Vitamin D3 inhibits expression and activities of matrix metalloproteinase-2 and -9 in human uterine fibroid cells

Human Reproduction

Volumn 28, Issue 9, 2013, Pages 2407-2416

  Halder, Sunil K ^a   Osteen, Kevin G ^b   Al Hendy, Ayman ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

fibroids; MMPs; TIMP 2; VDR; vitamin D3

Indexed keywords

COLECALCIFEROL; COLLAGENASE 3; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; VITAMIN D RECEPTOR;

ARTICLE; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UTERUS MYOMA; WESTERN BLOTTING;

FIBROIDS; MMPS; TIMP-2; VDR; VITAMIN D3;

ANTINEOPLASTIC AGENTS; CALCITRIOL; CELL LINE, TUMOR; ENZYME PRECURSORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEIOMYOMA; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MYOMETRIUM; NEOPLASM PROTEINS; OSMOLAR CONCENTRATION; RECEPTORS, CALCITRIOL; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TUMOR CELLS, CULTURED; UTERINE NEOPLASMS;

EID: 84883158440     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/det265     Document Type: Article

References (73)

1. Aimes RT, Quigley JP. Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4-and 1/4-length fragments. J Biol Chem 1995;270:5872-5876.
2. Allan JA, Docherty AJ, Barker PJ, Huskisson NS, Reynolds JJ, Murphy G. Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem J 1995;309(Pt 1):299-306.
3. Anand SP, Selvaraj P. Effect of 1, 25 dihydroxyvitamin D(3) on matrix metalloproteinases MMP-7, MMP-9 and the inhibitor TIMP-1 in pulmonary tuberculosis. Clin Immunol 2009;133:126-131.
4. Baird DD, Dunson DB. Why is parity protective for uterine fibroids? Epidemiology 2003;14:247-250. (Pubitemid 40417114)
5. Berto AG, Sampaio LO, Franco CR, Cesar RM Jr, Michelacci YM. A comparative analysis of structure and spatial distribution of decorin in human leiomyoma and normal myometrium. Biochim Biophys Acta 2003; 1619:98-112. (Pubitemid 35462123)
6. Blauer M, Rovio PH, Ylikomi T, Heinonen PK. Vitamin D inhibits myometrial and leiomyoma cell proliferation in vitro. Fertil Steril 2009; 91:1919-1925.
7. Bogusiewicz M, Stryjecka-Zimmer M, Postawski K, Jakimiuk AJ, Rechberger T. Activity of matrix metalloproteinase-2 and-9 and contents of their tissue inhibitors in uterine leiomyoma and corresponding myometrium. Gynecol Endocrinol 2007;23:541-546. (Pubitemid 47621524)
8. Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 2000;1477:267-283. (Pubitemid 30119906)
9. Butler GS, Will H, Atkinson SJ, Murphy G. Membrane-type-2 matrix metalloproteinase can initiate the processing of progelatinase A and is regulated by the tissue inhibitors of metalloproteinases. Eur J Biochem 1997;244:653-657. (Pubitemid 27110771)
10. Byers PH. Collagens: building blocks at the end of the development line. Clin Genet 2000;58:270-279.
11. Carney SA, Tahara H, Swartz CD, Risinger JI, He H, Moore AB, Haseman JK, Barrett JC, Dixon D. Immortalization of human uterine leiomyoma and myometrial cell lines after induction of telomerase activity: molecular and phenotypic characteristics. Lab Invest 2002;82:719-728. (Pubitemid 34633821)
12. Catherino WH, Leppert PC, Stenmark MH, Payson M, Potlog-Nahari C, Nieman LK, Segars JH. Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids. Genes Chromosomes Cancer 2004;40:204-217. (Pubitemid 38703097)
13. Chambers AF, Matrisian LM. Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst 1997; 89: 1260-1270. (Pubitemid 27371946)
14. Chang JC, Wysocki A, Tchou-Wong KM, Moskowitz N, Zhang Y, Rom WN. Effect of Mycobacterium tuberculosis and its components on macrophages and the release of matrix metalloproteinases. Thorax 1996;51:306-311. (Pubitemid 26086477)
15. Chirco R, Liu XW, Jung KK, Kim HR. NovelfunctionsofTIMPsincell signaling. Cancer Metastasis Rev 2006;25:99-113.
