Endogenous production of fibronectin is required for self-renewal of cultured mouse embryonic stem cells

Experimental Cell Research

Volumn 318, Issue 15, 2012, Pages 1820-1831

  Hunt, Geoffrey C ^a   Singh, Purva ^a   Schwarzbauer, Jean E ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Embryonic stem cell; Extracellular matrix; Fibronectin; Integrin; Self renewal

Indexed keywords

FIBRONECTIN; FOCAL ADHESION KINASE; INTEGRIN RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; STAGE SPECIFIC EMBRYO ANTIGEN 1; STAT3 PROTEIN; TRANSCRIPTION FACTOR NANOG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; CELL RENEWAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

EID: 84863775290     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.06.009     Document Type: Article

References (65)

1. Smith A.G. Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 2001, 17:435-462.
2. Solter D., Knowles B.B. Monoclonal antibody defining a stage-specific mouse embryonic antigen. Proc. Natl. Acad. Sci. 1978, 75:5565-5569.
3. Matsuda T., Nakamura T., Nakao K., Arai T., Katsuki M., Heike T., Yokota T. STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J. 1999, 18:4261-4269.
4. Chambers I., Colbya D., Robertsona M., Nicholsa J., Leea S., Tweediea S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
5. Mitsui K., Tokuzawa Y., Itoh H., Segaw K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
6. Okamoto K., Okazawa H., Okuda A., Sakai M., Muramatsu M., Hamada H. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 1990, 60:461-472.
7. Rosner M.H., Vigano M.A., Ozato K., Timmons P.M., Poirier F., Rigby P., Staudt L.M., POU A domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 1990, 345:686-692.
8. Ivanova N., Dobrin R., Lu R., Kotenko I., Levorse J., DeCoste C., Schafer X., Lun Y., Lemischka I.R. Dissecting self-renewal in stem cells with RNA interference. Nature 2006, 442:533-538.
9. Niwa H. How is pluripotency determined and maintained. Development 2007, 134:635-646s.
10. Smith A., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., Rogers D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988, 336:688-690.
11. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336:684-687.
12. Ying Q.L., Nichols J., Chambers I., Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003, 115:281-292.
13. Niwa H., Ogawa K., Shimosato D., Adachi K. A parallel circuit of LIF Signalling pathways maintains pluripotency of mouse ES cells. Nature 2009, 460:118-122.
14. Flaim C., Chien S., Bhatia S. An extracellular microarray for probing cellular differentiation. Nat. Methods 2005, 2:119-125.
15. Prudhomme W., Daley G.Q., Zandstra P., Lauffenburger D. Multivariate proteomic analysis of murine embryonic stem cell self-renewal versus differentiation signaling. Proc. Natl. Acad. Sci. 2004, 101:2900-2905.
16. Aszódi A., Legate K.R., Nakchbandi I., Fässler R. What mouse mutants teach us about extracellular matrix function. Annu. Rev. Cell Dev. Biol. 2006, 22:591-621.
17. Hayashi Y., Furue M.K., Okamoto T., Ohnuma K., Myoishi Y., Fukuhara Y., Abe T., Sato J.D., Ryu-Ichiro H., Asashima M. Integrins regulate mouse embryonic stem cell self-renewal. Stem Cells 2007, 25:3005-3015.
18. Smukler S.R., Runciman S.B., Xu S., v.d. Kooy D Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 2006, 172:79-90.
19. Yasunaga M., Tada S., Torikai-Nishikawa S., Nakano Y., Okada M., Jakt L.M., Nishikawa S., Chiba T., Era T., Nishikawa S.I. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat. Biotechnol. 2005, 23:1542-1550.
20. Nagy A., Vintersten K. Murine embryonic stem cells. Methods in Enzymology 2006, 418:3-21. Academic Press.
21. Mao Y., Schwarzbauer J. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 2005, 24:389-399.
22. Singh P., Carraher C., Schwarzbauer J.E. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 2010, 26:397-419.
23. Wartiovaara J., Leivo I., Vaheri A. Expression of the cell surface-associated glycoprotein, fibronectin, in the early mouse embryo. Dev. Biol. 1979, 69:247-257.
24. Zetter B.R., Martin G. Expression of a high molecular weight cell surface glycoprotein (LETS protein) by preimplantation mouse embryos and teratocarcinoma stem cells. Proc. Natl. Acad. Sci. 1978, 75:2324-2328.
25. Francis S.E., Goh K.L., Hodivala-Dilke K., Bader B.L., Stark M., Davidson D., Hynes R.O. Central roles of α5Β1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 2002, 22:927-933.
26. George E.L., Georges-Labouesse E.N., Patel-King R.S., Rayburn H., Hynes R.O. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 1993, 119:1079-1091.
27. Fässler R., Meyer M. Consequences of lack of beta1 integrin gene expression in mice. Genes Dev. 1995, 9:1883-1895.
28. Yang J.T., Rayburn H., Hynes R.O. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 1993, 119:1093-1105.
29. Schwarzbauer J.E., Desimone D.W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 2011, 3. 10.1101/cshperspect.a005041.
30. Keller G., Kennedy M., Papayannopoulou T., Wiles M.V. Hematopoietic commitment during embryonic stem cells differentiation in culture. Mol. Cell Biol. 1993, 13:473-486.
31. Robertson E., Bradley A., Keuhn M. Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 1986, 323:445-448.
