Linkage of regulators of TGF-β activity in the fetal ovary to polycystic ovary syndrome

FASEB Journal

Volumn 25, Issue 7, 2011, Pages 2256-2265

  Hatzirodos, Nicholas ^a   Bayne, Rosemary A ^c   Irving Rodgers, Helen F ^a,h   Hummitzsch, Katja ^a   Sabatier, Laetitia ^d   Lee, Sam ^a   Bonner, Wendy ^a   Gibson, Mark A ^b   Rainey, William E ^e   Carr, Bruce R ^f   Mason, Helen D ^g   Reinhardt, Dieter P ^d   Anderson, Richard A ^c   Rodgers, Raymond J ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d MCGILL UNIVERSITY   (Canada)

^e MEDICAL COLLEGE OF GEORGIA   (United States)

^f UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^g ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^h QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Fibrillin; Latent transforming growth factor binding protein

Indexed keywords

FIBRILLIN; FIBRILLIN 1; FIBRILLIN 2; FIBRILLIN 3; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 1; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 2; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 3; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 4; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG;

ADULT; ANIMAL TISSUE; ARTICLE; DISEASE PREDISPOSITION; FEMALE; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; OVARY DEVELOPMENT; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; CATTLE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; LATENT TGF-BETA BINDING PROTEINS; MICROFILAMENT PROTEINS; OVARIAN FOLLICLE; OVARY; POLYCYSTIC OVARY SYNDROME; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

BOVINAE;

EID: 79960162693     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-181099     Document Type: Article

References (49)

