CD9 negatively regulates CD26 expression and inhibits CD26-mediated enhancement of invasive potential of malignant mesothelioma cells

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Okamoto, Toshihiro ^a,b   Iwata, Satoshi ^a,b   Yamazaki, Hiroto ^a,b   Hatano, Ryo ^a,b   Komiya, Eriko ^a   Dang, Nam H ^c   Ohnuma, Kei ^a,b   Morimoto, Chikao ^a,b  

^a JUNTENDO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD9 ANTIGEN; DIPEPTIDYL PEPTIDASE IV; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL INVASION; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; MALIGNANT MESOTHELIOMA; MESOTHELIOMA CELL LINE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ANTIGENS, CD29; ANTIGENS, CD9; APOPTOSIS; BLOTTING, WESTERN; CELL MEMBRANE; CELL MOVEMENT; CELL PROLIFERATION; DIPEPTIDYL PEPTIDASE 4; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOPRECIPITATION; LUNG NEOPLASMS; MESOTHELIOMA; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84899788617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086671     Document Type: Article

References (47)

1. Ismail-Khan R, Robinson LA, Williams CC Jr., Garrett CR, Bepler G, et al. (2006) Malignant pleural mesothelioma: a comprehensive review. Cancer Control 13: 255-263. (Pubitemid 44600936)
2. Robinson BW, Lake RA (2005) Advances in malignant mesothelioma. N Engl J Med 353: 1591-1603. (Pubitemid 41434638)
3. Morimoto C, Schlossman SF (1998) The structure and function of CD26 in the T-cell immune response. Immunol Rev 161: 55-70.
4. Kameoka J, Tanaka T, Nojima Y, Schlossman SF, Morimoto C (1993) Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science 261: 466-469. (Pubitemid 23276554)
5. Ishii T, Ohnuma K, Murakami A, Takasawa N, Kobayashi S, et al. (2001) CD26-mediated signaling for T cell activation occurs in lipid rafts through its association with CD45RO. Proc Natl Acad Sci U S A 98: 12138-12143. (Pubitemid 32959840)
6. Ohnuma K, Yamochi T, Uchiyama M, Nishibashi K, Yoshikawa N, et al. (2004) CD26 up-regulates expression of CD86 on antigen-presenting cells by means of caveolin-1. Proc Natl Acad Sci U S A 101: 14186-14191. (Pubitemid 39305051)
7. Iwata S, Morimoto C (1999) CD26/dipeptidyl peptidase IV in context. The different roles of a multifunctional ectoenzyme in malignant transformation. J Exp Med 190: 301-306.
8. Kajiyama H, Kikkawa F, Suzuki T, Shibata K, Ino K, et al. (2002) Prolonged survival and decreased invasive activity attributable to dipeptidyl peptidase IV overexpression in ovarian carcinoma. Cancer Res 62: 2753-2757. (Pubitemid 34525756)
9. Carbone A, Gloghini A, Zagonel V, Aldinucci D, Gattei V, et al. (1995) The expression of CD26 and CD40 ligand is mutually exclusive in human T-cell non-Hodgkin's lymphomas/leukemias. Blood 86: 4617-4626.
10. Droz D, Zachar D, Charbit L, Gogusev J, Chretein Y, et al. (1990) Expression of the human nephron differentiation molecules in renal cell carcinomas. Am J Pathol 137: 895-905. (Pubitemid 20337804)
11. Yamaguchi U, Nakayama R, Honda K, Ichikawa H, Hasegawa T, et al. (2008) Distinct gene expression-defined classes of gastrointestinal stromal tumor. J Clin Oncol 26: 4100-4108.
12. Cro L, Morabito F, Zucal N, Fabris S, Lionetti M, et al. (2009) CD26 expression in mature B-cell neoplasia: its possible role as a new prognostic marker in BCLL. Hematol Oncol 27: 140-147.
