Cancer Cell Biology

You have full text access to this OnlineOpen article

The tetraspanin CD9 inhibits the proliferation and tumorigenicity of human colon carcinoma cells

  1. Susana Ovalle1,†,
  2. María Dolores Gutiérrez-López1,†,
  3. Nieves Olmo2,
  4. Javier Turnay2,
  5. María Antonia Lizarbe2,
  6. Pedro Majano3,
  7. Francisca Molina-Jiménez3,
  8. Manuel López-Cabrera3,
  9. María Yáñez-Mó4,5,
  10. Francisco Sánchez-Madrid4,5,
  11. Carlos Cabañas1,‡,*

Article first published online: 20 JUN 2007

DOI: 10.1002/ijc.22902

Issue

International Journal of Cancer

International Journal of Cancer

Volume 121, Issue 10, pages 2140–2152, 15 November 2007

Additional Information

How to Cite

Ovalle, S., Gutiérrez-López, M. D., Olmo, N., Turnay, J., Lizarbe, M. A., Majano, P., Molina-Jiménez, F., López-Cabrera, M., Yáñez-Mó, M., Sánchez-Madrid, F. and Cabañas, C. (2007), The tetraspanin CD9 inhibits the proliferation and tumorigenicity of human colon carcinoma cells. Int. J. Cancer, 121: 2140–2152. doi: 10.1002/ijc.22902

Author Information

  1. 1

    Instituto de Farmacología y Toxicología (CSIC-UCM), Facultad de Medicina, Universidad Complutense, Madrid, Spain

  2. 2

    Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Químicas, Universidad Complutense, Madrid, Spain

  3. 3

    Unidad de Biología Molecular, Hospital de la Princesa, Madrid, Spain

  4. 4

    Servicio de Inmunología, Hospital de la Princesa, Madrid, Spain

  5. 5

    Departamento de Biología Vascular e Inflamación, CNIC, Madrid, Spain

  1. †

    These two authors contributed equally to this work.

  2. ‡

    Fax: +34-91-3941469.

*Carlos Cabañas, Facultad de Medicina UCM, Instituto de Farmacología y Toxicología (CSIC-UCM), Pabellón III, 28040 Madrid, Spain

Publication History

  1. Issue published online: 25 SEP 2007
  2. Article first published online: 20 JUN 2007
  3. Manuscript Accepted: 9 MAY 2007
  4. Manuscript Received: 22 SEP 2006

Funded by

  • Fundación de Investigación Médica Mutua Madrileña
  • Dirección General de Investigación, Ministerio de Educación y Ciencia. Grant Numbers: SAF2004-01715, BFU2005-02671
  • Consejo Superior de Investigaciones Científicas (CSIC)

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (790K)

