Minocycline inhibits malignant ascites of ovarian cancer through targeting multiple signaling pathways

Gynecologic Oncology

Volumn 129, Issue 1, 2013, Pages 113-119

  Pourgholami, Mohammad Hossein ^a   Ataie Kachoie, Parvin ^a   Badar, Samina ^a   Morris, David Lawson ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

IL 6; Malignant ascites; Minocycline; sIL 6R; VEGF

Indexed keywords

DRINKING WATER; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SIZE; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MALIGNANT ASCITES; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TREATMENT DURATION;

ANIMALS; ASCITES; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INTERLEUKIN-6; MICE; MINOCYCLINE; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, INTERLEUKIN-6; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84884213782     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2012.12.031     Document Type: Article

References (51)

1. A.A. Ayantunde, and S.L. Parsons Pattern and prognostic factors in patients with malignant ascites: a retrospective study Ann Oncol 18 2007 945 949
2. J.A. Nagy, K.T. Herzberg, J.M. Dvorak, and H.F. Dvorak Pathogenesis of malignant ascites formation: initiating events that lead to fluid accumulation Cancer Res 53 1993 2631 2643
3. M.V. Barbolina, M. Kim, Y. Liu, J. Shepard, A. Belmadani, and R.J. Miller Microenvironmental regulation of chemokine (C-X-C-motif) receptor 4 in ovarian carcinoma Mol Cancer Res 8 2010 653 664
4. C.W. Lo, M.W. Chen, M. Hsiao, S. Wang, C.A. Chen, and S.M. Hsiao IL-6 trans-signaling in formation and progression of malignant ascites in ovarian cancer Cancer Res 71 2011 424 434
5. L. Hu, N. Ferrara, and R.B. Jaffe Paracrine VEGF/VE-cadherin action on ovarian cancer permeability Exp Biol Med (Maywood) 231 2006 1646 1652
6. A. Maccio, and C. Madeddu Inflammation and ovarian cancer Cytokine 58 2012 133 147
7. M.B. Nilsson, R.R. Langley, and I.J. Fidler Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine Cancer Res 65 2005 10794 10800
8. R.L. Stone, A.M. Nick, I.A. McNeish, F. Balkwill, H.D. Han, and J. Bottsford-Miller Paraneoplastic thrombocytosis in ovarian cancer N Engl J Med 366 2012 610 618
9. Y. Guo, J. Nemeth, C. O'Brien, M. Susa, X. Liu, and Z. Zhang Effects of siltuximab on the IL-6-induced signaling pathway in ovarian cancer Clin Cancer Res 16 2010 5759 5769
10. J. Coward, H. Kulbe, P. Chakravarty, D. Leader, V. Vassileva, and D.A. Leinster Interleukin-6 as a therapeutic target in human ovarian cancer Clin Cancer Res 17 2011 6083 6096
11. S. Cohen, I. Bruchim, D. Graiver, Z. Evron, V. Oron-Karni, and M. Pasmanik-Chor Platinum-resistance in ovarian cancer cells is mediated by IL-6 secretion via the increased expression of its target cIAP-2 J Mol Med (Berl) 2012
12. J.K. Soczynska, R.B. Mansur, E. Brietzke, W. Swardfager, S.H. Kennedy, and H.O. Woldeyohannes Novel therapeutic targets in depression: minocycline as a candidate treatment Behav Brain Res 235 2012 302 317
13. J. Chu, and D. Pratico 5-Lipoxygenase as an endogenous modulator of amyloid beta formation in vivo Ann Neurol 69 2011 34 46
14. M. Nowak, A. Strzelczyk, P.S. Reif, K. Schorlemmer, S. Bauer, and B.A. Norwood Minocycline as potent anticonvulsant in a patient with astrocytoma and drug resistant epilepsy Seizure 21 2012 227 228
15. F. Zhao, Y. Hua, Y. He, R.F. Keep, and G. Xi Minocycline-induced attenuation of iron overload and brain injury after experimental intracerebral hemorrhage Stroke 42 2011 3587 3593
