J. Goodman, E. A. Klein et al., “Designing the Selenium and Vitamin E Cancer Prevention Trial (SELECT),” Journal of the National Cancer Institute, vol. 97, no. 2, pp. 94–102, 2005. View at Publisher · View at Google Scholar · View at Scopus
  179. E. A. Klein, I. M. Thompson Jr., C. M. Tangen et al., “Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT),” Jama, vol. 306, no. 14, pp. 1549–1556, 2011. View at Publisher · View at Google Scholar · View at Scopus
  180. I. B. Weinstein and A. Joe, “Oncogene addiction,” Cancer Research, vol. 68, no. 9, pp. 3077–3080, 2008, discussion 3080. View at Publisher · View at Google Scholar · View at Scopus
  181. D. R. S. Bryan and G. Allen, “Metabolic production of H2O2 in carcinogenesis and cancer treatment,” Redox-Active Therapeutics, Springer International Publishing, Switzerland, 2016. View at Publisher · View at Google Scholar
  182. A. L. Simons, I. M. Ahmad, D. M. Mattson, K. J. Dornfeld, and D. R. Spitz, “2-Deoxy-D-glucose combined with cisplatin enhances cytotoxicity via metabolic oxidative stress in human head and neck cancer cells,” Cancer Research, vol. 67, no. 7, pp. 3364–3370, 2007. View at Publisher · View at Google Scholar · View at Scopus
  183. P. C. Hart, B. A. Ratti, M. Mao et al., “Caveolin-1 regulates cancer cell metabolism via scavenging Nrf2 and suppressing MnSOD-driven glycolysis,” Oncotarget, vol. 7, no. 1, pp. 308–322, 2016. View at Publisher · View at Google Scholar
  184. F. Sotgia, U. E. Martinez-Outschoorn, S. Pavlides, A. Howell, R. G. Pestell, and M. P. Lisanti, “Understanding the Warburg effect and the prognostic value of stromal caveolin-1 as a marker of a lethal tumor microenvironment,” Breast Cancer Research, vol. 13, no. 4, p. 213, 2011. View at Google Scholar
  185. G. Bonuccelli, D. Whitaker-Menezes, R. Castello-Cros et al., “The reverse Warburg effect: glycolysis inhibitors prevent the tumor promoting effects of caveolin-1 deficient cancer associated fibroblasts,” Cell Cycle, vol. 9, no. 10, pp. 1960–1971, 2010. View at Google Scholar
  186. V. Coelho-Santos, R. Socodato, C. Portugal et al., “Methylphenidate-triggered ROS generation promotes caveolae-mediated transcytosis via Rac1 signaling and c-Src-dependent caveolin-1 phosphorylation in human brain endothelial cells,” Cellular and Molecular Life Sciences: CMLS, vol. 24, no. 73, pp. 4701–4716, 2016. View at Publisher · View at Google Scholar · View at Scopus
  187. S. Agelaki, M. Spiliotaki, H. Markomanolaki et al., “Caveolin-1 regulates EGFR signaling in MCF-7 breast cancer cells and enhances gefitinib-induced tumor cell inhibition,” Cancer Biology & Therapy, vol. 8, no. 15, pp. 1470–1477, 2009. View at Google Scholar
  188. Z. Li, S. S. Yang, P. H. Yin et al., “Activated estrogen receptor-mitogen-activated protein kinases cross talk confer acquired resistance to lapatinib,” Thoracic Cancer, vol. 6, no. 6, pp. 695–703, 2015. View at Publisher · View at Google Scholar · View at Scopus
  189. G. E. Konecny, R. Glas, J. Dering et al., “Activity of the multikinase inhibitor dasatinib against ovarian cancer cells,” British Journal of Cancer, vol. 101, no. 10, pp. 1699–1708, 2009. View at Publisher · View at Google Scholar · View at Scopus
  190. D. Medina, F. Kittrell, J. Hill et al., “Prevention of tumorigenesis in p53-null mammary epithelium by rexinoid bexarotene, tyrosine kinase inhibitor gefitinib, and celecoxib,” Cancer Prevention Research (Philadelphia, Pa.), vol. 2, no. 2, pp. 168–174, 2009. View at Publisher · View at Google Scholar · View at Scopus
  191. X. Wan, X. Zheng, X. Pang et al., “Lapatinib-loaded human serum albumin nanoparticles for the prevention and treatment of triple-negative breast cancer metastasis to the brain,” Oncotarget, vol. 7, no. 23, pp. 34038–34051, 2016. View at Publisher · View at Google Scholar · View at Scopus
  192. B. Gril, D. Palmieri, Y. Qian et al., “Pazopanib reveals a role for tumor cell B-Raf in the prevention of HER2+ breast cancer brain metastasis,” Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, vol. 17, no. 1, pp. 142–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  193. C. Printz, “Clinical trials of note. Sorafenib as adjuvant treatment in the prevention of disease recurrence in patients with hepatocellular carcinoma (HCC) (STORM),” Cancer, vol. 115, no. 20, p. 4646, 2009. View at Publisher · View at Google Scholar
  194. M. P. Murphy and R. A. Smith, “Targeting antioxidants to mitochondria by conjugation to lipophilic cations,” Annual Review of Pharmacology and Toxicology, vol. 47, pp. 629–656, 2007. View at Publisher · View at Google Scholar · View at Scopus
  195. I. W. Asterholm, D. I. Mundy, J. Weng, R. G. Anderson, and P. E. Scherer, “Altered mitochondrial function and metabolic inflexibility associated with loss of caveolin-1,” Cell Metabolism, vol. 15, no. 2, pp. 171–185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  196. M. Bosch, M. Mari, A. Herms et al., “Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility,” Current Biology: CB, vol. 21, no. 8, pp. 681–686, 2011. View at Publisher · View at Google Scholar · View at Scopus
  197. D. Volonte, Z. Liu, S. Shiva, and F. Galbiati, “Caveolin-1 controls mitochondrial function through regulation of m-AAA mitochondrial protease,” Aging, vol. 8, no. 10, pp. 2355–2369, 2016. View at Publisher · View at Google Scholar