Natural mutations of the anti-Müllerian hormone type II receptor found in persistent Müllerian duct syndrome affect ligand binding, signal transduction and cellular transport

Human Molecular Genetics

Volumn 18, Issue 16, 2009, Pages 3002-3013

  Belville, Corinne ^a,b   Maréchal, Jean Didier ^c   Pennetier, Sophie ^a,b   Carmillo, Paul ^d   Masgrau, Laura ^c   Messika Zeitoun, Liza ^a,b   Galey, Julie ^a,b   Machado, Gabrielle ^a,b   Treton, Dominique ^a,b   Gonzalès, Jacques ^a,b   Picard, Jean Yves ^a,b   Josso, Nathalie ^a,b   Cate, Richard L ^a,b   Di Clemente, Nathalie ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MUELLERIAN INHIBITING FACTOR; MUELLERIAN INHIBITING FACTOR TYPE 2 RECEPTOR; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BETA SHEET; CELL SURFACE; CELL TRANSPORT; CONTROLLED STUDY; DISULFIDE BOND; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE MUTATION; GENE TRANSLOCATION; LIGAND BINDING; MOUSE; MUELLERIAN DUCT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ANTI-MULLERIAN HORMONE; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; LIGANDS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PSEUDOHERMAPHRODITISM; RECEPTORS, PEPTIDE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 68049088937     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp238     Document Type: Article

References (45)

