C-Met-Dependent Multipotent Labyrinth Trophoblast Progenitors Establish Placental Exchange Interface

Developmental Cell

Volumn 27, Issue 4, 2013, Pages 373-386

  Ueno, Masaya ^a   Lee, Lydia K ^a   Chhabra, Akanksha ^a   Kim, YeonJoo ^a   Sasidharan, Rajkumar ^a   VanHandel, Ben ^a   Wang, Ying ^c   Kamata, Masakazu ^a   Kamran, Paniz ^b,c   Sereti, Konstantina Ioanna ^b,c   Ardehali, Reza ^b,c   Jiang, Meisheng ^c   Mikkola, Hanna K A ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 26; SCATTER FACTOR RECEPTOR; TIGHT JUNCTION PROTEIN; UVOMORULIN; BIOLOGICAL MARKER; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL JUNCTION; CELL POLARITY; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTRON MICROSCOPY; FEMALE; FETUS GROWTH; FETUS LIVER; GIANT CELL; INNER EAR; INNER EAR DISEASE; MITOSIS RATE; MORPHOGENESIS; MOUSE; NONHUMAN; PLACENTA; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; STEM CELL; SYNCYTIOTROPHOBLAST; TROPHOBLAST; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DNA MICROARRAY; FETOMATERNAL TRANSFUSION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INTRAUTERINE GROWTH RETARDATION; LIVER; METABOLISM; PATHOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; EAR, INNER; FEMALE; FETAL GROWTH RETARDATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIVER; MATERNAL-FETAL EXCHANGE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLACENTA; PREGNANCY; PROTO-ONCOGENE PROTEINS C-MET; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; TROPHOBLASTS;

EID: 84888145208     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.10.019     Document Type: Article

References (49)

