Laminin α5 mediates ectopic adhesion of hepatocellular carcinoma through integrins and/or Lutheran/basal cell adhesion molecule

Experimental Cell Research

Volumn 314, Issue 14, 2008, Pages 2579-2590

  Kikkawa, Yamato ^a,b   Sudo, Ryo ^c   Kon, Junko ^b   Mizuguchi, Toru ^b   Nomizu, Motoyoshi ^a   Hirata, Koichi ^b   Mitaka, Toshihiro ^b  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c KEIO UNIVERSITY   (Japan)

Author keywords

Basal cell adhesion molecule; Hepatocellular carcinoma; Integrin; Laminin; Lutheran

Indexed keywords

ANTIBODY; CELL ADHESION MOLECULE; INTEGRIN; LAMININ; LAMININ ALPHA5; LUTHERAN BASAL CELL ADHESION MOLECULE; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 6;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL CELL; BASEMENT MEMBRANE; BILE DUCT; BLOOD VESSEL; CANCER GROWTH; CELL ADHESION; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; LIVER CELL CARCINOMA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

EID: 48849092900     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.05.021     Document Type: Article

References (67)

1. Llovet J.M., Burroughs A., and Bruix J. Hepatocellular carcinoma. Lancet 362 (2003) 1907-1917
2. Laurent C., Rullier E., Feyler A., Masson B., and Saric J. Resection of noncolorectal and nonneuroendocrine liver metastases: late metastases are the only chance of cure. World. J. Surg 25 (2001) 1532-1536
3. Boudreau N., and Bissell M.J. Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr. Opin. Cell Biol 10 (1998) 640-646
4. Donato M.F., Colombo M., Matarazzo M., and Paronetto F. Distribution of basement membrane components in human hepatocellular carcinoma. Cancer 63 (1989) 272-279
5. Torimura T., Ueno T., Inuzuka S., Kin M., Ohira H., Kimura Y., Majima Y., Sata M., Abe H., and Tanikawa K. The extracellular matrix in hepatocellular carcinoma shows different localization patterns depending on the differentiation and the histological pattern of tumors: immunohistochemical analysis. J. Hepatol 21 (1994) 37-46
6. Aumailley M., Bruckner-Tuderman L., Carter W.G., Deutzmann R., Edgar D., Ekblom P., Engel J., Engvall E., Hohenester E., Jones J.C., Kleinman H.K., Marinkovich M.P., Martin G.R., Mayer U., Meneguzzi G., Miner J.H., Miyazaki K., Patarroyo M., Paulsson M., Quaranta V., Sanes J.R., Sasaki T., Sekiguchi K., Sorokin L.M., Talts J.F., Tryggvason K., Uitto J., Virtanen I., von der Mark K., Wewer U.M., Yamada Y., and Yurchenco P.D. A simplified laminin nomenclature. Matrix Biol 24 (2005) 326-332
7. Colognato H., and Yurchenco P.D. Form and function: the laminin family of heterotrimers. Dev. Dyn 218 (2000) 213-234
8. Suzuki N., Yokoyama F., and Nomizu M. Functional sites in the laminin alpha chains. Connect Tissue Res 46 (2005) 142-152
9. Kikkawa Y., and Miner J.H. Review: Lutheran/B-CAM: a laminin receptor on red blood cells and in various tissues. Connect Tissue Res 46 (2005) 193-199
10. Miner J.H., Patton B.L., Lentz S.I., Gilbert D.J., Snider W.D., Jenkins N.A., Copeland N.G., and Sanes J.R. The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J. Cell Biol 137 (1997) 685-701
11. Sorokin L.M., Pausch F., Frieser M., Kroger S., Ohage E., and Deutzmann R. Developmental regulation of the laminin alpha5 chain suggests a role in epithelial and endothelial cell maturation. Dev. Biol 189 (1997) 285-300
12. Libby R.T., Champliaud M.F., Claudepierre T., Xu Y., Gibbons E.P., Koch M., Burgeson R.E., Hunter D.D., and Brunken W.J. Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J. Neurosci 20 (2000) 6517-6528
13. Miner J.H., Cunningham J., and Sanes J.R. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell Biol 143 (1998) 1713-1723
14. Miner J.H., and Li C. Defective glomerulogenesis in the absence of laminin α5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev. Biol 217 (2000) 278-289