16. M.C. Zink, J. Uhrlaub, J. DeWitt, T. Voelker, B. Bullock, and J. Mankowski Neuroprotective and anti-human immunodeficiency virus activity of minocycline JAMA 293 2005 2003 2011
17. J.H. Campbell, T.H. Burdo, P. Autissier, J.P. Bombardier, S.V. Westmoreland, and C. Soulas Minocycline inhibition of monocyte activation correlates with neuronal protection in SIV neuroAIDS PLoS One 6 2011 e18688
18. D.P. Stirling, K.M. Koochesfahani, J.D. Steeves, and W. Tetzlaff Minocycline as a neuroprotective agent Neuroscientist 11 2005 308 322
19. F. Bahrami, D.L. Morris, and M.H. Pourgholami Tetracyclines: drugs with huge therapeutic potential Mini Rev Med Chem 12 2012 44 52
20. R. Nakashima, K. Sakurai, S. Yamasaki, K. Nishino, and A. Yamaguchi Structures of the multidrug exporter AcrB reveal a proximal multisite drug-binding pocket Nature 480 2011 565 569
21. C. van den Bogert, B.H. Dontje, and A.M. Kroon The antitumour effect of doxycycline on a T-cell leukaemia in the rat Leuk Res 9 1985 617 623
22. C. van den Bogert, B.H. Dontje, M. Holtrop, T.E. Melis, J.C. Romijn, and J.W. van Dongen Arrest of the proliferation of renal and prostate carcinomas of human origin by inhibition of mitochondrial protein synthesis Cancer Res 46 1986 3283 3289
23. M.G. Selzer, B. Zhu, N.L. Block, and B.L. Lokeshwar CMT-3, a chemically modified tetracycline, inhibits bony metastases and delays the development of paraplegia in a rat model of prostate cancer Ann N Y Acad Sci 878 1999 678 682
24. B.L. Lokeshwar, M.G. Selzer, B.Q. Zhu, N.L. Block, and L.M. Golub Inhibition of cell proliferation, invasion, tumor growth and metastasis by an oral non-antimicrobial tetracycline analog (COL-3) in a metastatic prostate cancer model Int J Cancer 98 2002 297 309
25. H. Macdonald, R.G. Kelly, E.S. Allen, J.F. Noble, and L.A. Kanegis Pharmacokinetic studies on minocycline in man Clin Pharmacol Ther 14 1973 852 861
26. M.H. Pourgholami, A.H. Mekkawy, S. Badar, and D.L. Morris Minocycline inhibits growth of epithelial ovarian cancer Gynecol Oncol 125 2012 433 440
27. M.H. Pourgholami, Z. Yan Cai, Y. Lu, L. Wang, and D.L. Morris Albendazole: a potent inhibitor of vascular endothelial growth factor and malignant ascites formation in OVCAR-3 tumor-bearing nude mice Clin Cancer Res 12 2006 1928 1935
28. M.H. Pourgholami, Z.Y. Cai, L. Wang, S. Badar, M. Links, and D.L. Morris Inhibition of cell proliferation, vascular endothelial growth factor and tumor growth by albendazole Cancer Invest 27 2009 171 177
29. S. Masoumi Moghaddam, A. Amini, D.L. Morris, and M.H. Pourgholami Significance of vascular endothelial growth factor in growth and peritoneal dissemination of ovarian cancer Cancer Metastasis Rev 31 2012 143 162
30. T. Kitamura, N. Asai, A. Enomoto, K. Maeda, T. Kato, and M. Ishida Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin Nat Cell Biol 10 2008 329 337
31. L. Pertovaara, A. Kaipainen, T. Mustonen, A. Orpana, N. Ferrara, and O. Saksela Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells J Biol Chem 269 1994 6271 6274
32. S. Liao, J. Liu, P. Lin, T. Shi, R.K. Jain, and L. Xu TGF-beta blockade controls ascites by preventing abnormalization of lymphatic vessels in orthotopic human ovarian carcinoma models Clin Cancer Res 17 2011 1415 1424
33. E. Dejana, F. Orsenigo, and M.G. Lampugnani The role of adherens junctions and VE-cadherin in the control of vascular permeability J Cell Sci 121 2008 2115 2122