1. Anson-Cartwright L., Dawson K., Holmyard D., Fisher S.J., Lazzarini R.A., Cross J.C. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 2000, 25:311-314.
2. Basyuk E., Cross J.C., Corbin J., Nakayama H., Hunter P., Nait-Oumesmar B., Lazzarini R.A. Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev. Dyn. 1999, 214:303-311.
3. Bladt F., Riethmacher D., Isenmann S., Aguzzi A., Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 1995, 376:768-771.
4. Boccaccio C., Comoglio P.M. Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat. Rev. Cancer 2006, 6:637-645.
5. Chhabra A., Lechner A.J., Ueno M., Acharya A., Van Handel B., Wang Y., Iruela-Arispe M.L., Tallquist M.D., Mikkola H.K.A. Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling. Dev. Cell 2012, 22:651-659.
6. Christensen J.G., Schreck R., Burrows J., Kuruganti P., Chan E., Le P., Chen J., Wang X., Ruslim L., Blake R., et al. A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes invitro and exhibits cytoreductive antitumor activity invivo. Cancer Res. 2003, 63:7345-7355.
7. Furugori K., Kurauchi O., Itakura A., Kanou Y., Murata Y., Mizutani S., Seo H., Tomoda Y., Nakamura T. Levels of hepatocyte growth factor and its messenger ribonucleic acid in uncomplicated pregnancies and those complicated by preeclampsia. J.Clin. Endocrinol. Metab. 1997, 82:2726-2730.
8. Gabriel H.D., Jung D., Bützler C., Temme A., Traub O., Winterhager E., Willecke K. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J.Cell Biol. 1998, 140:1453-1461.
9. Gekas C., Dieterlen-Lièvre F., Orkin S.H., Mikkola H.K.A. The placenta is a niche for hematopoietic stem cells. Dev. Cell 2005, 8:365-375.
10. Genbacev O., Donne M., Kapidzic M., Gormley M., Lamb J., Gilmore J., Larocque N., Goldfien G., Zdravkovic T., McMaster M.T., Fisher S.J. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells 2011, 29:1427-1436.
11. Georgiades P., Ferguson-Smith A.C., Burton G.J. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002, 23:3-19.
12. Golachowska M.R., Hoekstra D., van IJzendoorn S.C. Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol. 2010, 20:618-626.
13. Grant B.D., Donaldson J.G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 2009, 10:597-608.
14. Hughes M., Dobric N., Scott I.C., Su L., Starovic M., St-Pierre B., Egan S.E., Kingdom J.C., Cross J.C. The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev. Biol. 2004, 271:26-37.
15. Hunter P.J., Swanson B.J., Haendel M.A., Lyons G.E., Cross J.C. Mrj encodes a DnaJ-related co-chaperone that is essential for murine placental development. Development 1999, 126:1247-1258.
16. Huh C.G., Factor V.M., Sánchez A., Uchida K., Conner E.A., Thorgeirsson S.S. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc. Natl. Acad. Sci. USA 2004, 101:4477-4482.
17. Kauma S.W., Bae-Jump V., Walsh S.W. Hepatocyte growth factor stimulates trophoblast invasion: a potential mechanism for abnormal placentation in preeclampsia. J.Clin. Endocrinol. Metab. 1999, 84:4092-4096.
18. Kokkinos M.I., Murthi P., Wafai R., Thompson E.W., Newgreen D.F. Cadherins in the human placenta-epithelial-mesenchymal transition (EMT) and placental development. Placenta 2010, 31:747-755.
19. Levy J.E., Jin O., Fujiwara Y., Kuo F., Andrews N.C. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 1999, 21:396-399.
20. Malhotra S., Kincade P.W. Canonical Wnt pathway signaling suppresses VCAM-1 expression by marrow stromal and hematopoietic cells. Exp. Hematol. 2009, 37:19-30.
21. Maltepe E., Bakardjiev A.I., Fisher S.J. The placenta: transcriptional, epigenetic, and physiological integration during development. J.Clin. Invest. 2010, 120:1016-1025.
22. Martin-Belmonte F., Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat. Rev. Cancer 2012, 12:23-38.
23. McQualter J.L., Yuen K., Williams B., Bertoncello I. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc. Natl. Acad. Sci. USA 2010, 107:1414-1419.
24. Morasso M.I., Grinberg A., Robinson G., Sargent T.D., Mahon K.A. Placental failure in mice lacking the homeobox gene Dlx3. Proc. Natl. Acad. Sci. USA 1999, 96:162-167.
25. Mould A., Morgan M.A., Li L., Bikoff E.K., Robertson E.J. Blimp1/Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta. Genes Dev. 2012, 26:2063-2074.
26. Nagai A., Takebe K., Nio-Kobayashi J., Takahashi-Iwanaga H., Iwanaga T. Cellular expression of the monocarboxylate transporter (MCT) family in the placenta of mice. Placenta 2010, 31:126-133.
27. Nasu K., Zhou Y., McMaster M.T., Fisher S.J. Upregulation of human cytotrophoblast invasion by hepatocyte growth factor. J.Reprod. Fertil. Suppl. 2000, 55:73-80.
28. Natale D.R.C., Starovic M., Cross J.C. Phenotypic analysis of the mouse placenta. Methods Mol. Med. 2006, 121:275-293.
29. Plum A., Winterhager E., Pesch J., Lautermann J., Hallas G., Rosentreter B., Traub O., Herberhold C., Willecke K. Connexin31-deficiency in mice causes transient placental dysmorphogenesis but does not impair hearing and skin differentiation. Dev. Biol. 2001, 231:334-347.
30. Rhodes K.E., Gekas C., Wang Y., Lux C.T., Francis C.S., Chan D.N., Conway S., Orkin S.H., Yoder M.C., Mikkola H.K.A. The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2008, 2:252-263.
31. Rinkevich Y., Lindau P., Ueno H., Longaker M.T., Weissman I.L. Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature 2011, 476:409-413.
32. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
33. Saito S., Sakakura S., Enomoto M., Ichijo M., Matsumoto K., Nakamura T. Hepatocyte growth factor promotes the growth of cytotrophoblasts by the paracrine mechanism. J.Biochem. 1995, 117:671-676.
34. Schmidt C., Bladt F., Goedecke S., Brinkmann V., Zschiesche W., Sharpe M., Gherardi E., Birchmeier C. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 1995, 373:699-702.
35. Scifres C.M., Nelson D.M. Intrauterine growth restriction, human placental development and trophoblast cell death. J.Physiol. 2009, 587:3453-3458.
36. Simmons D.G., Cross J.C. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 2005, 284:12-24.
37. Simmons D.G., Natale D.R.C., Begay V., Hughes M., Leutz A., Cross J.C. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008, 135:2083-2091.
38. Sivasubramaniyam T., Garcia J., Tagliaferro A., Melland-Smith M., Chauvin S., Post M., Todros T., Caniggia I. Where polarity meets fusion: role of Par6 in trophoblast differentiation during placental development and preeclampsia. Endocrinology 2013, 154:1296-1309.
39. Somerset D.A., Li X.F., Afford S., Strain A.J., Ahmed A., Sangha R.K., Whittle M.J., Kilby M.D. Ontogeny of hepatocyte growth factor (HGF) and its receptor (c-met) in human placenta: reduced HGF expression in intrauterine growth restriction. Am. J. Pathol. 1998, 153:1139-1147.
40. Stecca B., Nait-Oumesmar B., Kelley K.A., Voss A.K., Thomas T., Lazzarini R.A. Gcm1 expression defines three stages of chorio-allantoic interaction during placental development. Mech. Dev. 2002, 115:27-34.
41. Takayanagi T., Aoki Y., Tanaka K. Expression of constitutively active c-MET receptor in human choriocarcinoma. Gynecol. Obstet. Invest. 2000, 50:198-202.
42. Tanaka S., Kunath T., Hadjantonakis A.K., Nagy A., Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282:2072-2075.
43. Uehara Y., Minowa O., Mori C., Shiota K., Kuno J., Noda T., Kitamura N. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 1995, 373:702-705.
44. Unezaki S., Horai R., Sudo K., Iwakura Y., Ito S. Ovol2/Movo, a homologue of Drosophila ovo, is required for angiogenesis, heart formation and placental development in mice. Genes Cells 2007, 12:773-785.
45. Uy G.D., Downs K.M., Gardner R.L. Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 2002, 129:3913-3924.
46. Van Handel B., Prashad S.L., Hassanzadeh-Kiabi N., Huang A., Magnusson M., Atanassova B., Chen A., Hamalainen E.I., Mikkola H.K. The first trimester human placenta is a site for terminal maturation of primitive erythroid cells. Blood 2010, 116:3321-3330.
47. Watson E.D., Cross J.C. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 2005, 20:180-193.
48. Wynne F., Ball M., McLellan A.S., Dockery P., Zimmermann W., Moore T. Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature. Reproduction 2006, 131:721-732.
49. Young B.C., Levine R.J., Karumanchi S.A. Pathogenesis of preeclampsia. Annu. Rev. Pathol. 2010, 5:173-192.