Nodal signals through activin receptor-like kinase 7 to inhibit trophoblast migration and invasion: Implication in the pathogenesis of preeclampsia

American Journal of Pathology

Volumn 178, Issue 3, 2011, Pages 1177-1189

  Nadeem, Lubna ^a   Munir, Sadia ^a   Fu, Guodong ^a   Dunk, Caroline ^b   Baczyk, Dora ^b   Caniggia, Isabella ^b,c   Lye, Stephen ^b,c   Peng, Chun ^a  

^a YORK UNIVERSITY   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR; ACTIVIN RECEPTOR LIKE KINASE 7; GELATINASE A; GELATINASE B; NODAL SIGNALING PROTEIN; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADULT; APOPTOSIS; ARTICLE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; PATHOGENESIS; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; TROPHOBLAST;

EID: 79952751431     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.066     Document Type: Article

References (44)

1. Zhou X, Sasaki H, Lowe L, Hogan BL, Kuehn MR: Nodal is a novel TGF-β-like gene expressed in the mouse node during gastrulation. Nature 1993, 361:543-547
2. Reissmann E, Jornvall H, Blokzijl A, Andersson O, Chang C, Minchiotti G, Persico MG, Ibanez CF, Brivanlou AH: The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev 2001, 15:2010-2022 (Pubitemid 32738629)
3. Bianco C, Adkins HB, Wechselberger C, Seno M, Normanno N, De Luca A, Sun Y, Khan N, Kenney N, Ebert A, Williams KP, Sanicola M, Salomon DS: Cripto-1 activates nodal- and ALK4-dependent and -independent signaling pathways in mammary epithelial cells. Mol Cell Biol 2002, 22:2586-2597 (Pubitemid 34262981)
4. Brennan J, Norris DP, Robertson EJ: Nodal activity in the node governs left-right asymmetry. Genes Dev 2002, 16:2339-2344 (Pubitemid 35034403)
5. Eimon PM, Harland RM: Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: implications for mesoderm induction in Xenopus. Development 2002, 129:3089-3103 (Pubitemid 34874284)
6. Nonaka S, Shiratori H, Saijoh Y, Hamada H: Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002, 418:96-99 (Pubitemid 34742578)
7. Duboc V, Lapraz F, Saudemont A, Bessodes N, Mekpoh F, Haillot E, Quirin M, Lepage T: Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo. Development 2010, 137:223-235
8. Ma GT, Soloveva V, Tzeng SJ, Lowe LA, Pfendler KC, Iannaccone PM, Kuehn MR, Linzer DI: Nodal regulates trophoblast differentiation and placental development. Dev Biol 2001, 236:124-135
9. Guzman-Ayala M, Ben-Haim N, Beck S, Constam DB: Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc Natl Acad Sci U S A 2004, 101:15656-15660 (Pubitemid 39473543)
10. Roberts HJ, Hu S, Qiu Q, Leung PC, Caniggia I, Gruslin A, Tsang B, Peng C: Identification of novel isoforms of activin receptor-like kinase 7 (ALK7) generated by alternative splicing and expression of ALK7 and its ligand, Nodal, in human placenta. Biol Reprod 2003, 68:1719-1726 (Pubitemid 36519777)
11. Munir S, Xu G, Wu Y, Yang B, Lala PK, Peng C: Nodal and ALK7 inhibit proliferation and induce apoptosis in human trophoblast cells. J Biol Chem 2004, 279:31277-31286 (Pubitemid 39037793)
12. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M: Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFβ(3). J Clin Invest 2000, 105:577-587 (Pubitemid 30146504)
13. Chakraborty C, Gleeson LM, McKinnon T, Lala PK: Regulation of human trophoblast migration and invasiveness. Can J Physiol Pharmacol 2002, 80:116-124 (Pubitemid 34258660)
14. Knofler M: Critical growth factors and signalling pathways controlling human trophoblast invasion. Int J Dev Biol 2009, 54:269-280
15. Aplin JD: In vitro analysis of trophoblast invasion. Methods Mol Med 2006, 122:45-57
16. Caniggia I, Winter J, Lye SJ, Post M: Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta 2000, 21(Suppl A):S25-S30
17. Cross JC: Placental function in development and disease. Reprod Fertil Dev 2006, 18:71-76
18. Noris M, Perico N, Remuzzi G: Mechanisms of disease: Pre-eclampsia. Nat Clin Pract Nephrol 2005, 1:98-114; quiz 120
19. Chelbi ST, Vaiman D: Genetic and epigenetic factors contribute to the onset of preeclampsia. Mol Cell Endocrinol 2008, 282:120-129
20. Caniggia I, Grisaru-Gravnosky S, Kuliszewsky M, Post M, Lye SJ: Inhibition of TGF-β 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J Clin Invest 1999, 103: 1641-1650 (Pubitemid 29534358)
