1,25-Dihydroxyvitamin D3 reduces extracellular matrix-associated protein expression in human uterine fibroid cells

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

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

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

Extracellular matrix (ECM); Fibroids; Vitamin d receptor (VDR)

Indexed keywords

BIGLYCAN; CALCITRIOL; COLLAGEN TYPE 1; FIBROMODULIN; FIBRONECTIN; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEOGLYCAN; SMOOTH MUSCLE ACTIN; VERSICAN; VITAMIN D RECEPTOR;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMORTALIZED CELL LINE; MYOMETRIUM; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; UTERUS MYOMA; VITAMIN BLOOD LEVEL; WESTERN BLOTTING;

1,25-DIHYDROXYVITAMIN D3 (1,25[OH]2D3); EXTRACELLULAR MATRIX (ECM); FIBROIDS; VITAMIN D RECEPTOR (VDR);

ADULT; CELLS, CULTURED; DOWN-REGULATION; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEIOMYOMA; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; RECEPTORS, CALCITRIOL; UTERINE NEOPLASMS; UTERUS; VITAMIN D;

EID: 84901252966     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.107714     Document Type: Article

References (70)

1. 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.
2. Surrey ES, Lietz AK, Schoolcraft WB. Impact of intramural leiomyomata in patients with a normal endometrial cavity on in vitro fertilization-embryo transfer cycle outcome. Fertil Steril 2001; 75:405-410.
3. 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.
4. Wilson EA, Yang F, Rees ED. Estradiol and progesterone binding in uterine leiomyomata and in normal uterine tissues. Obstet Gynecol 1980; 55:20-24.
5. Rein MS, Barbieri RL, Friedman AJ. Progesterone: a critical role in the pathogenesis of uterine myomas. Am J Obstet Gynecol 1995; 172:14-18.
6. Baird DD, Dunson DB. Why is parity protective for uterine fibroids? Epidemiology 2003; 14:247-250.
7. 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.
8. Walker CL, Stewart EA. Uterine fibroids: the elephant in the room. Science 2005; 308:1589-1592.
9. 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.
10. Tsibris JC, Segars J, Coppola D, Mane S, Wilbanks GD, O'Brien WF, Spellacy WN. Insights from gene arrays on the development and growth regulation of uterine leiomyomata. Fertil Steril 2002; 78:114-121.
11. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol 1990; 6:597-641.
12. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997; 390: 465-471.
13. Schnaper HW, Hayashida T, Hubchak SC, Poncelet AC. TGF-beta signal transduction and mesangial cell fibrogenesis. Am J Physiol Renal Physiol 2003; 284:F243-F252.
14. Verrecchia F, Mauviel A. Transforming growth factor-beta signaling through the Smad pathway: role in extracellular matrix gene expression and regulation. J Invest Dermatol 2002; 118:211-215.
15. Arici A, Sozen I. Transforming growth factor-beta3 is expressed at high levels in leiomyoma where it stimulates fibronectin expression and cell proliferation. Fertil Steril 2000; 73:1006-1011.
16. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000; 19:1745-1754.
17. 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.
18. Ding L, Xu J, Luo X, Chegini N. Gonadotropin releasing hormone and transforming growth factor beta activate mitogen-activated protein kinase/ extracellularly regulated kinase and differentially regulate fibronectin, type I collagen, and plasminogen activator inhibitor-1 expression in leiomyoma and myometrial smooth muscle cells. J Clin Endocrinol Metab 2004; 89: 5549-5557.
19. 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.
20. Massague J. Receptors for the TGF-beta family. Cell 1992; 69:1067-1070.
21. Barnard JA, Lyons RM, Moses HL. The cell biology of transforming growth factor beta. Biochim Biophys Acta 1990; 1032:79-87.
22. Luo X, Ding L, Xu J, Chegini N. Gene expression profiling of leiomyoma and myometrial smooth muscle cells in response to transforming growth factor-beta. Endocrinology 2005; 146:1097-1118.