32. Schaniel C., Li F., Schafer X.L., Moore T., Lemischka I.R., Paddison P.J. Delivery of short hairpin RNAs-triggers of gene silencing-into mouse embryonic stem cells. Nat. Methods 2006, 3:397-400.
33. Aguirre K., McCormick R., Schwarzbauer J. Fibronectin self-association is mediated by complementary sites within the amino-terminal one-third of the molecule. J. Biol. Chem. 1994, 269:27863-27868.
34. Wierzbicka-Patynowski I., Mao Y., Schwarzbauer J.E. Continuous requirement for pp60-Src and phospho-paxillin during fibronectin matrix assembly by transformed cells. J. Cell Physiol. 2007, 210:750-756.
35. Engvall E., Ruoslahti E. Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer 1977, 20:1-5.
36. Tomasini-Johansson B.R., Kaufman N.R., Ensenberger M.G., Ozeri V., Hanski E., Mosher D.F. A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 2001, 276:23430-23439.
37. Ang Y.S., Tsai S.Y., Lee D.F., Monk J., Su J., Ratnakumar K., Ding J., Ge Y., Darr H., Chang B., Wang J., Rendl M., Bernstein E., Schaniel C., Lemischka I.R. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 2011, 145:183-197.
38. Sepulveda D.E., Andrews B.A., Asenjo J.A., Papoutsakis E.T. Comparative transcriptional analysis of embryoid body versus two-dimenstional differentiation of murine embryonic stem cells. Tissue Eng. Part A 2008, 14:1603-1614.
39. Schaller M.D. Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 2001, 1540:1-21.
40. Burdon T., Smith A., Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 2002, 12:432-438.
41. Hynes R.O. Fibronectins 1990, Springer-Verlag Inc., New York, NY.
42. Ensenberger M.G., Tomasini-Johansson B.R., Sottile J., Ozeri V., Hanski E., Mosher D.F. Specific interactions between F1 adhesin of Streptococcus pyogenes and N-terminal modules of fibronectin. J. Biol. Chem. 2001, 276:35606-35613.
43. Maurer L.M., Tomasini-Johansson B.R., Ma W., Annis D.S., Eickstaedt N.L., Ensenberger M.G., Satyshur K.A., Mosher D.F. Extended binding site on fibronectin for the functional upstream domain of protein F1 of Streptococcus pyogenes. J. Biol. Chem. 2010, 285:41087-41099.
44. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005, 19:1129-1155.
45. Chambers I., Silva J., Colby D., Nichols J., Nijmeijer B., Robertson M., Vrana J., Jones K., Grotewold L., Smith A. Nanog safeguards pluripotency and mediates germline development. Nature 2007, 450:1230-1234.
46. Singh A.M., Hamazaki T., Hankowski K.E., Terada N. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 2007, 25:2534-2542.
47. Niwa H., Miyazaki J.i., Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 2000, 24:372-376.
48. Redmer T., Diecke S., Grigoryan T., Quiroga-Negreira A., Birchmeier W., Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO. Rep. 2011, 12:720-726.
49. Xu Y., Zhu X., Hahm H.S., Wei W., Hao E., Hayek A., Ding S. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc. Natl. Acad. Sci. USA 2010, 107:8129-8134.
50. Pease S., Braghetta P., Gearing J.D., Grail D., Williams R.L. Isolation of embryonic stem (ES) cells in media supplemented with recombinant Leukemia Inhibitory Factor (LIF). Dev. Biol. 1990, 141.
51. Chen H.-C., Appeddu P., Isoda H., Guan J.-L. Phosphorylation of tyrosine 397 in Focal Adhesion Kinase is required for binding Phosphatidylinositol 3-Kinase. J. Biol. Chem. 1996, 271:26329-26334.
52. Dike L., Ingber D. Integrin-dependent induction of early growth response genes in capillary endothelial cells. J. Cell Sci. 1996, 109:2855-2863.
53. Paling N.R.D., Wheadon H., Bone H.K., Welham M.J. Regulation of embryonic stem cell self-renewal by Phosphoinositide 3-Kinase-dependent signaling. J. Biol. Chem. 2004, 279:48063-48070.
54. Park J.H., Ryu J.M., Han H.J. Involvement of caveolin-1 in fibronectin-induced mouse embryonic stem cell proliferation: role of FAK, RhoA, PI3K/Akt, and ERK1/2 pathways. J. Cell Physiol. 2010, 226:267-275.
55. Shain K.H., Yarde D.N., Meads M.B., Huang M., Jove R., Hazlehurst L.A., Dalton W.S. -1 integrin adhesion enhances IL-6-mediated STAT3 signaling in myeloma cells: implications for microenvironment influence on tumor survival and proliferation. Cancer Res. 2009, 69:1009-1015.
56. Burdon T., Stracey C., Chambers I., Nichols J., Smith A. Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol. 1999, 210:30-43.
57. Guan J.L. Role of focal adhesion kinase in integrin signaling. Int. J. Biochem. Cell Biol. 1997, 8-9:1085-1096.
58. Huveneers S., Danen E.H.J. Adhesion signaling-crosstalk between integrins, Src and Rho. J. Cell Sci. 2009, 122:1059-1069.
59. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276:1425-1428.
60. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 2004, 6:483-495.
61. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-155.
62. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. 1981, 78:7634-7638.
63. Hamazaki T., Oka M., Yamanaka S., Terada N. Aggregation of embryonic stem cells induces Nanog repression and primitive endoderm differentiation. J. Cell Sci. 2004, 117:5681-5686.
64. Murray P., Edgar D. The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation 2001, 68:227-234.
65. Domogatskaya A., Rodin S., Boutaud A., Tryggvason K. Laminin-511, but not -332, -111 or -411 enables mouse embryonic stem cell self-renewal in vitro. Stem Cells 2008, 26:2800-2809.