Differential activation of noncanonical SMAD2/SMAD3 signaling by bone morphogenetic proteins causes disproportionate induction of hyaluronan production in immortalized human granulosa cells

Molecular and Cellular Endocrinology

Volumn 428, Issue , 2016, Pages 17-27

  Zhang, Han ^a,b   Tian, Shen ^a,c   Klausen, Christian ^a   Zhu, Hua ^a   Liu, Ruizhi ^b   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b JILIN UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

BMP; HAS2; Human granulosa cell; Hyaluronan; SMAD1 5 8; SMAD2; SMAD3

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; HYALURONAN SYNTHASE; HYALURONIC ACID; MESSENGER RNA; OSTEOGENIC PROTEIN 1; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SMALL INTERFERING RNA; SYNTHETASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; GLUCURONOSYLTRANSFERASE; HAS2 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN, HUMAN; SMAD3 PROTEIN, HUMAN; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; CONTROLLED STUDY; GENETIC TRANSFECTION; GRANULOSA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMORTALIZED CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECTS; FEMALE; LUTEAL CELL; METABOLISM; PHOSPHORYLATION;

BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; FEMALE; GLUCURONOSYLTRANSFERASE; GRANULOSA CELLS; HUMANS; HYALURONIC ACID; LUTEAL CELLS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; UP-REGULATION;

EID: 84989257471     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2016.03.016     Document Type: Article

References (51)