1. Baarends, W.M., van Helmond, M.J.L., Post, M., van der Schoot, P.C.J.M., Hoogerbrugge, J.W., De Winter, J.P., Uilenbroek, J.T.J., Karels, B., Wilming, L.G., Meijers, J.H.C. et al. (1994) A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the Müllerian duct. Development, 120, 189-197.
2. di Clemente, N., Wilson, C.A., Faure, E., Boussin, L., Carmillo, P., Tizard, R., Picard, J.Y., Vigier, B., Josso, N. and Cate, R.L. (1994) Cloning, expression and alternative splicing of the receptor for anti-Müllerian hormone. Mol. Endocrinol., 8, 1006-1020.
3. Gouédard, L., Chen, Y.G., Thevenet, L., Racine, C., Borie, S., Lamarre, I., Josso, N., Massagué, J. and di Clemente, N. (2000) Engagement of bone morphogenetic protein type IB receptor and Smad1 signaling by anti-Müllerian hormone and its type II receptor. J. Biol. Chem., 275, 27973-27978.
4. Clarke, T.R., Hoshiya, Y., Yi, S.E., Liu, X.H., Lyons, K.M. and Donahoe, P.K. (2001) Müllerian inhibiting substance signaling uses a bone morphogenetic protein (BMP)-like pathway mediated by ALK2 and induces Smad6 expression. Mol. Endocrinol., 15, 946-959.
5. Visser, J.A., Olaso, R., Verhoef-Post, M., Kramer, P., Themmen, A.P.N. and Ingraham, H.A. (2001) The serine/threonine transmembrane receptor ALK2 mediates Mullerian inhibiting substance signaling. Mol. Endocrinol., 15, 936-945.
6. Jamin, S.P., Arango, N.A., Mishina, Y., Hanks, M.C. and Behringer, R.R. (2002) Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat. Genet., 32, 408-410.
7. Orvis, G.D., Jamin, S.P., Kwan, K.M., Mishina, Y., Kaartinen, V.M., Huang, S., Roberts, A.B., Umans, L., Huylebroeck, D., Zwijsen, A. et al. (2008) Functional redundancy of TGF-beta family type receptors and receptor-Smads in mediating anti-Mullerian hormone-induced Mullerian duct regression in the mouse. Biol. Reprod., 78, 994-1001.
8. Josso, N., Belville, C., di Clemente, N. and Picard, J.Y. (2005) AMH and AMH receptor defects in persistent Müllerian duct syndrome. Hum. Reprod. Update, 11, 351-356.
9. Rey, R. (1998) Endocrine, paracrine and cellular regulation of post-natal anti-Müllerian hormone secretion by Sertoli cells. Trends Endocrinol. Metab., 9, 271-275.
10. Imbeaud, S., Faure, E., Lamarre, I., Mattei, M.G., di Clemente, N., Tizard, R., Carré-Eusèbe, D., Belville, C., Tragethon, L., Tonkin, C. et al. (1995) Insensitivity to anti-Müllerian hormone due to a spontaneous mutation in the human anti-Müllerian hormone receptor. Nat. Genet., 11, 382-388.
11. Goder, V. and Spiess, M. (2001) Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett., 504, 87-93.
12. Imbeaud, S., Belville, C., Messika-Zeitoun, L., Rey, R., di Clemente, N., Josso, N. and Picard, J.Y. (1996) A 27 base-pair deletion of the anti-Müllerian type II receptor gene is the most common cause of the persistent Müllerian duct syndrome. Hum. Mol. Genet., 5, 1269-1279.
13. Faure, E., Gouédard, L., Imbeaud, S., Cate, R.L., Picard, J.Y., Josso, N. and di Clemente, N. (1996) Mutant isoforms of the anti-Müllerian hormone type II receptor are not expressed at the cell membrane. J. Biol. Chem., 271, 30571-30575.
14. Messika-Zeitoun, L., Gouédard, L., Belville, C., Dutertre, M., Lins, L., Imbeaud, S., Hughes, I.A., Picard, J.Y., Josso, N. and di Clemente, N. (2001) Autosomal recessive segregation of a truncating mutation of anti-Müllerian hormone type II receptor in a family affected by the persistent Müllerian duct syndrome contrasts with its dominant negative activity in vitro. J. Clin. Endocrinol. Metab., 86, 4390-4397.
15. Greenwald, J., Fischer, W.H., Vale, W.W. and Choe, S. (1999) Three-finger toxin fold for the extracellular ligand-binding domain of the type II activin receptor serine kinase. Nat. Struct. Biol., 6, 18-22.
16. Han, S., Loulakis, P., Griffor, M. and Xie, Z. (2007) Crystal structure of activin receptor type IIB kinase domain from human at 2.0 Angstrom resolution. Protein Sci., 16, 2272-2277.
17. Fiser, A., Do, R.K.G. and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci., 9, 1753-1773.
18. Takenoshita, S., Tani, M., Nagashima, M., Hagiwara, K., Bennett, W.P., Yokota, J. and Harris, C.C. (1997) Mutation analysis of coding sequences of the entire transforming growth factor beta type II receptor gene in sporadic human colon cancer using genomic DNA and intron primers. Oncogene, 14, 1255-1258.
19. Lücke, C.D., Philpott, A., Metcalfe, J.C., Thompson, A.M., Hughes-Davies, L., Kemp, P.R. and Hesketh, R. (2001) Inhibiting mutations in the transforming growth factor b type 2 receptor in recurrent human breast cancer. Cancer Res., 61, 482-485.
