BMP15 c.-9C>G promoter sequence variant may contribute to the cause of non-syndromic premature ovarian failure

Reproductive BioMedicine Online

Volumn 29, Issue 5, 2014, Pages 627-633

  Fonseca, Dora Janeth ^a,b   Ortega Recalde, Oscar ^a   Esteban Perez, Clara ^c   Moreno Ortiz, Harold ^c   Patiño, Liliana Catherine ^a   Bermúdez, Olga María ^a   Ortiz, Angela María ^a   Restrepo, Carlos M ^a,b   Lucena, Elkin ^a   Laissue, Paul ^a,b  

^a UNIVERSIDAD DEL ROSARIO   (Colombia)

^b Genética Molecular de Colombia Ltda   (Colombia)

^c Reproductive Immunology Division   (Colombia)

Author keywords

bioinformatics; BMP15; female infertility; PITX1; premature ovarian failure

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX1; UNCLASSIFIED DRUG; BMP15 PROTEIN, HUMAN; HOMEOBOX PROTEIN PITX1; LUCIFERASE; PAIRED BOX TRANSCRIPTION FACTOR;

ADULT; ALLELE; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOINFORMATICS; COMPUTER MODEL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUCIFERASE ASSAY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PREMATURE OVARIAN FAILURE; PROMOTER REGION; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSACTIVATION; ANIMAL; BIOLOGY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; METABOLISM; MUTATION; OVARY; PHENOTYPE; TRANSCRIPTION INITIATION;

ALLELES; ANIMALS; BINDING SITES; BONE MORPHOGENETIC PROTEIN 15; CERCOPITHECUS AETHIOPS; COMPUTATIONAL BIOLOGY; COS CELLS; FEMALE; GENETIC VARIATION; HUMANS; LUCIFERASES; MICE; MUTATION; OVARY; PAIRED BOX TRANSCRIPTION FACTORS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PRIMARY OVARIAN INSUFFICIENCY; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84908454917     PISSN: 14726483     EISSN: 14726491     Source Type: Journal    
DOI: 10.1016/j.rbmo.2014.07.018     Document Type: Article

References (53)