13. Ho L, Aytac U, Stephens LC, Ohnuma K, Mills GB, et al. (2001) In vitro and in vivo antitumor effect of the anti-CD26 monoclonal antibody 1F7 on human CD30+ anaplastic large cell T-cell lymphoma Karpas 299. Clin Cancer Res 7: 2031-2040. (Pubitemid 32994842)
14. Inamoto T, Yamochi T, Ohnuma K, Iwata S, Kina S, et al. (2006) Anti-CD26 monoclonal antibody-mediated G1-S arrest of human renal clear cell carcinoma Caki-2 is associated with retinoblastoma substrate dephosphorylation, cyclin-dependent kinase 2 reduction, p27(kip1) enhancement, and disruption of binding to the extracellular matrix. Clin Cancer Res 12: 3470-3477.
15. Amatya VJ, Takeshima Y, Kushitani K, Yamada T, Morimoto C, et al. (2011) Overexpression of CD26/DPPIV in mesothelioma tissue and mesothelioma cell lines. Oncol Rep 26: 1369-1375.
16. Inamoto T, Yamada T, Ohnuma K, Kina S, Takahashi N, et al. (2007) Humanized anti-CD26 monoclonal antibody as a treatment for malignant mesothelioma tumors. Clin Cancer Res 13: 4191-4200. (Pubitemid 47105983)
17. Zoller M (2009) Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 9: 40-55.
18. Ikeyama S, Koyama M, Yamaoko M, Sasada R, Miyake M (1993) Suppression of cell motility and metastasis by transfection with human motility-related protein (MRP-1/CD9) DNA. J Exp Med 177: 1231-1237. (Pubitemid 23117114)
19. Higashiyama M, Taki T, Ieki Y, Adachi M, Huang CL, et al. (1995) Reduced motility related protein-1 (MRP-1/CD9) gene expression as a factor of poor prognosis in non-small cell lung cancer. Cancer Res 55: 6040-6044.
20. Hori H, Yano S, Koufuji K, Takeda J, Shirouzu K (2004) CD9 expression in gastric cancer and its significance. J Surg Res 117: 208-215. (Pubitemid 38393645)
21. Kawashima M, Doh-ura K, Mekada E, Fukui M, Iwaki T (2002) CD9 expression in solid non-neuroepithelial tumors and infiltrative astrocytic tumors. J Histochem Cytochem 50: 1195-1203. (Pubitemid 34988448)
22. Ghani FI, Yamazaki H, Iwata S, Okamoto T, Aoe K, et al. (2011) Identification of cancer stem cell markers in human malignant mesothelioma cells. Biochem Biophys Res Commun 404: 735-742.
23. Yamazaki H, Naito M, Ghani FI, Dang NH, Iwata S, et al. (2012) Characterization of cancer stem cell properties of CD24 and CD26-positive human malignant mesothelioma cells. Biochem Biophys Res Commun 419: 529-536.
24. Hemler ME (2005) Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6: 801-811.
25. Kobayashi H, Hosono O, Iwata S, Kawasaki H, Kuwana M, et al. (2004) The tetraspanin CD9 is preferentially expressed on the human CD4(+)CD45RA+ naive T cell population and is involved in T cell activation. Clin Exp Immunol 137: 101-108. (Pubitemid 38869783)
26. Ohashi Y, Iwata S, Kamiguchi K, Morimoto C (1999) Tyrosine phosphorylation of Crk-associated substrate lymphocyte-type is a critical element in TCR- and beta 1 integrin-induced T lymphocyte migration. J Immunol 163: 3727-3734. (Pubitemid 29450895)
27. Nojima Y, Humphries MJ, Mould AP, Komoriya A, Yamada KM, et al. (1990) VLA-4 mediates CD3-dependent CD4+ T cell activation via the CS1 alternatively spliced domain of fibronectin. J Exp Med 172: 1185-1192. (Pubitemid 20343219)
28. Iwata S, Kobayashi H, Miyake-Nishijima R, Sasaki T, Souta-Kuribara A, et al. (2002) Distinctive signaling pathways through CD82 and beta1 integrins in human T cells. Eur J Immunol 32: 1328-1337. (Pubitemid 34546260)
29. Torimoto Y, Dang NH, Vivier E, Tanaka T, Schlossman SF, et al. (1991) Coassociation of CD26 (dipeptidyl peptidase IV) with CD45 on the surface of human T lymphocytes. J Immunol 147: 2514-2517.
