Overexpression and β-1,6-N-Acetylglucosaminylation-initiated aberrant glycosylation of TIMP-1: A "double whammy" strategy in colon cancer progression

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32467-32478

  Kim, Yong Sam ^a   Ahn, Yeong Hee ^b   Song, Kyoung Jin ^a   Kang, Jeong Gu ^a   Lee, Ju Hee ^a   Jeon, Seong Kook ^a   Kim, Hyoung Chin ^a   Yoo, Jong Shin ^b   Ko, Jeong Heon ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BASEMENT MEMBRANE; COLON CANCER; COLON CANCER CELLS; GLYCOFORMS; IN-VITRO; IN-VIVO; OVER-EXPRESSION; PHYSICAL BARRIERS; THREE-DIMENSIONAL CULTURE SYSTEM; TISSUE INHIBITOR; TUMOR CELLS; TUMOR FORMATION; TUMOR GROWTH;

CELL PROLIFERATION;

TUMORS;

ALPHA 1,3(6) MANNOSYLGLYCOPROTEIN BETA 1,6 N ACETYLGLUCOSAMINYLTRANSFERASE; COLLAGENASE; INTERLEUKIN 2; N ACETYLGLUCOSAMINYLTRANSFERASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASEMENT MEMBRANE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CELL PROLIFERATION; CLONOGENESIS; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DEGRADATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; INTERSTITIAL MATRIX; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; TUMOR GROWTH;

CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; GLYCOSYLATION; HUMANS; INTEGRIN ALPHAVBETA3; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEOPLASM PROTEINS; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84866551038     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.370064     Document Type: Article

References (53)

1. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8
2. Zhao, Y., Sato, Y., Isaji, T., Fukuda, T., Matsumoto, A., Miyoshi, E., Gu, J., and Taniguchi, N. (2008) BranchedN-glycans regulate the biological functions of integrins and cadherins. FEBS J. 275, 1939-1948 (Pubitemid 351569538)
3. Chen, G., Howe, A. G., Xu, G., Fröhlich, O., Klein, J. D., and Sands, J. M. (2011) Mature N-linked glycans facilitate UT-A1 urea transporter lipid raft compartmentalization. FASEB J. 25, 4531-4539
4. Jaeken, J. (2010) Congenital disorders of glycosylation. Ann. N.Y. Acad. Sci. 1214, 190-198
5. Dall'Olio, F., Malagolini, N., Trinchera, M., and Chiricolo, M. (2012) Mechanisms of cancer-associated glycosylation changes. Front. Biosci. 17, 670-699
6. Whiteside, T. L. (2008) The tumor microenvironment and its role in promoting tumor growth. Oncogene 27, 5904-5912
7. Lu, P., Weaver, V. M., and Werb, Z. (2012) The extracellular matrix. A dynamic niche in cancer progression. J. Cell Biol. 196, 395-406
8. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D. L., and Weaver, V. M. (2009) Matrix cross-linking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906
9. Egeblad, M., and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174 (Pubitemid 37328786)
10. Docherty, A. J., Lyons, A., Smith, B. J., Wright, E. M., Stephens, P. E., Harris, T. J., Murphy, G., and Reynolds, J. J. (1985) Sequence of human tissue inhibitor of metalloproteinases and its identity to erythroid-potentiating activity. Nature 318, 66-69 (Pubitemid 16230337)
11. Taube, M. E., Liu, X. W., Fridman, R., and Kim H. R. (2006) TIMP-1 regulation of cell cycle in human breast epithelial cells via stabilization of p27KIP1 protein. Oncogene 25, 3041-3048 (Pubitemid 43780468)
12. Bloomston, M., Shafii, A., Zervos, E., and Rosemurgy, A. S. (2005) TIMP-1 antisense gene transfection attenuates the invasive potential of pancreatic cancer cells in vitro and inhibits tumor growth in vivo. Am. J. Surg. 189, 675-679 (Pubitemid 40725737)
13. Rho, S. B., Chung, B. M., and Lee, J. H. (2007) TIMP-1 regulates cell proliferation by interacting with the ninth zinc finger domain of PLZF. J. Cell. Biochem. 101, 57-67
14. Fowell, A. J., Collins, J. E., Duncombe, D. R., Pickering, J. A., Rosenberg, W. M., and Benyon, R. C. (2011) Silencing tissue inhibitors of metalloproteinases (TIMPs) with short interfering RNA reveals a role for TIMP-1 in hepatic stellate cell proliferation. Biochem. Biophys. Res. Commun. 407, 277-282
15. Tsagaraki, I., Tsilibary, E. C., and Tzinia, A. K. (2010) TIMP-1 interaction with αvβ3 integrin confers resistance to human osteosarcoma cell line MG-63 against TNF-α-induced apoptosis. Cell Tissue Res. 342, 87-96
16. Davidsen, M. L., Würtz, S. Ø., Rømer, M. U., Sørensen, N. M., Johansen, S. K., Christensen, I. J., Larsen, J. K., Offenberg, H., Brünner, N., and Lademann, U. (2006) TIMP-1 gene deficiency increases tumor cell sensitivity to chemotherapy-induced apoptosis. Br. J. Cancer 95, 114-120
17. Khokha, R. (1994) Suppression of the tumorigenic and metastatic abilities of murine B16-F10 melanoma cells in vivo by the overexpression of the tissue inhibitor of the metalloproteinases-1. J. Natl. Cancer Inst. 86, 299-304
18. Martin, D. C., Rüther, U., Sanchez-Sweatman, O. H., Orr, F. W., and Khokha, R. (1996) Inhibition of SV40 T antigen-induced hepatocellular carcinoma in TIMP-1 transgenic mice. Oncogene 13, 569-576 (Pubitemid 26283853)
19. Aljada, I. S., Ramnath, N., Donohue, K., Harvey, S., Brooks, J. J., Wiseman, S. M., Khoury, T., Loewen, G., Slocum, H. K., Anderson, T. M., Bepler, G., and Tan, D. (2004) Up-regulation of the tissue inhibitor of metalloproteinase-1 protein is associated with progression of human non-small cell lung cancer. J. Clin. Oncol. 22, 3218-3229 (Pubitemid 41103676)
20. Korpi, J. T., Hagström, J., Lehtonen, N., Parkkinen, J., Sorsa, T., Salo, T., and Laitinen, M. (2011) Expression of matrix metalloproteinases-2, -8, -13, -26, and tissue inhibitors of metalloproteinase-1 in human osteosarcoma. Surg. Oncol. 20, e18-e22
21. Inagaki, D., Oshima, T., Yoshihara, K., Tamura, S., Kanazawa, A., Yamada, T., Yamamoto, N., Sato, T., Shiozawa, M., Morinaga, S., Akaike, M., Fujii, S., Numata, K., Kunisaki, C., Rino, Y., Tanaka, K., Masuda, M., and Imada, T. (2010) Overexpression of tissue inhibitor of metalloproteinase-1 gene correlates with poor outcomes in colorectal cancer. Anticancer Res. 30, 4127-4130
22. Chen, T. R., Drabkowski, D., Hay, R. J., Macy, M., and Peterson, W. Jr. (1987) WiDr is a derivative of another colon adenocarcinoma cell line, HT-29. Cancer Genet. Cytogenet. 27, 125-134
23. Cullinan, A. E., and Brandt, C. R. (2004) Cytokine-induced apoptosis in human retinoblastoma cells. Mol. Vis. 10, 315-322 (Pubitemid 38628946)
24. Lee, G. Y., Kenny, P. A., Lee, E. H., and Bissell, M. J. (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods 4, 359-365 (Pubitemid 46766981)
25. Taniguchi, N., Miyoshi, E., Ko, J. H., Ikeda, Y., and Ihara, Y. (1999) Implication of N-acetylglucosaminyltransferases III and V in cancer. Gene regulation and signaling mechanism. Biochim. Biophys. Acta 1455, 287-300 (Pubitemid 29435995)
