miR-200c is aberrantly expressed in leiomyomas in an ethnic-dependent manner and targets ZEBs, VEGFA, TIMP2, and FBLN5

Endocrine-Related Cancer

Volumn 19, Issue 4, 2012, Pages 541-556

  Chuang, Tsai Der ^a   Panda, Harekrushna ^a   Luo, Xiaoping ^a   Chegini, Nasser ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

FIBULIN 5; GELATINASE B; GONADORELIN AGONIST; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MEDROXYPROGESTERONE ACETATE; MICRORNA 200C; ORAL CONTRACEPTIVE AGENT; PROGESTERONE RECEPTOR MODULATOR; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UVOMORULIN; VASCULOTROPIN A; VIMENTIN;

AFRICAN AMERICAN; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CAUCASIAN; CONTROLLED STUDY; ETHNICITY; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; HORMONAL THERAPY; HUMAN; HUMAN TISSUE; LEIOMYOMA; LEIOMYOSARCOMA; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; MYOMETRIUM; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UTERUS BLEEDING; UTERUS TUMOR;

ADULT; CASE-CONTROL STUDIES; ETHNIC GROUPS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; LEIOMYOMA; MICRORNAS; MIDDLE AGED; REPRESSOR PROTEINS; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TRANSCRIPTION FACTORS; UTERINE NEOPLASMS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; YOUNG ADULT;

EID: 84864404690     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0007     Document Type: Article

References (69)

