Collagen IV significantly enhances migration and transplantation of embryonic stem cells: Involvement of α2β1 integrin-mediated actin remodeling

Cell Transplantation

Volumn 20, Issue 6, 2011, Pages 893-907

  Li, Hsin Yang ^a,b   Liao, Chen Yi ^b   Lee, Kun Hsiung ^c   Chang, Hung Chi ^a   Chen, Yi Jen ^a,b   Chao, Kuan Chong ^a,b   Chang, Sheng Ping ^a,b   Cheng, Hsin Yi ^a,b   Chang, Chia Ming ^a,b   Chang, Yuh Lih ^a,b   Hung, Shih Chieh ^a   Sung, Yen Jen ^b   Chiou, Shih Hwa ^a,b  

^a TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c ANIMAL TECHNOLOGY INSTITUTE TAIWAN   (Taiwan)

Author keywords

Collagen iv; Embryonic stem (ES) cells; Extracellular matrix (ECM); Migration;

Indexed keywords

ACTIN; ARGINYLGLYCYLASPARTIC ACID; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; LAMININ; MATRIGEL; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; STEM CELL TRANSPLANTATION;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; ANTIBODIES; CELL DIFFERENTIATION; CELL MOVEMENT; COLLAGEN TYPE IV; CYTOCHALASIN D; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX PROTEINS; INTEGRIN ALPHA2BETA1; MICE; MICE, NUDE; OLIGOPEPTIDES;

MUS MUSCULUS;

EID: 80051762039     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X550206     Document Type: Article

References (53)