21. Muttukrishna S, North RA, Morris J, Schellenberg JC, Taylor RS, Asselin J, Ledger W, Groome N, Redman CW: Serum inhibin A and activin A are elevated prior to the onset of pre-eclampsia. Hum Reprod 2000, 15:1640-1645
22. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA: Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006, 12:642-649 (Pubitemid 43865232)
23. Wang A, Rana S, Karumanchi SA: Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 2009, 24: 147-158
24. Moses EK, Fitzpatrick E, Freed KA, Dyer TD, Forrest S, Elliott K, Johnson MP, Blangero J, Brennecke SP: Objective prioritization of positional candidate genes at a quantitative trait locus for pre-eclampsia on 2q22. Mol Hum Reprod 2006, 12:505-512 (Pubitemid 44288196)
25. Roten LT, Johnson MP, Forsmo S, Fitzpatrick E, Dyer TD, Brennecke SP, Blangero J, Moses EK, Austgulen R: Association between the candidate susceptibility gene ACVR2A on chromosome 2q22 and pre-eclampsia in a large Norwegian population-based study (the HUNT study). Eur J Hum Genet 2009, 17:250-257
26. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, Lala PK: Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 1993, 206:204-211 (Pubitemid 23212937)
27. Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, Kingdom J: Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 2009, 16:719-727
28. Genbacev O, Schubach SA, Miller RK: Villous culture of first trimester human placenta-model to study extravillous trophoblast (EVT) differentiation. Placenta 1992, 13:439-461
29. Nishimura T, Dunk C, Lu Y, Feng X, Gellhaus A, Winterhager E, Rossant J, Lye SJ: Gap junctions are required for trophoblast proliferation in early human placental development. Placenta 2004, 25: 595-607 (Pubitemid 38950313)
30. Xu G, Zhong Y, Munir S, Yang BB, Tsang BK, Peng C: Nodal induces apoptosis and inhibits proliferation in human epithelial ovarian cancer cells via activin receptor-like kinase 7. J Clin Endocrinol Metab 2004, 89:5523-5534 (Pubitemid 39518436)
31. Khoo NK, Bechberger JF, Shepherd T, Bond SL, McCrae KR, Hamilton GS, Lala PK: SV40 Tag transformation of the normal invasive trophoblast results in a premalignant phenotype, I: mechanisms responsible for hyperinvasiveness and resistance to anti-invasive action of TGFβ. Int J Cancer 1998, 77:429-439
32. Morrish DW, Whitley GSJ, Cartwright JE, Graham CH, Caniggia I: In vitro models to study trophoblast function and dysfunction: a workshop report. Placenta 2002, 23:S114-S118
33. Kilburn BA, Wang J, Duniec-Dmuchowski ZM, Leach RE, Romero R, Armant DR: Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol Reprod 2000, 62:739-747 (Pubitemid 30118317)
34. Chirco R, Liu XW, Jung KK, Kim HR: Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev 2006, 25:99-113 (Pubitemid 43723986)
35. Huppertz B, Frank HG, Reister F, Kingdom J, Korr H, Kaufmann P: Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 1999, 79:1687-1702 (Pubitemid 30013932)
36. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ: Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 1996, 97:540-550 (Pubitemid 26039422)
37. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ: Regulation of human placental development by oxygen tension. Science 1997, 277:1669-1672 (Pubitemid 27446230)
38. Nishi H, Nakada T, Hokamura M, Osakabe Y, Itokazu O, Huang LE, Isaka K: Hypoxia-inducible factor-1 transactivates transforming growth factor-β3 in trophoblast. Endocrinology 2004, 145:4113-4118 (Pubitemid 39120559)
39. Harris LK: Review: trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta 2010, 31(Suppl):S93-S98
40. Anin SA, Vince G, Quenby S: Trophoblast invasion. Hum Fertil (Camb) 2004, 7:169-174 (Pubitemid 40011966)
41. Caniggia I, Lye SJ, Cross JC: Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology 1997, 138: 3976-3986 (Pubitemid 27351954)
42. Cohen M, Bischof P: Factors regulating trophoblast invasion. Gynecol Obstet Invest 2007, 64:126-130 (Pubitemid 47574869)
43. Huppertz B, Kadyrov M, Kingdom JC: Apoptosis and its role in the trophoblast. Am J Obstet Gynecol 2006, 195:29-39 (Pubitemid 43927489)
44. Myers JE, Merchant SJ, Macleod M, Mires GJ, Baker PN, Davidge ST: MMP-2 levels are elevated in the plasma of women who subsequently develop preeclampsia. Hypertens Pregnancy 2005, 24:103-115 (Pubitemid 40911348)