23. Holick MF. Vitamin D: A millenium perspective. J Cell Biochem 2003; 88:296-307.
24. Ylikomi T, Laaksi I, Lou YR, Martikainen P, Miettinen S, Pennanen P, Purmonen S, Syvala H, Vienonen A, Tuohimaa P. Antiproliferative action of vitamin D. Vitam Horm 2002; 64:357-406.
25. Tang XM, Dou Q, Zhao Y, McLean F, Davis J, Chegini N. The expression of transforming growth factor-beta s and TGF-beta receptor mRNA and protein and the effect of TGF-beta s on human myometrial smooth muscle cells in vitro. Mol Hum Reprod 1997; 3:233-240.
26. Light BW, Yu WD, McElwain MC, Russell DM, Trump DL, Johnson CS. Potentiation of cisplatin antitumor activity using a vitamin D analogue in a murine squamous cell carcinoma model system. Cancer Res 1997; 57: 3759-3764.
27. Sharan C, Halder SK, Thota C, Jaleel T, Nair S, Al-Hendy A. Vitamin D inhibits proliferation of human uterine leiomyoma cells via catechol-Omethyltransferase. Fertil Steril 2011; 95:247-253.
28. Blauer M, Rovio PH, Ylikomi T, Heinonen PK. Vitamin D inhibits myometrial and leiomyoma cell proliferation in vitro. Fertil Steril 2009; 91:1919-1925.
29. 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, 1-10.
30. 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.
31. Sabry M, Halder SK, Allah AS, Roshdy E, Rajaratnam V, Al-Hendy A. Serum vitamin D3 level inversely correlated with uterine fibroid volume in different ethnic groups: a cross-sectional observational study. Int J Womens Health 2013; 5:93-100.
32. Baird DD, Hill MC, Schectman JM, Hollis BW. Vitamin D and the risk of uterine fibroids. Epidemiology 2013; 24:447-453.
33. Paffoni A, Somigliana E, Vigano P, Benaglia L, Cardellicchio L, Pagliardini L, Papaleo E, Candiani M, Fedele L. Vitamin D status in women with uterine leiomyomas. J Clin Endocrinol Metab 2013; 98: E1374-E1378.
34. 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.
35. Ishida Y, Kubota H, Yamamoto A, Kitamura A, Bachinger HP, Nagata K. Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol Biol Cell 2006; 17:2346-2355.
36. Halder SK, Anumanthan G, Maddula R, Mann J, Chytil A, Gonzalez AL, Washington MK, Moses HL, Beauchamp RD, Datta PK. Oncogenic function of a novel WD-domain protein, STRAP, in human carcinogenesis. Cancer Res 2006; 66:6156-6166.
37. 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.
38. Levens E, Luo X, Ding L, Williams RS, Chegini N. Fibromodulin is expressed in leiomyoma and myometrium and regulated by gonadotropinreleasing hormone analogue therapy and TGF-beta through Smad and MAPK-mediated signalling. Mol Hum Reprod 2005; 11:489-494.
39. Honardoust D, Varkey M, Hori K, Ding J, Shankowsky HA, Tredget EE. Small leucine-rich proteoglycans, decorin and fibromodulin, are reduced in postburn hypertrophic scar. Wound Repair Regen 2011; 19:368-378.
40. Attia M, Scott A, Duchesnay A, Carpentier G, Soslowsky LJ, Huynh MB, Van Kuppevelt TH, Gossard C, Courty J, Tassoni MC, Martelly I. Alterations of overused supraspinatus tendon: a possible role of glycosaminoglycans and HARP/pleiotrophin in early tendon pathology. J Orthop Res 2012; 30:61-71.
41. Didangelos A, Mayr U, Monaco C, Mayr M. Novel role of ADAMTS-5 protein in proteoglycan turnover and lipoprotein retention in atherosclerosis. J Biol Chem 2012; 287:19341-19345.
42. Shi-Wen X, Renzoni EA, Kennedy L, Howat S, Chen Y, Pearson JD, Bou-Gharios G, Dashwood MR, du Bois RM, Black CM, Denton CP, Abraham DJ, et al. Endogenous endothelin-1 signaling contributes to type I collagen and CCN2 overexpression in fibrotic fibroblasts. Matrix Biol 2007; 26: 625-632.
43. Halder SK, Osteen KG, Al-Hendy A. Vitamin D3 inhibits expression and activities of matrix metalloproteinase-2 and -9 in human uterine fibroid cells. Hum Reprod 2013; 28:2407-2416.
44. Martin I, Jakob M, Schafer D, Dick W, Spagnoli G, Heberer M. Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritic joints. Osteoarthritis Cartilage 2001; 9:112-118.
45. Adesida AB, Mulet-Sierra A, Laouar L, Jomha NM. Oxygen tension is a determinant of the matrix-forming phenotype of cultured human meniscal fibrochondrocytes. PLoS ONE 2012; 7:e39339.
