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BioMed Research International
Volume 2015, Article ID 161508, 8 pages
http://dx.doi.org/10.1155/2015/161508
Research Article

Morphine Promotes Tumor Angiogenesis and Increases Breast Cancer Progression

Istituto Nazionale per lo Studio e la Cura dei Tumori “Fondazione G. Pascale”, IRCCS, Via Mariano Semmola, 80131 Naples, Italy

Received 31 July 2014; Accepted 14 October 2014

Academic Editor: Andrea Vecchione

Copyright © 2015 Sabrina Bimonte 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. J. N. Lickiss, “Approaching cancer pain relief,” European Journal of Pain, vol. 5, pp. 5–14, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Schmitz, “Friedrich Wilhelm Sertürner and the discovery of morphine,” Pharmacy in History, vol. 27, no. 2, pp. 61–74, 1985. View at Google Scholar · View at Scopus
  3. G. W. Pasternak, “Pharmacological mechanisms of opioid analgesics,” Clinical Neuropharmacology, vol. 16, no. 1, pp. 1–18, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. B. L. Kieffer and C. Gavériaux-Ruff, “Exploring the opioid system by gene knockout,” Progress in Neurobiology, vol. 66, no. 5, pp. 285–306, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. P. W. Mantyh, “Cancer pain and its impact on diagnosis, survival and quality of life,” Nature Reviews Neuroscience, vol. 7, no. 10, pp. 797–809, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Sueoka, E. Sueoka, S. Okabe, and H. Fujiki, “Anti-cancer effects of morphine through inhibition of tumour necrosis factor-α release and mRNA expression,” Carcinogenesis, vol. 17, no. 11, pp. 2337–2341, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Maneckjee and J. D. Minna, “Opioids induce while nicotine suppresses apoptosis in human lung cancer cells,” Cell Growth and Differentiation, vol. 5, no. 10, pp. 1033–1040, 1994. View at Google Scholar · View at Scopus
  8. A. Pasi, B. Qu, R. Steiner, H.-J. Senn, W. Bar, and F. S. Messiha, “Angiogenesis: modulation with opioids,” General Pharmacology, vol. 22, no. 6, pp. 1077–1079, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Hatzoglou, E. Bakogeorgou, E. Papakonstanti, C. Stournaras, D. S. Emmanouel, and E. Castanas, “Identification and characterization of opioid and somatostatin binding sites in the opossum kidney (OK) cell line and their effect on growth,” Journal of Cellular Biochemistry, vol. 63, no. 4, pp. 410–421, 1996. View at Google Scholar
  10. A. Hatzoglou, L. Ouafik, E. Bakogeorgou, K. Thermos, and E. Castanas, “Morphine cross-reacts with somatostatin receptor SSTR2 in the T47D human breast cancer cell line and decreases cell growth,” Cancer Research, vol. 55, no. 23, pp. 5632–5636, 1995. View at Google Scholar · View at Scopus
  11. R. Maneckjee, R. Biswas, and B. K. Vonderhaar, “Binding of opioids to human MCF-7 breast cancer cells and their effects on growth,” Cancer Research, vol. 50, no. 8, pp. 2234–2238, 1990. View at Google Scholar · View at Scopus
  12. M. Kampa, E. Bakogeorgou, A. Hatzoglou, A. Damianaki, P.-M. Martin, and E. Castanas, “Opioid alkaloids and casomorphin peptides decrease the proliferation of prostatic cancer cell lines (LNCaP, PC3 and DU145) through a partial interaction with opioid receptors,” European Journal of Pharmacology, vol. 335, no. 2-3, pp. 255–265, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Tegeder, S. Grösch, A. Schmidtko et al., “G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cells: involvement of p53 phosphorylation,” Cancer Research, vol. 63, no. 8, pp. 1846–1852, 2003. View at Google Scholar · View at Scopus
  14. M. P. Yeager and T. A. Colacchio, “Effect of morphine on growth of metastatic colon cancer in vivo,” Archives of Surgery, vol. 126, no. 4, pp. 454–456, 1991. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Sasamura, S. Nakamura, Y. Iida et al., “Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain produced by orthotopic tumor inoculation,” European Journal of Pharmacology, vol. 441, no. 3, pp. 185–191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Harimaya, K. Koizumi, T. Andoh, H. Nojima, Y. Kuraishi, and I. Saiki, “Potential ability of morphine to inhibit the adhesion, invasion and metastasis of metastatic colon 26-L5 carcinoma cells,” Cancer Letters, vol. 187, no. 1-2, pp. 121–127, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. R. H. Simon and T. E. Arbo, “Morphine increases metastatic tumor growth,” Brain Research Bulletin, vol. 16, no. 3, pp. 363–367, 1986. View at Publisher · View at Google Scholar · View at Scopus
