Laminin Isoforms in Human Embryonic Stem Cells: Synthesis, Receptor Usage and Growth Support

Overview

Journal J Cell Mol Med

Specialties Cell Biology
Molecular Biology

Date 2009 Apr 29

PMID 19397785

Citations 25

Authors

Sanna Vuoristo

Ismo Virtanen

Minna Takkunen

Jaan Palgi

Yamato Kikkawa

Patricia Rousselle

Kiyotoshi Sekiguchi

Timo Tuuri

Timo Otonkoski

Affiliations

Soon will be listed here.

Abstract

To reveal the functional intrinsic niche of human embryonic stem cells (hESC) we examined the production of basement membrane (BM) proteins and the presence of their receptors in feeder-free cell culture conditions. In addition, we investigated binding of hESCs to purified human BM proteins and identified the receptors mediating these contacts. Also, we tested whether purified human laminin (Lm) isoforms have a role in hESC self-renewal and growth in short-term cultures. The results show that hESCs synthesize Lm alpha(1) and Lm alpha(5) chains together with Lm beta(1) and gamma(1) chains suggesting the production of Lms-111 and -511 into the culture medium and deposits on cells. hESCs contain functionally important integrin (Int) subunits, Int beta(1), alpha(3), alpha(6), alpha(5), beta(5) and alpha(V), as well as the Lm alpha(5) receptor, Lutheran (Lu) glycoprotein and its truncated form, basal cell adhesion molecule (B-CAM). In cell adhesion experiments, Int beta(1) was crucial for adhesion to most of the purified human BM proteins. Lu/B-CAM mediated adhesion to Lm-511 together with Int alpha(3)beta(1), and was essential for the adhesion of hESCs to embryonic feeder cells. Adhesion to Lm-411 was mediated by Int alpha(6)beta(1). Lm-511 supported hESC growth in defined medium equally well as Matrigel. These results provide consequential information of the biological role of BM in hESCs, warranting further investigation of BM biology of human pluripotent stem cells.

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References

Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S . Differences between human and mouse embryonic stem cells. Dev Biol. 2004; 269(2):360-80. DOI: 10.1016/j.ydbio.2003.12.034. View

Fujiwara H, Kikkawa Y, Sanzen N, Sekiguchi K . Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through alpha3beta1 and alpha6beta1 integrins. J Biol Chem. 2001; 276(20):17550-8. DOI: 10.1074/jbc.M010155200. View

Xu C, Inokuma M, Denham J, Golds K, Kundu P, Gold J . Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol. 2001; 19(10):971-4. DOI: 10.1038/nbt1001-971. View

Kikkawa Y, Moulson C, Virtanen I, Miner J . Identification of the binding site for the Lutheran blood group glycoprotein on laminin alpha 5 through expression of chimeric laminin chains in vivo. J Biol Chem. 2002; 277(47):44864-9. DOI: 10.1074/jbc.M208731200. View

Ylanne J, HORMIA M, Jarvinen M, Vartio T, Virtanen I . Platelet glycoprotein IIb/IIIa complex in cultured cells. Localization in focal adhesion sites in spreading HEL cells. Blood. 1988; 72(5):1478-86. View

Kikkawa Y, Miner J . Review: Lutheran/B-CAM: a laminin receptor on red blood cells and in various tissues. Connect Tissue Res. 2006; 46(4-5):193-9. DOI: 10.1080/03008200500344074. View

Pasqualini R, Bodorova J, Ye S, Hemler M . A study of the structure, function and distribution of beta 5 integrins using novel anti-beta 5 monoclonal antibodies. J Cell Sci. 1993; 105 ( Pt 1):101-11. DOI: 10.1242/jcs.105.1.101. View

Ullmann U, Int Veld P, Gilles C, Sermon K, De Rycke M, van de Velde H . Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions. Mol Hum Reprod. 2006; 13(1):21-32. DOI: 10.1093/molehr/gal091. View

Virtanen I, Banerjee M, Palgi J, Korsgren O, Lukinius A, Thornell L . Blood vessels of human islets of Langerhans are surrounded by a double basement membrane. Diabetologia. 2008; 51(7):1181-91. DOI: 10.1007/s00125-008-0997-9. View

10.

Tamura R, Rozzo C, Starr L, Chambers J, Reichardt L, Cooper H . Epithelial integrin alpha 6 beta 4: complete primary structure of alpha 6 and variant forms of beta 4. J Cell Biol. 1990; 111(4):1593-604. PMC: 2116232. DOI: 10.1083/jcb.111.4.1593. View

11.

Engvall E, Ruoslahti E . Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer. 1977; 20(1):1-5. DOI: 10.1002/ijc.2910200102. View

12.

Li S, Harrison D, Carbonetto S, Fassler R, Smyth N, Edgar D . Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J Cell Biol. 2002; 157(7):1279-90. PMC: 2173546. DOI: 10.1083/jcb.200203073. View

13.

Werb Z, Tremble P, Behrendtsen O, Crowley E, Damsky C . Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J Cell Biol. 1989; 109(2):877-89. PMC: 2115739. DOI: 10.1083/jcb.109.2.877. View

14.

Li S, Edgar D, Fassler R, Wadsworth W, Yurchenco P . The role of laminin in embryonic cell polarization and tissue organization. Dev Cell. 2003; 4(5):613-24. DOI: 10.1016/s1534-5807(03)00128-x. View

15.

Hemler M, Sanchez-Madrid F, Flotte T, Krensky A, Burakoff S, Bhan A . Glycoproteins of 210,000 and 130,000 m.w. on activated T cells: cell distribution and antigenic relation to components on resting cells and T cell lines. J Immunol. 1984; 132(6):3011-8. View

16.

Takkunen M, Grenman R, Hukkanen M, Korhonen M, Garcia de Herreros A, Virtanen I . Snail-dependent and -independent epithelial-mesenchymal transition in oral squamous carcinoma cells. J Histochem Cytochem. 2006; 54(11):1263-75. DOI: 10.1369/jhc.6A6958.2006. View

17.

Cooper H, Tamura R, 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. 1991; 115(3):843-50. PMC: 2289180. DOI: 10.1083/jcb.115.3.843. View

18.

Wondimu Z, Geberhiwot T, Ingerpuu S, Juronen E, Xie X, Lindbom L . An endothelial laminin isoform, laminin 8 (alpha4beta1gamma1), is secreted by blood neutrophils, promotes neutrophil migration and extravasation, and protects neutrophils from apoptosis. Blood. 2004; 104(6):1859-66. DOI: 10.1182/blood-2004-01-0396. View

19.

Hemler M, Brenner M, McLEAN J, Strominger J . Antigenic stimulation regulates the level of expression of interleukin 2 receptor on human T cells. Proc Natl Acad Sci U S A. 1984; 81(7):2172-5. PMC: 345459. DOI: 10.1073/pnas.81.7.2172. View

20.

Fradet Y, Cordon-Cardo C, Thomson T, Daly M, WHITMORE Jr W, LLOYD K . Cell surface antigens of human bladder cancer defined by mouse monoclonal antibodies. Proc Natl Acad Sci U S A. 1984; 81(1):224-8. PMC: 344644. DOI: 10.1073/pnas.81.1.224. View