A covalently dimerized recombinant human bone morphogenetic protein-15 variant identifies bone morphogenetic protein receptor type 1B as a key cell surface receptor on ovarian granulosa cells

Endocrinology

Volumn 153, Issue 3, 2012, Pages 1509-1518

  Pulkki, Minna M ^a   Mottershead, David G ^a,b   Pasternack, Arja H ^a   Muggalla, Pranuthi ^a   Ludlow, Helen ^c   Van Dinther, Maarten ^d   Myllymaa, Samu ^f   Koli, Katri ^e   Ten Dijke, Peter ^d   Laitinen, Mika ^a   Ritvos, Olli ^a  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c OXFORD BROOKES UNIVERSITY   (United Kingdom)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF HELSINKI   (Finland)

^f Biotechvisions Ltd   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CELL SURFACE RECEPTOR; DIMER; INHIBIN B; RECOMBINANT PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

ARTICLE; FEMALE FERTILITY; GRANULOSA CELL; HUMAN; HUMAN CELL; IODINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; DIMERIZATION; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; GRANULOSA CELLS; HOMOZYGOTE; HUMANS; OVARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 84857374828     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2010-1390     Document Type: Article

References (51)

1. Laitinen M, Vuojolainen K, Jaatinen R, Ketola I, Aaltonen J, Lehtonen E, Heikinheimo M, Ritvos O 1998 A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev 78:135-140 (Pubitemid 28566220)
2. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM 1998 The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 12:1809-1817 (Pubitemid 28544177)
3. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppä L, Louhio H, Tuuri T, Sjöberg J, Bützow R, Hovata O, Dale L, Ritvos O 1999 Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab 84:2744-2750 (Pubitemid 30642005)
4. McPherron AC, Lee SJ 1993 GDF-3 and GDF-9: two new members of the transforming growth factor-β superfamily containing a novel pattern of cysteines. J Biol Chem 268:3444-3449 (Pubitemid 23070981)
5. Bodin L, Di Pasquale E, Fabre S, Bontoux M, Monget P, Persani L, Mulsant P 2007 A novel mutation in the BMP15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology 148:393-400 (Pubitemid 46021472)
6. Di Pasquale E, Beck-Peccoz P, Persani L 2004 Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet 75:106-111 (Pubitemid 38801906)
7. Di Pasquale E, Rossetti R, Marozzi A, Bodega B, Borgato S, Cavallo L, Einaudi S, Radetti G, Russo G, Sacco M, Wasniewska M, Cole T, Beck-Peccoz P, Nelson LM, Persani L 2006 Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. J Clin Endocrinol Metab 91:1976-1979
8. Dixit H, Rao LK, Padmalatha VV, Kanakavalli M, Deenadayal M, Gupta N, Chakrabarty B, Singh L 2006 Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet 119:408-415
9. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O 2000 Mutations in an oocytederived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 25:279-283 (Pubitemid 30437312)
10. Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM 2004 Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod 70:900-909 (Pubitemid 38387698)
11. Laissue P, Christin-Maitre S, Touraine P, Kuttenn F, Ritvos O, Aittomaki K, Bourcigaux N, Jacquesson L, Bouchard P, Frydman R, Dewailly D, Reyss AC, Jeffery L, Bachelot A, Massin N, Fellous M, Veitia RA 2006 Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol 154:739-744 (Pubitemid 43810861)
12. Martinez-Royo A, Jurado JJ, Smulders JP, Martí JI, Alabart JL, Roche A, Fantova E, Bodin L, Mulsant P, Serrano M, Folch J, Calvo JH 2008 A deletion in the bone morphogenetic protein 15 gene causes sterility and increased prolificacy in Rasa Aragonesa sheep. Anim Genet 39:294-297
13. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM 1996 Growth differentiation facto-9 is required during early ovarian folliculogenesis. Nature 383:531-535 (Pubitemid 26346180)
14. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM 2001 Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 15:854-866 (Pubitemid 32510635)
15. Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, Chang RJ, Shimasaki S, Erickson GF 2002 Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab 87:1337-1344 (Pubitemid 36121106)
16. Massagué J 1998 TGF-β signal transduction. Annu Rev Biochem 67:753-791
17. Sun PD, Davies DR 1995 The cystine-knot growth-factor superfamily. Annu Rev Biophys Biomol Struct 24:269-291
18. Heldin CH, Miyazono K, ten Dijke P 1997 TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471 (Pubitemid 28013118)
19. Daopin S, Piez KA, Ogawa Y, Davies DR 1992 Crystal structure of transforming growth factor-β2: an unusual fold for the superfamily. Science 257:369-373
20. Griffith DL, Keck PC, Sampath TK, Rueger DC, Carlson WD 1996 Three-dimensional structure of recombinant human osteogenic protein 1: structural paradigm for the transforming growth factor β superfamily. Proc Natl Acad Sci USA 93:878-883 (Pubitemid 26041187)
21. Schlunegger MP, Cerletti N, Cox DA, McMaster GK, Schmitz A, Grütter MG 1992 Crystallization and preliminary x-ray analysis of recombinant human transforming growth factor β2. FEBS Lett 303:91-93
22. Pulkki MM, Myllymaa S, Pasternack A, Lun S, Ludlow H, Al-Qahtani A, Korchynskyi O, Groome N, Juengel JL, Kalkkinen N, Laitinen M, Ritvos O, Mottershead DG 2011 The bioactivity of human bone morphogenetic protein-15 is sensitive to C-terminal modification: characterization of the purified untagged processed mature region. Mol Cell Endocrinol 332:106-115
23. Myllymaa S, Pasternack A, Mottershead DG, Poutanen M, Pulkki MM, Pelliniemi LJ, Ritvos O, Laitinen MP 2010 Inhibition of oocyte growth factors in vivo modulates ovarian folliculogenesis in neonatal and immature mice. Reproduction 139:587-598
24. Korchynskyi O, ten Dijke P 2002 Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277:4883-4891 (Pubitemid 34968524)
25. Mottershead DG, Pulkki MM, Muggalla P, Pasternack A, Tolonen M, Myllymaa S, Korchynskyi O, Nishi Y, Yanase T, Lun S, Juengel JL, Laitinen M, Ritvos O 2008 Characterization of recombinant human growth differentiation factor-9 signaling in ovarian granulosa cells. Mol Cell Endocrinol 283:58-67
26. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, Pukac L, Löwik CW, ten Dijke P 2007 BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 120:964-972 (Pubitemid 46638511)
27. Li Q, Rajanahally S, Edson MA, Matzuk MM 2009 Stable expression and characterization of N-terminal tagged recombinant human bone morphogenetic protein 15. Mol Hum Reprod 15:779-788
28. Saito S, Yano K, Sharma S, McMahon HE, Shimasaki S 2008 Characterization of the post-translational modification of recombinant human BMP-15 mature protein. Protein Sci 17:362-370 (Pubitemid 351171848)
29. Moore RK, Otsuka F, Shimasaki S 2003 Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem 278:304-310 (Pubitemid 36043577)
30. Kaivo-Oja N, Bondestam J, Kämäräinen M, Koskimies J, Vitt U, Cranfield M, Vuojolainen K, Kallio JP, Olkkonen VM, Hayashi M, Moustakas A, Groome NP, ten Dijke P, Hsueh AJ, Ritvos O 2003 Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosa-luteal cells. J Clin Endocrinol Metab 88:755-762 (Pubitemid 36207819)
31. Kaivo-Oja N, Mottershead DG, Mazerbourg S, Myllymaa S, Duprat S, Gilchrist RB, Groome NP, Hsueh AJ, Ritvos O 2005 Adenoviral gene transfer allows Smad-responsive gene promoter analyses and delineation of type I receptor usage of transforming growth factor-βfamily ligands in cultured human granulosa luteal cells. J Clin Endocrinol Metab 90:271-278 (Pubitemid 40116668)
32. Roh JS, Bondestam J, Mazerbourg S, Kaivo-Oja N, Groome N, Ritvos O, Hsueh AJ 2003 Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 144:172-178 (Pubitemid 36076106)
33. Piek E, Franzén P, Heldin CH, ten Dijke P 1997 Characterization of a 60-kDa cell surface-associated transforming growth factor-β binding protein that can interfere with transforming growth factor-β receptor binding. J Cell Physiol 173:447-459 (Pubitemid 27481102)
