Function and Histopathology of a Cell Adhesion Molecule TSLC1 in Cancer

REFERENCES

• Kuramochi M, Fukuhara H, Nobukuni T, Kanbe T, Maruyama T, Ghosh HP, Pletcher M, Isomura M, Onizuka M, Kitamura T, Sekiya T, Reeves RH, Murakami Y. TSLC1 is a tumor suppressor gene in human non-small cell lung cancer. Nat Genet 2001;27:427–430.
   PubMed Web of Science ®Google Scholar
• Watabe K, Ito A, Koma YI, Kitamura Y. IGSF4: a new intercellular adhesion molecule that is called by three names, TSLC1, SgIGSF and SynCAM, by virtue of its diverse function. Histol Histopathol 2003;18:1321–1329.
   PubMedGoogle Scholar
• Takai Y, Irie K, Shimizu K, Sakisaka T, Ikeda W. Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci 2003;94:655–667.
   PubMed Web of Science ®Google Scholar
• Murakami Y. Involvement of a cell adhesion molecule, TSLC1/ IGSF4, in human oncogenesis. Cancer Sci 2005;96:543–552.
   PubMed Web of Science ®Google Scholar
• Yamada D, Yoshida M, Williams YN, Fukami T, Kikuchi S, Masuda M, Maruyama T, Ohta T, Nakae D, Maekawa A, Kitamura T, Murakami Y. Disruption of spermatogenic cell adhesion and male infertility in mice lacking TSLC1/IGSF4, an immunoglobulin superfamily cell adhesion molecule. Mol Cell Biol 2006;26:3610–3624.
   PubMedGoogle Scholar
• van der Weyden L, Arends MJ, Chausiaux OE, Ellis PJ, Lange UC, Surani MA, Affara N, Murakami Y, Adams DJ, Bradley A. Loss of TSLC1 causes male infertility due to a defect at the spermatid stage of spermatogenesis. Mol Cell Biol 2006;26:3595–3609.
   PubMed Web of Science ®Google Scholar
• Shingai T, Ikeda W, Kakunaga S, Morimoto K, Takekuni K, Itoh S, Satoh K, Takeuchi M, Imai T, Monden M, Takai Y. Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAM1 in cell–cell adhesion and transmembrane protein localization in epithelial cells. J Biol Chem 2003;278:35421–35427.
   PubMed Web of Science ®Google Scholar
• Boles KS, Barchet W, Diacovo T, Cella M, Colonna M. The tumor suppressor TSLC1/NECL-2 triggers NK-cell and CD8+ T-cell responses through the cell-surface receptor CRTAM. Blood 2005;106:779–869.
   PubMed Web of Science ®Google Scholar
• Kakunaga S, Ikeda W, Itoh S, Deguchi-Tawarada M, Ohtsuka T, Mizoguchi A, Takai Y. Nectin-like molecule-1/TSLL1/ SynCAM3: a neural tissue-specific immunoglobulin-like cell–cell adhesion molecule localizing at non-junctional contact sites of presynaptic nerve terminals, axons and glia cell processes. J Cell Sci 2005;118:1267–1277.
   PubMed Web of Science ®Google Scholar
• Hirohashi S, Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci 2003;94:575–581.
   PubMed Web of Science ®Google Scholar
• Mao X, Seidlitz E, Ghosh K, Murakami Y, Ghosh HP. The cytoplasmic domain is critical to the tumor suppressor activity of TSLC1 in non-small cell lung cancer. Cancer Res 2003;63: 7979–7985.
   PubMed Web of Science ®Google Scholar
• Hoover KB, Bryant PJ. The genetics of the protein 4.1 family: organizers of the membrane and cytoskeleton. Curr Opin Cell Biol 2000;12:229–234.
   PubMed Web of Science ®Google Scholar
• Yageta M, Kuramochi M, Masuda M, Fukami T, Fukuhara H, Maruyama T, Shibuya M, Murakami Y. Direct association of TSLC1 and DAL-1, two distinct tumor suppressor proteins in lung cancer. Cancer Res 2002;62:5129–5133.
