Posttranslational activation of bone morphogenetic protein 2 is mediated by proprotein convertase 6 during decidualization for pregnancy establishment

Endocrinology

Volumn 151, Issue 8, 2010, Pages 3909-3917

  Heng, Sophea ^a   Paule, Sarah ^a   Hardman, Belinda ^a   Li, Ying ^a   Singh, Harmeet ^a   Rainczuk, Adam ^a   Stephens, Andrew N ^a   Nie, Guiying ^a  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; PROPROTEIN CONVERTASE 6; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; DECIDUALIZATION; ENDOMETRIUM; FEMALE INFERTILITY; HUMAN; HUMAN CELL; NIDATION; PREGNANCY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROCESSING; STROMA CELL; UPREGULATION;

AMINO ACID SEQUENCE; BONE MORPHOGENETIC PROTEIN 2; CATALYTIC DOMAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO IMPLANTATION; ENDOMETRIUM; ENZYME INHIBITORS; FEMALE; FLUORESCEINS; HUMANS; PREGNANCY; PREGNANCY MAINTENANCE; PROPROTEIN CONVERTASE 5; PROTEIN PROCESSING, POST-TRANSLATIONAL; UP-REGULATION; VALIDATION STUDIES AS TOPIC;

EID: 77954929367     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0326     Document Type: Article

References (39)

1. Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG 1998 Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat Med 4:303-308 (Pubitemid 28144088)
2. Wang H, Dey SK 2006 Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185-199 (Pubitemid 43361530)
3. Kurihara I, Lee DK, Petit FG, Jeong J, Lee K, Lydon JP, DeMayo FJ, Tsai MJ, Tsai SY 2007 COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLOS Genet 3:e102
4. Gellersen B, Brosens J 2003 Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 178:357-372
5. Salamonsen LA, Dimitriadis E, Jones RL, Nie G 2003 Complex regulation of decidualization: a role for cytokines and proteases-a review. Placenta 17:S76-S85
6. Salamonsen LA, Nie G, Hannan NJ, Dimitriadis E 2009 Society for Reproductive Biology Founders' Lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod Fertil Dev 21:923-934
7. Dimitriadis E, Nie G, Hannan NJ, Paiva P, Salamonsen LA 2010 Local regulation of implantation at the human fetal-maternal interface. Int J Dev Biol 54:313-322
8. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, Tsai SY, Lydon JP, DeMayo FJ 2007 Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol 27:5468-5478 (Pubitemid 47124399)
9. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK, Bagchi IC 2007 Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem 282:31725-31732 (Pubitemid 350044887)
10. Hogan BLM 1996 Bone morphogenetic proteins in development. Curr Opin Genet Dev 6:432-438
11. Chen D, Zhao M, Mundy GR 2004 Bone morphogenetic proteins. Growth Factors 22:233-241
12. David L, Feige JJ, Bailly S 2009 Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev 20:203-212
13. Ying Y, Zhao GQ 2000 Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biol Reprod 63:1781-1786
14. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BL 2001 Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA 98:1047-1052 (Pubitemid 32121184)
15. Stoikos CJ, Harrison CA, Salamonsen LA, Dimitriadis E 2008 A distinct cohort of the TGFβ superfamily members expressed in human endometrium regulate decidualization. Hum Reprod 23:1447-1456 (Pubitemid 351770587)
16. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA 1988 Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534 (Pubitemid 19023695)
17. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P 1990 Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224
18. Constam DB, Robertson EJ 1999 Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J Cell Biol 144:139-149
19. Cui Y, Jean F, Thomas G, Christian JL 1998 BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J 17:4735-4743
20. Nelsen SM, Christian JL 2009 Site-specific cleavage of BMP4 by furin, PC6, and PC7. J Biol Chem 284:27157-27166
21. Seidah NG, Mayer G, Zaid A, Rousselet E, Nassoury N, Poirier S, Essalmani R, Prat A 2008 The activation and physiological functions of the proprotein convertases. Int J Biochem Cell Biol 40:1111-1125
22. Seidah NG, Day R, Marcinkiewicz M, Chrétien M 1998 Precursor convertases: an evolutionary ancient, cell-specific, combinatorial mechanism yielding diverse bioactive peptides and proteins. Ann NY Acad Sci 839:9-24
23. Seidah NG, Chrétien M 1999 Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 848:45-62
24. Rockwell NC, Thorner JW 2004 The kindest cuts of all: crystal structures of Kex2 and furin reveal secrets of precursor processing. Trends Biochem Sci 29:80-87
25. Scamuffa N, Siegfried G, Bontemps Y, Ma L, Basak A, Cherel G, Calvo F, Seidah NG, Khatib AM 2008 Selective inhibition of proprotein convertases represses the metastatic potential of human colorectal tumor cells. J Clin Invest 118:352-363
26. Dubois CM, Blanchette F, Laprise MH, Leduc R, Grondin F, Seidah NG 2001 Evidence that furin is an authentic transforming growth factor-β1- converting enzyme. Am J Pathol 158:305-316
27. Freyer C, Kilpatrick LM, Salamonsen LA, Nie G 2007 Pro-protein convertases (PCs) other than PC6 are not tightly regulated for implantation in the human endometrium. Reproduction 133:1189-1197
28. Nie G, Li Y, Wang M, Liu YX, Findlay JK, Salamonsen LA 2005 Inhibiting uterine PC6 blocks embryo implantation: an obligatory role for a proprotein convertase in fertility. Biol Reprod 72:1029-1036
29. Okada H, Nie G, Salamonsen LA 2005 Requirement for proprotein convertase 5/6 during decidualization of human endometrial stromal cells in vitro. J Clin Endocrinol Metab 90:1028-1034
30. Nie GY, Li Y, Minoura H, Findlay JK, Salamonsen LA 2003 Specific and transient up-regulation of proprotein convertase 6 at the site of embryo implantation and identification of a unique transcript in mouse uterus during early pregnancy. Biol Reprod 68:439-447
31. Tang M, Mikhailik A, Pauli I, Giudice LC, Fazelabas AT, Tulac S, Carson DD, Kaufman DG, Barbier C, Creemers JW, Tabibzadeh S 2005 Decidual differentiation of stromal cells promotes proprotein convertase 5/6 expression and lefty processing. Endocrinology 146:5313-5320
32. Nie G, Li Y, Hale K, Okada H, Manuelpillai U, Wallace EM, Salamonsen LA 2006 Serine protease HTRA3 is closely associated with human placental development and is detectable in pregnancy serum. Biol Reprod 74:366-374
33. Fugere M, Appel J, Houghten RA, Lindberg I, Day R 2007 Short polybasic peptide sequences are potent inhibitors of PC5/6 and PC7: use of positional scanning-synthetic peptide combinatorial libraries as a tool for the optimization of inhibitory sequences. Mol Pharmacol 71:323-332 (Pubitemid 46021002)
34. Dubois CM, Laprise MH, Blanchette F, Gentry LE, Leduc R 1995 Processing of transforming growth factor [β]1 precursor by human furin convertase. J Biol Chem 270:10618-10624
35. Roebroek AJ, Creemers JW, Pauli IG, Bogaert T, Van de Ven WJ 1993 Generation of structural and functional diversity in furin-like proteins in Drosophila melanogaster by alternative splicing of the Dfur1 gene. EMBO J 12:1853-1870 (Pubitemid 23157701)
36. Nachtigal MW, Ingraham HA 1996 Bioactivation of Müllerian inhibiting substance during gonadal development by a kex2/subtilisinlike endoprotease. Proc Natl Acad Sci USA 93:7711-7716 (Pubitemid 26277102)
37. Kilpatrick LM, Stephens AN, Hardman BM, Salamonsen LA, Li Y, Stanton PG, Nie G 2009 Proteomic identification of caldesmon as a physiological substrate of proprotein convertase 6 in human uterine decidual cells essential for pregnancy establishment. J Proteome Res 8:4983-4992
38. Matsumoto H, Sakai K, Iwashita M 2008 Insulin-like growth factor binding protein-1 induces decidualization of human endometrial stromal cells via α5β1 integrin. Mol Hum Reprod 14:485-489
39. Nie G, Findlay JK, Salamonsen LA 2005 Identification of novel endometrial targets for contraception. Contraception 71:272-281 (Pubitemid 40410077)