34. N.R. Miselis, B.W. Lau, Z. Wu, and A.B. Kane Kinetics of host cell recruitment during dissemination of diffuse malignant peritoneal mesothelioma Cancer Microenviron 4 2010 39 50
35. E.M. Dijkgraaf, M.J. Welters, J.W. Nortier, S.H. van der Burg, and J.R. Kroep Interleukin-6/interleukin-6 receptor pathway as a new therapy target in epithelial ovarian cancer Curr Pharm Des 18 2012 3816 3827
36. M. Plante, S.C. Rubin, G.Y. Wong, M.G. Federici, C.L. Finstad, and G.A. Gastl Interleukin-6 level in serum and ascites as a prognostic factor in patients with epithelial ovarian cancer Cancer 73 1994 1882 1888
37. W.G. Roberts, and G.E. Palade Neovasculature induced by vascular endothelial growth factor is fenestrated Cancer Res 57 1997 765 772
38. N. Maruo, I. Morita, M. Shirao, and S. Murota IL-6 increases endothelial permeability in vitro Endocrinology 131 1992 710 714
39. M.H. Ali, S.A. Schlidt, N.S. Chandel, K.L. Hynes, P.T. Schumacker, and B.L. Gewertz Endothelial permeability and IL-6 production during hypoxia: role of ROS in signal transduction Am J Physiol 277 1999 L1057 L1065
40. T. Cohen, D. Nahari, L.W. Cerem, G. Neufeld, and B.Z. Levi Interleukin 6 induces the expression of vascular endothelial growth factor J Biol Chem 271 1996 736 741
41. H. Nakahara, and N. Nishimoto Anti-interleukin-6 receptor antibody therapy in rheumatic diseases Endocr Metab Immune Disord Drug Targets 6 2006 373 381
42. S. Loeffler, B. Fayard, J. Weis, and J. Weissenberger Interleukin-6 induces transcriptional activation of vascular endothelial growth factor (VEGF) in astrocytes in vivo and regulates VEGF promoter activity in glioblastoma cells via direct interaction between STAT3 and Sp1 Int J Cancer 115 2005 202 213
43. Z. Culig, H. Steiner, G. Bartsch, and A. Hobisch Interleukin-6 regulation of prostate cancer cell growth J Cell Biochem 95 2005 497 505
44. T. Hideshima, N. Nakamura, D. Chauhan, and K.C. Anderson Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma Oncogene 20 2001 5991 6000
45. G. Gliki, C. Wheeler-Jones, and I. Zachary Vascular endothelial growth factor induces protein kinase C (PKC)-dependent Akt/PKB activation and phosphatidylinositol 3′-kinase-mediates PKC delta phosphorylation: role of PKC in angiogenesis Cell Biol Int 26 2002 751 759
46. M. Kato, S. Putta, M. Wang, H. Yuan, L. Lanting, and I. Nair TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN Nat Cell Biol 11 2009 881 889
47. O. Eickelberg, A. Pansky, R. Mussmann, M. Bihl, M. Tamm, and P. Hildebrand Transforming growth factor-beta1 induces interleukin-6 expression via activating protein-1 consisting of JunD homodimers in primary human lung fibroblasts J Biol Chem 274 1999 12933 12938
48. C.N. Nagineni, W. Samuel, S. Nagineni, K. Pardhasaradhi, B. Wiggert, and B. Detrick Transforming growth factor-beta induces expression of vascular endothelial growth factor in human retinal pigment epithelial cells: involvement of mitogen-activated protein kinases J Cell Physiol 197 2003 453 462
49. J.A. Nagy, A.M. Dvorak, and H.F. Dvorak VEGF-A and the induction of pathological angiogenesis Annu Rev Pathol 2 2007 251 275
50. A. Le Guelte, J. Dwyer, and J. Gavard Jumping the barrier: VE-cadherin, VEGF and other angiogenic modifiers in cancer Biol Cell 103 2011 593 605
51. J. Gavard, and J.S. Gutkind VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin Nat Cell Biol 8 2006 1223 1234