1. Baek D, Villen J, Shin C, Camargo FD, Gygi SP & Bartel DP 2008 The impact of microRNAs on protein output. Nature 455 64-71. (doi:10.1038/ nature07242)
2. Baird DD, Garrett TA, Laughlin SK, Davis B, Semelka RC & Peddada SD 2011 Short-term change in growth of uterine leiomyoma: tumor growth spurts. Fertility and Sterility 95 242-246. (doi:10.1016/j.fertnstert.2010.05.011)
3. Bendoraite A, Knouf EC, Garg KS, Parkin RK, Kroh EM, O'Briant KC, Ventura AP, Godwin AK, Karlan BY, Drescher CW et al. 2010 Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: evidence supporting a mesothelial-to-epithelial transition. Gynecological Oncology 116 117-125. (doi:10.1016/j.ygyno.2009.08.009)
4. Bhat-Nakshatri P, Wang G, Collins NR, Thomson MJ, Geistlinger TR, Carroll JS, Brown M, Hammond S, Srour EF, Liu Y et al. 2009 Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Research 37 4850-4861. (doi:10.1093/nar/gkp500)
5. Bogusiewicz M, Stryjecka-Zimmer M, Postawski K, Jakimiuk AJ & Rechberger T 2007 Activity of matrix metalloproteinase-2 and -9 and contents of their tissue inhibitors in uterine leiomyoma and corresponding myometrium. Gynecological Endocrinology 23 541-546. (doi:10.1080/09513590701557416)
6. Budatha M, Roshanravan S, Zheng Q, Weislander C, Chapman SL, Davis EC, Starcher B, Word RA & Yanagisawa H 2011 Extracellular matrix proteases contribute to progression of pelvic organ prolapse in mice and humans. Journal of Clinical Investigation 121 2048-2059. (doi:10.1172/JCI45636)
7. Chai JY, Modak C, Mouazzen W, Narvaez R & Pham J 2010 Epithelial or mesenchymal: where to draw the line? Bioscience Trends 4 130-142.
8. Chan YC, Khanna S, Roy S & Sen CK 2011 miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. Journal of Biological Chemistry 286 2047-2056. (doi:10.1074/jbc.M110.158790)
9. Chang HL, Senaratne TN, Zhang L, Szotek PP, Stewart E, Dombkowski D, Preffer F, Donahoe PK & Teixeira J 2010 Uterine leiomyomas exhibit fewer stem/progenitor cell characteristics when compared with corresponding normal myometrium. Reproductive Sciences 17 158-167. (doi:10.1177/1933719109348924)
10. Chegini N 2010 Proinflammatory and profibrotic mediators: principal effectors of leiomyoma development as a fibrotic disorder. Seminars in Reproductive Medicine 28 180-203. (doi:10.1055/s-0030-1251476)
11. Chegini N, Ma C, Tang XM & Williams RS 2002 Effects of GnRH analogues, 'add-back' steroid therapy, antiestrogen and antiprogestins on leiomyoma and myometrial smooth muscle cell growth and transforming growth factor-beta expression. Molecular Human Reproduction 8 1071-1078. (doi:10.1093/molehr/8.12.1071)
12. Chen Y, Ge W, Xu L, Qu C, Zhu M, Zhang W & Xiao Y 2012 miR-200b is involved in intestinal fibrosis of Crohn's disease. International Journal of Molecular Medicine 29 601-606. (doi:10.3892/ijmm.2012.894)
13. Chuang TD, Luo X, Panda H & Chegini N 2012 miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Molecular Endocrinology 26 1028-1042. (doi:10.1210/me.2012-1075)
14. Ciarmela P, Islam MS, Reis FM, Gray PC, Bloise E, Petraglia F, Vale W & Castellucci M 2011 Growth factors andmyometrium: biological effects in uterine fibroid and possible clinical implications. Human Reproduction Update 17 772-790. (doi:10.1093/humupd/dmr031)
15. Dahiya N, Sherman-Baust CA, Wang TL, Davidson B, Shih I, Zhang Y, Wood W III, Becker KG & Morin PJ 2008 MicroRNA expression and identification of putative miRNA targets in ovarian cancer. PLoS ONE 3 e2436. (doi:10.1371/ journal.pone.0002436)
16. Davalos V & Esteller M 2009 Opening the treasure chest of miR-200s family members. Cell Cycle 8 2141-2142. (doi:10.4161/cc.8.14.9201)
17. Devitt MH, Ralfkjaer U, Cremers N, Frankel M, Troelsgaard PR, Klingelhofer J, Yanagisawa H, Grigorian M, Guldberg P, Sleeman J et al. 2011 Role of fibulin-5 in metastatic organ colonization. Molecular Cancer Research 9 553-563. (doi:10.1158/1541-7786.MCR-11-0093)
