Thrombin-cleaved fragments of osteopontin are overexpressed in malignant glial tumors and provide a molecular niche with survival advantage

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3097-3111

  Yamaguchi, Yasuto ^a,b   Shao, Zhifei ^a,b   Sharif, Shadi ^a   Du, Xiao Yan ^a   Myles, Timothy ^a   Merchant, Milton ^a   Harsh, Griffith ^a   Glantz, Michael ^c   Recht, Lawrence ^a   Morser, John ^a,b   Leung, Lawrence L K ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DEATH; CELL SIGNALING; DISEASES; ENZYMES; GENE EXPRESSION; TUMORS;

ANTIAPOPTOTIC PROPERTIES; CELL CYCLE REGULATION; CEREBRO SPINAL FLUIDS; EXTRACELLULAR COMPARTMENTS; HIGHLY-CORRELATED; INFLAMMATORY ACTIVITY; PROTEOLYTIC CLEAVAGE; SIGNALING FUNCTIONS;

CEREBROSPINAL FLUID;

ARGINYLGLYCYLASPARTIC ACID; CARBOXYPEPTIDASE B; CARBOXYPEPTIDASE B2; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; OSTEOPONTIN; THROMBIN; THROMBIN ANTITHROMBIN COMPLEX; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER PATIENT; CANCER SURVIVAL; CANCER TISSUE; CARCINOGENESIS; CELL ADHESION; CELL CYCLE REGULATION; CELL DEATH; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SPACE; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MAJOR CLINICAL STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION;

EID: 84873318410     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362954     Document Type: Article

References (59)