References

  • 1
    Boucheix C, Duc GHT, Jasmin C, Rubinstein E. Tetraspanins and malignancy. Expert Rev Mol Med 2001; 31: 1–17.
  • 2
    Boucheix C, Rubinstein E. Tetraspanins. Cell Mol Life Sci 2001; 58: 1189–4.
  • 3
    Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 2003; 19: 397–422.
  • 4
    Si Z, Hersey P. Expression of the neuroglandular antigen and analogues in melanoma. CD9 expression appears inversely related to metastatic potential of melanoma. Int J Cancer 1993; 54: 37–43.
    Direct Link:
  • 5
    Mori M, Mimori K, Shiraishi T, Haraguchi M, Ueo H, Barnard GF, Akiyoshi T. Motility related protein 1 (MRP1/CD9) expression in colon cancer. Clin Cancer Res 1998; 4: 1507–10.
  • 6
    Miyake M, Nakano K, Itoi SI, Koh T, Taki T. Motility-related protein-1 (MRP-1/CD9) reduction as a factor of poor prognosis in breast cancer. Cancer Res 1996; 56: 1244–9.
  • 7
    Higashiyama M, Taki T, Ieki Y, Adachi M, Huang CL, Koh T, Kodama K, Doi O, Miyake M. Reduced motility related protein-1 (MRP-1/CD9) gene expression as a factor of poor prognosis in non-small cell lung cancer. Cancer Res 1995; 55: 6040–4.
  • 8
    Huang CI, Kohno N, Ogawa E, Adachi M, Taki T, Miyake M. Correlation of reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am J Pathol 1998; 153: 973–83.
  • 9
    Ikeyama S, Koyama M, Yamaoko M, Sasada R, Miyake M. Suppression of cell motility and metastasis by transfection with human motility-related protein (MRP-1/CD9) DNA. J Exp Med 1993; 177: 1231–7.
  • 10
    Sho M, Adachi M, Taki T, Hashida H, Konishi T, Huang CL, Ikeda N, Nakajima Y, Kanehiro H, Hisanaga M, Nakano H, Miyake M. Transmembrane 4 superfamily as a prognostic factor in pancreatic cancer. Int J Cancer 1998; 79: 509–16.
    Direct Link:
  • 11
    Miyake M, Koyama M, Seno M, Ikeyama S. Identification of the motility-related protein (MRP-1), recognized by monoclonal antibody M31-15, which inhibits cell motility. J Exp Med 1991; 174: 1347–54.
  • 12
    Cajot JF, Sordat I, Silvestre T, Sordat B. Differential display cloning identifies motility-related protein (MRP1/CD9) as highly expressed in primary compared to metastatic human colon carcinoma cells. Cancer Res 1997; 57: 2593–7.
  • 13
    Longo N, Yanez-Mo M, Mittelbrunn M, de la Rosa G, Munoz ML, Sanchez-Madrid F, Sanchez-Mateos P. Regulatory role of tetraspanin CD9 in tumor-endothelial cell interaction during transendothelial invasion of melanoma cells. Blood 2001; 98: 3717–26.
  • 14
    Gutierrez-Lopez MD, Ovalle S, Yanez-Mo M, Sanchez-Sanchez N, Rubinstein E, Olmo N, Lizarbe MA, Sanchez-Madrid F, Cabanas C. A functionally relevant conformational epitope on the CD9 tetraspanin depends on the association with activated beta1 integrin. J Biol Chem 2003; 278: 208–18.
  • 15
    Lopez-Conejo MT, Olmo N, Turnay J, Lopez De Silanes I, Lizarbe MA. Interaction of fibronectin with human colon adenocarcinoma cells: effect on the in vivo tumorigenic capacity. Oncology 2002; 62: 371–80.
  • 16
    Lopez-Conejo T, Olmo N, Turnay J, Navarro J, Lizarbe A. Characterization of tumorigenic sub-lines from a poorly tumorigenic human colon-adenocarcinoma cell line. Int J Cancer 1996; 67: 668–75.
    Direct Link:
  • 17
    Arroyo AG, Sanchez-Mateos P, Campanero MR, Martin-Padura I, Dejana E, Sanchez-Madrid F. Regulation of the VLA integrin–ligand interactions through the beta 1 subunit. J Cell Biol 1992; 117: 659–70.
  • 18
    Campanero MR, Arroyo AG, Pulido R, Ursa A, de Matias MS, Sanchez-Mateos P, Kassner PD, Chan BM, Hemler ME, Corbi AL, et al. Functional role of alpha 2/beta 1 and alpha 4/beta 1 integrins in leukocyte intercellular adhesion induced through the common beta 1 subunit. Eur J Immunol 1992; 22: 3111–9.
    Direct Link:
  • 19
    Luque A, Gomez M, Puzon W, Takada Y, Sanchez-Madrid F, Cabanas C. Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355–425) of the common beta 1 chain. J Biol Chem 1996; 271: 11067–75.
  • 20