46. Artaza JN, Norris KC. Vitamin D reduces the expression of collagen and key profibrotic factors by inducing an antifibrotic phenotype in mesenchymal multipotent cells. J Endocrinol 2009; 200:207-221.
47. Ordonez-Moran P, Larriba MJ, Palmer HG, Valero RA, Barbachano A, Dunach M, de Herreros AG, Villalobos C, Berciano MT, Lafarga M, Munoz A. RhoA-ROCK and p38MAPK-MSK1 mediate vitamin D effects on gene expression, phenotype, and Wnt pathway in colon cancer cells. J Cell Biol 2008; 183:697-710.
48. Yanagishita M. Function of proteoglycans in the extracellular matrix. Acta Pathol Jpn 1993; 43:283-293.
49. Makinen N, Mehine M, Tolvanen J, Kaasinen E, Li Y, Lehtonen HJ, Gentile M, Yan J, Enge M, Taipale M, Aavikko M, Katainen R, et al. MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas. Science 2011; 334:252-255.
50. McGuire MM, Yatsenko A, Hoffner L, Jones M, Surti U, Rajkovic A. Whole exome sequencing in a random sample of North American women with leiomyomas identifies MED12 mutations in majority of uterine leiomyomas. PLoS ONE 2012; 7:e33251.
51. 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.
52. 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.
53. Norian JM, Owen CM, Taboas J, Korecki C, Tuan R, Malik M, Catherino WH, Segars JH. Characterization of tissue biomechanics and mechanical signaling in uterine leiomyoma. Matrix Biol 2012; 31:57-65.
54. Malik M, Catherino WH. Development and validation of a threedimensional in vitro model for uterine leiomyoma and patient-matched myometrium. Fertil Steril 2012; 97:1287-1293.
55. Calabresi C, Arosio B, Galimberti L, Scanziani E, Bergottini R, Annoni G, Vergani C. Natural aging, expression of fibrosis-related genes and collagen deposition in rat lung. Exp Gerontol 2007; 42:1003-1011.
56. Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007; 293:L525-L534.
57. Yata Y, Gotwals P, Koteliansky V, Rockey DC. Dose-dependent inhibition of hepatic fibrosis in mice by a TGF-beta soluble receptor: implications for antifibrotic therapy. Hepatology 2002; 35:1022-1030.
58. Verrecchia F, Mauviel A, Farge D. Transforming growth factor-beta signaling through the Smad proteins: role in systemic sclerosis. Autoimmun Rev 2006; 5:563-569.
59. Bonniaud P, Margetts PJ, Ask K, Flanders K, Gauldie J, Kolb M. TGFbeta and Smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 2005; 175:5390-5395.
60. Ignotz RA, Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem 1986; 261:4337-4345.
61. Sporn MB, Roberts AB, Wakefield LM, de Crombrugghe B. Some recent advances in the chemistry and biology of transforming growth factor-beta. J Cell Biol 1987; 105:1039-1045.
62. 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.
63. 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.
64. Romberger DJ. Fibronectin. Int J Biochem Cell Biol 1997; 29:939-943.
65. Limper AH, Roman J. Fibronectin. A versatile matrix protein with roles in thoracic development, repair and infection. Chest 1992; 101:1663-1673.
66. Samarakoon R, Higgins PJ. Integration of non-SMAD and SMAD signaling in TGF-beta1-induced plasminogen activator inhibitor type-1 gene expression in vascular smooth muscle cells. Thromb Haemost 2008; 100:976-983.
67. Hu B, Thirtamara-Rajamani KK, Sim H, Viapiano MS. Fibulin-3 is uniquely upregulated in malignant gliomas and promotes tumor cell motility and invasion. Mol Cancer Res 2009; 7:1756-1770.
68. Polgar A, Falus A, Koo E, Ujfalussy I, Sesztak M, Szuts I, Konrad K, Hodinka L, Bene E, Meszaros G, Ortutay Z, Farkas E, 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.
69. Ohara N. A putative role of versican in uterine leiomyomas. Clin Exp Obstet Gynecol 2009; 36:74-75.
70. Rogers R, Norian J, Malik M, Christman G, Abu-Asab M, Chen F, Korecki C, Iatridis J, Catherino WH, Tuan RS, Dhillon N, Leppert P, et al. Mechanical homeostasis is altered in uterine leiomyoma. Am J Obstet Gynecol 2008; 198:474.e1-474.e11.