1. Denhardt, D. T., Noda, M., O'Regan, A. W., Pavlin, D., and Berman, J. S. (2001) Osteopontin as a means to cope with environmental insults. Regulation of inflammation, tissue remodeling, and cell survival. J. Clin. Invest. 107, 1055-1061
2. Han, M. H., Hwang, S. I., Roy, D. B., Lundgren, D. H., Price, J. V., Ousman, S. S., Fernald, G. H., Gerlitz, B., Robinson, W. H, Baranzini, S. E., Grinnell, B. W., Raine, C. S., Sobel, R. A., Han, D. K., and Steinman, L. (2008) Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 451, 1076-1081
3. Wang, K. X., and Denhardt, D. T. (2008) Osteopontin. Role in immune regulation and stress responses. Cytokine Growth Factor Rev. 19, 333-345
4. El-Tanani, M. K., Campbell, F. C., Kurisetty, V., Jin, D., McCann, M., and Rudland, P. S. (2006) The regulation and role of osteopontin in malignant transformation and cancer. Cytokine Growth Factor Rev. 17, 463-474
5. Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., and Massague, J. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524
6. Van De Vijver, M. J., He, Y. D., Van't Veer, L. J., Dai, H., Hart, A. A., Voskuil, D. W., Schreiber, G. J., Peterse, J. L., Roberts, C., Marton, M. J., Parrish, M., Atsma, D., Witteveen, A., Glas, A., Delahaye, L., Van Der Velde, T., Bartelink, H, Rodenhuis, S., Rutgers, E. T., Friend, S. H., and Bernards, R. (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl. J. Med. 347, 1999-2009
7. Rudland, P. S., Platt-Higgins, A., El-Tanani, M., De Silva Rudland, S., Barraclough, R., Winstanley, J. H., Howitt, R., and West, C. R. (2002) Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res. 62, 3417-3427
8. Colin, C, Baeza, N., Bartoli, C, Fina, F., Eudes, N., Nanni, I., Martin, P. M., Ouafik, L., and Figarella-Branger, D. (2006) Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using suppression subtractive hybridization. Oncogene 25, 2818-2826
9. Atai, N. A., Bansal, M., Lo, C, Bosman, J., Tigchelaar, W., Bosch, K. S., Jonker, A., De Witt Hamer, P. C, Troost, D., McCulloch, C. A., Everts, V., Van Noorden, C. J., and Sodek, J. (2011) Osteopontin is up-regulated and associated with neutrophil and macrophage infiltration in glioblastoma. Immunology 132, 39-48
10. Tuck, A. B., Chambers, A. F., and Allan, A. L. (2007) Osteopontin overexpression in breast cancer. Knowledge gained and possible implications for clinical management. J. Cell. Biochem. 102, 859-868
11. Formolo, C. A., Williams, R., Gordish-Dressman, H., MacDonald, T. J., Lee, N. H., and Hathout, Y. (2011) Secretome signature of invasive glioblastoma multiforme. J. Proteome Res. 10, 3149-3159
12. Jan, H. J., Lee, C. C, Shih, Y. L., Hueng, D. Y., Ma, H. I., Lai, J. H., Wei, H. W., and Lee, H. M. (2010) Osteopontin regulates human glioma cell invasiveness and tumor growth in mice. Neuro-oncol. 12, 58-70
13. Lamour, V., Le Mercier, M., Lefranc, F., Hagedorn, M., Javerzat, S., Bikfalvi, A., Kiss, R., Castronovo, V., and Bellahcene, A. (2010) Selective osteopontin knockdown exerts anti-tumoral activity in a human glioblastoma model. Int. J. Cancer 126, 1797-1805
14. Lin, Y. H., and Yang-Yen, H. F. (2001) The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J. Biol. Chem. 276, 46024-46030
15. Denhardt, D. T., Giachelli, C. M., and Rittling, S. R. (2001) Role of osteopontin in cellular signaling and toxicant injury. Annu. Rev. Pharmacol. Toxicol. 41, 723-749
16. Wai, P. Y., and Kuo, P. C (2004) The role of osteopontin in tumor metastasis. J. Surg. Res. 121, 228-241
17. Myles, T., and Leung, L. L. (2008) Thrombin hydrolysis of human osteopontin is dependent on thrombin anion-binding exosites. J. Biol. Chem. 283, 17789-17796
18. Smith, L. L., and Giachelli, C. M. (1998) Structural requirements for α9β1-mediated adhesion and migration to thrombin-cleaved osteopontin. Exp. Cell Res. 242, 351-360
19. Taooka, Y., Chen, J., Yednock, T., and Sheppard, D. (1999) The integrin α9β1 mediates adhesion to activated endothelial cells and transendothelial neutrophil migration through interaction with vascular cell adhesion molecule-1. J. Cell Biol. 145, 413-420
20. 1 binds to a novel recognition sequence (SVVYGLR) in the thrombin-cleaved amino-terminal fragment of osteopontin. J. Biol. Chem. 274, 36328-36334
