Abstract
Gicerin is an immunoglobulin superfamily cell adhesion molecule purified from chicken gizzards. This molecule displays an adhesive interaction with a laminin-like protein as well as with gicerin itself. Gicerin appears in embryonic tissues and plays a role in chick development through its cell adhesive properties. An increase in gicerin expression is found in some sporadic tumors of the chicken. To elucidate the possible role of gicerin in tumor progression in chickens, we introduced gicerin cDNA into an endogenous gicerin negative lymphoma MDCC-MSB1 cell line, and subsequently analyzed them for changes in their metastatic potentials. After intravenous implantation of the gicerin transfectants into chickens, the metastatic potential to the lung, liver and kidney was enhanced compared with parental MDCC-MSB1 cells. Self-aggregation activity was increased in gicerin transfectants. In addition, adhesive and migratory activities of the gicerin transfectants to the gicerin ligands were enhanced in vitro. These findings indicate that gicerin can contribute to the malignancy and metastatic properties of lymphoma.
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Alais S, Allioli N, Pujades C, Duband JL, Vainio O, Imhof BA, Dunon D (2001) HEMCAM/CD146 downregulates cell surface expression of beta 1 integrins. J Cell Sci 114:1847–1859
Albelda SM (1993) Role of integrins and other cell adhesion molecules in tumor progression and metastasis. Lab Invest 68:4–17
Calnek BW, Witter RL (1997) Marek's disease. In: Calnek BW (ed) Diseases of poultry, 10th edn. Iowa State University Press, Ames, IA, pp 369–413
Edelman GM (1983) Cell adhesion and the molecular processes of morphogenesis. Rev Biochem 54:5–169
Hayashi Y, Miki N (1985) Purification and characterization of a neurite outgrowth factor from chicken gizzard smooth muscle. J Biol Chem 260:14269–14278
Hirai K, Maotani K, Ikuta K, Ysue H, Ishibashi M, Kato S (1986) Chromosomal sites for Marek's disease virus DNA in two chicken lymphoblastoid cell lines MDCC-MSB1 and MDCC-RP1. Virology 152:256–261
Johnson JP, Bar-Eli M, Jansen B, Markhof E (1997) Melanoma progression-associated glycoprotein MUC18/MCAM mediates homophilic adhesion through interaction with a heterophilic ligand. Int J Cancer 73:769–774
Kato S, Taniura H, Taira E, Miki N (1992) Involvement of a receptor for neurite outgrowth factor (NOFR) in the cerebellar neurogenesis. Neurosci Lett 140:78–80
Klymkowsky MW, Parr B (1995) The body language of cells: the intimate connection between cell adhesion and behavior. Cell 83:5–8
Obrink B (1986) Epithelial cell adhesion molecules. Exp Cell Res 163:1–21
Ohashi K, Mikami T, Kodama H, Izawa H (1987) Suppression of NK activity of spleen cells by chicken fetal antigen present on Marek's disease lymphoblastoid cell line cells. Int J Cancer 40:378–382
Okumura S, Muraoka O, Tanaka H, Tsukamoto Y, Kohama K, Miki N, Taira E (2001) Involvement of gicerin in the extension of microvilli. Exp Cell Res 271:269–276
Sers C, Kirsch K, Rothbacher U, Riethmuller G, Johnson JP (1993) Genomic organization of the melanoma-associated glycoprotein MUC18: implications for the evolution of the immunoglobulin domains. Proc Natl Acad Sci U S A 90:8514–8518
Shih IM (1999) The role of CD146 (Mel-CAM) in biology and pathology. J Pathol 189:4–11
Shih IM, Speicher D, Hsu MY, Levine E, Herlyn M (1997) Melanoma cell-cell interactions are mediated through heterophilic Mel-CAM/ligand adhesion. Cancer Res 57:3835–3840
Taira E, Takaha N, Miki N (1993) Extracellular matrix proteins with neurite promoting activity and their receptors. Neurosci Res 17:1–8
Taira E, Takaha N, Taniura H, Kim CH, Miki N (1994) Molecular cloning and functional expression of gicerin, a novel cell adhesion molecule that binds to neurite outgrowth factor. Neuron 12:861–872