30. Le Naour F, Andre M, Greco C, Billard M, Sordat B, et al. (2006) Profiling of the tetraspanin web of human colon cancer cells. Mol Cell Proteomics 5: 845-857. (Pubitemid 43792794)
31. Barkan D, Chambers AF (2011) beta1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin Cancer Res 17: 7219-7223.
32. Minegishi M, Tachibana K, Sato T, Iwata S, Nojima Y, et al. (1996) Structure and function of Cas-L, a 105-kD Crk-associated substrate-related protein that is involved in beta 1 integrin-mediated signaling in lymphocytes. J Exp Med 184: 1365-1375. (Pubitemid 26354693)
33. Kumar S, Tomooka Y, Noda M (1992) Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185: 1155-1161.
34. Law SF, Estojak J, Wang B, Mysliwiec T, Kruh G, et al. (1996) Human enhancer of filamentation 1, a novel p130cas-like docking protein, associates with focal adhesion kinase and induces pseudohyphal growth in Saccharomyces cerevisiae. Mol Cell Biol 16: 3327-3337.
35. Kondo S, Iwata S, Yamada T, Inoue Y, Ichihara H, et al. (2012) Impact of the integrin signaling adaptor protein NEDD9 on prognosis and metastatic behavior of human lung cancer. Clin Cancer Res 18: 6326-6338.
36. Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci U S A 99: 13663-13668. (Pubitemid 35215438)
37. Lafleur MA, Xu D, Hemler ME (2009) Tetraspanin proteins regulate membrane type-1 matrix metalloproteinase-dependent pericellular proteolysis. Mol Biol Cell 20: 2030-2040.
38. Guilmain W, Colin S, Legrand E, Vannier JP, Steverlynck C, et al. (2011) CD9P-1 expression correlates with the metastatic status of lung cancer, and a truncated form of CD9P-1, GS-168AT2, inhibits in vivo tumour growth. Br J Cancer 104: 496-504.
39. Wary KK, Mariotti A, Zurzolo C, Giancotti FG (1998) A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634. (Pubitemid 28427581)
40. del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-Garcia A, et al. (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 7: 901-908. (Pubitemid 41486291)
41. Charrin S, Manie S, Thiele C, Billard M, Gerlier D, et al. (2003) A physical and functional link between cholesterol and tetraspanins. Eur J Immunol 33: 2479-2489. (Pubitemid 37138980)
42. Friedl P, Alexander S (2011) Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147: 992-1009.
43. Pang R, Law WL, Chu AC, Poon JT, Lam CS, et al. (2010) A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6: 603-615.
44. Amatya VJ, Takeshima Y, Aoe K, Fujimoto N, Okamoto T, et al. (2013) CD9 expression as a favorable prognostic marker for patients with malignant mesothelioma. Oncol Rep 29: 21-28.
45. Furuya M, Kato H, Nishimura N, Ishiwata I, Ikeda H, et al. (2005) Downregulation of CD9 in human ovarian carcinoma cell might contribute to peritoneal dissemination: morphologic alteration and reduced expression of beta1 integrin subsets. Cancer Res 65: 2617-2625. (Pubitemid 40490060)
46. Funakoshi T, Tachibana I, Hoshida Y, Kimura H, Takeda Y, et al. (2003) Expression of tetraspanins in human lung cancer cells: frequent downregulation of CD9 and its contribution to cell motility in small cell lung cancer. Oncogene 22: 674-687. (Pubitemid 36269281)
47. Huang CL, Ueno M, Liu D, Masuya D, Nakano J, et al. (2006) MRP-1/CD9 gene transduction regulates the actin cytoskeleton through the downregulation of WAVE2. Oncogene 25: 6480-6488. (Pubitemid 44607080)