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Mediators of Inflammation
Volume 2014, Article ID 478138, 11 pages
http://dx.doi.org/10.1155/2014/478138
Research Article

Deregulation of Annexin-A1 and Galectin-1 Expression in Precancerous Gastric Lesions: Intestinal Metaplasia and Gastric Ulcer

1Department of Biology, São Paulo State University (UNESP), Câmpus São José do Rio Preto, Rua Cristóvão Colombo 2265, 15054-000 São José do Rio Preto, SP, Brazil
2Legal Medicine Department and Pathology Service, Hospital de Base, Avenida Brigadeiro Faria Lima 5544, 15090-000 São José do Rio Preto, SP, Brazil

Received 14 October 2013; Revised 15 January 2014; Accepted 15 January 2014; Published 25 February 2014

Academic Editor: Fulvio D’Acquisto

Copyright © 2014 Ana Flávia Teixeira Rossi 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. P. Correa, “A human model of gastric carcinogenesis,” Cancer Research, vol. 48, no. 13, pp. 3554–3560, 1988. View at Google Scholar · View at Scopus
  2. H. Watanabe, “Intestinal metaplasia—the effect of acid on the gastric mucosa and gastric carcinogenesis,” Journal of Toxicologic Pathology, vol. 23, no. 3, pp. 115–123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. R. A. Busuttil and A. Boussioutas, “Intestinal metaplasia: a premalignant lesion involved in gastric carcinogenesis,” Journal of Gastroenterology and Hepatology, vol. 24, no. 2, pp. 193–201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. J. A. Todd, C. J. Richards, A. Dixon, and R. J. Robinson, “Gastric ulcer and malignancy—is there a need for follow-up endoscopy?” Alimentary Pharmacology & Therapeutics, vol. 19, no. 9, pp. 989–991, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. J. G. Kusters, A. H. M. van Vliet, and E. J. Kuipers, “Pathogenesis of Helicobacter pylori infection,” Clinical Microbiology Reviews, vol. 19, no. 3, pp. 449–490, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Bauer and T. F. Meyer, “The human gastric pathogen Helicobacter pylori and its association with gastric cancer and ulcer disease,” Ulcers, vol. 2011, Article ID 340157, 23 pages, 2011. View at Publisher · View at Google Scholar
  7. A. S. T. de Carvalho, “Peptic ulcer,” Jornal de Pediatria, vol. 76, 2, pp. S127–S134, 2000. View at Google Scholar · View at Scopus
  8. C. Resende, A. Thiel, J. C. Machado, and A. Ristimäki, “Gastric câncer: basic aspects,” Helicobacter, vol. 16, supplement 1, pp. 38–44, 2011. View at Publisher · View at Google Scholar
  9. T. Chiba, H. Marusawa, and T. Ushijima, “Inflammation-associated cancer development in digestive organs: mechanisms and roles for genetic and epigenetic modulation,” Gastroenterology, vol. 143, no. 3, pp. 550–563, 2012. View at Publisher · View at Google Scholar
  10. D. B. Polk and R. M. Peek Jr., “Helicobacter pylori: gastric cancer and beyond,” Nature Reviews, vol. 10, no. 6, pp. 403–414, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Hatakeyama, “Helicobacter pylori and gastric carcinogenesis,” Journal of Gastroenterology, vol. 44, no. 4, pp. 239–248, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. B. X. Truong, V. T. C. Mai, H. Tanaka et al., “Diverse characteristics of the cagA gene of Helicobacter pylori strains collected from patients from Southern Vietnam with gastric cancer and peptic ulcer,” Journal of Clinical Microbiology, vol. 47, no. 12, pp. 4021–4028, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. V. Bizzarro, A. Petrella, and L. Parente, “Annexin A1: novel roles in skeletal muscle biology,” Journal of Cellular Physiology, vol. 227, no. 8, pp. 3007–3015, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Cedeno-Laurent and C. J. Dimitroff, “Galectin-1 research in T cell immunity: past, present and future,” Clinical Immunology, vol. 142, no. 2, pp. 107–116, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. L. H. K. Lim and S. Pervaiz, “Annexin 1: the new face of an old molecule,” The FASEB Journal, vol. 21, no. 4, pp. 968–975, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. J. P. Vago, C. R. C. Nogueira, L. P. Tavares et al., “Annexin A1 modulates natural and glucocorticoid-induced resolution of inflammation by enhancing neutrophil apoptosis,” Journal of Leukocyte Biology, vol. 92, no. 2, pp. 249–258, 2012. View at Publisher · View at Google Scholar
  17. R. J. Flower and G. J. Blackwell, “Anti-inflammatory steroids induce biosynthesis of a phospholipase A2 inhibitor which prevents prostaglandin generation,” Nature, vol. 278, no. 5703, pp. 456–459, 1979. View at Publisher · View at Google Scholar · View at Scopus