1. Azziz, R., Marin, C., Hoq, L., Badamgarav, E., and Song, P. (2005) Health care-related economic burden of the polycystic ovary syndrome during the reproductive life span. J. Clin. Endocrinol. Metab. 90, 4650-4658
2. Padmanabhan, V. (2009) Polycystic ovary syndrome-"a riddle wrapped in a mystery inside an enigma." J. Clin. Endocrinol. Metab. 94, 1883-1885
3. Norman, R. J., Dewailly, D., Legro, R. S., and Hickey, T. E. (2007) Polycystic ovary syndrome. Lancet 370, 685-697
4. Diamanti-Kandarakis, E., Kandarakis, H., and Legro, R. S. (2006) The role of genes and environment in the etiology of PCOS. Endocrine 30, 19-26 (Pubitemid 46020326)
5. Veiga-Lopez, A., Ye, W., Phillips, D. J., Herkimer, C., Knight, P. G., and Padmanabhan, V. (2008) Developmental programming: deficits in reproductive hormone dynamics and ovulatory outcomes in prenatal, testosterone-treated sheep. Biol. Reprod. 78, 636-647
6. Abbott, D. H., Barnett, D. K., Bruns, C. M., and Dumesic, D. A. (2005) Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum. Reprod. Update 11, 357-374
7. Webber, L. J., Stubbs, S., Stark, J., Trew, G. H., Margara, R., Hardy, K., and Franks, S. (2003) Formation and early development of follicles in the polycystic ovary. Lancet 362, 1017-1021 (Pubitemid 37186878)
8. Forsdike, R. A., Hardy, K., Bull, L., Stark, J., Webber, L. J., Stubbs, S., Robinson, J. E., and Franks, S. (2007) Disordered follicle development in ovaries of prenatally androgenized ewes. J. Endocrinol. 192, 421-428 (Pubitemid 46444443)
9. Hague, W. M., Adams, J., Rodda, C., Brook, C. G., de Bruyn, R., Grant, D. B., and Jacobs, H. S. (1990) The prevalence of polycystic ovaries in patients with congenital adrenal hyperplasia and their close relatives. Clin. Endocrinol. (Oxf.) 33, 501-510
10. Barnes, R. B., Rosenfield, R. L., Ehrmann, D. A., Cara, J. F., Cuttler, L., Levitsky, L. L., and Rosenthal, I. M. (1994) Ovarian hyperandrogynism as a result of congenital adrenal virilizing disorders: evidence for perinatal masculinization of neuroendocrine function in women. J. Clin. Endocrinol. Metab. 79, 1328-1333
11. Amato, P., and Simpson, J. L. (2004) The genetics of polycystic ovary syndrome. Best Pract. Res. Clin. Obstet. Gynaecol. 18, 707-718
12. Legro, R. S., Bentley-Lewis, R., Driscoll, D., Wang, S. C., and Dunaif, A. (2002) Insulin resistance in the sisters of women with polycystic ovary syndrome: association with hyperandrogenemia rather than menstrual irregularity. J. Clin. Endocrinol. Metab. 87, 2128-2133
13. Yildiz, B. O., Yarali, H., Oguz, H., and Bayraktar, M. (2003) Glucose intolerance, insulin resistance, and hyperandrogenemia in first degree relatives of women with polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 88, 2031-2036
14. Urbanek, M., Sam, S., Legro, R. S., and Dunaif, A. (2007) Identification of a polycystic ovary syndrome susceptibility variant in fibrillin-3 and association with a metabolic phenotype. J. Clin. Endocrinol. Metab. 92, 4191-4198
15. Urbanek, M., Legro, R. S., Driscoll, D. A., Azziz, R., Ehrmann, D. A., Norman, R. J., Strauss, J. F., 3rd, Spielman, R. S., and Dunaif, A. (1999) Thirty-seven candidate genes for polycystic ovary syndrome: strongest evidence for linkage is with follistatin. Proc. Natl. Acad. Sci. U. S. A. 96, 8573-8578
16. Stewart, D. R., Dombroski, B. A., Urbanek, M., Ankener, W., Ewens, K. G., Wood, J. R., Legro, R. S., Strauss, J. F., 3rd, Dunaif, A., and Spielman, R. S. (2006) Fine mapping of genetic susceptibility to polycystic ovary syndrome on chromosome 19p13.2 and tests for regulatory activity. J. Clin. Endocrinol. Metab. 91, 4112-4117
17. Thompson, T. B., Lerch, T. F., Cook, R. W., Woodruff, T. K., and Jardetzky, T. S. (2005) The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 9, 535-543 (Pubitemid 41430736)
18. Ramirez, F., and Pereira, L. (1999) The fibrillins. Int. J. Biochem. Cell Biol. 31, 255-259
19. Kielty, C. M., Sherratt, M. J., and Shuttleworth, C. A. (2002) Elastic fibres. J. Cell Sci. 115, 2817-2828
20. Hirani, R., Hanssen, E., and Gibson, M. A. (2007) LTBP-2 specifically interacts with the amino-terminal region of fibrillin- 1 and competes with LTBP-1 for binding to this microfibrillar protein. Matrix Biol. 26, 213-223
21. LeClair, R., and Lindner, V. (2007) The role of collagen triple helix repeat containing 1 in injured arteries, collagen expression, and transforming growth factor beta signaling. Trends Cardiovasc. Med. 17, 202-205
22. Christner, P. J., and Ayitey, S. (2006) Extracellular matrix containing mutated fibrillin-1 (Fbn1) down regulates Col1 Col1a2, Col3a1, Col5a1, and Col5a2 mRNA levels in Tsk/+ and Tsk/Tsk embryonic fibroblasts. Amino Acids 30, 445-451 (Pubitemid 43886905)
23. Verrecchia, F., and Mauviel, A. (2004) TGF-beta and TNF-alpha: antagonistic cytokines controlling type I collagen gene expression. Cell. Signal. 16, 873-880
24. Govinden, R., and Bhoola, K. D. (2003) Genealogy, expression, and cellular function of transforming growth factor-beta. Pharmacol. Ther. 98, 257-265
25. Khan, R., and Sheppard, R. (2006) Fibrosis in heart disease: understanding the role of transforming growth factor-beta in cardiomyopathy, valvular disease and arrhythmia. Immunology 118, 10-24
26. Chapman, H. A. (2004) Disorders of lung matrix remodeling. J. Clin. Invest. 113, 148-157