18. Djuranovic S, Nahvi A & Green R 2011 A parsimonious model for gene regulation by miRNAs. Science 331 550-553. (doi:10.1126/science.1191138)
19. Dykxhoorn DM 2010 MicroRNAs and metastasis: little RNAs go a long way. Cancer Research 70 6401-6406. (doi:10.1158/0008-5472.CAN-10-1346)
20. Fabian MR, Sonenberg N & Filipowicz W 2010 Regulation of mRNA translation and stability by microRNAs. Annual Review of Biochemistry 79 351-379. (doi:10.1146/annurev-biochem-060308-103103)
21. Fragiadaki M & Mason RM 2011 Epithelial-mesenchymal transition in renal fibrosis the evidence for and against. International Journal of Experimental Pathology 92 143-150. (doi:10.1111/j.1365-2613.2011.00775.x)
22. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S, Morris M, Wyatt L, Farshid G, Lim YY et al. 2011 An autocrine TGF-{beta}/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Molecular Biology of the Cell 22 1686-1698. (doi:10.1091/mbc.E11-02-0103)
23. Guadall A, Orriols M, Rodriguez-Calvo R, Calvayrac O, Crespo J, Aledo R, Martinez-Gonzalez J & Rodriguez C 2011 Fibulin-5 is up-regulated by hypoxia in endothelial cells through a hypoxia-inducible factor-1 (HIF-1alpha)-dependent mechanism. Journal of Biological Chemistry 286 7093-7103. (doi:10.1074/jbc. M110.162917)
24. Guo H, Ingolia NT, Weissman JS & Bartel DP 2010 Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 835-840. (doi:10.1038/nature09267)
25. Harper SJ & Bates DO 2008 VEGF-A splicing: the key to anti-angiogenic therapeutics? Nature Reviews. Cancer 8 880-887. (doi:10.1038/nrc2505)
26. Harrison-Woolrych ML, Sharkey AM, Charnock-Jones DS & Smith SK 1995 Localization and quantification of vascular endothelial growth factor messenger ribonucleic acid in human myometrium and leiomyomata. Journal of Clinical Endocrinology and Metabolism 80 1853-1858. (doi:10.1210/jc.80.6.1853)
27. Hawkins SM, Buchold GM & Matzuk MM 2011a Minireview: the roles of small RNA pathways in reproductive medicine. Molecular Endocrinology 25 1257-1279. (doi:10.1210/me.2011-0099)
28. Hawkins SM, Creighton CJ, Han DY, Zariff A, Anderson ML, Gunaratne PH & Matzuk MM 2011b Functional microRNA involved in endometriosis. Molecular Endocrinology 25 821-832. (doi:10.1210/me.2010-0371)
29. Hinz B 2007 Formation and function of the myofibroblast during tissue repair. Journal of Investigative Dermatology 127 526-537. (doi:10.1038/sj.jid. 5700613)
30. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML & Gabbiani G 2007 The myofibroblast: one function, multiple origins. American Journal of Pathology 170 1807-1816. (doi:10.2353/ajpath.2007.070112)
31. Inomata M, Tagawa H, Guo YM, Kameoka Y, Takahashi N & Sawada K 2009 MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood 113 396-402. (doi:10.1182/blood-2008-07-163907)
32. Jiang X, Tsitsiou E, Herrick SE & Lindsay MA 2010 MicroRNAs and the regulation of fibrosis. FEBS Journal 277 2015-2021. (doi:10.1111/j.1742-4658. 2010.07632.x)
33. Kalluri R & Weinberg RA 2009 The basics of epithelial-mesenchymal transition. Journal of Clinical Investigation 119 1420-1428. (doi:10.1172/JCI39104)
34. Katoh M & Katoh M 2009 Integrative genomic analyses of ZEB2: transcriptional regulation of ZEB2 based on SMADs, ETS1, HIF1alpha, POU/OCT, and NF-kappaB. International Journal of Oncology 34 1737-1742. (doi:10.3892/ijo- 00000304)
35. Korpal M & Kang Y 2008 The emerging role of miR-200 family of microRNAs in epithelial-mesenchymal transition and cancer metastasis. RNA Biology 5 115-119. (doi:10.4161/rna.5.3.6558)
36. Lee YH, Albig AR, Regner M, Schiemann BJ & Schiemann WP 2008 Fibulin-5 initiates epithelial-mesenchymal transition (EMT) and enhances EMT induced by TGF-beta in mammary epithelial cells via a MMP-dependent mechanism. Carcinogenesis 29 2243-2251. (doi:10.1093/carcin/bgn199)