  18. S. M. Oliani and C. D. Gil, “Proteína antiinflamatória anexina 1: mecanismos celulares e relevância clínica,” Revista Arquivos de Ciências da Saúde, vol. 13, pp. 186–191, 2006. View at Google Scholar
  19. V. A. F. Alves, S. Nonogaki, P. M. Cury et al., “Annexin A1 subcellular expression in laryngeal squamous cell carcinoma,” Histopathology, vol. 53, no. 6, pp. 715–727, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C.-Y. Lin, Y.-M. Jeng, H.-Y. Chou et al., “Nuclear localization of annexin A1 is a prognostic factor in oral squamous cell carcinoma,” Journal of Surgical Oncology, vol. 97, no. 6, pp. 544–550, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Nomura, K. Uzawa, Y. Yamano et al., “Down-regulation of plasma membranous annexin A1 protein expression in premalignant and malignant lesions of the oral cavity: correlation with epithelial differentiation,” Journal of Cancer Research and Clinical Oncology, vol. 135, no. 7, pp. 943–949, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. W.-Y. Kang, W.-T. Chen, Y.-C. Huang, Y.-C. Su, and C.-Y. Chai, “Overexpression of annexin 1 in the development and differentiation of urothelial carcinoma,” Kaohsiung Journal of Medical Sciences, vol. 28, no. 3, pp. 145–150, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. F.-T. Liu and G. A. Rabinovich, “Galectins: regulators of acute and chronic inflammation,” Annals of the New York Academy of Sciences, vol. 1183, pp. 158–182, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Brandt, E. F. Abou-Eladab, M. Tiedge, and H. Walzel, “Role of the JNK/c-Jun/AP-1 signaling pathway in galectin-1-induced T-cell death,” Cell Death & Disease, vol. 1, article e23, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. R. C. Hughes, “Galectins as modulators of cell adhesion,” Biochimie, vol. 83, no. 7, pp. 667–676, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Scott and C. Weinberg, “Galectin-1: a bifunctional regulator of cellular proliferation,” Glycoconjugate Journal, vol. 19, no. 7–9, pp. 467–477, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Matarrese, A. Tinari, E. Mormone et al., “Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission,” The Journal of Biological Chemistry, vol. 280, no. 8, pp. 6969–6985, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. G. A. Rabinovich, G. Daly, H. Dreja et al., “Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis,” The Journal of Experimental Medicine, vol. 190, no. 3, pp. 385–398, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Santucci, S. Fiorucci, N. Rubinstein et al., “Galectin-1 suppresses experimental colitis in mice,” Gastroenterology, vol. 124, no. 5, pp. 1381–1394, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Ito, K. Stannard, E. Gabutero et al., “Galectin-1 as a potent target for cancer therapy: role in the tumor microenvironment,” Cancer and Metastasis Reviews, vol. 31, no. 3-4, pp. 763–778, 2012. View at Publisher · View at Google Scholar
  31. T. Dalotto-Moreno, D. O. Croci, J. P. Cerliani et al., “Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease,” Cancer Research, vol. 73, no. 3, pp. 1107–1117, 2013. View at Publisher · View at Google Scholar
  32. R. Soldati, E. Berger, A. C. Zenclussen et al., “Neuroblastoma triggers an immunoevasive program involving galectin-1-dependent modulation of T cell and dendritic cell compartments,” International Journal of Cancer, vol. 131, no. 5, pp. 1131–1141, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. D. O. Croci, M. Salatino, N. Rubinstein et al., “Disrupting galectin-1 interactions with N-glycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi’s sarcoma,” The Journal of Experimental Medicine, vol. 209, no. 11, pp. 1985–2000, 2012. View at Publisher · View at Google Scholar
  34. Y. L. Hsu, C. Y. Wu, J. Y. Hung, Y. S. Lin, M. S. Huang, and P. L. Kuo, “Galectin-1 promotes lung cancer tumor metastasis by potentiating integrin α6β4 and Notch1/Jagged2 signaling pathway,” Carcinogenesis, vol. 34, no. 6, pp. 1370–1381, 2013. View at Publisher · View at Google Scholar
  35. A. Paz, R. Haklai, G. Elad-Sfadia, E. Ballan, and Y. Kloog, “Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation,” Oncogene, vol. 20, no. 51, pp. 7486–7493, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. H.-J. Kim, H.-K. Jeon, Y. J. Cho et al., “High galectin-1 expression correlates with poor prognosis and is involved in epithelial ovarian cancer proliferation and invasion,” European Journal of Cancer, vol. 48, no. 12, pp. 1914–1921, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Wu, P. Chen, R. Liao et al., “Overexpression of galectin-1 is associated with poor prognosis in human hepatocellular carcinoma following resection,” Journal of Gastroenterology and Hepatology, vol. 27, no. 8, pp. 1312–1319, 2012. View at Publisher · View at Google Scholar