20. Stheneur, C., Collod-Beroud, G., Faivre, L., Gouya, L., Sultan, G., Le Parc, J.M., Moura, B., Attias, D., Muti, C., Sznajder, M. et al. (2008) Identification of 23 TGFBR2 and 6 TGFBR1 gene mutations and genotype-phenotype investigations in 457 patients with Marfan syndrome type I and II, Loeys-Dietz syndrome and related disorders. Hum. Mutat., 29, E284-E295.
21. Mizuguchi, T., Collod-Beroud, G., Akiyama, T., Abifadel, M., Harada, N., Morisaki, T., Allard, D., Varret, M., Claustres, M., Morisaki, H. et al. (2004) Heterozygous TGFBR2 mutations in Marfan syndrome. Nat. Genet., 36, 855-860.
22. Loeys, B.L., Chen, J., Neptune, E.R., Judge, D.P., Podowski, M., Holm, T., Meyers, J., Leitch, C.C., Katsanis, N., Sharifi, N. et al. (2005) A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat. Genet., 37, 275-281.
23. Deng, Z.M., Morse, J.H., Slager, S.L., Cuervo, N., Moore, K.J., Venetos, G., Kalachikov, S., Cayanis, E., Fischer, S.G., Barst, R.J. et al. (2000) Familial primary pulmonary hypertension (Gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am. J. Hum. Genet., 67, 737-744.
24. Thompson, J.D., Plewniak, F., Thierry, J.C. and Poch, O. (2000) DbClustal: Rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acids Res., 28 2919-2926.
25. Machado, R.D., Pauciulo, M.W., Thomson, J.R., Lane, K.B., Morgan, N.V., Wheeler, L., Phillips, J.A., Newman, J., Williams, D., Galie, N. et al. (2001) BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am. J. Hum. Genet., 68, 92-102.
26. Nishihara, A., Watabe, T., Imamura, T. and Miyazono, K. (2002) Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol. Biol. Cell., 13, 3055-3063.
27. Rudarakanchana, N. and Morrell, N.W. (2004) Primary pulmonary hypertension: Molecular basis and potential for therapy. Expert Rev. Mol. Med., 6, 1-15.
28. Greenwald, J., Vega, M.E., Allendorph, G.P., Fischer, W.H., Vale, W. and Choe, S. (2004) A flexible activin explains the membrane-dependent cooperative assembly of TGF-beta family receptors. Mol. Cell, 15, 485-489.
29. Thompson, T.B., Woodruff, T.K. and Jardetzky, T.S. (2003) Structures of an ActRIIB: Activin A complex reveal a novel binding mode for TGF-beta ligand: Receptor interactions. EMBO J., 22, 1555-1566.
30. Allendorph, G.P., Vale, W.W. and Choe, S. (2006) Structure of the ternary signaling complex of a TGF-beta superfamily member. Proc. Natl Acad. Sci. USA, 103, 7643-7648.
31. Wieser, R., Attisano, L., Wrana, J.L. and Massagué, J. (1993) Signaling activity of transforming growth factor b type II receptors lacking specific domains in the cytoplasmic region. Mol. Cell. Biol. 13, 7239-7247.
32. Tanaka, S., Mori, M., Mafune, K., Ohno, S. and Sugimachi, K. (2000) A dominant negative mutation of transforming growth factor-β receptor type II gene in microsatellite stable oesophageal carcinoma. Br. J. Cancer, 82, 1557-1560.
33. Grady, W.M., Myeroff, L.L., Swinler, S.E., Rajput, A., Thiagalingam, S., Lutterbaugh, J.D., Neumann, A., Brattain, M.G., Chang, J., Kim, S.J. et al. (1999) Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res., 59, 320-324.
34. Blom, N., Gammeltoft, S. and Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol., 294, 1351-1362.
35. Carcamo, J., Zentella, A. and Massagué, J. (1995) Disruption of transforming growth factor beta signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol. Cell. Biol. 15, 1573-1581.
36. Pannu, H., Fadulu, V.T., Chang, J., Lafont, A., Hasham, S.N., Sparks, E., Giampietro, P.F., Zaleski, C., Estrera, A.L., Safi, H.J. et al. (2005) Mutations in transforming growth factor-beta receptor type II cause familial thoracic aortic aneurysms and dissections. Circulation 112, 513-520.
37. Heany, M.L. and Golde, D.W. (1998) Soluble receptors in human disease. J. Leukoc. Biol., 64, 135-146.
38. Zettimeissi, G., Gregersen, J.P., Duport, J.M., Mehdi, S., Reiner, G. and Seed, B. (1990) Expression and characterization of human CD4:iMmunoglobulin fusion proteins. DNA Cell Biol., 9, 347-353.
39. Bendtsen, J., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol., 340 783-795.
40. Park, S.H., Bolender, N., Eisele, F., Kostova, Z., Takeuchi, J., Coffino, P. and Wolf, D.H. (2007) The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome system. Mol. Biol. Cell, 18, 153-165.
41. McGuffin, L.J., Bryson, K. and Jones, D.T. (2000) The PSIPRED protein structure prediction server. Bioinformatics, 16, 404-405.
42. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acid Res., 25, 3389-3402.
43. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acid Res., 28, 235-242.
44. Sali, A. and Blundell, T.L. (1993) Comparative protein modelling by satisfaction of protein restraints. J. Mol. Biol., 234, 779-815.
45. Colovos, C. and Yeatest, O. (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci., 2, 1511-1519.