1. Berrier A. L.; Yamada K. M. Cell-matrix adhesion. J. Cell. Physiol. 213:565-573; 2007.
2. Braam S. R.; Zeinstra L.; Litjens S.; Ward-van Oostwaard D.; van den Brink S.; van Laake L.; Lebrin F.; Kats P.; Hochstenbach R.; Passier R.; Sonnenberg A.; Mummery C. L. Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells 26:2257-2265; 2008.
3. Brakebusch C.; Fassler R. The integrin-actin connection, an eternal love affair. EMBO J. 22:2324-2333; 2003.
4. Busser B. W.; Bulyk M. L.; Michelson A. M. Toward a systems-level understanding of developmental regulatory networks. Curr. Opin. Genet. Dev. 18:521-529; 2008.
5. Casella J. F.; Flanagan M. D.; Lin S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293:302-305; 1981.
6. Ceradini D. J.; Kulkarni A. R.; Callaghan M. J.; Tepper O. M.; Bastidas N.; Kleinman M. E.; Capla J. M.; Galiano R. D.; Levine J. P.; Gurtner G. C. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10:858-864; 2004.
7. Chelberg M. K.; Tsilibary E. C.; Hauser A. R.; McCarthy J. B. Type IV collagen-mediated melanoma cell adhesion and migration: Involvement of multiple, distinct domains of the collagen molecule. Cancer Res. 49:4796-4802; 1989.
8. Chiou S. H.; Kao C. L.; Peng C. H.; Chen S. J.; Tarng Y. W.; Ku H. H.; Chen Y. C.; Shyr Y. M.; Liu R. S.; Hsu C. J.; Yang D. M.; Hsu W. M.; Kuo C. D.; Lee C. H. A novel in vitro retinal differentiation model by co-culturing adult human bone marrow stem cells with retinal pigmented epithelium cells. Biochem. Biophys. Res. Commun. 326:578-585; 2005.
9. Choi J. S.; Yang H. J.; Kim B. S.; Kim J. D.; Kim J. Y.; Yoo B.; Park K.; Lee H. Y.; Cho Y. W. Human extracellular matrix (ECM) powders for injectable cell delivery and adipose tissue engineering. J. Control. Release 139:2-7; 2009.
10. Cooper H. M.; Tamura R. N.; Quaranta V. The major laminin receptor of mouse embryonic stem cells is a novel isoform of the alpha 6 beta 1 integrin. J. Cell Biol. 115:843-850; 1991.
11. Czirok A.; Zamir E. A.; Filla M. B.; Little C. D.; Rongish B. J. Extracellular matrix macroassembly dynamics in early vertebrate embryos. Curr. Top. Dev. Biol. 73:237-258; 2006.
12. Decline F.; Rousselle P. Keratinocyte migration requires alpha2beta1 integrin-mediated interaction with the laminin 5 gamma2 chain. J. Cell Sci. 114:811-823; 2001.
13. Desban N.; Lissitzky J. C.; Rousselle P.; Duband J. L. alpha1beta1-integrin engagement to distinct laminin-1 domains orchestrates spreading, migration and survival of neural crest cells through independent signaling pathways. J. Cell Sci. 119:3206-3218; 2006.
14. Goto M.; Sumiyoshi H.; Sakai T.; Fassler R.; Ohashi S.; Adachi E.; Yoshioka H.; Fujiwara S. Elimination of epiplakin by gene targeting results in acceleration of keratinocyte migration in mice. Mol. Cell. Biol. 26:548-558; 2006.
15. Hayashi Y.; Furue M. K.; Okamoto T.; Ohnuma K.; Myoishi Y.; Fukuhara Y.; Abe T.; Sato J. D.; Hata R.; Asashima M. Integrins regulate mouse embryonic stem cell self-renewal. Stem Cells 25:3005-3015; 2007.
16. Hehlgans S.; Haase M.; Cordes N. Signalling via integrins: Implications for cell survival and anticancer strategies. Biochim. Biophys. Acta 1775:163-180; 2007.
17. Hynes R. O. Integrins: Bidirectional, allosteric signaling machines. Cell 110:673-687; 2002.
18. Khoshnoodi J.; Pedchenko V.; Hudson B. G. Mammalian collagen IV. Microsc. Res. Tech. 71:357-370; 2008.
19. Kim Y. S.; Park H. J.; Hong M. H.; Kang P. M.; Morgan J. P.; Jeong M. H.; Cho J. G.; Park J. C.; Ahn Y. TNF-alpha enhances engraftment of mesenchymal stem cells into infarcted myocardium. Front. Biosci. 14:2845-2856; 2009.
20. Kitaori T.; Ito H.; Schwarz E. M.; Tsutsumi R.; Yoshitomi H.; Oishi S.; Nakano M.; Fujii N.; Nagasawa T.; Nakamura T. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum. 60:813-823; 2009.
21. Kofidis T.; de Bruin J. L.; Yamane T.; Balsam L. B.; Lebl D. R.; Swijnenburg R. J.; Tanaka M.; Weissman I. L.; Robbins R. C. Insulin-like growth factor promotes engraftment, differentiation, and functional improvement after transfer of embryonic stem cells for myocardial restoration. Stem Cells 22:1239-1245; 2004.
22. Kofidis T.; de Bruin J. L.; Yamane T.; Tanaka M.; Lebl D. R.; Swijnenburg R. J.; Weissman I. L.; Robbins R. C. Stimulation of paracrine pathways with growth factors enhances embryonic stem cell engraftment and host-specific differentiation in the heart after ischemic myocardial injury. Circulation 111:2486-2493; 2005.
23. Laflamme M. A.; Chen K. Y.; Naumova A. V.; Muskheli V.; Fugate J. A.; Dupras S. K.; Reinecke H.; Xu C.; Hassanipour M.; Police S.; O'Sullivan C.; Collins L.; Chen Y.; Minami E.; Gill E. A.; Ueno S.; Yuan C.; Gold J.; Murry C. E. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25:1015-1024; 2007.
24. Lee J. M.; Dedhar S.; Kalluri R.; Thompson E. W. The epithelial-mesenchymal transition: New insights in signaling, development, and disease. J. Cell Biol. 172:973-981; 2006.