37. Lee JW, Park YA, Choi JJ, Lee YY, Kim CJ, Choi C, Kim TJ, Lee NW, Kim BG & Bae DS 2011 The expression of the miRNA-200 family in endometrial endometrioid carcinoma. Gynecological Oncology 120 56-62. (doi:10.1016/j.ygyno. 2010.09.022)
38. Leppert PC, Catherino WH & Segars JH 2006 A new hypothesis about the origin of uterine fibroids based on gene expression profiling with microarrays. American Journal of Obstetrics and Gynecology 195 415-420. (doi:10.1016/j.ajog. 2005.12.059)
39. Lewicka A, Osuch B, Cendrowski K, Zegarska J & Stelmachow J 2010 Expression of vascular endothelial growth factor mRNA in human leiomyomas. Gynecological Endocrinology 26 451-455. (doi:10.3109/09513591003632159)
40. Lewis BP, Burge CB & Bartel DP 2005 Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 15-20. (doi:10.1016/j.cell.2004.12.035)
41. Luo X & Chegini N 2008 The expression and potential regulatory function of microRNAs in the pathogenesis of leiomyoma. Seminars in Reproductive Medicine 26 500-514. (doi:10.1055/s-0028-1096130)
42. Luo X, Ding L, Xu J, Williams RS & Chegini N 2005 Leiomyoma and myometrial gene expression profiles and their responses to gonadotropin- releasing hormone analog therapy. Endocrinology 146 1074-1096. (doi:10.1210/en.2004-1384)
43. Maillot G, Lacroix-Triki M, Pierredon S, Gratadou L, Schmidt S, Benes V, Roche H, Dalenc F, Auboeuf D, Millevoi S et al. 2009 Widespread estrogen-dependent repression of micrornas involved in breast tumor cell growth. Cancer Research 69 8332-8340. (doi:10.1158/0008-5472.CAN-09-2206)
44. Nakayama T, Cho YC, Mine Y, Yoshizaki A, Naito S, Wen CY & Sekine I 2006 Expression of vascular endothelial growth factor and its receptors VEGFR-1 and 2 in gastrointestinal stromal tumors, leiomyomas and schwannomas. World Journal of Gastroenterology 12 6182-6187.
45. Nothnick WB & Healy C 2010 Estrogen induces distinct patterns of microRNA expression within the mouse uterus. Reproductive Sciences 17 987-994. (doi:10.1177/1933719110377472)
46. Oba S, Kumano S, Suzuki E, Nishimatsu H, Takahashi M, Takamori H, Kasuya M, Ogawa Y, Sato K, Kimura K et al. 2010 miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS ONE 5 e13614. (doi:10.1371/journal.pone. 0013614)
47. Ono M, Maruyama T, Masuda H, Kajitani T, Nagashima T, Arase T, Ito M, Ohta K, Uchida H, Asada H et al. 2007 Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells. PNAS 104 18700-18705. (doi:10.1073/pnas.0704472104)
48. Panda H, Pelakh L, Chuang TD, Luo X, Bukulmez O & Chegini N 2012 Endometrial miR-200c is altered during transformation into cancerous states and targets the expression of ZEBs, VEGFA, FLT1, IKKbeta, KLF9, and FBLN5. Reproductive Sciences [in press]. (doi:10.1177/1933719112438448)
49. Parker WH 2007 Etiology, symptomatology, and diagnosis of uterine myomas. Fertility and Sterility 87 725-736. (doi:10.1016/j.fertnstert.2007.01.093)
50. Peddada SD, Laughlin SK, Miner K, Guyon JP, Haneke K, Vahdat HL, Semelka RC, Kowalik A, Armao D, Davis B et al. 2008 Growth of uterine leiomyomata among premenopausal black and white women. PNAS 105 19887-19892. (doi:10.1073/pnas. 0808188105)
51. Peng Y, Laser J, Shi G, Mittal K, Melamed J, Lee P & Wei JJ 2008 Antiproliferative effects by Let-7 repression of high-mobility group A2 in uterine leiomyoma. Molecular Cancer Research 6 663-673. (doi:10.1158/1541-7786. MCR-07-0370)
52. Pollard P, Wortham N, Barclay E, Alam A, Elia G, Manek S, Poulsom R & Tomlinson I 2005 Evidence of increased microvessel density and activation of the hypoxia pathway in tumours from the hereditary leiomyomatosis and renal cell cancer syndrome. Journal of Pathology 205 41-49. (doi:10.1002/path.1686)