16. Chung L, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, Nagase H. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 2004;23:3020-3030. (Pubitemid 39093596)
17. Coussens A, Timms PM, Boucher BJ, Venton TR, Ashcroft AT, Skolimowska KH, Newton SM, Wilkinson KA, Davidson RN, Griffiths CJ et al. 1alpha, 25-dihydroxyvitamin D3 inhibits matrix metalloproteinases induced by Mycobacterium tuberculosis infection. Immunology 2009; 127:539-548.
18. Dou Q, Tarnuzzer RW, Williams RS, Schultz GS, Chegini N. Differential expression of matrix metalloproteinases and their tissue inhibitors in leiomyomata: a mechanism for gonadotrophin releasing hormone agonist-induced tumour regression. Mol Hum Reprod 1997;3:1005-1014. (Pubitemid 127509967)
19. Farhi J, Ashkenazi J, Feldberg D, Dicker D, Orvieto R, Ben Rafael Z. Effect of uterine leiomyomata on the results of in-vitro fertilization treatment. Hum Reprod 1995;10:2576-2578.
20. Gelse K, Poschl E, Aigner T. Collagens-structure, function, and biosynthesis. Adv Drug Deliv Rev 2003;55:1531-1546.
21. Gilad LA, Tirosh O, Schwartz B. Phytoestrogens regulate transcription and translation of vitamin D receptor in colon cancer cells. J Endocrinol 2006; 191:387-398. (Pubitemid 44830614)
22. Gioia M, Monaco S, Fasciglione GF, Coletti A, Modesti A, Marini S, Coletta M. Characterization of the mechanisms by which gelatinase A, neutrophil collagenase, and membrane-type metalloproteinase MMP-14 recognize collagen I and enzymatically process the two alpha-chains. J Mol Biol 2007;368:1101-1113. (Pubitemid 46574666)
23. Halder SK, Beauchamp RD, Datta PK. Smad7 induces tumorigenicity by blocking TGF-beta-induced growth inhibition and apoptosis. Exp Cell Res 2005;307:231-246. (Pubitemid 40732749)
24. Halder SK, Goodwin JS, Al-Hendy A. 1, 25-Dihydroxyvitamin D3 reduces TGF-beta3-induced fibrosis-related gene expression in human uterine leiomyoma cells. J Clin Endocrinol Metab 2011;96:E754-E762.
25. Halder SK, Sharan C, Al-Hendy A. 1, 25-dihydroxyvitamin D3 treatment shrinks uterine leiomyoma tumors in the Eker rat model. Biol Reprod 2012;86:116.
26. Hibbs MS, Hasty KA, Seyer JM, Kang AH, Mainardi CL. Biochemical and immunological characterization of the secreted forms of human neutrophil gelatinase. J Biol Chem 1985;260:2493-2500. (Pubitemid 15104858)
27. Holick MF. Vitamin D: a millennium perspective. J Cell Biochem 2003; 88:296-307.
28. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 2004;101:17192-17197. (Pubitemid 39627796)
29. Koli K, Keski-Oja J. 1alpha, 25-dihydroxyvitamin D3 and its analogues down-regulate cell invasion-associated proteases in cultured malignant cells. Cell Growth Differ 2000;11:221-229. (Pubitemid 30211011)
30. Lambert E, Dasse E, Haye B, Petitfrere E. TIMPs as multifacial proteins. Crit Rev Oncol Hematol 2004;49:187-198. (Pubitemid 38251351)
31. Leppert PC, Baginski T, Prupas C, Catherino WH, Pletcher S, Segars JH. Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium. Fertil Steril 2004;82:1182-1187. (Pubitemid 39335936)
32. Leppert PC, Catherino WH, Segars JH. A new hypothesis about the origin of uterine fibroids based on gene expression profiling with microarrays. Am J Obstet Gynecol 2006;195:415-420. (Pubitemid 44142369)
33. Levens E, Luo X, Ding L, Williams RS, Chegini N. Fibromodulinisexpressed in leiomyoma and myometrium and regulated by gonadotropin-releasing hormone analogue therapy and TGF-beta through Smad and MAPK-mediated signalling. Mol Hum Reprod 2005;11:489-494. (Pubitemid 41258235)
34. Li YY, McTiernan CF, Feldman AM. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc Res 2000;46:214-224. (Pubitemid 30204593)
