MiR-92a inhibits peritoneal dissemination of ovarian cancer cells by inhibiting integrin α5 expression

American Journal of Pathology

Volumn 182, Issue 5, 2013, Pages 1876-1889

  Ohyagi Hara, Chifumi ^a   Sawada, Kenjiro ^a   Kamiura, Shoji ^b   Tomita, Yasuhiko ^b   Isobe, Aki ^a   Hashimoto, Kae ^a   Kinose, Yasuto ^a   Mabuchi, Seiji ^a   Hisamatsu, Takeshi ^a   Takahashi, Toshifumi ^c   Kumasawa, Keiichi ^a   Nagata, Shigenori ^b   Morishige, Ken Ichirou ^d   Lengyel, Ernst ^e   Kurachi, Hirohisa ^c   Kimura, Tadashi ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

^c YAMAGATA UNIVERSITY   (Japan)

^d GIFU UNIVERSITY   (Japan)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5 INTEGRIN; MICRORNA; MICRORNA 92A; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ALGORITHM; ARTICLE; CANCER STAGING; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; OVARY CANCER; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; XENOGRAFT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BASE SEQUENCE; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHA5; MICE; MICE, NUDE; MICRORNAS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM STAGING; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; PROGNOSIS; PROTEIN BINDING; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 84876565511     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.01.039     Document Type: Article

References (52)