15. Nguyen N.M., Miner J.H., Pierce R.A., and Senior R.M. Laminin α5 is required for lobar septation and visceral pleural basement membrane formation in the developing mouse lung. Dev. Biol 246 (2002) 231-244
16. Bolcato-Bellemin A.L., Lefebvre O., Arnold C., Sorokin L., Miner J.H., Kedinger M., and Simon-Assmann P. Laminin α5 chain is required for intestinal smooth muscle development. Dev. Biol 260 (2003) 376-390
17. Kikkawa Y., Virtanen I., and Miner J.H. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J. Cell Biol 161 (2003) 187-196
18. Fukumoto S., Miner J.H., Ida H., Fukumoto E., Yuasa K., Miyazaki H., Hoffman M.P., and Yamada Y. Laminin alpha5 is required for dental epithelium growth and polarity and the development of tooth bud and shape. J. Biol. Chem 281 (2006) 5008-5016
19. Coles E.G., Gammill L.S., Miner J.H., and Bronner-Fraser M. Abnormalities in neural crest cell migration in laminin alpha5 mutant mice. Dev. Biol 289 (2006) 218-228
20. Rebustini I.T., Patel V.N., Stewart J.S., Layvey A., Georges-Labouesse E., Miner J.H., and Hoffman M.P. Laminin alpha5 is necessary for submandibular gland epithelial morphogenesis and influences FGFR expression through beta1 integrin signaling. Dev. Biol 308 (2007) 15-29
21. Li J., Tzu J., Chen Y., Zhang Y.P., Nguyen N.T., Gao J., Bradley M., Keene D.R., Oro A.E., Miner J.H., and Marinkovich M.P. Laminin-10 is crucial for hair morphogenesis. EMBO J 22 (2003) 2400-2410
22. Nguyen N.M., Kelley D.G., Schlueter J.A., Meyer M.J., Senior R.M., and Miner J.H. Epithelial laminin alpha5 is necessary for distal epithelial cell maturation, VEGF production, and alveolization in the developing murine lung. Dev. Biol 282 (2005) 111-125
23. Shannon M.B., Patton B.L., Harvey S.J., and Miner J.H. A hypomorphic mutation in the mouse laminin alpha5 gene causes polycystic kidney disease. J. Am. Soc. Nephrol 17 (2006) 1913-1922
24. Kikkawa Y., Mochizuki Y., Miner J.H., and Mitaka T. Transient expression of laminin alpha1 chain in regenerating murine liver: restricted localization of laminin chains and nidogen-1. Exp. Cell Res 305 (2005) 99-109
25. Seebacher T., Medina J.L., and Bade E.G. Laminin alpha 5, a major transcript of normal and malignant rat liver epithelial cells, is differentially expressed in developing and adult liver. Exp. Cell Res 237 (1997) 70-76
26. Hoshiba T., Cho C.S., Murakawa A., Okahata Y., and Akaike T. The effect of natural extracellular matrix deposited on synthetic polymers on cultured primary hepatocytes. Biomaterials 27 (2006) 4519-4528
27. Cui S., Hano H., Sakata A., Harada T., Liu T., Takai S., and Ushigome S. Enhanced CD34 expression of sinusoid-like vascular endothelial cells in hepatocellular carcinoma. Pathol. Int 46 (1996) 751-756
28. Torimura T., Ueno T., Kin M., Inuzuka S., Sugawara H., Tamaki S., Tsuji R., Sujaku K., Sata M., and Tanikawa K. Coordinated expression of integrin alpha6beta1 and laminin in hepatocellular carcinoma. Hum. Pathol 28 (1997) 1131-1138
29. Primary liver cancer in Japan. Clinicopathologic features and results of surgical treatment. Liver Cancer Study Group of Japan, Ann. Surg. 211 (1990) 277-287.
30. Virtanen I., Gullberg D., Rissanen J., Kivilaakso E., Kiviluoto T., Laitinen L.A., Lehto V.P., and Ekblom P. Laminin alpha1-chain shows a restricted distribution in epithelial basement membranes of fetal and adult human tissues. Exp. Cell Res 257 (2000) 298-309
31. Cheng Y.S., Champliaud M.F., Burgeson R.E., Marinkovich M.P., and Yurchenco P.D. Self-assembly of laminin isoforms. J. Biol. Chem 272 (1997) 31525-31532
32. Tunggal L., Ravaux J., Pesch M., Smola H., Krieg T., Gaill F., Sasaki T., Timpl R., Mauch C., and Aumailley M. Defective laminin 5 processing in cylindroma cells. Am. J. Pathol 160 (2002) 459-468