27. Hetzel, M., Bachem, M., Anders, D., Trischler, G., and Faehling, M. (2005) Different effects of growth factors on proliferation and matrix production of normal and fibrotic human lung fibroblasts. Lung 183, 225-237 (Pubitemid 41428095)
28. Kisseleva, T., and Brenner, D. A. (2007) Role of hepatic stellate cells in fibrogenesis and the reversal of fibrosis. J. Gastroenterol. Hepatol. 22(Suppl. 1), S73-S78
29. Prud'homme, G. J. (2007) Pathobiology of transforming growth factor beta in cancer, fibrosis and immunologic disease, and therapeutic considerations. Lab. Invest. 87, 1077-1091
30. Bottinger, E. P. (2007) TGF-beta in renal injury and disease. Semin. Nephrol. 27, 309-320
31. Hughesdon, P. E. (1982) Morphology and morphogenesis of the Stein-Leventhal ovary and of so-called "hyperthecosis." Obstet. Gynecol. Surv. 37, 59-77
32. Nelson, V. L., Legro, R. S., Strauss, J. F., 3rd, and McAllister, J. M. (1999) Augmented androgen production is a stable steroidogenic phenotype of propagated theca cells from polycystic ovaries. Mol Endocrinol 13, 946-957
33. Nelson, V. L., Qin, K. N., Rosenfield, R. L., Wood, J. R., Penning, T. M., Legro, R. S., Strauss, J. F., 3rd, and McAllister, J. M. (2001) The biochemical basis for increased testosterone production in theca cells propagated from patients with polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 86, 5925-5933
34. Prodoehl, M. J., Irving-Rodgers, H. F., Bonner, W., Sullivan, T. M., Micke, G. C., Gibson, M. A., Perry, V. E., and Rodgers, R. J. (2009) Fibrillins and latent TGFβ binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol. Cell. Endocrinol. 307, 133-144
35. Prodoehl, M. J., Hatzirodos, N., Irving-Rodgers, H. F., Zhao, Z. Z., Painter, J. N., Hickey, T. E., Gibson, M. A., Rainey, W. E., Carr, B. R., Mason, H. D., Norman, R. J., Montgomery, G. W., and Rodgers, R. J. (2009) Genetic and gene expression analyses of the polycystic ovary syndrome candidate gene fibrillin-3 and other fibrillin family members in human ovaries. Mol. Hum. Reprod. 15, 829-841
36. Jordan, C. D., Bohling, S. D., Charbonneau, N. L., and Sakai, L. Y. (2010) Fibrillins in adult human ovary and polycystic ovary syndrome: is fibrillin-3 affected in PCOS? J. Histochem. Cytochem. 58, 903-915
37. Corson, G. M., Charbonneau, N. L., Keene, D. R., and Sakai, L. Y. (2004) Differential expression of fibrillin-3 adds to microfibril variety in human and avian, but not rodent, connective tissues. Genomics 83, 461-472
38. Sabatier, L., Miosge, N., Hubmacher, D., Lin, G., Davis, E. C., and Reinhardt, D. P. (2010) Fibrillin-3 expression in human development. Matrix Biol. 21, 21
39. Russe, I. (1983) Oogenesis in cattle and sheep. Bibl. Anat. 24, 77-92
40. Prodoehl, M. J., Irving-Rodgers, H. F., Bonner, W. M., Sullivan, T. M., Micke, G. C., Gibson, M. A., Perry, V. E., and Rodgers, R. J. (2009) Fibrillins and latent TGFbeta binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol. Cell. Endocrinol. 307, 133-141
41. Sullivan, T. M., Micke, G. C., Greer, R. M., Irving-Rodgers, H. F., Rodgers, R. J., and Perry, V. E. (2009) Dietary manipulation of Bos indicus x heifers during gestation affects the reproductive development of their heifer calves.
42. Coutts, S. M., Childs, A. J., Fulton, N., Collins, C., Bayne, R. A., McNeilly, A. S., and Anderson, R. A. (2008) Activin signals via SMAD2/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression. Dev. Biol. 314, 189-199
43. Friel, A., Houghton, J. A., Glennon, M., Lavery, R., Smith, T., Nolan, A., and Maher, M. (2002) A preliminary report on the implication of RT-PCR detection of DAZ, RBMY1, USP9Y and protamine-2 mRNA in testicular biopsy samples from azoospermic men. Int. J. Androl. 25, 59-64
44. Mason, H. D., Willis, D. S., Beard, R. W., Winston, R. M., Margara, R., and Franks, S. (1994) Estradiol production by granulosa cells of normal and polycystic ovaries: relationship to menstrual cycle history and concentrations of gonadotropins and sex steroids in follicular fluid. J. Clin. Endocrinol. Metab. 79, 1355-1360
45. Kenney, M. C., Zorapapel, N., Atilano, S., Chwa, M., Ljubimov, A., and Brown, D. (2003) Insulin-like growth factor-I (IGF-I) and transforming growth factor-beta (TGF-beta) modulate tenascin- C and fibrillin-1 in bullous keratopathy stromal cells in vitro. Exp. Eye Res. 77, 537-546
46. Wen, Y., Polan, M. L., and Chen, B. (2006) Do extracellular matrix protein expressions change with cyclic reproductive hormones in pelvic connective tissue from women with stress urinary incontinence? Hum. Reprod. 21, 1266-1273
47. Son, E. D., Lee, J. Y., Lee, S., Kim, M. S., Lee, B. G., Chang, I. S., and Chung, J. H. (2005) Topical application of 17beta-estradiol increases extracellular matrix protein synthesis by stimulating tgf-Beta signaling in aged human skin in vivo. J. Invest. Dermatol. 124, 1149-1161
48. Natoli, A. K., Medley, T. L., Ahimastos, A. A., Drew, B. G., Thearle, D. J., Dilley, R. J., and Kingwell, B. A. (2005) Sex steroids modulate human aortic smooth muscle cell matrix protein deposition and matrix metalloproteinase expression. Hypertension 46, 1129-1134
49. Samuel, C. S., Sakai, L. Y., and Amento, E. P. (2003) Relaxin regulates fibrillin 2, but not fibrillin-1, mRNA and protein expression by human dermal fibroblasts and murine fetal skin. Arch. Biochem. Biophys. 411, 47-55