   PubMed Web of Science ®Google Scholar
• Fukuhara H, Masuda M, Yageta M, Fukami T, Kuramochi M, Maruyama T, Kitamura T, Murakami Y. Association of a lung tumor suppressor TSLC1 with MPP3, a human homologue of Drosophila tumor suppressor Dlg. Oncogene 2003;22:6160–6165.
   PubMed Web of Science ®Google Scholar
• Masuda M, Kikuchi S, Maruyama T, Sakurai-Yageta M, Williams YN, Ghosh HP, Murakami Y. Tumor suppressor in lung cancer (TSLC) 1 suppresses epithelial cell scattering and tubulogenesis. J Biol Chem 2005;280:42164–42171.
   PubMed Web of Science ®Google Scholar
• Sussan TE, Pletcher MT, Murakami Y, Reeves RH. Tumor suppressor in lung cancer 1 (TSLC1) alters tumorigenic growth properties and gene expression. Mol Cancer 2005;4:28.
   PubMedGoogle Scholar
• Lung HL, Cheung AK, Xie D, Cheng Y, Kwong FM, Murakami Y, Guan XY, Sham JS, Chua D, Protopopov AI, Zabarovsky ER, Tsao SW, Stanbridge EJ, Lung ML. TSLC1 is a tumor suppressor gene associated with metastasis in nasopharyngeal carcinoma. Cancer Res 2006;66:9385–9392.
   PubMed Web of Science ®Google Scholar
• Mao X, Seidlitz E, Truant R, Hitt M, Ghosh HP. Re-expression of TSLC1 in a non-small-cell lung cancer cell line induces apoptosis and inhibits tumor growth. Oncogene 2004;23:5632–5642.
   PubMed Web of Science ®Google Scholar
• Hellwinkel OJ, Kedia M, Isbarn H, Budäus L, Friedrich MG. Methylation of the TPEF- and PAX6-promoters is increased in early bladder cancer and in normal mucosa adjacent to pTa tumours. BJU Int 2008;101:753–757.
   PubMed Web of Science ®Google Scholar
• Ando K, Ohira M, Ozaki T, Nakagawa A, Akazawa K, Suenaga Y, Nakamura Y, Koda T, Kamijo T, Murakami Y, Nakagawara A. Expression of TSLC1, a candidate tumor suppressor gene mapped to chromosome 11q23, is downregulated in unfavorable neuroblastoma without promoter hypermethylation. Int J Cancer 2008;123:2087–2094.
   PubMed Web of Science ®Google Scholar
• Ochiai H, Takenobu H, Nakagawa A, Yamaguchi Y, Kimura M, Ohira M, Okimoto Y, Fujimura Y, Koseki H, Kohno Y, Nakagawara A, Kamijo T. Bmi1 is a MYCN target gene that regulates tumorigenesis through repression of KIF1Bbeta and TSLC1 in neuroblastoma. Oncogene 2010;29:2681–2690.
   Google Scholar
• Ito A, Okada M, Uchino K, Wakayama T, Koma Y, Iseki S, Tsubota N, Okita Y, Kitamura Y. Expression of the TSLC1 adhesion molecule in pulmonary epithelium and its down-regulation in pulmonary adenocarcinoma other than bronchioloalveolar carcinoma. Lab Invest 2003;83:1175–1183.
   Google Scholar
• Fukami T, Fukuhara H, Kuramochi M, Maruyama T, Isogai K, Sakamoto M, Takamoto S, Murakami Y. Promoter methylation of the TSLC1 gene in advanced lung tumors and various cancer cell lines. Int J Cancer 2003;107:53–59.
