Connexin31.1 (Gjb5) deficiency blocks trophoblast stem cell differentiation and delays placental development

Stem Cells and Development

Volumn 23, Issue 21, 2014, Pages 2649-2660

  Kibschull, Mark ^a   Colaco, Keith ^a   Matysiak Zablocki, Elzbieta ^a   Winterhager, Elke ^b   Lye, Stephen J ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ASCL2 PROTEIN; CONNEXIN 31; CONNEXIN 31.1; CTSQ PROTEIN; INHIBITOR OF DIFFERENTIATION 2; PL 2 PROTEIN; PRL3B1 PROTEIN; PROTEIN; TPBPA PROTEIN; UNCLASSIFIED DRUG; CDKN1C PROTEIN, MOUSE; CONNEXIN 26; CYCLIN DEPENDENT KINASE INHIBITOR 1C; GAP JUNCTION PROTEIN; PLACENTA PROTEIN; TPBPA PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FETUS BLOOD; IN SITU HYBRIDIZATION; MARKER GENE; MOUSE; NONHUMAN; PLACENTA DEVELOPMENT; PLACENTA WEIGHT; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPRODUCTION; STEM CELL; STEREOLOGY; TROPHOBLAST; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DEFICIENCY; EMBRYOLOGY; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; METABOLISM; PLACENTA; PREGNANCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CONNEXINS; CYCLIN-DEPENDENT KINASE INHIBITOR P57; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLACENTA; PREGNANCY; PREGNANCY PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TROPHOBLASTS;

EID: 84913610764     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0013     Document Type: Article

References (31)