53. Renthal NE, Chen CC, Williams KC, Gerard RD, Prange-Kiel J & Mendelson CR 2010 miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. PNAS 107 20828-20833. (doi:10.1073/pnas.1008301107)
54. Roybal JD, Zang Y, Ahn YH, Yang Y, Gibbons DL, Baird BN, Alvarez C, Thilaganathan N, Liu DD, Saintigny P et al. 2011 miR-200 Inhibits lung adenocarcinoma cell invasion and metastasis by targeting Flt1/VEGFR1. Molecular Cancer Research 9 25-35. (doi:10.1158/1541-7786.MCR-10-0497)
55. Sanci M, Dikis C, Inan S, Turkoz E, Dicle N & Ispahi C 2011 Immunolocalization of VEGF, VEGF receptors, EGF-R and Ki-67 in leiomyoma, cellular leiomyoma and leiomyosarcoma. Acta Histochemica 113 317-325. (doi:10.1016/j.acthis.2010.01.001)
56. Small EM & Olson EN 2011 Pervasive roles of microRNAs in cardiovascular biology. Nature 469 336-342. (doi:10.1038/nature09783)
57. Spoelstra NS, Manning NG, Higashi Y, Darling D, Singh M, Shroyer KR, Broaddus RR, Horwitz KB & Richer JK 2006 The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers. Cancer Research 66 3893-3902. (doi:10.1158/0008-5472.CAN-05-2881)
58. Tanwar PS, Lee HJ, Zhang L, Zukerberg LR, Taketo MM, Rueda BR & Teixeira JM 2009 Constitutive activation of beta-catenin in uterine stroma and smooth muscle leads to the development of mesenchymal tumors in mice. Biology of Reproduction 81 545-552. (doi:10.1095/biolreprod.108.075648)
59. Thiery JP,AcloqueH, HuangRY&NietoMA2009 Epithelial-mesenchymal transitions in development and disease. Cell 139 871-890. (doi:10.1016/j.cell. 2009.11.007)
60. Walker CL & Stewart EA 2005 Uterine fibroids: the elephant in the room. Science 308 1589-1592. (doi:10.1126/science.1112063)
61. Wallez Y, Vilgrain I & Huber P 2006 Angiogenesis: the VE-cadherin switch. Trends in Cardiovascular Medicine 16 55-59. (doi:10.1016/j.tcm.2005.11. 008)
62. Wang T, Zhang X, Obijuru L, Laser J, Aris V, Lee P, Mittal K, Soteropoulos P & Wei JJ 2007 A micro-RNA signature associated with race, tumor size, and target gene activity in human uterine leiomyomas. Genes, Chromosomes & Cancer 46 336-347. (doi:10.1002/gcc.20415)
63. Wynn TA 2008 Cellular and molecular mechanisms of fibrosis. Journal of Pathology 214 199-210. (doi:10.1002/path.2277)
64. Xu Q, Ohara N, Chen W, Liu J, Sasaki H, Morikawa A, Sitruk-Ware R, Johansson ED & Maruo T 2006 Progesterone receptor modulator CDB-2914 down-regulates vascular endothelial growth factor, adrenomedullin and their receptors and modulates progesterone receptor content in cultured human uterine leiomyoma cells. Human Reproduction 21 2408-2416. (doi:10.1093/humrep/del159)
65. Xu Q, Ohara N, Liu J, Amano M, Sitruk-Ware R, Yoshida S & Maruo T 2008 Progesterone receptor modulator CDB-2914 induces extracellular matrix metalloproteinase inducer in cultured human uterine leiomyoma cells. Molecular Human Reproduction 14 181-191. (doi:10.1093/molehr/gan004)
66. Yanagisawa H, Schluterman MK & Brekken RA 2009 Fibulin-5, an integrin-binding matricellular protein: its function in development and disease. Journal of Cell Communication and Signaling 3 337-347. (doi:10.1007/s12079-009- 0065-3)
67. Yang S, Banerjee S, de Freitas A, Sanders YY, Ding Q, Matalon S, Thannickal VJ, Abraham E & Liu G 2012 Participation of miR-200 in pulmonary fibrosis. American Journal of Pathology 180 484-493. (doi:10.1016/j.ajpath.2011. 10.005)
68. Yoshimoto N, Toyama T, Takahashi S, Sugiura H, Endo Y, Iwasa M, Fujii Y & Yamashita H 2011 Distinct expressions of microRNAs that directly target estrogen receptor alpha in human breast cancer. Breast Cancer Research and Treatment 130 331-339. (doi:10.1007/s10549-011-1672-2)
69. Yue W, Sun Q, Landreneau R, Wu C, Siegfried JM, Yu J & Zhang L 2009 Fibulin-5 suppresses lung cancer invasion by inhibiting matrix metalloproteinase-7 expression. Cancer Research 69 6339-6346. (doi:10.1158/0008-5472.CAN-09-0398)