1. S.A. Cannistra Cancer of the ovary N Engl J Med 351 2004 2519 2529
2. A. Jemal, R. Siegel, J. Xu, and E. Ward Cancer statistics, 2010 CA Cancer J Clin 60 2010 277 300
3. K.K. Shih, and D.S. Chi Maximal cytoreductive effort in epithelial ovarian cancer surgery J Gynecol Oncol 21 2010 75 80
4. R.C. Bast, B. Hennessy, and G.B. Mills The biology of ovarian cancer: new opportunities for translation Nat Rev Cancer 9 2009 415 428
5. E. Lengyel Ovarian cancer development and metastasis Am J Pathol 177 2010 1053 1064
6. N. Auersperg, A.S. Wong, K.C. Choi, S.K. Kang, and P.C. Leung Ovarian surface epithelium: biology, endocrinology, and pathology Endocr Rev 22 2001 255 288
7. N. Ahmed, E.W. Thompson, and M.A. Quinn Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm J Cell Physiol 213 2007 581 588
8. R.J. Kurman, and I.M. Shih The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory Am J Surg Pathol 34 2010 433 443
9. R.J. Kurman, and I.M. Shih Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer: shifting the paradigm Hum Pathol 42 2011 918 931
10. D.W. Kindelberger, Y. Lee, A. Miron, M.S. Hirsch, C. Feltmate, F. Medeiros, M.J. Callahan, E.O. Garner, R.W. Gordon, C. Birch, R.S. Berkowitz, M.G. Muto, and C.P. Crum Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship Am J Surg Pathol 31 2007 161 169
11. K. Sawada, C. Ohyagi-Hara, T. Kimura, and K. Morishige Integrin inhibitors as a therapeutic agent for ovarian cancer J Oncol 2012 2012 915140
12. H.A. Kenny, S. Dogan, M. Zillhardt, A. K Mitra, S.D. Yamada, T. Krausz, and E. Lengyel Organotypic models of metastasis: a three-dimensional culture mimicking the human peritoneum and omentum for the study of the early steps of ovarian cancer metastasis Cancer Treat Res 149 2009 335 351
13. R.C. Casey, K.M. Burleson, K.M. Skubitz, S.E. Pambuccian, T.R. Oegema, L.E. Ruff, and A.P. Skubitz Beta 1-integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids Am J Pathol 159 2001 2071 2080
14. T. Strobel, and S.A. Cannistra Beta1-integrins partly mediate binding of ovarian cancer cells to peritoneal mesothelium in vitro Gynecol Oncol 73 1999 362 367
15. K. Sawada, A.K. Mitra, A.R. Radjabi, V. Bhaskar, E.O. Kistner, M. Tretiakova, S. Jagadeeswaran, A. Montag, A. Becker, H.A. Kenny, M.E. Peter, V. Ramakrishnan, S.D. Yamada, and E. Lengyel Loss of E-cadherin promotes ovarian cancer metastasis via alpha 5-integrin, which is a therapeutic target Cancer Res 68 2008 2329 2339
16. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
17. H. Wang, J. Wu, X. Meng, X. Ying, Y. Zuo, R. Liu, Z. Pan, T. Kang, and W. Huang MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1 Carcinogenesis 32 2011 1033 1042
18. S. Griffiths-Jones, R.J. Grocock, S. van Dongen, A. Bateman, and A.J. Enright miRBase: microRNA sequences, targets and gene nomenclature Nucleic Acids Res 34 2006 D140 D144
19. G.A. Calin, C. Sevignani, C.D. Dumitru, T. Hyslop, E. Noch, S. Yendamuri, M. Shimizu, S. Rattan, F. Bullrich, M. Negrini, and C.M. Croce Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers Proc Natl Acad Sci U S A 101 2004 2999 3004
20. T. Shatseva, D.Y. Lee, Z. Deng, and B.B. Yang MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2 J Cell Sci 124 2011 2826 2836
21. W.C. Cho Exploiting the therapeutic potential of microRNAs in human cancer Expert Opin Ther Targets 16 2012 345 350
22. S. Shell, S.M. Park, A.R. Radjabi, R. Schickel, E.O. Kistner, D.A. Jewell, C. Feig, E. Lengyel, and M.E. Peter Let-7 expression defines two differentiation stages of cancer Proc Natl Acad Sci U S A 104 2007 11400 11405
23. A. Bonauer, G. Carmona, M. Iwasaki, M. Mione, M. Koyanagi, A. Fischer, J. Burchfield, H. Fox, C. Doebele, K. Ohtani, E. Chavakis, M. Potente, M. Tjwa, C. Urbich, A.M. Zeiher, and S. Dimmeler MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice Science 324 2009 1710 1713
24. M. Maragkakis, P. Alexiou, G.L. Papadopoulos, M. Reczko, T. Dalamagas, G. Giannopoulos, G. Goumas, E. Koukis, K. Kourtis, V.A. Simossis, P. Sethupathy, T. Vergoulis, N. Koziris, T. Sellis, P. Tsanakas, and A.G. Hatzigeorgiou Accurate microRNA target prediction correlates with protein repression levels BMC Bioinformatics 10 2009 295
25. M. Maragkakis, M. Reczko, V.A. Simossis, P. Alexiou, G.L. Papadopoulos, T. Dalamagas, G. Giannopoulos, G. Goumas, E. Koukis, K. Kourtis, T. Vergoulis, N. Koziris, T. Sellis, P. Tsanakas, and A.G. Hatzigeorgiou DIANA-microT web server: elucidating microRNA functions through target prediction Nucleic Acids Res 37 2009 W273 W276
26. B.P. Lewis, C.B. Burge, and D.P. Bartel Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 120 2005 15 20
27. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res 19 2009 92 105