    Yanez-Mo M, Alfranca A, Cabanas C, Marazuela M, Tejedor R, Ursa MA, Ashman LK, de Landazuri MO, Sanchez-Madrid F. Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/PETA-3 with alpha3 beta1 integrin localized at endothelial lateral junctions. J Cell Biol 1998; 141: 791–804.
  • 21
    Cebrian M, Yague E, Rincon M, Lopez-Botet M, de Landazuri MO, Sanchez-Madrid F. Triggering of T cell proliferation through AIM, an activation inducer molecule expressed on activated human lymphocytes. J Exp Med 1988; 168: 1621–37.
  • 22
    Gonzalez-Amaro R, Garcia-Monzon C, Garcia-Buey L, Moreno-Otero R, Alonso JL3, Yague E, Pivel JP, Lopez-Cabrera M, Fernandez-Ruiz E, Sanchez-Madrid F. Induction of tumor necrosis factor alpha production by human hepatocytes in chronic viral hepatitis. J Exp Med 1994; 179: 841–8.
  • 23
    Olmo N, Turnay J, Gonzalez de Buitrago G, Lopez de Silanes I, Gavilanes JG, Lizarbe MA. Cytotoxic mechanism of the ribotoxin alpha-sarcin. Induction of cell death via apoptosis. Eur J Biochem 2001; 268: 2113–23.
    Direct Link:
  • 24
    van de Loosdrecht AA, Beelen RH, Ossenkoppele GJ, Broekhoven MG, Langenhuijsen MM. A tetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. J Immunol Methods 1994; 174: 311–20.
  • 25
    Perez-Ramos P, Olmo N, Turnay J, Lecona E, de Buitrago GG, Portoles MT, Lizarbe MA. Effect of bile acids on butyrate-sensitive and -resistant human colon adenocarcinoma cells. Nutr Cancer 2005; 53: 208–19.
  • 26
    Horiuchi T, Morita C, Tsukamoto H, Mitoma H, Sawabe T, Harashima S, Kashiwagi Y, Okamura S. Increased expression of membrane TNF-alpha on activated peripheral CD8+ T cells in systemic lupus erythematosus. Int J Mol Med 2006; 17: 875–9.
  • 27
    Li Q, Li L, Shi W, Jiang X, Xu Y, Gong F, Zhou M, Edwards CK,III, Li Z. Mechanism of action differences in the antitumor effects of transmembrane and secretory tumor necrosis factor-alpha in vitro and in vivo. Cancer Immunol Immunother 2006; 55: 1470–9.
  • 28
    Gomez M, Luque A, del Pozo MA, Hogg N, Sanchez-Madrid F, Cabanas C. Functional relevance during lymphocyte migration and cellular localization of activated beta1 integrins. Eur J Immunol 1997; 27: 8–16.
    Direct Link:
  • 29
    Kovarikova M, Pachernik J, Hofmanova J, Zadak Z, Kozubik A. TNF-alpha modulates the differentiation induced by butyrate in the HT-29 human colon adenocarcinoma cell line. Eur J Cancer 2000; 36: 1844–52.
  • 30
    Besnard V, Nabeyrat E, Henrion-Caude A, Chadelat K, Perin L, Le Bouc Y, Clement A. Protective role of retinoic acid from antiproliferative action of TNF-alpha on lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002; 282: L863–71.
  • 31
    Kuninaka S, Yano T, Yokoyama H, Fukuyama Y, Terazaki Y, Uehara T, Kanematsu T, Asoh H, Ichinose Y. Direct influences of pro-inflammatory cytokines (IL-1beta, TNF-alpha, IL-6) on the proliferation and cell-surface antigen expression of cancer cells. Cytokine 2000; 12: 8–11.
  • 32
    Scallon B, Cai A, Solowski N, Rosenberg A, Song XY, Shealy D, Wagner C. Binding and functional comparisons of two types of tumor necrosis factor antagonists. J Pharmacol Exp Ther 2002; 301: 418–26.
  • 33
    Mitoma H, Horiuchi T, Hatta N, Tsukamoto H, Harashima S, Kikuchi Y, Otsuka J, Okamura S, Fujita S, Harada M. Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-alpha. Gastroenterology 2005; 128: 376–92.
  • 34
    Uchida S, Shimada Y, Watanabe G, Li ZG, Hong T, Miyake M, Imamura M. Motility-related protein (MRP-1/CD9) and KAI1/CD82 expression inversely correlate with lymph node metastasis in oesophageal squamous cell carcinoma. Br J Cancer 1999; 79: 1168–73.
  • 35
    Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 2001; 114: 4143–51.
  • 36
    Masellis-Smith A, Shaw AR. CD9-regulated adhesion. Anti-CD9 monoclonal antibody induce pre-B cell adhesion to bone marrow fibroblasts through de novo recognition of fibronectin. J Immunol 1994; 152: 2768–77.
  • 37
    Furuya M, Kato H, Nishimura N, Ishiwata I, Ikeda H, Ito R, Yoshiki T, Ishikura H. Down-regulation of CD9 in human ovarian carcinoma cell might contribute to peritoneal dissemination: morphologic alteration and reduced expression of beta1 integrin subsets. Cancer Res 2005; 65: 2617–25.