33. Sasaki T., Mann K., and Timpl R. Modification of the laminin alpha 4 chain by chondroitin sulfate attachment to its N-terminal domain. FEBS Lett 505 (2001) 173-178
34. Kikkawa Y., Sanzen N., and Sekiguchi K. Isolation and characterization of laminin-10/11 secreted by human lung carcinoma cells. laminin-10/11 mediates cell adhesion through integrin alpha3 beta1. J. Biol. Chem 273 (1998) 15854-15859
35. Tanimizu N., Nishikawa M., Saito H., Tsujimura T., and Miyajima A. Isolation of hepatoblasts based on the expression of Dlk/Pref-1. J. Cell Sci 116 (2003) 1775-1786
36. Kikkawa Y., Moulson C.L., Virtanen I., and Miner J.H. 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 277 (2002) 44864-44869
37. Kikkawa Y., Sasaki T., Nguyen M.T., Nomizu M., Mitaka T., and Miner J.H. The LG1-3 tandem of laminin alpha5 harbors the binding sites of Lutheran/basal cell adhesion molecule and alpha3beta1/alpha6beta1 integrins. J. Biol. Chem 282 (2007) 14853-14860
38. Mitaka T., Sato F., Mizuguchi T., Yokono T., and Mochizuki Y. Reconstruction of hepatic organoid by rat small hepatocytes and hepatic nonparenchymal cells. Hepatology 29 (1999) 111-125
39. Ido H., Nakamura A., Kobayashi R., Ito S., Li S., Futaki S., and Sekiguchi K. The requirement of the glutamic acid residue at the third position from the carboxyl termini of the laminin gamma chains in integrin binding by laminins. J. Biol. Chem 282 (2007) 11144-11154
40. Kikkawa Y., Sanzen N., Fujiwara H., Sonnenberg A., and Sekiguchi K. Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J. Cell Sci. 113 Pt 5 (2000) 869-876
41. Shimizu H., Hosokawa H., Ninomiya H., Miner J.H., and Masaki T. Adhesion of cultured bovine aortic endothelial cells to laminin-1 mediated by dystroglycan. J. Biol. Chem 274 (1999) 11995-12000
42. Udani M., Zen Q., Cottman M., Leonard N., Jefferson S., Daymont C., Truskey G., and Telen M.J. Basal cell adhesion molecule/Lutheran protein. The receptor critical for sickle cell adhesion to laminin. J. Clin. Invest 101 (1998) 2550-2558
43. El Nemer W., Gane P., Colin Y., Bony V., Rahuel C., Galacteros F., Cartron J.P., and Le Van Kim C. The Lutheran blood group glycoproteins, the erythroid receptors for laminin, are adhesion molecules. J. Biol. Chem 273 (1998) 16686-16693
44. Moulson C.L., Li C., and Miner J.H. Localization of Lutheran, a novel laminin receptor, in normal, knockout, and transgenic mice suggests an interaction with laminin α5 in vivo. Dev. Dyn 222 (2001) 101-114
45. Campbell I.G., Foulkes W.D., Senger G., Trowsdale J., Garin-Chesa P., and Rettig W.J. Molecular cloning of the B-CAM cell surface glycoprotein of epithelial cancers: a novel member of the immunoglobulin superfamily. Cancer Res 54 (1994) 5761-5765
46. Parsons S.F., Mallinson G., Holmes C.H., Houlihan J.M., Simpson K.L., Mawby W.J., Spurr N.K., Warne D., Barclay A.N., and Anstee D.J. The Lutheran blood group glycoprotein, another member of the immunoglobulin superfamily, is widely expressed in human tissues and is developmentally regulated in human liver. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 5496-5500
47. Forsberg E., Paulsson M., Timpl R., and Johansson S. Characterization of a laminin receptor on rat hepatocytes. J. Biol. Chem 265 (1990) 6376-6381
48. Timpl R., Tisi D., Talts J.F., Andac Z., Sasaki T., and Hohenester E. Structure and function of laminin LG modules. Matrix Biol 19 (2000) 309-317
49. Koch M., Olson P.F., Albus A., Jin W., Hunter D.D., Brunken W.J., Burgeson R.E., and Champliaud M.F. Characterization and expression of the laminin gamma3 chain: a novel, non-basement membrane-associated, laminin chain. J. Cell Biol. 145 (1999) 605-618