21. Barry, S. T., Ludbrook, S. B., Murrison, E., and Horgan, C. M. (2000) A regulated interaction between α5β1 integrin and osteopontin. Biochem. Biophys. Res. Commun. 267, 764-769
22. Barry, S. T., Ludbrook, S. B., Murrison, E., and Horgan, C. M. (2000) Analysis of the α4β1 integrin-osteopontin interaction. Exp. Cell Res. 258, 342-351
23. Bayless, K. J., and Davis, G. E. (2001) Identification of dual α4β1 integrin binding sites within a 38-amino acid domain in the N-terminal thrombin fragment of human osteopontin. J. Biol. Chem. 276, 13483-13489
24. 4 integrins. FEBS Lett. 503, 75-79
25. Sharif, S. A., Du, X., Myles, T., Song, J. J., Price, E., Lee, D. M., Goodman, S. B., Nagashima, M., Morser, J., Robinson, W. H., and Leung, L. L. (2009) Thrombin-activatable carboxypeptidase B cleavage of osteopontin regulates neutrophil survival and synoviocyte binding in rheumatoid arthritis. Arthritis Rheum. 60, 2902-2912
26. Myles, T., Nishimura, T., Yun, T. H., Nagashima, M., Morser, J., Patterson, A. J., Pearl, R. G., and Leung, L. L. (2003) Thrombin activatable fibrinolysis inhibitor, a potential regulator of vascular inflammation. J. Biol. Chem. 278, 51059-51067
27. Reynes, G., Vila, V., Martín, M., Parada, A., Fleitas, T., Reganon, E., and Martínez-Sales, V. (2011) Circulating markers of angiogenesis, inflammation, and coagulation in patients with glioblastoma. J. Neurooncol. 102, 35-41
28. Tehrani, M., Friedman, T. M., Olson, J. J., and Brat, D. J. (2008) Intravascular thrombosis in central nervous system malignancies. A potential role in astrocytoma progression to glioblastoma. Brain Pathol. 18, 164-171
29. Yamaguchi, Y., Du, X. Y., Zhao, L., Morser, J., and Leung, L. L. (2011) Proteolytic cleavage of chemerin protein is necessary for activation to the active form, Chem157S, which functions as a signaling molecule in glioblastoma. J. Biol. Chem. 286, 39510-39519
30. Hsieh, J., Aimone, J. B., Kaspar, B. K., Kuwabara, T., Nakashima, K., and Gage, F. H. (2004) IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J. Cell Biol. 164, 111-122
31. Anand, M., and Brat, D. J. (2012) Oncogenic regulation of tissue factor and thrombosis in cancer. Thromb. Res. 129, S46-S49
32. Hua, Y., Tang, L., Keep, R. F., Schallert, T., Fewel, M. E., Muraszko, K. M., Hoff, J. T., and Xi, G. (2005) The role of thrombin in gliomas. J. Thromb. Haemost. 3, 1917-1923
33. Yan, W., Qian, C., Zhao, P., Zhang, J., Shi, L., Qian, J., Liu, N, Fu, Z., Kang, C., Pu, P., and You, Y. (2010) Expression pattern of osteopontin splice variants and its functions on cell apoptosis and invasion in glioma cells. Neuro-oncol. 12, 765-775
34. Rice, J., Courter, D. L., Giachelli, C. M., and Scatena, M. (2006) Molecular mediators of αvβ3-induced endothelial cell survival. J. Vasc. Res. 43, 422-436
35. Singh, S. K., Hawkins, C., Clarke, I. D., Squire, J. A., Bayani, J., Hide, T., Henkelman, R. M., Cusimano, M. D., and Dirks, P. B. (2004) Identification of human brain tumour initiating cells. Nature 432, 396-401
36. Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C, Squire, J., and Dirks, P. B. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821-5828
37. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., and Clarke, M. F. (2003) Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 100, 3983-3988
38. Li, C, Heidt, D. G., Dalerba, P., Burant, C. F., Zhang, L., Adsay, V., Wicha, M., Clarke, M. F., and Simeone, D. M. (2007) Identification of pancreatic cancer stem cells. Cancer Res. 67, 1030-1037
39. Patrawala, L., Calhoun, T., Schneider-Broussard, R., Li, H, Bhatia, B., Tang, S., Reilly, J. G., Chandra, D., Zhou, J., Claypool, K., Coghlan, L., and Tang, D. G. (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25, 1696-1708
40. Pollard, S. M., Yoshikawa, K., Clarke, I. D., Danovi, D., Stricker, S., Russell, R., Bayani, J., Head, R., Lee, M., Bernstein, M., Squire, J. A., Smith, A., and Dirks, P. (2009) Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4, 568-580
41. Jijiwa, M., Demir, H., Gupta, S., Leung, C, Joshi, K., Orozco, N, Huang, T., Yildiz, V. O., Shibahara, I., De Jesus, J. A., Yong, W. H, Mischel, P. S., Fernandez, S., Kornblum, H. I., and Nakano, I. (2011) CD44v6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway. PLoS ONE 6, e24217