26. Kim, Y. S., Hwang, S. Y., Kang, H. Y., Sohn, H., Oh, S., Kim, J. Y., Yoo, J. S., Kim, Y. H., Kim, C. H., Jeon, J. H., Lee, J. M., Kang, H. A., Miyoshi, E., Taniguchi, N., Yoo, H. S., and Ko, J. H. (2008) Functional proteomics study reveals that N-acetylglucosaminyltransferase V reinforces the invasive/metastatic potential of colon cancer through aberrant glycosylation on tissue inhibitor of metalloproteinase-1. Mol. Cell. Proteomics 7, 1-14 (Pubitemid 351248231)
27. Chirco, R., Liu, X. W., Jung, K. K., and Kim, H. R. (2006) Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev. 25, 99-113 (Pubitemid 43723986)
28. Caterina, N. C., Windsor, L. J., Bodden, M. K., Yermovsky, A. E., Taylor, K. B., Birkedal-Hansen, H., and Engler, J. A. (1998) Glycosylation and NH2-terminal domain mutants of the tissue inhibitor of metalloproteinases-1 (TIMP-1). Biochim. Biophys. Acta 14, 21-34 (Pubitemid 28468601)
29. Roehm, N. W., Rodgers, G. H., Hatfield, S. M., and Glasebrook, A. L. (1991) An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J. Immunol. Methods 142, 257-265
30. Chen, G., and Goeddel, D. (2002) TNF-R1 signaling. A beautiful pathway. Science 296, 1634-1635
31. Winkelhake, J. L., Stampfl, S., and Zimmerman, R. J. (1987) Synergistic effects of combination therapy with human recombinant interleukin-2 and tumor necrosis factor in murine tumor models. Cancer Res. 47, 3948-3953 (Pubitemid 17108451)
32. Oshima, H., and Oshima, M. (2012) The inflammatory network in the gastrointestinal tumor microenvironment. Lessons from mouse models. J. Gastroenterol. 47, 97-106
33. Liao, D., Luo, Y., Markowitz, D., Xiang, R., and Reisfeld, R. A. (2009) Cancer-associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One 4, e7965
34. Yang, S. C., Grimm, E. A., Parkinson, D. R., Carinhas, J., Fry, K. D., Mendiguren-Rodriguez, A., Licciardello, J., Owen-Schaub, L. B., Hong, W. K., and Roth, J. A. (1991) Clinical and immunomodulatory effects of combination immunotherapy with low dose interleukin 2 and tumor necrosis factor α in patients with advanced non-small cell lung cancer. A phase I trial. Cancer Res. 51, 3669-3676
35. Balkwill, F. (2006) TNF-α in promotion and progression of cancer. Cancer Metastasis Rev. 25, 409-416
36. Itoh, T., Tanioka, M., Matsuda, H., Nishimoto, H., Yoshioka, T., Suzuki, R., and Uehira, M. (1999) Experimental metastasis is suppressed in MMP-9-deficient mice. Clin. Exp. Metastasis 17, 177-181 (Pubitemid 29335445)
37. Itoh, T., Tanioka, M., Yoshida, H., Yoshioka, T., Nishimoto, H., and Itohara, S. (1998) Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res. 58, 1048-1051 (Pubitemid 28182477)
38. Sodek, K. L., Brown, T. J., and Ringuette, M. J. (2008) Collagen I but not Matrigel matrices provide an MMP-dependent barrier to ovarian cancer cell penetration. BMC Cancer 8, 223
39. Hughes, C. S., Postovit, L. M., and Lajoie, G. A. (2010) Matrigel.Acomplex protein mixture required for optimal growth of cell culture. Proteomics 10, 1886-1890
40. Jiang, Y., Goldberg, I. D., and Shi, Y. E. (2002) Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 21, 2245-2252 (Pubitemid 34311378)
41. Martin-Belmonte, F., and Perez-Moreno, M. (2012) Epithelial cell polarity, stem cells, and cancer. Nat. Rev. Cancer 12, 23-38
42. Royer, C., and Lu, X. (2011) Epithelial cell polarity. A major gatekeeper against cancer? Cell Death Differ. 18, 1470-1477
43. Zavadil, J., and Böttinger, E. P. (2005) TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24, 5764-5774
44. Bachelder, R. E., Yoon, S. O., Franci, C., de Herreros, A. G., and Mercurio, A. M. (2005) Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription. Implications for the epithelial-mesenchymal transition. J. Cell Biol. 168, 29-33 (Pubitemid 40111054)
45. Lester, R. D., Jo, M., Montel, V., Takimoto, S., and Gonias, S. L. (2007) uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J. Cell Biol. 178, 425-436 (Pubitemid 47196151)
46. Yang, M. H., Wu, M. Z., Chiou, S. H., Chen, P. M., Chang, S. Y., Liu, C. J., Teng, S. C., and Wu, K. J. (2008) Direct regulation of TWIST by HIF-1αpromotes metastasis. Nat. Cell Biol. 10, 295-305
47. Ciruna, B., and Rossant, J. (2001) FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 1, 37-49 (Pubitemid 33586067)
48. Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., Leake, D., Godden, E. L., Albertson, D. G., Nieto, M. A., Werb, Z., and Bissell, M. J. (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123-127 (Pubitemid 40966197)
49. Illman, S. A., Lehti, K., Keski-Oja, J., and Lohi, J. (2006) Epilysin (MMP-28) induces TGF-β-mediated epithelial to mesenchymal transition in lung carcinoma cells. J. Cell Sci. 119, 3856-3865 (Pubitemid 44614437)
50. McGuire, J. K., Li, Q., and Parks, W. C. (2003) Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium. Am. J. Pathol. 162, 1831-1843 (Pubitemid 36613042)
51. Song, W., Jackson, K., and McGuire, P. G. (2000) Degradation of type IV collagen by matrix metalloproteinases is an important step in the epithelial-mesenchymal transformation of the endocardial cushions. Dev. Biol. 227, 606-617
52. Terao, M., Ishikawa, A., Nakahara, S., Kimura, A., Kato, A., Moriwaki, K., Kamada, Y., Murota, H., Taniguchi, N., Katayama, I., and Miyoshi, E. (2011) Enhanced epithelial-mesenchymal transition-like phenotype in N-acetylglucosaminyltransferase V transgenic mouse skin promotes wound healing. J. Biol. Chem. 286, 28303-28311
53. Leung, C. T., and Brugge, J. S. (2012) Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 482, 410-413