35. Li YY, Kadokami T, Wang P, McTiernan CF, Feldman AM. MMP inhibition modulates TNF-alpha transgenic mouse phenotype early in the development of heart failure. Am J Physiol Heart Circ Physiol 2002; 282:H983-H989. (Pubitemid 34654937)
36. Limper AH, Roman J. Fibronectin. A versatile matrix protein with roles in thoracic development, repair and infection. Chest 1992;101:1663-1673.
37. Malik M, Catherino WH. Novel method to characterize primary cultures of leiomyoma and myometrium with theuseofconfirmatorybiomarkergene arrays. Fertil Steril 2007;87:1166-1172. (Pubitemid 46659932)
38. Malik M, Norian J, McCarthy-Keith D, Britten J, Catherino WH. Why leiomyomas are called fibroids: the central role of extracellular matrix in symptomatic women. Semin Reprod Med 2010;28:169-179.
39. Matrisian LM. The matrix-degrading metalloproteinases. Bioessays 1992; 14:455-463.
40. Meems LM, Cannon MV, Mahmud H, Voors AA, van Gilst WH, Sillje HH, Ruifrok WP, de Boer RA. The vitamin D receptor activator paricalcitol prevents fibrosis and diastolic dysfunction in a murine model of pressure overload. J Steroid Biochem Mol Biol 2012;132:282-289.
41. Mook OR, Frederiks WM, Van Noorden CJ. The role of gelatinases in colorectal cancer progression and metastasis. Biochim Biophys Acta 2004; 1705:69-89. (Pubitemid 39592897)
42. Mujumdar VS, Tyagi SC. Temporal regulation of extracellular matrix components in transition from compensatory hypertrophy to decompensatory heart failure. J Hypertens 1999;17:261-270. (Pubitemid 29074115)
43. Murphy G, Segain JP, O'Shea M, Cockett M, Ioannou C, Lefebvre O, Chambon P, Basset P. The 28-kDa N-terminal domain of mouse stromelysin-3 has the general properties of a weak metalloproteinase. J Biol Chem 1993;268:15435-15441. (Pubitemid 23222033)
44. Nagase H. Cell surface activation of progelatinase A (proMMP-2) and cell migration. Cell Res 1998;8:179-186. (Pubitemid 128544278)
45. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006;69:562-573. (Pubitemid 43139720)
46. Nesby-O'Dell S, Scanlon KS, Cogswell ME, Gillespie C, Hollis BW, Looker AC, Allen C, Doughertly C, Gunter EW, Bowman BA. Hypovitaminosis D prevalence and determinants among African American and white women of reproductive age: third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr 2002;76:187-192. (Pubitemid 34686565)
47. Nnoaham KE, Clarke A. Low serum vitamin D levels and tuberculosis: a systematic review and meta-analysis. Int J Epidemiol 2008;37:113-119. (Pubitemid 351228619)
48. Norian JM, Malik M, Parker CY, Joseph D, Leppert PC, Segars JH, Catherino WH. Transforming growth factor beta3 regulates the versican variants in the extracellular matrix-rich uterine leiomyomas. Reprod Sci 2009;16:1153-1164.
49. Ohara N. A putative role of versican in uterine leiomyomas. Clin Exp Obstet Gynecol 2009;36:74-75.
50. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 1997;272:2446-2451. (Pubitemid 27058534)
51. Olson MW, Bernardo MM, Pietila M, Gervasi DC, Toth M, Kotra LP, Massova I, Mobashery S, Fridman R. Characterization of the monomeric and dimeric forms of latent and active matrix metalloproteinase-9. Differential rates for activation by stromelysin 1. J Biol Chem 2000; 275:2661-2668. (Pubitemid 30082034)
52. Ottino P, Taheri F, Bazan HE. Platelet-activating factor induces the gene expression of TIMP-1,-2, and PAI-1: imbalance between the gene expression of MMP-9 and TIMP-1 and-2. Exp Eye Res 2002;74:393-402. (Pubitemid 34948385)
53. Patterson ML, Atkinson SJ, Knauper V, Murphy G. Specific collagenolysis by gelatinase A, MMP-2, isdetermined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett 2001;503:158-162. (Pubitemid 32763197)