28. A. Grimson, K.K. Farh, W.K. Johnston, P. Garrett-Engele, L.P. Lim, and D.P. Bartel MicroRNA targeting specificity in mammals: determinants beyond seed pairing Mol Cell 27 2007 91 105
29. D.M. Garcia, D. Baek, C. Shin, G.W. Bell, A. Grimson, and D.P. Bartel Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs Nat Struct Mol Biol 18 2011 1139 1146
30. H. Liu, P. D'Andrade, S. Fulmer-Smentek, P. Lorenzi, K.W. Kohn, J.N. Weinstein, Y. Pommier, and W.C. Reinhold mRNA and microRNA expression profiles of the NCI-60 integrated with drug activities Mol Cancer Ther 9 2010 1080 1091
31. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
32. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
33. F.G. Giancotti, and E. Ruoslahti Integrin signaling Science 285 1999 1028 1032
34. E.A. Clark, and J.S. Brugge Integrins and signal transduction pathways: the road taken Science 268 1995 233 239
35. J.J. Rossi New hope for a microRNA therapy for liver cancer Cell 137 2009 990 992
36. G.A. Calin, and C.M. Croce MicroRNA-cancer connection: the beginning of a new tale Cancer Res 66 2006 7390 7394
37. K. Behbakht, T.C. Randall, I. Benjamin, M.A. Morgan, S. King, and S.C. Rubin Clinical characteristics of clear cell carcinoma of the ovary Gynecol Oncol 70 1998 255 258
38. K.M. Bell-McGuinn, C.M. Matthews, S.N. Ho, M. Barve, L. Gilbert, R.T. Penson, E. Lengyel, R. Palaparthy, K. Gilder, A. Vassos, W. McAuliffe, S. Weymer, J. Barton, and R.J. Schilder A phase II, single-arm study of the anti-α5β1 integrin antibody volociximab as monotherapy in patients with platinum-resistant advanced epithelial ovarian or primary peritoneal cancer Gynecol Oncol 121 2011 273 279
39. M.E. Cianfrocca, K.A. Kimmel, J. Gallo, T. Cardoso, M.M. Brown, G. Hudes, N. Lewis, L. Weiner, G.N. Lam, S.C. Brown, D.E. Shaw, A.P. Mazar, and R.B. Cohen Phase 1 trial of the antiangiogenic peptide ATN-161 (Ac-PHSCN-NH(2)), a beta integrin antagonist, in patients with solid tumours Br J Cancer 94 2006 1621 1626
40. L. He, J.M. Thomson, M.T. Hemann, E. Hernando-Monge, D. Mu, S. Goodson, S. Powers, C. Cordon-Cardo, S.W. Lowe, G.J. Hannon, and S.M. Hammond A microRNA polycistron as a potential human oncogene Nature 435 2005 828 833
41. A. Ventura, A.G. Young, M.M. Winslow, L. Lintault, A. Meissner, S.J. Erkeland, J. Newman, R.T. Bronson, D. Crowley, J.R. Stone, R. Jaenisch, P.A. Sharp, and T. Jacks Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters Cell 132 2008 875 886
42. A. Bonauer, and S. Dimmeler The microRNA-17-92 cluster: still a miRacle? Cell Cycle 8 2009 3866 3873
43. A. Ota, H. Tagawa, S. Karnan, S. Tsuzuki, A. Karpas, S. Kira, Y. Yoshida, and M. Seto Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma Cancer Res 64 2004 3087 3095
44. B. Diosdado, M.A. van de Wiel, J.S. Terhaar Sive Droste, S. Mongera, C. Postma, W.J. Meijerink, B. Carvalho, and G.A. Meijer MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression Br J Cancer 101 2009 707 714
45. E. Connolly, M. Melegari, P. Landgraf, T. Tchaikovskaya, B.C. Tennant, B.L. Slagle, L.E. Rogler, M. Zavolan, T. Tuschl, and C.E. Rogler Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype Am J Pathol 173 2008 856 864
46. Z.L. Chen, X.H. Zhao, J.W. Wang, B.Z. Li, Z. Wang, J. Sun, F.W. Tan, D.P. Ding, X.H. Xu, F. Zhou, X.G. Tan, J. Hang, S.S. Shi, X.L. Feng, and J. He microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin J Biol Chem 286 2011 10725 10734
47. L. Zhang, J. Huang, N. Yang, J. Greshock, M.S. Megraw, A. Giannakakis, S. Liang, T.L. Naylor, A. Barchetti, M.R. Ward, G. Yao, A. Medina, A. O'brien-Jenkins, D. Katsaros, A. Hatzigeorgiou, P.A. Gimotty, B.L. Weber, and G. Coukos microRNAs exhibit high frequency genomic alterations in human cancer Proc Natl Acad Sci U S A 103 2006 9136 9141
48. S. Nilsson, C. Möller, K. Jirström, A. Lee, S. Busch, R. Lamb, and G. Landberg Downregulation of miR-92a is associated with aggressive breast cancer features and increased tumour macrophage infiltration PLoS One 7 2012 e36051
49. M.V. Iorio, R. Visone, G. Di Leva, V. Donati, F. Petrocca, P. Casalini, C. Taccioli, S. Volinia, C.G. Liu, H. Alder, G.A. Calin, S. Ménard, and C.M. Croce MicroRNA signatures in human ovarian cancer Cancer Res 67 2007 8699 8707
50. M.V. Iorio, and C.M. Croce MicroRNAs in cancer: small molecules with a huge impact J Clin Oncol 27 2009 5848 5856
51. J.F. Wiggins, L. Ruffino, K. Kelnar, M. Omotola, L. Patrawala, D. Brown, and A.G. Bader Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34 Cancer Res 70 2010 5923 5930
52. R.E. Lanford, E.S. Hildebrandt-Eriksen, A. Petri, R. Persson, M. Lindow, M.E. Munk, S. Kauppinen, and H. Ørum Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection Science 327 2010 198 201