  38. H. Barrow, J. M. Rhodes, and L.-G. Yu, “The role of galectins in colorectal cancer progression,” International Journal of Cancer, vol. 129, no. 1, pp. 1–8, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Yu, J. Wang, Y. Chen et al., “Tissue microarray analysis reveals strong clinical evidence for a close association between loss of annexin A1 expression and nodal metastasis in gastric cancer,” Clinical & Experimental Metastasis, vol. 25, no. 7, pp. 695–702, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Bektas, B. Bahadir, B. H. Ucan, and S. O. Ozdamar, “CD24 and galectin-1 expressions in gastric adenocarcinoma and clinicopathologic significance,” Pathology & Oncology Research, vol. 16, no. 4, pp. 569–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Zhu, C. Xu, Z. Jiang et al., “Nuclear localization of annexin A1 correlates with advanced disease and peritoneal dissemination in patients with gastric carcinoma,” Anatomical Record, vol. 293, no. 8, pp. 1310–1314, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. W. Lim, H. Kim, and K. H. Kim, “Cell adhesion-related gene expression by Helicobacter pylori in gastric epithelial AGS cells,” International Journal of Biochemistry & Cell Biology, vol. 35, no. 8, pp. 1284–1296, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. Y.-R. Chen, H.-F. Juan, H.-C. Huang et al., “Quantitative proteomic and genomic profiling reveals metastasis-related protein expression patterns in gastric cancer cells,” Journal of Proteome Research, vol. 5, no. 10, pp. 2727–2742, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. C.-M. Wu, Y.-S. Lee, T.-H. Wang et al., “Identification of differential gene expression between intestinal and diffuse gastric cancer using cDNA microarray,” Oncology Reports, vol. 15, no. 1, pp. 57–64, 2006. View at Google Scholar · View at Scopus
  45. G. R. Martin, M. Perretti, R. J. Flower, and J. L. Wallace, “Annexin-1 modulates repair of gastric mucosal injury,” American Journal of Physiology, vol. 294, no. 3, pp. G764–G769, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. C. Jorge, M. M. Mataruco, L. P. Araújo et al., “Expression of annexin-A1 and galectin-1 anti-inflammatory proteins and mRNA in chronic gastritis and gastric cancer,” Mediators of Inflammation, vol. 2013, Article ID 152860, 11 pages, 2013. View at Publisher · View at Google Scholar
  47. B.-G. Jang and W. H. Kim, “Molecular pathology of gastric carcinoma,” Pathobiology, vol. 78, no. 6, pp. 302–310, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. M. C. Duarte, E. Babeto, K. R. M. Leite et al., “Expression of TERT in precancerous gastric lesions compared to gastric cancer,” Brazilian Journal of Medical and Biological Research, vol. 44, no. 2, pp. 100–104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Chen, T. G. Gharib, C.-C. Huang et al., “Discordant protein and mRNA expression in lung adenocarcinomas,” Molecular & Cellular Proteomics, vol. 1, no. 4, pp. 304–313, 2002. View at Google Scholar · View at Scopus
  51. D. Greenbaum, C. Colangelo, K. Williams, and M. Gerstein, “Comparing protein abundance and mRNA expression levels on a genomic scale,” Genome Biology, vol. 4, no. 9, article 117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Guo, P. Xiao, S. Lei et al., “How is mRNA expression predictive for protein expression? A correlation study on human circulating monocytes,” Acta Biochimica et Biophysica Sinica, vol. 40, no. 5, pp. 426–436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Y. Cheng, M. S. Wu, J. T. Lin et al., “Annexin A1 is associated with gastric cancer survival and promotes gastric cancer cell invasiveness through the formyl peptide receptor/extracellular signal-regulated kinase/integrin beta-1-binding protein 1 pathway,” Cancer, vol. 118, no. 23, pp. 5757–5767, 2012. View at Publisher · View at Google Scholar
  54. L. C. Alldridge, H. J. Harris, R. Plevin, R. Hannon, and C. E. Bryant, “The annexin protein lipocortin 1 regulates the MAPK/ERK pathway,” The Journal of Biological Chemistry, vol. 274, no. 53, pp. 37620–37628, 1999. View at Publisher · View at Google Scholar · View at Scopus
  55. V. Gerke and S. E. Moss, “Annexins: from structure to function,” Physiological Reviews, vol. 82, no. 2, pp. 331–371, 2002. View at Google Scholar · View at Scopus