Taira E, Nagino T, Taniura H, Takaha N, Kim CH, Kuo CH, Li BS, Higuchi H, Miki N (1995) Expression and functional analysis of a novel isoform of gicerin, an immunoglobulin superfamily cell adhesion molecule. J Biol Chem 270:28681–28687
Taira E, Kohama K, Tsukamoto Y, Okumura S, Miki N (2003) Characterization of gicerin/MUC18/CD146 in the rat nervous system. J Cell Physiol (in press)
Takeichi M (1977) Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol 75:993–1001
Takeichi M (1993) Cadherins in cancer; implications for invasion and metastasis. Curr Opin Cell Biol 5:806–811
Taniura H, Kuo CH, Hayashi Y, Miki N (1991) Purification and characterization of an 82-kD membrane protein as a neurite outgrowth factor binding protein: possible involvement of NOF binding protein in axonal outgrowth in developing retina. J Cell Biol 112:313–322
Tsukamoto Y, Taira E, Kotani T, Yamate J, Wada S, Takaha N, Miki N, Sakuma S (1996) Involvement of gicerin, a cell adhesion molecule, in tracheal development and regeneration. Cell Growth Differ 7:1761–1767
Tsukamoto Y, Matsumoto M, Kotani T, Taira E, Takaha N, Miki N, Yamate J, Sakuma S (1997a) The expression of gicerin, a cell adhesion molecule, in regenerating process of collecting ducts and ureters of the chicken kidney after the nephrotrophic strain of infectious bronchitis virus infection. Avian Pathol 26:245–255
Tsukamoto Y, Taira E, Yamate J, Nakane Y, Kajimura K, Tsudzuki M, Kiso Y, Kotani T, Miki N, Sakuma S (1997b) Gicerin, a cell adhesion molecule, participates in the histogenesis of retina. J Neurobiol 33:769–780
Tsukamoto Y, Matsumoto T, Taira E, Kotani T, Yamate J, Takaha N, Tatesaki R, Namikawa T, Miki N, Sakuma S (1998) Adhesive ability of gicerin, a cell adhesion molecule, in kidneys and nephroblastomas of chickens. Cell Tissue Res 292:137–142
Tsukamoto Y, Taira E, Kajimura K, Yamate J, Kotani T, Amin H, Kohama K, Sakuma S, Miki N, Sasaki F (1999a) Involvement of gicerin, a cell adhesion molecule, in development and regeneration of oviduct, and metastasis of oviductal adenocarcinomas of the chicken. Exp Cell Res 247:329–338
Tsukamoto Y, Taira E, Nakane Y, Tsudzuki M, Kohama K, Amin H, Miki N, Sasaki F (1999b) Expression of gicerin, a cell adhesion molecule, in the abnormal retina in Silver Plumage Color Mutation of Japanese quail (Coturnix japonica). Neurosci Lett 266:53–56
Tsukamoto Y, Taira E, Miki N, Sasaki F (2001a) The role of gicerin, a novel cell adhesion molecule, in development, regeneration and neoplasia. Histol Histopathol 16:563–571
Tsukamoto Y, Kotani T, Hiroi S, Egawa M, Ogawa K, Sasaki F, Taira E (2001b) Expression and adhesive ability of gicerin, a cell adhesion molecule, in the pock lesions of chorioallantoic membranes infected with an avian poxvirus. Can J Vet Res 65:248–253
Vainio O, Dunon D, Aissi F, Dangy JP, McNagny KM, Imhof BA (1996) HEMCAM, an adhesion molecule expressed by c-kit+ hemopoietic progenitors. J Cell Biol 135:1655–1668
Venugopal K, Payne LM (1995) Molecular pathogenesis of Marek's disease—recent developments. Avian Pathol 24:597–609
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We thank Miss Mahiro Hattori and Miss Naoko Wada for their technical assistance.
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This work was supported in part by a Grant-in-Aid for Scientific Research (No. 13760210), and a grant for Scientific Research on Priority Areas "Cancer" (No. 12215133), from the Ministry of Education, Science, Sports and Culture, Japan, grants from the Uehara Memorial Foundation and Senri Life Science and a Grant-in-Aid for Advanced Scientific Research from Osaka Prefecture University
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Tsuchiya, S., Tsukamoto, Y., Furuya, M. et al. Gicerin, a cell adhesion molecule, promotes the metastasis of lymphoma cells of the chicken. Cell Tissue Res 314, 389–397 (2003). https://doi.org/10.1007/s00441-003-0810-5
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DOI: https://doi.org/10.1007/s00441-003-0810-5