  18. J. W. Lewis, Y. Shavit, G. W. Terman, L. R. Nelson, R. P. Gale, and J. C. Liebeskind, “Apparent involvement of opioid peptides in stress-induced enhancement of tumor growth,” Peptides, vol. 4, no. 5, pp. 635–638, 1983. View at Publisher · View at Google Scholar · View at Scopus
  19. M. G. Sergeeva, Z. V. Grishina, and S. D. Varfolomeyev, “Morphine effect on proliferation of normal and tumor cells of immune origin,” Immunology Letters, vol. 36, no. 2, pp. 215–218, 1993. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Gupta, S. Kshirsagar, L. Chang et al., “Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth,” Cancer Research, vol. 62, no. 15, pp. 4491–4498, 2002. View at Google Scholar · View at Scopus
  21. M. Farooqui, Y. Li, T. Rogers et al., “COX-2 inhibitor celecoxib prevents chronic morphine-induced promotion of angiogenesis, tumour growth, metastasis and mortality, without compromising analgesia,” British Journal of Cancer, vol. 97, no. 11, pp. 1523–1531, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Zong and G. M. Pollack, “Morphine antinociception is enhanced in mdr1a gene-deficient mice,” Pharmaceutical Research, vol. 17, no. 6, pp. 749–753, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Bimonte, A. Barbieri, G. Palma, and C. Arra, “The role of morphine in animal models of human cancer: does morphine promote or inhibit the tumor growth?” BioMed Research International, vol. 2013, Article ID 258141, 4 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Nguyen, “Morphine stimulates cancer progression and mast cell activation and impairs survival in transgenic mice with breast cancer,” British Journal of Anaesthesia, vol. 113, supplement 1, pp. i4–i13, 2014. View at Google Scholar
  25. M. Ishikawa, K. Tanno, A. Kamo, Y. Takayanagi, and K.-I. Sasaki, “Enhancement of tumor growth by morphine and its possible mechanism in mice,” Biological and Pharmaceutical Bulletin, vol. 16, no. 8, pp. 762–766, 1993. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Iglesias, M. F. Segura, J. X. Comella, and G. Olmos, “μ-opioid receptor activation prevents apoptosis following serum withdrawal in differentiated SH-SY5Y cells and cortical neurons via phosphatidylinositol 3-kinase,” Neuropharmacology, vol. 44, no. 4, pp. 482–492, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Gach, J. Szemraj, J. Fichna, M. Piestrzeniewicz, D. S. Delbro, and A. Janecka, “The influence of opioids on urokinase plasminogen activator on protein and mRNA level in MCF-7 breast cancer cell line,” Chemical Biology and Drug Design, vol. 74, no. 4, pp. 390–396, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. P. A. Singleton and J. Moss, “Effect of perioperative opioids on cancer recurrence: a hypothesis,” Future Oncology, vol. 6, no. 8, pp. 1237–1242, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Chen, M. Farooqui, and K. Gupta, “Morphine stimulates vascular endothelial growth factor-like signaling in mouse retinal endothelial cells,” Current Neurovascular Research, vol. 3, no. 3, pp. 171–180, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. D. R. Green and J. C. Reed, “Mitochondria and apoptosis,” Science, vol. 281, no. 5381, pp. 1309–1312, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Ashkenazi and V. M. Dixit, “Apoptosis control by death and decoy receptors,” Current Opinion in Cell Biology, vol. 11, no. 2, pp. 255–260, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. M. O. Hengartner, “The biochemistry of apoptosis,” Nature, vol. 407, no. 6805, pp. 770–776, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. P.-N. Hsiao, M.-C. Chang, W.-F. Cheng et al., “Morphine induces apoptosis of human endothelial cells through nitric oxide and reactive oxygen species pathways,” Toxicology, vol. 256, no. 1-2, pp. 83–91, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. A. A. Kapasi, S. A. Coscia, M. P. Pandya, and P. C. Singhal, “Morphine modulates HIV-1 gp160-induced murine macrophage and human monocyte apoptosis by disparate ways,” Journal of Neuroimmunology, vol. 148, no. 1-2, pp. 86–96, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. X. Lin, Q. Li, Y.-J. Wang et al., “Morphine inhibits doxorubicin-induced reactive oxygen species generation and nuclear factor κB transcriptional activation in neuroblastoma SH-SY5Y cells,” Biochemical Journal, vol. 406, no. 2, pp. 215–221, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Arerangaiah, N. Chalasani, A. M. Udager et al., “Opioids induce renal abnormalities in tumor-bearing mice,” Nephron—Experimental Nephrology, vol. 105, no. 3, pp. e80–e89, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Salvemini, T. P. Misko, J. L. Masferrer, K. Seibert, M. G. Currie, and P. Needleman, “Nitric oxide activates cyclooxygenase enzymes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 15, pp. 7240–7244, 1993. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Nédélec, A. Abid, C. Cipolletta et al., “Stimulation of cyclooxygenase-2-activity by nitric oxide-derived species in rat chondrocyte: lack of contribution to loss of cartilage anabolism,” Biochemical Pharmacology, vol. 61, no. 8, pp. 965–978, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Farooqui, Z. H. Geng, E. J. Stephenson, N. Zaveri, D. Yee, and K. Gupta, “Naloxone acts as an antagonist of estrogen receptor activity in MCF-7 cells,” Molecular Cancer Therapeutics, vol. 5, no. 3, pp. 611–620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Salvemini, K. Seibert, J. L. Masferrer, T. P. Misko, M. G. Currie, and P. Needleman, “Endogenous nitric oxide enhances prostaglandin production in a model of renal inflammation,” Journal of Clinical Investigation, vol. 93, no. 5, pp. 1940–1947, 1994. View at Publisher · View at Google Scholar · View at Scopus
  42. R. J. Griffin, B. W. Williams, R. Wild, J. M. Cherrington, H. Park, and C. W. Song, “Simultaneous inhibition of the receptor kinase activity of vascular endothelial, fibroblast, and platelet-derived growth factors suppresses tumor growth and enhances tumor radiation response,” Cancer Research, vol. 62, no. 6, pp. 1702–1706, 2002. View at Google Scholar · View at Scopus
  43. K. M. Leahy, R. L. Ornberg, Y. Wang, B. S. Zweifel, A. T. Koki, and J. L. Masferrer, “Cyclooxygenase-2 inhibition by celecoxib reduces proliferation and induces apoptosis in angiogenic endothelial cells in vivo,” Cancer Research, vol. 62, no. 3, pp. 625–631, 2002. View at Google Scholar · View at Scopus
  44. S. H. Chang, C. H. Liu, and R. Conway, “Role of prostaglandin E2-dependent angiogenic switch in cyclooxygenase 2-induced breast cancer progression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 2, pp. 591–596, 2004. View at Google Scholar
  45. C.-F. Lam, Y.-C. Liu, F.-L. Tseng et al., “High-dose morphine impairs vascular endothelial function by increased production of superoxide anions,” Anesthesiology, vol. 106, no. 3, pp. 532–537, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Blebea, J. E. Mazo, T. K. Kihara et al., “Opioid growth factor modulates angiogenesis,” Journal of Vascular Surgery, vol. 32, no. 2, pp. 364–373, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. C.-F. Lam, P.-J. Chang, Y.-S. Huang et al., “Prolonged use of high-dose morphine impairs angiogenesis and mobilization of endothelial progenitor cells in mice,” Anesthesia and Analgesia, vol. 107, no. 2, pp. 686–692, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. J. L. Martin, R. Charboneau, R. A. Barke, and S. Roy, “Chronic morphine treatment inhibits LPS-induced angiogenesis: implications in wound healing,” Cellular Immunology, vol. 265, no. 2, pp. 139–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Roy, S. Balasubramanian, J. Wang, Y. Chandrashekhar, R. Charboneau, and R. Barke, “Morphine inhibits VEGF expression in myocardial ischemia,” Surgery, vol. 134, no. 2, pp. 336–344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Koodie, S. Ramakrishnan, and S. Roy, “Morphine suppresses tumor angiogenesis through a HIF-1α/p38MAPK pathway,” The American Journal of Pathology, vol. 177, no. 2, pp. 984–997, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Faramarzi, A. Abbasi, S. M. Tavangar, M. Mazouchi, and A. R. Dehpour, “Opioid receptor antagonist promotes angiogenesis in bile duct ligated rats,” Journal of Gastroenterology and Hepatology, vol. 24, no. 7, pp. 1226–1229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. R. L. Shapiro, J. G. Duquette, D. F. Roses et al., “Induction of primary cutaneous melanocytic neoplasms in urokinase-type plasminogen activator (uPA)-deficient and wild-type mice: cellular blue nevi invade but do not progress to malignant melanoma in uPA-deficient animals,” Cancer Research, vol. 56, no. 15, pp. 3597–3604, 1996. View at Google Scholar · View at Scopus
  53. J. A. Engbring and H. K. Kleinman, “The basement membrane matrix in malignancy,” Journal of Pathology, vol. 200, no. 4, pp. 465–470, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. M. S. Widel, “Mechanisms of metastasis and molecular markers of malignant tumor progression. I. Colorectal cancer,” Postępy Higieny i Medycyny Doświadczalnej, vol. 60, pp. 453–470, 2006. View at Google Scholar