1. Kibschull M, A Gellhaus and E Winterhager. (2008). Analogous and unique functions of connexins in mouse and human placental development. Placenta 29:848-854.
2. Malassine A and L Cronier. (2005). Involvement of gap junctions in placental functions and development. Biochim Biophys Acta 1719:117-124.
3. Dunk CE, A Gellhaus, S Drewlo, D Baczyk, AJ Potgens, E Winterhager, JC Kingdom and SJ Lye. (2012). The molecular role of connexin 43 in human trophoblast cell fusion. Biol Reprod 86:115.
4. Valiunas V, YY Polosina, H Miller, IA Potapova, L Valiuniene, S Doronin, RT Mathias, RB Robinson, MR Rosen, IS Cohen and PR Brink. (2005). Connexin-specific cell-Tocell transfer of short interfering RNA by gap junctions. J Physiol 568:459-468.
5. Ek-Vitorin JF and JM Burt. (2013). Structural basis for the selective permeability of channels made of communicating junction proteins. Biochim Biophys Acta 1828:51-68.
6. Herve JC and M Derangeon. (2013). Gap-junctionmediated cell-To-cell communication. Cell Tissue Res 352:21-31.
7. Oyamada M, Y Oyamada and T Takamatsu. (2005). Regulation of connexin expression. Biochim Biophys Acta 1719:6-23.
8. Hennemann H, E Dahl, JB White, HJ Schwarz, PA Lalley, S Chang, BJ Nicholson and K Willecke. (1992). Two gap junction genes, connexin 31.1 and 30.3, are closely linked on mouse chromosome 4 and preferentially expressed in skin. J Biol Chem 267:17225-17233.
9. Kibschull M, TM Magin, O Traub and E Winterhager. (2005). Cx31 and Cx43 double-deficient mice reveal independent functions in murine placental and skin development. Dev Dyn 233:853-863.
10. Plum A, E Winterhager, J Pesch, J Lautermann, G Hallas, B Rosentreter, O Traub, C Herberhold and K Willecke. (2001). Connexin31-deficiency in mice causes transient placental dysmorphogenesis but does not impair hearing and skin differentiation. Dev Biol 231:334-347.
11. Zheng-Fischhofer Q, M Kibschull, M Schnichels, M Kretz, E Petrasch-Parwez, J Strotmann, H Reucher, BD Lynn, JI Nagy, et al. (2007). Characterization of connexin31.1-deficient mice reveals impaired placental development. Dev Biol 312: 258-271.
12. Kibschull M, M Nassiry, C Dunk, A Gellhaus, JA Quinn, J Rossant, SJ Lye and E Winterhager. (2004). Connexin31-deficient trophoblast stem cells: A model to analyze the role of gap junction communication in mouse placental development. Dev Biol 273:63-75.
13. Koch Y, B van Furden, S Kaiser, D Klein, M Kibschull, H Schorle, A Carpinteiro, A Gellhaus and E Winterhager. (2012). Connexin 31 (GJB3) deficiency in mouse trophoblast stem cells alters giant cell differentiation and leads to loss of oxygen sensing. Biol Reprod 87:37.
14. Kibschull M and E Winterhager. (2006). Connexins and trophoblast cell lineage development. Methods Mol Med 121:149-158.
15. Kibschull M, M Mileikovsky, IP Michael, SJ Lye and A Nagy. (2011). Human embryonic fibroblasts support single cell enzymatic expansion of human embryonic stem cells in xeno-free cultures. Stem Cell Res 6:70-82.
16. Colosi P, F Talamantes and DI Linzer. (1987). Molecular cloning and expression of mouse placental lactogen I complementary deoxyribonucleic acid. Mol Endocrinol 1:767-776.
17. Jackson LL, P Colosi, F Talamantes and DI Linzer. (1986). Molecular cloning of mouse placental lactogen cDNA. Proc Natl Acad Sci U S A 83:8496-8500.
18. Linzer DI and JC Mordacq. (1987). Transcriptional regulation of proliferin gene expression in response to serum in transfected mouse cells. EMBO J 6:2281-2288.
19. Guillemot F, T Caspary, SM Tilghman, NG Copeland, DJ Gilbert, NA Jenkins, DJ Anderson, AL Joyner, J Rossant and A Nagy. (1995). Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet 9:235-242.
20. Maltepe E and MC Simon. (1998). Oxygen, genes, and development: An analysis of the role of hypoxic gene regulation during murine vascular development. J Mol Med (Berl) 76:391-401.
21. Hu D and JC Cross. (2011). Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev Biol 358:231-239.
22. Yamaguchi M, L Ogren, H Endo, G Thordarson, RM Bigsby and F Talamantes. (1992). Production of mouse placental lactogen-I and placental lactogen-II by the same giant cell. Endocrinology 131:1595-1602.
23. Simmons DG, AL Fortier and JC Cross. (2007). Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 304:567-578.
24. Hughes M, N Dobric, IC Scott, L Su, M Starovic, B St-Pierre, SE Egan, JC Kingdom and JC Cross. (2004). The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev Biol 271:26-37.
25. Tanaka S, T Kunath, AK Hadjantonakis, A Nagy and J Rossant. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072-2075.
26. Richard G, LE Smith, RA Bailey, P Itin, D Hohl, EH Epstein, Jr., JJ DiGiovanna, JG Compton and SJ Bale. (1998). Mutations in the human connexin gene GJB3 cause erythrokeratodermia variabilis. Nat Genet 20:366-369.
27. Scott CA, D Tattersall, EA OToole and DP Kelsell. (2012). Connexins in epidermal homeostasis and skin disease. Biochim Biophys Acta 1818:1952-1961.
28. Schnichels M, P Worsdorfer, R Dobrowolski, C Markopoulos, M Kretz, G Schwarz, E Winterhager and K Willecke. (2007). The connexin31 F137L mutant mouse as a model for the human skin disease erythrokeratodermia variabilis (EKV). Hum Mol Genet 16:1216-1224.
29. Simon AM and AR McWhorter. (2003). Role of connexin37 and connexin40 in vascular development. Cell Commun Adhes 10:379-385.
30. Fang JS, SN Angelov, AM Simon and JM Burt. (2012). Cx40 is required for, and cx37 limits, postischemic hindlimb perfusion, survival and recovery. J Vasc Res 49:2-12.
31. Houghton FD, KJ Barr, G Walter, HD Gabriel, R Grummer, O Traub, HJ Leese, E Winterhager and GM Kidder. (2002). Functional significance of gap junctional coupling in preimplantation development. Biol Reprod 66:1403-1412.