1. Abir R., Ben-Haroush A., Melamed N., Felz C., Krissi H., Fisch B. Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertil. Steril. 2008, 89:1430-1440.
2. Caixeta E.S., Sutton-McDowall M.L., Gilchrist R.B., Thompson J.G., Price C.A., Machado M.F., Lima P.F., Buratini J. Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus-oocyte complexes. Reproduction 2013, 146:27-35.
3. Camenisch T.D., Spicer A.P., Brehm-Gibson T., Biesterfeldt J., Augustine M.L., Calabro A., Kubalak S., Klewer S.E., McDonald J.A. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J. Clin. Investig. 2000, 106:349-360.
4. Chang H.M., Cheng J.C., Leung P.C. Theca-derived BMP4 and BMP7 down-regulate connexin43 expression and decrease gap junction intercellular communication activity in immortalized human granulosa cells. J. Clin. Endocrinol. Metab. 2013, 98:E437-E445.
5. Chang H.M., Klausen C., Leung P.C. Antimullerian hormone inhibits follicle-stimulating hormone-induced adenylyl cyclase activation, aromatase expression, and estradiol production in human granulosa-lutein cells. Fertil. Steril. 2013, 100. 585-592 e581.
6. Chang H.M., Cheng J.C., Taylor E., Leung P.C. Oocyte-derived BMP15 but not GDF9 down-regulates connexin43 expression and decreases gap junction intercellular communication activity in immortalized human granulosa cells. Mol. Hum. Reprod. 2014, 20:373-383.
7. Chen L., Russell P.T., Larsen W.J. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol. Reprod. Dev. 1993, 34:87-93.
8. Chen Y.G., Hata A., Lo R.S., Wotton D., Shi Y., Pavletich N., Massague J. Determinants of specificity in TGF-beta signal transduction. Genes Dev. 1998, 12:2144-2152.
9. Dragovic R.A., Ritter L.J., Schulz S.J., Amato F., Thompson J.G., Armstrong D.T., Gilchrist R.B. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol. Reprod. 2007, 76:848-857.
10. Drummond A.E. TGFbeta signalling in the development of ovarian function. Cell Tissue Res. 2005, 322:107-115.
11. Dube J.L., Wang P., Elvin J., Lyons K.M., Celeste A.J., Matzuk M.M. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 1998, 12:1809-1817.
12. Elvin J.A., Clark A.T., Wang P., Wolfman N.M., Matzuk M.M. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 1999, 13:1035-1048.
13. Elvin J.A., Yan C., Matzuk M.M. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell. Endocrinol. 2000, 159:1-5.
14. Eppig J.J. FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature 1979, 281:483-484.
15. Erickson G.F., Shimasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol. 2003, 1:9.
16. Fatehi A.N., van den Hurk R., Colenbrander B., Daemen A.J., van Tol H.T., Monteiro R.M., Roelen B.A., Bevers M.M. Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 2005, 63:872-889.
17. Fukui Y. Effect of follicle cells on the acrosome reaction, fertilization, and developmental competence of bovine oocytes matured in vitro. Mol. Reprod. Dev. 1990, 26:40-46.
18. Fulop C., Salustri A., Hascall V.C. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch. Biochem. Biophys. 1997, 337:261-266.
19. Gilchrist R.B., Ritter L.J. Differences in the participation of TGFB superfamily signalling pathways mediating porcine and murine cumulus cell expansion. Reproduction 2011, 142:647-657.
20. Glister C., Richards S.L., Knight P.G. Bone morphogenetic proteins (BMP) -4, -6, and -7 potently suppress basal and luteinizing hormone-induced androgen production by bovine theca interna cells in primary culture: could ovarian hyperandrogenic dysfunction be caused by a defect in thecal BMP signaling?. Endocrinology 2005, 146:1883-1892.
21. Hao J., Ho J.N., Lewis J.A., Karim K.A., Daniels R.N., Gentry P.R., Hopkins C.R., Lindsley C.W., Hong C.C. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem. Biol. 2010, 5:245-253.
22. Holtzhausen A., Golzio C., How T., Lee Y.H., Schiemann W.P., Katsanis N., Blobe G.C. Novel bone morphogenetic protein signaling through Smad2 and Smad3 to regulate cancer progression and development. FASEB J. 2014, 28:1248-1267.
23. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 2005, 118:5257-5268.
24. Inman G.J., Nicolas F.J., Callahan J.F., Harling J.D., Gaster L.M., Reith A.D., Laping N.J., Hill C.S. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 2002, 62:65-74.
25. Itano N., Kimata K. Mammalian hyaluronan synthases. IUBMB Life 2002, 54:195-199.
26. Kayamori T., Kosaka N., Miyamoto A., Shimizu T. The differential pathways of bone morphogenetic protein (BMP)-4 and -7 in the suppression of the bovine granulosa cell apoptosis. Mol. Cell. Biochem. 2009, 323:161-168.
27. Li Q., Pangas S.A., Jorgez C.J., Graff J.M., Weinstein M., Matzuk M.M. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol. Cell. Biol. 2008, 28:7001-7011.
28. Lie B.L., Leung E., Leung P.C., Auersperg N. Long-term growth and steroidogenic potential of human granulosa-lutein cells immortalized with SV40 large T antigen. Mol. Cell. Endocrinol. 1996, 120:169-176.
29. Lin Z.L., Li Y.H., Xu Y.N., Wang Q.L., Namgoong S., Cui X.S., Kim N.H. Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod. Domest. Anim. 2014, 49:219-227.
30. Mack J.A., Feldman R.J., Itano N., Kimata K., Lauer M., Hascall V.C., Maytin E.V. Enhanced inflammation and accelerated wound closure following tetraphorbol ester application or full-thickness wounding in mice lacking hyaluronan synthases Has1 and Has3. J. Investig. Dermatol. 2012, 132:198-207.
31. Mueller T.D., Nickel J. Promiscuity and specificity in BMP receptor activation. FEBS Lett. 2012, 586:1846-1859.
32. Murakami M., Kawachi H., Ogawa K., Nishino Y., Funaba M. Receptor expression modulates the specificity of transforming growth factor-beta signaling pathways. Genes Cells 2009, 14:469-482.
33. Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem. 2000, 275:39523-39528.
34. Otsuka F., Moore R.K., Shimasaki S. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J. Biol. Chem. 2001, 276:32889-32895.
35. Peng J., Li Q., Wigglesworth K., Rangarajan A., Kattamuri C., Peterson R.T., Eppig J.J., Thompson T.B., Matzuk M.M. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E776-E785.
36. Pienimaki J.P., Rilla K., Fulop C., Sironen R.K., Karvinen S., Pasonen S., Lammi M.J., Tammi R., Hascall V.C., Tammi M.I. Epidermal growth factor activates hyaluronan synthase 2 in epidermal keratinocytes and increases pericellular and intracellular hyaluronan. J. Biol. Chem. 2001, 276:20428-20435.
37. Russell D.L., Salustri A. Extracellular matrix of the cumulus-oocyte complex. Semin. Reprod. Med. 2006, 24:217-227.
38. Salustri A., Ulisse S., Yanagishita M., Hascall V.C. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J. Biol. Chem. 1990, 265:19517-19523.
39. Schoenfelder M., Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol. Reprod. 2003, 69:269-277.
40. Shimasaki S., Zachow R.J., Li D., Kim H., Iemura S., Ueno N., Sampath K., Chang R.J., Erickson G.F. A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7282-7287.
41. Shimizu T., Kayamori T., Murayama C., Miyamoto A. Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptosis via different pathways: BMP-4 via PI3K/PDK-1/Akt and BMP-7 via PI3K/PDK-1/PKC. Biochem. Biophys. Res. Commun. 2012, 417:869-873.
42. Sugiura K., Su Y.Q., Eppig J.J. Does bone morphogenetic protein 6 (BMP6) affect female fertility in the mouse?. Biol. Reprod. 2010, 83:997-1004.
43. Takahashi N, Tarumi W, Ishizuka B. Involvement of hyaluronan synthesis in ovarian follicle growth in rats. Reproduction 147:189-197.
44. Tunjung W.A., Yokoo M., Hoshino Y., Miyake Y., Kadowaki A., Sato E. Effect of hyaluronan to inhibit caspase activation in porcine granulosa cells. Biochem. Biophys. Res. Commun. 2009, 382:160-164.
45. Varnosfaderani Sh R., Ostadhosseini S., Hajian M., Hosseini S.M., Khashouei E.A., Abbasi H., Hosseinnia P., Nasr-Esfahani M.H. Importance of the GDF9 signaling pathway on cumulus cell expansion and oocyte competency in sheep. Theriogenology 2013, 80:470-478.
46. Wang Y., Ho C.C., Bang E., Rejon C.A., Libasci V., Pertchenko P., Hebert T.E., Bernard D.J. Bone morphogenetic protein 2 stimulates noncanonical SMAD2/3 signaling via the BMP type 1A receptor in gonadotrope-like cells: implications for FSH synthesis. Endocrinology 2014, 155:1970-1981.
47. Yan C., Wang P., DeMayo J., DeMayo F.J., Elvin J.A., Carino C., Prasad S.V., Skinner S.S., Dunbar B.S., Dube J.L., Celeste A.J., Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15:854-866.
48. Yoshino O., McMahon H.E., Sharma S., Shimasaki S. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10678-10683.
49. Yu P.B., Hong C.C., Sachidanandan C., Babitt J.L., Deng D.Y., Hoyng S.A., Lin H.Y., Bloch K.D., Peterson R.T. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 2008, 4:33-41.
50. Zhang H., Klausen C., Zhu H., Chang H.M., Leung P.C. BMP4 and BMP7 suppress StAR and progesterone production via ALK3 and SMAD1/5/8-SMAD4 in human granulosa-lutein cells. Endocrinology 2015, 156:4269-4280.
51. Zhuo L., Kimata K. Cumulus oophorus extracellular matrix: its construction and regulation. Cell Struct. Funct. 2001, 26:189-196.