  56. C.-H. Hsiang, T. Tunoda, Y. E. Whang, D. R. Tyson, and D. K. Ornstein, “The impact of altered annexin I protein levels on apoptosis and signal transduction pathways in prostate cancer cells,” Prostate, vol. 66, no. 13, pp. 1413–1424, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. L. C. Alldridge and C. E. Bryant, “Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK1/2 MAPK signal,” Experimental Cell Research, vol. 290, no. 1, pp. 93–107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. J. D. Croxtall and R. J. Flower, “Lipocortin 1 mediates dexamethasone-induced growth arrest of the A549 lung adenocarcinoma cell line,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 8, pp. 3571–3575, 1992. View at Publisher · View at Google Scholar · View at Scopus
  59. C. de Coupade, R. Gillet, M. Bennoun, P. Briand, F. Russo-Marie, and E. Solito, “Annexin 1 expression and phosphorylation are upregulated during liver regeneration and transformation in antithrombin III SV40 T large antigen transgenic mice,” Hepatology, vol. 31, no. 2, pp. 371–380, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Khau, S. Y. Langenbach, M. Schuliga et al., “Annexin-1 signals mitogen-stimulated breast tumor cell proliferation by activation of the formyl peptide receptors (FPRs) 1 and 2,” The FASEB Journal, vol. 25, no. 2, pp. 483–496, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. G. A. Rabinovich, “Galectin-1 as a potential cancer target,” British Journal of Cancer, vol. 92, no. 7, pp. 1188–1192, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. S. J. Rodig, J. Ouyang, P. Juszczynski et al., “AP1-dependent galectin-1 expression delineates classical hodgkin and anaplastic large cell lymphomas from other lymphoid malignancies with shared molecular features,” Clinical Cancer Research, vol. 14, no. 11, pp. 3338–3344, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. Y.-M. Ding, J.-H. Dong, L.-L. Chen, and H.-D. Zhang, “Increased expression of galectin-1 is associated with human oral squamous cell carcinoma development,” Oncology Reports, vol. 21, no. 4, pp. 983–987, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Zheng-Hao, W. Ji-Fang, X. de-Sheng, and Z. Jian-Hua, “Galectin-1 is up-regulated by RASSF1A gene in human gastric carcinoma cell line SGC7901,” Acta Pathologica, Microbiologica, et Immunologica Scandinavica, vol. 120, no. 7, pp. 582–590, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. F. F. Lam, L. Jankova, O. F. Dent et al., “Identification of distinctive protein expression patterns in colorectal adenoma,” Proteomics, vol. 4, no. 1, pp. 60–70, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. N. L. Perillo, K. E. Pace, J. J. Seilhamer, and L. G. Baum, “Apoptosis of T cells mediated by galectin-1,” Nature, vol. 378, no. 6558, pp. 736–739, 1995. View at Publisher · View at Google Scholar · View at Scopus
  67. V. L. Thijssen, B. Barkan, H. Shoji et al., “Tumor cells secrete galectin-1 to enhance endothelial cell activity,” Cancer Research, vol. 70, no. 15, pp. 6216–6224, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. H. J. Rhee, G.-Y. Kim, J. W. Huh, S.-W. Kim, and D. S. Na, “Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent,” European Journal of Biochemistry, vol. 267, no. 11, pp. 3220–3225, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Hittelet, H. Legendre, N. Nagy et al., “Upregulation of galectins-1 and -3 in human colon cancer and their role in regulating cell migration,” International Journal of Cancer, vol. 103, no. 3, pp. 370–379, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. M. von Wolff, X. Wang, H.-J. Gabius, and T. Strowitzki, “Galectin fingerprinting in human endometrium and decidua during the menstrual cycle and in early gestation,” Molecular Human Reproduction, vol. 11, no. 3, pp. 189–194, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. S. Choe, C. Shim, D. Choi, C. S. Lee, K. K. Lee, and K. Kim, “Expression of galectin-1 mRNA in the mouse uterus in under the control of ovarian steroids during blastocyst implantation,” Molecular Reproduction and Development, vol. 48, no. 2, pp. 261–266, 1997. View at Google Scholar
  72. N. G. Than, R. Romero, O. Erez et al., “Emergence of hormonal and redox regulation of galectin-1 in placental mammals: implication in maternal-fetal immune tolerance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 41, pp. 15819–15824, 2008. View at Publisher · View at Google Scholar · View at Scopus