1. Aaltonen J., Laitinen M.P., Vuojolainen K., Jaatinen R., Horelli-Kuitunen N., Seppä L., Louhio H., Tuuri T., Sjöberg J., Bützow R., Hovata O., Dale L., and Ritvos O. 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 1999 2744 2750
2. Abir R., and Fisch B. Invited commentary: a single nucleotide polymorphism in BMP15 is associated with high response to controlled ovarian hyperstimulation Reprod. Biomed. Online 23 2011 77 80
3. Aittomäki K., Lucena J.L., Pakarinen P., Sistonen P., Tapanainen J., Gromoll J., Kaskikari R., Sankila E.M., Lehväslaiho H., Engel A.R., Nieschlag E., Huhtaniemi I., and de la Chapelle A. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure Cell 82 1995 959 968
4. Beau I., Touraine P., Meduri G., Gougeon A., Desroches A., Matuchansky C., Milgrom E., Kuttenn F., and Misrahi M. A novel phenotype related to partial loss of function mutations of the follicle stimulating hormone receptor J. Clin. Invest 102 1998 1352 1359
5. Bodensteiner K.J., Clay C.M., Moeller C.L., and Sawyer H.R. Molecular cloning of the ovine Growth/Differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries Biol. Reprod 60 1999 381 386
6. Bragdon B., Moseychuk O., Saldanha S., King D., Julian J., and Nohe A. Bone morphogenetic proteins: a critical review Cell. Signal 23 2011 609 620
7. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., and Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites Bioinformatics 21 2005 2933 2942
8. Chang H., Brown C.W., and Matzuk M.M. Genetic analysis of the mammalian transforming growth factor-beta superfamily Endocr. Rev 23 2002 787 823
9. Conway G.S. Premature ovarian failure Br. Med. Bull 56 2000 643 649
10. Coulam C.B., Adamson S.C., and Annegers J.F. Incidence of premature ovarian failure Obstet. Gynecol 67 1986 604 606
11. Di Pasquale E., Beck-Peccoz P., and Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene Am. J. Hum. Genet 75 2004 106 111
12. Dixit H., Rao L.K., Padmalatha V. V, Kanakavalli M., Deenadayal M., Gupta N., Chakrabarty B., and Singh L. Missense mutations in the BMP15 gene are associated with ovarian failure Hum. Genet 119 2006 408 415
13. Doherty E., Pakarinen P., Tiitinen A., Kiilavuori A., Huhtaniemi I., Forrest S., and Aittomäki K. A Novel mutation in the FSH receptor inhibiting signal transduction and causing primary ovarian failure J. Clin. Endocrinol. Metab 87 2002 1151 1155
14. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., and Matzuk M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis Nature 383 1996 531 535
15. Dube J.L., Wang P., Elvin J., Lyons K.M., Celeste A.J., and Matzuk M.M. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes Mol. Endocrinol 12 1998 1809 1817
16. Galloway S.M., McNatty K.P., Cambridge L.M., Laitinen M.P., Juengel J.L., Jokiranta T.S., McLaren R.J., Luiro K., Dodds K.G., Montgomery G.W., Beattie A.E., Davis G.H., and Ritvos O. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner Nat. Genet 25 2000 279 283
17. Gónzalez A., Ramírez-Lorca R., Calatayud C., Mendoza N., Ruiz A., Sáez M.E., and Morón F.J. Association of genetic markers within the BMP15 gene with anovulation and infertility in women with polycystic ovary syndrome Fertil. Steril 90 2008 447 449
18. Gurnett C.A., Alaee F., Kruse L.M., Desruisseau D.M., Hecht J.T., Wise C.A., Bowcock A.M., and Dobbs M.B. Asymmetric lower-limb malformations in individuals with homeobox PITX1 gene mutation Am. J. Hum. Genet 83 2008 616 622
19. Hanevik H.I., Hilmarsen H.T., Skjelbred C.F., Tanbo T., and Kahn J.A. A single nucleotide polymorphism in BMP15 is associated with high response to ovarian stimulation Reprod. Biomed. Online 23 2011 97 104
20. Hanrahan J.P., Gregan S.M., Mulsant P., Mullen M., Davis G.H., Powell R., and Galloway S.M. 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 2004 900 909
21. Hashimoto O., Moore R.K., and Shimasaki S. Posttranslational processing of mouse and human BMP-15: potential implication in the determination of ovulation quota Proc. Natl Acad. Sci. U.S.A. 102 2005 5426 5431
22. Juengel J.L., and McNatty K.P. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development Hum. Reprod. Update 11 2005 143 160
23. Kedem A., Fisch B., Garor R., Ben-Zaken A., Gizunterman T., Felz C., Ben-Haroush A., Kravarusic D., and Abir R. Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9 J. Clin. Endocrinol. Metab 96 2011 E1246 E1254
24. Laissue P., Vinci G., Veitia R.A., and Fellous M. Recent advances in the study of genes involved in non-syndromic premature ovarian failure Mol. Cell. Endocrinol 282 2008 101 111
25. Laitinen M., Vuojolainen K., Jaatinen R., Ketola I., Aaltonen J., Lehtonen E., Heikinheimo M., and Ritvos O. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis Mech. Dev 78 1998 135 140
26. Latronico A.C., Anasti J., Arnhold I.J., Rapaport R., Mendonca B.B., Bloise W., Castro M., Tsigos C., and Chrousos G.P. Brief report: testicular and ovarian resistance to luteinizing hormone caused by inactivating mutations of the luteinizing hormone-receptor gene N. Engl. J. Med 334 1996 507 512