34. Gilchrist RB, Ritter LJ, Cranfield M, Jeffery LA, Amato F, Scott SJ, Myllymaa S, Kaivo-Oja N, Lankinen H, Mottershead DG, Groome NP, Ritvos O 2004 Immunoneutralization of growth differentiation factor 9 reveals it partially accounts for mouse oocyte mitogenic activity. Biol Reprod 71:732-739 (Pubitemid 39108632)
35. McIntosh CJ, Lun S, Lawrence S, Western AH, McNatty KP, Juengel JL 2008 The proregion of mouse BMP15 regulates the cooperative interactions of BMP15 and GDF9. Biol Reprod 79:889-896
36. McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP, Ritvos O, Laitinen MP 2005 Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129:473-480 (Pubitemid 40542173)
37. Hussein TS, Thompson JG, Gilchrist RB 2006 Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 296:514-521 (Pubitemid 44189356)
38. Mottershead DG, Watson AJ 2009 Oocyte peptides as paracrine tools for ovarian stimulation and oocyte maturation. Mol Hum Reprod 15:789-794
39. Moore RK, Shimasaki S 2005 Molecular biology and physiological role of the oocyte factor, BMP-15. Mol Cell Endocrinol 234:67-73
40. Bondestam J, Kaivo-oja N, Kallio J, Groome N, Hydén-Granskog C, Fujii M, Moustakas A, Jalanko A, ten Dijke P, Ritvos O 2002 Engagement of activin and bone morphogenetic protein signaling pathway Smad proteins in the induction of inhibin B production in ovarian granulosa cells. Mol Cell Endocrinol 195:79-88 (Pubitemid 35287163)
41. Liao WX, Moore RK, Otsuka F, Shimasaki S 2003 Effect of intracellular interactions on the processing and secretion of bone morphogenetic protein-15 (BMP-15) and growth and differentiation factor-9. Implication of the aberrant ovarian phenotype of BMP-15 mutant sheep. J Biol Chem 278:3713-3719 (Pubitemid 36801096)
42. Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, Ritvos O, Hsueh AJ 2004 Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol 18:653-665 (Pubitemid 38328209)
43. Vitt UA, Mazerbourg S, Klein C, Hsueh AJ 2002 Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod 67:473-480 (Pubitemid 34803932)
44. McMahon HE, Sharma S, Shimasaki S 2008 Phosphorylation of bone morphogenetic protein-15 and growth and differentiation factor- 9 plays a critical role in determining agonistic or antagonistic functions. Endocrinology 149:812-817 (Pubitemid 351159362)
45. Edwards SJ, Reader KL, Lun S, Western A, Lawrence S, McNatty KP, Juengel JL 2008 The cooperative effect of growth and differentiation factor-9 and bone morphogenetic protein (BMP)-15 on granulosa cell function is modulated primarily through BMP receptor II. Endocrinology 149:1026-1030 (Pubitemid 351397961)
46. Demirhan O, Türkmen S, Schwabe GC, Soyupak S, Akgül E, Tastemir D, Karahan D, Mundlos S, Lehmann K 2005 A homozygous BMPR1B mutation causes a new subtype of acromesomelic chondrodysplasia with genital anomalies. J Med Genet 42:314-317 (Pubitemid 40523953)
47. Mulsant P, Lecerf F, Fabre S, Schibler L, Monget P, Lanneluc I, Pisselet C, Riquet J, Monniaux D, Callebaut I, Cribiu E, Thimonier J, Teyssier J, Bodin L, Cognié Y, Chitour N, Elsen JM 2001 Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc Natl Acad Sci USA 98:5104-5109 (Pubitemid 32397090)
48. Souza CJ, MacDougall C, MacDougall C, Campbell BK, McNeilly AS, Baird DT 2001 The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J Endocrinol 169:R1-R6 (Pubitemid 32447622)
49. Wilson T, Wu XY, Juengel JL, Ross IK, Lumsden JM, Lord EA, Dodds KG, Walling GA, McEwan JC, O'Connell AR, McNatty KP, Montgomery GW 2001 Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol Reprod 64:1225-1235 (Pubitemid 32239195)
50. Yi SE, LaPolt PS, Yoon BS, Chen JY, Lu JK, Lyons KM 2001 The type I BMP receptor BmprIB is essential for female reproductive function. Proc Natl Acad Sci USA 98:7994-7999 (Pubitemid 32642675)
51. Crawford JL, Heath DA, Reader KL, Quirke LD, Hudson NL, Juengel JL, McNatty KP 2011 Oocytes in sheep homozygous for a mutation in bone morphogenetic protein receptor 1B express lower mRNA levels of bone morphogenetic protein 15 but not growth differentiation factor 9. Reproduction 142:53-61