50. Yamanaka N., Okamoto E., Toyosaka A., Mitunobu M., Fujihara S., Kato T., Fujimoto J., Oriyama T., Furukawa K., and Kawamura E. Prognostic factors after hepatectomy for hepatocellular carcinomas. A univariate and multivariate analysis. Cancer 65 (1990) 1104-1110
51. Gu J., Sumida Y., Sanzen N., and Sekiguchi K. Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130(Cas)-CrkII-DOCK180 pathway. J. Biol. Chem 276 (2001) 27090-27097
52. Gu J., Fujibayashi A., Yamada K.M., and Sekiguchi K. Laminin-10/11 and fibronectin differentially prevent apoptosis induced by serum removal via phosphatidylinositol 3-kinase/Akt- and MEK1/ERK-dependent pathways. J. Biol. Chem 277 (2002) 19922-19928
53. Gu J., Nishiuchi R., and Sekiguchi K. Matrix metalloproteinase-2 is involved in A549 cell migration on laminin-10/11. Biochem. Biophys. Res. Commun 296 (2002) 73-77
54. Folkman J., Watson K., Ingber D., and Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 339 (1989) 58-61
55. Anthony P.P., and Ramani P. Endothelial markers in malignant vascular tumours of the liver: superiority of QB-END/10 over von Willebrand factor and Ulex europaeus agglutinin 1. J. Clin. Pathol 44 (1991) 29-32
56. Thyboll J., Kortesmaa J., Cao R., Soininen R., Wang L., Iivanainen A., Sorokin L., Risling M., Cao Y., and Tryggvason K. Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Mol. Cell. Biol 22 (2002) 1194-1202
57. Colognato-Pyke H., O'Rear J.J., Yamada Y., Carbonetto S., Cheng Y.S., and Yurchenco P.D. Mapping of network-forming, heparin-binding, and alpha 1 beta 1 integrin-recognition sites within the alpha-chain short arm of laminin-1. J. Biol. Chem 270 (1995) 9398-9406
58. Torimura T., Ueno T., Kin M., Ogata R., Inuzuka S., Sugawara H., Kurotatsu R., Shimada M., Yano H., Kojiro M., Tanikawa K., and Sata M. Integrin alpha6beta1 plays a significant role in the attachment of hepatoma cells to laminin. J. Hepatol 31 (1999) 734-740
59. Nejjari M., Hafdi Z., Dumortier J., Bringuier A.F., Feldmann G., and Scoazec J.Y. alpha6beta1 integrin expression in hepatocarcinoma cells: regulation and role in cell adhesion and migration. Int. J. Cancer 83 (1999) 518-525
60. Giannelli G., Fransvea E., Bergamini C., Marinosci F., and Antonaci S. Laminin-5 chains are expressed differentially in metastatic and nonmetastatic hepatocellular carcinoma. Clin. Cancer Res 9 (2003) 3684-3691
61. Bergamini C., Sgarra C., Trerotoli P., Lupo L., Azzariti A., Antonaci S., and Giannelli G. Laminin-5 stimulates hepatocellular carcinoma growth through a different function of alpha6beta4 and alpha3beta1 integrins. Hepatology 46 (2007) 1801-1809
62. Roskam T., De Vos R., David G., Van Dammw B., and Desmet V. Heparan sulphate proteoglycan expression in human primary liver tumours. J. Pathol 185 (1998) 290-297
63. Hines P.C., Zen Q., Burney S.N., Shea D.A., Ataga K.I., Orringer E.P., Telen M.J., and Parise L.V. Novel epinephrine and cyclic AMP-mediated activation of BCAM/Lu-dependent sickle (SS) RBC adhesion. Blood 101 (2003) 3281-3287
64. Gauthier E., Rahuel C., Wautier M.P., El Nemer W., Gane P., Wautier J.L., Cartron J.P., Colin Y., and Le Van Kim C. Protein kinase A-dependent phosphorylation of Lutheran/basal cell adhesion molecule glycoprotein regulates cell adhesion to laminin alpha5. J. Biol. Chem 280 (2005) 30055-30062
65. Murphy M.M., Zayed M.A., Evans A., Parker C.E., Ataga K.I., Telen M.J., and Parise L.V. Role of Rap1 in promoting sickle red blood cell adhesion to laminin via BCAM/LU. Blood 105 (2005) 3322-3329
66. Sakamoto M., Hirohashi S., and Shimosato Y. Early stages of multistep hepatocarcinogenesis: adenomatous hyperplasia and early hepatocellular carcinoma. Hum. Pathol 22 (1991) 172-178
67. Fujiwara H., Kikkawa Y., Sanzen N., and Sekiguchi K. Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through α3β1 and α6β1 integrins. J. Biol. Chem. 276 (2001) 17550-17558