27. Liao W.X., Moore R.K., Otsuka F., and Shimasaki S. 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 2003 3713 3719
28. Liao W.X., Moore R.K., and Shimasaki S. Functional and molecular characterization of naturally occurring mutations in the oocyte-secreted factors bone morphogenetic protein-15 and growth and differentiation factor-9 J. Biol. Chem 279 2004 17391 17396
29. Lourenço D., Brauner R., Lin L., De Perdigo A., Weryha G., Muresan M., Boudjenah R., Guerra-Junior G., Maciel-Guerra A.T., Achermann J.C., McElreavey K., and Bashamboo A. Mutations in NR5A1 associated with ovarian insufficiency N. Engl. J. Med 360 2009 1200 1210
30. Luborsky J.L., Meyer P., Sowers M.F., Gold E.B., and Santoro N. Premature menopause in a multi-ethnic population study of the menopause transition Hum. Reprod 18 2003 199 206
31. Massagué J., Seoane J., and Wotton D. Smad transcription factors Genes Dev 19 2005 2783 2810
32. Matzuk M.M., and Burns K.H. Genetics of mammalian reproduction: modeling the end of the germline Annu. Rev. Physiol 74 2012 503 528
33. Matzuk M.M., and Lamb D.J. Genetic dissection of mammalian fertility pathways Nat. Cell Biol 4 Suppl. 2002 s41 s49
34. Matzuk M.M., and Lamb D.J. The biology of infertility: research advances and clinical challenges Nat. Med 14 2008 1197 1213
35. McMahon H.E., Hashimoto O., Mellon P.L., and Shimasaki S. Oocyte-specific overexpression of mouse bone morphogenetic protein-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice Endocrinology 149 2008 2807 2815
36. Moore R.K., Otsuka F., and Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells J. Biol. Chem 278 2003 304 310
37. Morón F.J., de Castro F., Royo J.L., Montoro L., Mira E., Sáez M.E., Real L.M., González A., Mañes S., and Ruiz A. Bone morphogenetic protein 15 (BMP15) alleles predict over-response to recombinant follicle stimulation hormone and iatrogenic ovarian hyperstimulation syndrome (OHSS) Pharmacogenet. Genomics 16 2006 485 495
38. Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F., and Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions J. Biol. Chem 275 2000 39523 39528
39. Otsuka F., McTavish K.J., and Shimasaki S. Integral role of GDF-9 and BMP-15 in ovarian function Mol. Reprod. Dev 78 2011 9 21
40. Pangas S.A., and Matzuk M.M. Genetic models for transforming growth factor beta superfamily signaling in ovarian follicle development Mol. Cell. Endocrinol 225 2004 83 91
41. Peng J., Li Q., Wigglesworth K., Rangarajan A., Kattamuri C., Peterson R.T., Eppig J.J., Thompson T.B., and 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. 110 2013 E776 E785
42. Pulkki M.M., Mottershead D.G., Pasternack A.H., Muggalla P., Ludlow H., van Dinther M., Myllymaa S., Koli K., ten Dijke P., Laitinen M., and Ritvos O. 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 153 2012 1509 1518
43. Quandt K., Frech K., Karas H., Wingender E., and Werner T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data Nucleic Acids Res 23 1995 4878 4884
44. Quentien M.H., Barlier A., Franc J.L., Pellegrini I., Brue T., and Enjalbert A. Pituitary transcription factors: from congenital deficiencies to gene therapy J. Neuroendocrinol 18 2006 633 642
45. Quinn A., and Koopman P. The molecular genetics of sex determination and sex reversal in mammals Semin. Reprod. Med 30 2012 351 363
46. Rannikko A., Pakarinen P., Manna P.R., Beau I., Misrahi M., Aittomäki K., and Huhtaniemi I. Functional characterization of the human FSH receptor with an inactivating Ala189Val mutation Mol. Hum. Reprod 8 2002 311 317
47. Rossetti R., Di Pasquale E., Marozzi A., Bione S., Toniolo D., Grammatico P., Nelson L.M., Beck-Peccoz P., and Persani L. BMP15 mutations associated with primary ovarian insufficiency cause a defective production of bioactive protein Hum. Mutat 30 2009 804 810
48. Shimasaki S., Moore R.K., Otsuka F., and Erickson G.F. The bone morphogenetic protein system in mammalian reproduction Endocr. Rev 25 2004 72 101
49. Touraine P., Beau I., Gougeon A., Meduri G., Desroches A., Pichard C., Detoeuf M., Paniel B., Prieur M., Zorn J.R., Milgrom E., Kuttenn F., and Misrahi M. New natural inactivating mutations of the follicle-stimulating hormone receptor: correlations between receptor function and phenotype Mol. Endocrinol 13 1999 1844 1854
50. Tremblay J.J., Lanctôt C., and Drouin J. The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3 Mol. Endocrinol 12 1998 428 441
51. 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., and Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function Mol. Endocrinol 15 2001 854 866
52. Yoshino O., McMahon H.E., Sharma S., and 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. 103 2006 10678 10683
53. Zhao H., Chen Z.-J., Qin Y., Shi Y., Wang S., Choi Y., Simpson J.L., and Rajkovic A. Transcription factor FIGLA is mutated in patients with premature ovarian failure Am. J. Hum. Genet 82 2008 1342 1348