42. Yao, X. H, Ping, Y. F., Chen, J. H, Xu, C. P., Chen, D. L., Zhang, R., Wang, J. M., and Bian, X. W. (2008) Glioblastoma stem cells produce vascular endothelial growth factor by activation of a G-protein coupled formylpeptide receptor FPR. J. Pathol. 215, 369-376
43. Annabi, B., Laflamme, C, Sina, A., Lachambre, M. P., and Beliveau, R. (2009) A MT1-MMP/NF-κB signaling axis as a checkpoint controller of COX-2 expression in CD133+ U87 glioblastoma cells. J. Neuroinflammation 6, 8
44. Scheinkestel, C. D., Jones, K., Myles, P. S., Cooper, D. J., Millar, I. L., and Tuxen, D. V. (2004) Where to now with carbon monoxide poisoning? Emerg. Med. Australas. 16, 151-154
45. Brandsma, D., Stalpers, L., Taal, W., Sminia, P., and Van Den Bent, M. J. (2008) Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 9, 453-461
46. Norden, A. D., Young, G. S., Setayesh, K., Muzikansky, A., Klufas, R., Ross, G. L., Ciampa, A. S., Ebbeling, L. G., Levy, B., Drappatz, J., Kesari, S., and Wen, P. Y. (2008) Bevacizumab for recurrent malignant gliomas. Efficacy, toxicity, and patterns of recurrence. Neurology 70, 779-787
47. Sreekanthreddy, P., Srinivasan, H, Kumar, D. M., Nijaguna, M. B., Sridevi, S., Vrinda, M., Arivazhagan, A., Balasubramaniam, A., Hegde, A. S., Chandramouli, B. A., Santosh, V., Rao, M. R., Kondaiah, P., and Somasundaram, K. (2010) Identification of potential serum biomarkers of glioblastoma. Serum osteopontin levels correlate with poor prognosis. Cancer Epidemiol. Biomarkers Prev. 19, 1409-1422
48. Schuhmann, M. U., Zucht, H. D., Nassimi, R., Heine, G., Schneekloth, C. G., Stuerenburg, H. J., and Selle, H. (2010) Peptide screening of cerebrospinal fluid in patients with glioblastoma multiforme. Eur. J. Surg. Oncol. 36, 201-207
49. Lahav, J., Gofer-Dadosh, N, Luboshitz, J., Hess, O., and Shaklai, M. (2000) Protein-disulfide isomerase mediates integrin-dependent adhesion. FEBS Lett. 475, 89-92
50. Selistre-de-Araujo, H. S., Pontes, C. L., Montenegro, C. F., and Martin, A. C. (2010) Snake venom disintegrins and cell migration. Toxins 2, 2606-2621
51. Lu, X., Lu, D., Scully, M. F., and Kakkar, V. V. (2007) Structure-activity relationship studies on ADAM protein-integrin interactions. Cardiovasc. Hematol. Agents Med. Chem. 5, 29-42
52. Qi, B., Newcomer, R. G., and Sang, Q. X. (2009) ADAM19/adamalysin 19 structure, function, and role as a putative target in tumors and inflammatory diseases. Curr. Pharm. Des. 15, 2336-2348
53. Stanton, H, Melrose, J., Little, C. B., and Fosang, A. J. (2011) Proteoglycan degradation by the ADAMTS family of proteinases. Biochim. Biophys. Acta 1812, 1616-1629
54. Grassinger, J., Haylock, D. N, Storan, M. J., Haines, G. O., Williams, B., Whitty, G. A., Vinson, A. R., Be, C. L., Li, S., Sørensen, E. S., Tam, P. P., Denhardt, D. T., Sheppard, D., Choong, P. F., and Nilsson, S. K. (2009) Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with α9β1 and α4β1 integrins. Blood 114, 49-59
55. McAllister, S. S., Gifford, A. M., Greiner, A. L., Kelleher, S. P., Saelzler, M. P., Ince, T. A., Reinhardt, F., Harris, L. N, Hylander, B. L., Repasky, E. A., and Weinberg, R. A. (2008) Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 133, 994-1005
56. Wels, J., Kaplan, R. N, Rafii, S., and Lyden, D. (2008) Migratory neighbors and distant invaders. Tumor-associated niche cells. Genes Dev. 22, 559-574
57. Takano, S., Tsuboi, K., Tomono, Y., Mitsui, Y., and Nose, T. (2000) Tissue factor, osteopontin, αvβ3 integrin expression in microvasculature of gliomas associated with vascular endothelial growth factor expression. Br. J. Cancer 82, 1967-1973
58. Hua, Y., Tang, L. L., Fewel, M. E., Keep, R. F., Schallert, T., Muraszko, K. M., Hoff, J. T., and Xi, G. H. (2005) Systemic use of argatroban reduces tumor mass, attenuates neurological deficits, and prolongs survival time in rat glioma models. Acta Neurochir. Suppl. 95, 403-406
59. Ornstein, D. L., Meehan, K. R., and Zacharski, L. R. (2002) The coagulation system as a target for the treatment of human gliomas. Semin. Thromb. Hemost. 28, 19-28