   PubMed Web of Science ®Google Scholar
• Uchino K, Ito A, Wakayama T, Koma Y, Okada T, Ohbayashi C, Iseki S, Kitamura Y, Tsubota N, Okita Y, Okada M. Clinical implication and prognostic significance of the tumor suppressor TSLC1 gene detected in adenocarcinoma of the lung. Cancer 2003;98:1002–1007.
   PubMed Web of Science ®Google Scholar
• Goto A, Niki T, Chi-Pin L, Matsubara D, Murakami Y, Funata N, Fukayama M. Loss of TSLC1 expression in lung adenocarcinoma: relationships with histological subtypes, sex and prognostic significance. Cancer Sci 2005;96:480–486.
   PubMed Web of Science ®Google Scholar
• Kikuchi S, Yamada D, Fukami T, Maruyama T, Ito A, Asamura H, Matsuno Y, Onizuka M, Murakami Y. Hypermethylation of the TSLC1/IGSF4 promoter is associated with tobacco smoking and a poor prognosis in primary nonsmall cell lung carcinoma. Cancer 2006;106:1751–1758.
   PubMed Web of Science ®Google Scholar
• Allinen M, Peri L, Kujala S, Lahti-Domenici J, Outila K, Karppinen SM, Launonen V, Winqvist R. Analysis of 11q21–24 loss of heterozygosity candidate target genes in breast cancer: indications of TSLC1 promoter hypermethylation. Genes Chromosomes Cancer 2002;34:384–389.
   PubMed Web of Science ®Google Scholar
• Heller G, Geradts J, Ziegler B, Newsham I, Filipits M, Markis-Ritzinger EM, Kandioler D, Berger W, Stiglbauer W, Depisch D, Pirker R, Zielinski CC, Zöchbauer-Müller S. Downregulation of TSLC1 and DAL-1 expression occurs frequently in breast cancer. Breast Cancer Res Treat 2007;103:283–291.
   PubMed Web of Science ®Google Scholar
• Lung HL, Cheng Y, Kumaran MK, Liu ET, Murakami Y, Chan CY, Yau WL, Ko JM, Stanbridge EJ, Lung ML. Fine mapping of the 11q22–23 tumor suppressive region and involvement of TSLC1 in nasopharyngeal carcinoma. Int J Cancer 2004;112:628–635.
   PubMed Web of Science ®Google Scholar
• Hui AB, Lo KW, Kwong J, Lam EC, Chan SY, Chow LS, Chan AS, Teo PM, Huang DP. Epigenetic inactivation of TSLC1 gene in nasopharyngeal carcinoma. Mol Carcinog 2003;38:170–178.
   PubMed Web of Science ®Google Scholar
• Ito T, Shimada Y, Hashimoto Y, Kaganoi J, Kan T, Watanabe G, Murakami Y, Imamura M. Involvement of TSLC1 in progression of esophageal squamous cell carcinoma. Cancer Res 2003;63:6320–6326.
   Google Scholar
• Honda T, Tamura G, Waki T, Jin Z, Sato K, Motoyama T, Kawata S, Kimura W, Nishizuka S, Murakami Y. Hypermethylation of the TSLC1 gene promoter in primary gastric cancers and gastric cancer cell lines. Jpn J Cancer Res 2002;93:857–860.
   PubMedGoogle Scholar
• Tamura G. Promoter methylation status of tumor suppressor and tumor-related genes in neoplastic and non-neoplastic gastric epithelia. Histol Histopathol 2004;19:221–228.
   PubMed Web of Science ®Google Scholar
• Fukuhara H, Kuramochi M, Fukami T, Kasahara K, Furuhata M, Nobukuni T, Maruyama T, Isogai K, Sekiya T, Shuin T, Kitamura T, Reeves RH, Murakami Y. Promoter methylation of TSLC1 and tumor suppression by its gene product in human prostate cancer. Jpn J Cancer Res 2002;93:605–609.