25. Lee K. H.; Chuang C. K.; Wang H. W.; Stone L.; Chen C. H.; Tu C. F. An alternative simple method for mass production of chimeric embryos by coculturing denuded embryos and embryonic stem cells in Eppendorf vials. Theriogenology 67:228-237; 2007.
26. Leitinger B.; Hohenester E. Mammalian collagen receptors. Matrix Biol. 26:146-155; 2007.
27. Li K.; Chuen C. K.; Lee S. M.; Law P.; Fok T. F.; Ng P. C.; Li C. K.; Wong D.; Merzouk A.; Salari H.; Gu G. J.; Yuen P. M. Small peptide analogue of SDF-1alpha supports survival of cord blood CD34+ cells in synergy with other cytokines and enhances their ex vivo expansion and engraftment into nonobese diabetic/severe combined immunodeficient mice. Stem Cells 24:55-64; 2006.
28. Li S.; Tanaka H.; Wang H. H.; Yoshiyama S.; Kumagai H.; Nakamura A.; Brown D. L.; Thatcher S. E.; Wright G. L.; Kohama K. Intracellular signal transduction for migration and actin remodeling in vascular smooth muscle cells after sphingosylphosphorylcholine stimulation. Am. J. Physiol. Heart Circ. Physiol. 291:H1262-1272; 2006.
29. Lock J. G.; Wehrle-Haller B.; Stromblad S. Cell-matrix adhesion complexes: Master control machinery of cell migration. Semin. Cancer Biol. 18:65-76; 2008.
30. Matsuda R.; Yoshikawa M.; Kimura H.; Ouji Y.; Nakase H.; Nishimura F.; Nonaka J.; Toriumi H.; Yamada S.; Nishiofuku M.; Moriya K.; Ishizaka S.; Nakamura M.; Sakaki T. Cotransplantation of mouse embryonic stem cells and bone marrow stromal cells following spinal cord injury suppresses tumor development. Cell Transplant. 18:39-54; 2009.
31. Mooney D. J.; Vandenburgh H. Cell delivery mechanisms for tissue repair. Cell Stem Cell 2:205-213; 2008.
32. Murry C. E.; Keller G. Differentiation of embryonic stem cells to clinically relevant populations: Lessons from embryonic development. Cell 132:661-680; 2008.
33. Nishikawa S.; Jakt L. M.; Era T. Embryonic stem-cell culture as a tool for developmental cell biology. Nat. Rev. Mol. Cell Biol. 8:502-507; 2007.
34. Pan G.; Thomson J. A. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res. 17:42-49; 2007.
35. Parameswaran K.; Radford K.; Zuo J.; Janssen L. J.; O'Byrne P. M.; Cox P. G. Extracellular matrix regulates human airway smooth muscle cell migration. Eur. Respir. J. 24:545-551; 2004.
36. Passier R.; van Laake L. W.; Mummery C. L. Stem-cell-based therapy and lessons from the heart. Nature 453:322-329; 2008.
37. Perris R.; Syfrig J.; Paulsson M.; Bronner-Fraser M. Molecular mechanisms of neural crest cell attachment and migration on types I and IV collagen. J. Cell Sci. 106(Pt. 4):1357-1368; 1993.
38. Poschl E.; Schlotzer-Schrehardt U.; Brachvogel B.; Saito K.; Ninomiya Y.; Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:1619-1628; 2004.
39. Rhoads D. S.; Guan J. L. Analysis of directional cell migration on defined FN gradients: Role of intracellular signaling molecules. Exp. Cell Res. 313:3859-3867; 2007.
40. Rosova I.; Dao M.; Capoccia B.; Link D.; Nolta J. A. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26:2173-2182; 2008.
41. Salamat M.; Miosge N.; Herken R. Development of Reichert's membrane in the early mouse embryo. Anat. Embryol. 192:275-281; 1995.
42. Schwarzbauer J. Basement membranes: Putting up the barriers. Curr. Biol. 9:R242-244; 1999.
43. Shim J. H.; Kim S. E.; Woo D. H.; Kim S. K.; Oh C. H.; McKay R.; Kim J. H. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 50:1228-1238; 2007.
44. Stendahl J. C.; Kaufman D. B.; Stupp S. I. Extracellular matrix in pancreatic islets: Relevance to scaffold design and transplantation. Cell Transplant. 18:1-12; 2009.
45. Tabata Y. Biomaterial technology for tissue engineering applications. J. R. Soc. Interface 6(Suppl. 3):S311-324; 2009.
46. Teti A. Regulation of cellular functions by extracellular matrix. J. Am. Soc. Nephrol. 2:S83-87; 1992.
47. Thiery J. P.; Sleeman J. P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7:131-142; 2006.
48. Thorsteinsdottir S. Basement membrane and fibronectin matrix are distinct entities in the developing mouse blastocyst. Anat. Rec. 232:141-149; 1992.
49. van Horssen R.; Galjart N.; Rens J. A.; Eggermont A. M.; ten Hagen T. L. Differential effects of matrix and growth factors on endothelial and fibroblast motility: Application of a modified cell migration assay. J. Cell. Biochem. 99:1536-1552; 2006.
50. Vogel W. F.; Abdulhussein R.; Ford C. E. Sensing extracellular matrix: An update on discoidin domain receptor function. Cell. Signal. 18:1108-1116; 2006.
51. Williamson R. A.; Henry M. D.; Daniels K. J.; Hrstka R. F.; Lee J. C.; Sunada Y.; Ibraghimov-Beskrovnaya O.; Campbell K. P. Dystroglycan is essential for early embryonic development: Disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6:831-841; 1997.
52. Wong P.; Coulombe P. A. Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. J. Cell Biol. 163:327-337; 2003.
53. Yamaguchi J.; Kusano K. F.; Masuo O.; Kawamoto A.; Silver M.; Murasawa S.; Bosch-Marce M.; Masuda H.; Losordo D. W.; Isner J. M.; Asahara T. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322-1328; 2003