54. Polgar A, Falus A, Koo E, Ujfalussy I, Sesztak M, Szuts I, Konrad K, Hodinka L, Bene E, Meszaros G et al. Elevated levels of synovial fluid antibodies reactive with the small proteoglycans biglycan and decorin in patients with rheumatoid arthritis or other joint diseases. Rheumatology (Oxford) 2003;42:522-527. (Pubitemid 36432470)
55. Rahman A, Hershey S, Ahmed S, Nibbelink K, Simpson RU. Heart extracellular matrix gene expression profile in the vitamin D receptor knockout mice. J Steroid Biochem Mol Biol 2007;103:416-419. (Pubitemid 46415673)
56. Rein MS, Barbieri RL, Friedman AJ. Progesterone: a critical role in the pathogenesis of uterine myomas. Am J Obstet Gynecol 1995;172:14-18.
57. Sabry M, Halder SK, Allah AS, Roshdy E, Rajaratnam V, Al-Hendy A. Serum vitamin D3 level inversely correlates with uterine fibroid volume in different ethnic groups: a cross-sectional observational study. Int J Womens Health 2013;5:93-100.
58. Sharan C, Halder SK, Thota C, Jaleel T, Nair S, Al-Hendy A. Vitamin D inhibits proliferation of human uterine leiomyoma cells via catechol-O- methyltransferase. Fertil Steril 2011;95:247-253.
59. Sintov AC, Berkovich L, Ben-Shabat S. Inhibition of cancer growth and induction of apoptosis by BGP-13 and BGP-15, new calcipotriene-derived vitamin D(3) analogs, in-vitro and in-vivo studies. Invest New Drugs 2013; 31:247-255.
60. Sozen I, Arici A. Interactions of cytokines, growth factors, and the extracellular matrix in the cellular biology of uterine leiomyomata. Fertil Steril 2002;78:1-12. (Pubitemid 34722662)
61. Spinale FG. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ Res 2002;90:520-530. (Pubitemid 34640901)
62. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463-516. (Pubitemid 33096184)
63. Stewart EA, Friedman AJ, Peck K, Nowak RA. Relative overexpression of collagen type I and collagen type III messenger ribonucleic acids by uterine leiomyomas during the proliferative phase of the menstrual cycle. J Clin Endocrinol Metab 1994;79:900-906. (Pubitemid 24286424)
64. Tempfer H, Gehwolf R, Lehner C, Wagner A, Mtsariashvili M, Bauer HC, Resch H, Tauber M. Effects of crystalline glucocorticoid triamcinolone acetonide on cultered human supraspinatus tendon cells. Acta Orthop 2009;80:357-362.
65. Tetlow LC, Woolley DE. The effects of 1alpha, 25-dihydroxyvitamin D(3) on matrix metalloproteinase and prostaglandin E(2) production by cells of the rheumatoid lesion. Arthritis Res 1999;1:63-70. (Pubitemid 32223674)
66. Timms PM, Mannan N, Hitman GA, Noonan K, Mills PG, Syndercombe-Court D, Aganna E, Price CP, Boucher BJ. Circulating MMP9, vitamin D and variation in the TIMP-1 response with VDR genotype: mechanisms for inflammatory damage in chronic disorders? QJM 2002;95:787-796. (Pubitemid 36032948)
67. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92:827-839. (Pubitemid 36542523)
68. Walker CL, Stewart EA. Uterine fibroids: the elephant in the room. Science 2005;308:1589-1592. (Pubitemid 40807499)
69. Wilcox LS, Koonin LM, Pokras R, Strauss LT, Xia Z, Peterson HB. Hysterectomy in the United States, 1988-1990. Obstet Gynecol 1994; 83:549-555. (Pubitemid 24221795)
70. Wilson EA, Yang F, Rees ED. Estradiol and progesterone binding in uterine leiomyomata and in normal uterine tissues. Obstet Gynecol 1980; 55:20-24. (Pubitemid 10205557)
71. Woessner JF Jr. The family of matrix metalloproteinases. Ann N Y Acad Sci 1994;732:11-21.
72. Wolanska M, Sobolewski K, Bankowski E, Jaworski S. Matrix metalloproteinases of human leiomyoma in various stages of tumor growth. Gynecol Obstet Invest 2004;58:14-18. (Pubitemid 39140401)
73. Zucker S, Lysik RM, Zarrabi MH, Moll U. M(r) 92, 000 type IV collagenase is increasedinplasmaofpatients with colon cancer and breast cancer. Cancer Res 1993;53:140-146. (Pubitemid 23019389)