   PubMedGoogle Scholar
• Williams YN, Masuda M, Sakurai-Yageta M, Maruyama T, Shibuya M, Murakami Y. Cell adhesion and prostate tumor-suppressor activity of TSLL2/IGSF4C, an immunoglobulin superfamily molecule homologous to TSLC1/IGSF4. Oncogene 2006;25:1446–1453.
   PubMedGoogle Scholar
• Jansen M, Fukushima N, Rosty C, Walter K, Altink R, Heek TV, Hruban R, Offerhaus JG, Goggins M. Aberrant methylation of the 5′ CpG island of TSLC1 is common in pancreatic ductal adenocarcinoma and is first manifest in high-grade PanlNs. Cancer Biol Ther 2002;1:293–296.
   PubMed Web of Science ®Google Scholar
• Hong SM, Kelly D, Griffith M, Omura N, Li A, Li CP, Hruban RH, Goggins M. Multiple genes are hypermethylated in intraductal papillary mucinous neoplasms of the pancreas. Mod Pathol 2008;21:1499–1507.
   PubMed Web of Science ®Google Scholar
• Chen K, Wang G, Peng L, Liu S, Fu X, Zhou Y, Yu H, Li A, Li J, Zhang S, Bai Y, Zhang Y. CADM1/TSLC1 inactivation by promoter hypermethylation is a frequent event in colorectal carcinogenesis and correlates with late stages of the disease. Int J Cancer 2011;128:266–273.
   PubMed Web of Science ®Google Scholar
• Steenbergen RD, Kramer D, Braakhuis BJ, Stern PL, Verheijen RH, Meijer CJ, Snijders PJ. TSLC1 gene silencing in cervical cancer cell lines and cervical neoplasia. J Natl Cancer Inst 2004;96:294–305.
   PubMedGoogle Scholar
• Yang YX, Yang AH, Yang ZJ, Wang ZR, Xia XH. Involvement of tumor suppressor in lung cancer 1 gene expression in cervical carcinogenesis. Int J Gynecol Cancer 2006;16:1868–1872.
   PubMed Web of Science ®Google Scholar
• Overmeer RM, Henken FE, Snijders PJ, Claassen-Kramer D, Berkhof J, Helmerhorst TJ, Heideman DA, Wilting SM, Murakami Y, Ito A, Meijer CJ, Steenbergen RD. Association between dense CADM1 promoter methylation and reduced protein expression in high-grade CIN and cervical SCC. J Pathol 2008;215:388–397.
   PubMed Web of Science ®Google Scholar
• You Y, Ma L, You M, Li X, Wang S, Li H, Wu D, Yang H, Li ZY. TSLC1 gene silencing in cutaneous melanoma. Melanoma Res 2010;20:179–183.
   PubMed Web of Science ®Google Scholar
• Surace EI, Lusis E, Murakami Y, Scheithauer BW, Perry A, Gutmann DH. Loss of tumor suppressor in lung cancer-1 (TSLC1) expression in meningioma correlates with increased malignancy grade and reduced patient survival. J Neuropathol Exp Neurol 2004;63:1015–1027.
   PubMed Web of Science ®Google Scholar
• Houshmandi SS, Surace EI, Zhang HB, Fuller GN, Gutmann DH. Tumor suppressor in lung cancer-1 (TSLC1) functions as a glioma tumor suppressor. Neurology 2006;67:1863–1866.
   PubMed Web of Science ®Google Scholar
• Heller G, Fong KM, Girard L, Seidl S, End-Pfützenreuter A, Lang G, Gazdar AF, Minna JD, Zielinski CC, Zöchbauer-Müller S. Expression and methylation pattern of TSLC1 cascade genes in lung carcinomas. Oncogene 2006;25:959–968.
   Google Scholar
• Hurtubise A, Bernstein ML, Momparler RL. Preclinical evaluation of the antineoplastic action of 5-aza-2′-deoxycytidine and different histone deacetylase inhibitors on human Ewing's sarcoma cells. Cancer Cell Int 2008;8:16.
   PubMed Web of Science ®Google Scholar