  • 38
    Cook GA, Wilkinson DA, Crossno JTJr., Raghow R, Jennings LK. The tetraspanin CD9 influences the adhesion, spreading, and pericellular fibronectin matrix assembly of Chinese hamster ovary cells on human plasma fibronectin. Exp Cell Res 1999; 251: 356–71.
  • 39
    Ziyyat A, Rubinstein E, Monier-Gavelle F, Barraud V, Kulski O, Prenant M, Boucheix C, Bomsel M, Wolf JP. CD9 controls the formation of clusters that contain tetraspanins and the integrin alpha 6 beta 1, which are involved in human and mouse gamete fusion. J Cell Sci 2006; 119: 416–24.
  • 40
    Nishiuchi R, Sanzen N, Nada S, Sumida Y, Wada Y, Okada M, Takagi J, Hasegawa H, Sekiguchi K. Potentiation of the ligand-binding activity of integrin alpha3beta1 via association with tetraspanin CD151. Proc Natl Acad Sci U S A 2005; 102: 1939–44.
  • 41
    Ponz de Leon M, Percesepe A. Pathogenesis of colorectal cancer. Dig Liver Dis 2000; 32: 807–21.
  • 42
    Pinto D, Clevers H. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp Cell Res 2005; 306: 357–63.
  • 43
    Risio M, Rocci MP. Intermediate biomarkers in the colorectal tumor progression. Tumori 1995; 81: 16–8.
  • 44
    Murayama Y, Miyagawa J, Oritani K, Yoshida H, Yamamoto K, Kishida O, Miyazaki T, Tsutsui S, Kiyohara T, Miyazaki Y, Higashiyama S, Matsuzawa Y, et al. CD9-mediated activation of the p46 Shc isoform leads to apoptosis in cancer cells. J Cell Sci 2004; 117: 3379–88.
  • 45
    Zheng R, Yano S, Zhang H, Nakataki E, Tachibana I, Kawase I, Hayashi S, Sone S. CD9 overexpression suppressed the liver metastasis and malignant ascites via inhibition of proliferation and motility of small-cell lung cancer cells in NK cell-depleted SCID mice. Oncol Res 2005; 15: 365–72.
  • 46
    Oren R, Takahashi S, Doss C, Levy R, Levy S. TAPA-1, the target of an antiproliferative antibody, defines a new family of transmembrane proteins. Mol Cell Biol 1990; 10: 4007–15.
  • 47
    Levy S, Todd SC, Maecker HT. CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu Rev Immunol 1998; 16: 89–109.
  • 48
    Hagenaars M, Ensink NG, Basse PH, Hokland M, Nannmark U, Eggermont AM, van de Velde CJ, Fleuren GJ, Kuppen PJ. The microscopic anatomy of experimental rat CC531 colon tumour metastases: consequences for immunotherapy? Clin Exp Metastasis 2000; 18: 189–96.
  • 49
    Sordat I, Rousselle P, Chaubert P, Petermann O, Aberdam D, Bosman FT, Sordat B. Tumor cell budding and laminin-5 expression in colorectal carcinoma can be modulated by the tissue micro-environment. Int J Cancer 2000; 88: 708–17.
    Direct Link:
  • 50
    Sordat I, Bosman FT, Dorta G, Rousselle P, Aberdam D, Blum AL, Sordat B. Differential expression of laminin-5 subunits and integrin receptors in human colorectal neoplasia. J Pathol 1998; 185: 44–52.
    Direct Link:
  • 51
    Hashida H, Takabayashi A, Tokuhara T, Hattori N, Taki T, Hasegawa H, Satoh S, Kobayashi N, Yamaoka Y, Miyake M. Clinical significance of transmembrane 4 superfamily in colon cancer. Br J Cancer 2003; 89: 158–67.
  • 52
    Nash PT, Florin TH. Tumour necrosis factor inhibitors. Med J Aust 2005; 183: 205–8.
  • 53
    Yamane H, Tachibana I, Takeda Y, Saito Y, Tamura Y, He P, Suzuki M, Shima Y, Yoneda T, Hoshino S, Inoue K, Kijima T, et al. Propionibacterium acnes-induced hepatic granuloma formation is impaired in mice lacking tetraspanin CD9. J Pathol 2005; 206: 486–92.
    Direct Link:
  • 54
    Grell M, Douni E, Wajant H, Lohden M, Clauss M, Maxeiner B, Georgopoulos S, Lesslauer W, Kollias G, Pfizenmaier K, Scheurich P. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 1995; 83: 793–802.
  • 55
    Tres LL, Kierszenbaum AL. The ADAM–integrin–tetraspanin complex in fetal and postnatal testicular cords. Birth Defects Res C Embryo Today 2005; 75: 130–41.
    Direct Link:
  • 56
    Moss ML, Bartsch JW. Therapeutic benefits from targeting of ADAM family members. Biochemistry 2004; 43: 7227–35.
View Full Article (HTML) Get PDF (790K)