The RGD domain of human osteopontin promotes tumor growth and metastasis through activation of survival pathways

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Courter, Donald ^a   Cao, Hongbin ^a   Kwok, Shirley ^b   Kong, Christina ^b   Banh, Alice ^a   Kuo, Peiwen ^a   Bouley, Donna M ^a   Vice, Carmen ^a   Brustugun, Odd Terje ^c   Denko, Nicholas C ^a   Koong, Albert C ^a   Giaccia, Amato ^a   Le, Quynh Thu ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; ARGINYLGLYCYLASPARTIC ACID; FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OSTEOPONTIN; OSTEOPONTIN A; OSTEOPONTIN B; SMALL INTERFERING RNA; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; ARGINYL-GLYCYL-ASPARTIC ACID; ISOPROTEIN; OLIGOPEPTIDE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL ADHESION; CELL MIGRATION; CELL MUTANT; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPOXIA; IN VITRO STUDY; LUNG CARCINOMA; LUNG METASTASIS; METASTASIS; MUTATION; NICK END LABELING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERE COMBINED IMMUNODEFICIENCY; SOFT TISSUE SARCOMA; STARVATION; SURVIVAL; TUMOR GROWTH; TUMOR LOCALIZATION; XENOGRAFT; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; MOUSE; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MUTATION; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; OLIGOPEPTIDES; OSTEOPONTIN; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY;

EID: 77949818678     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009633     Document Type: Article

References (65)

1. Denhardt DT, Noda M (1998) Osteopontin expression and function: role in bone remodeling. J Cell Biochem Suppl 30-31: 92-102.
2. Ashkar S, Weber GF, Panoutsakopoulou V, Sanchirico ME, Jansson M, et al. (2000) Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287: 860-864.
3. Gravallese EM (2003) Osteopontin: a bridge between bone and the immune system. J Clin Invest 112: 147-149.
4. Tuck AB, Chambers AF, Allan AL (2007) Osteopontin overexpression in breast cancer: knowledge gained and possible implications for clinical management. J Cell Biochem 102: 859-868.
5. Wai PY, Kuo PC (2004) The role of Osteopontin in tumor metastasis. J Surg Res 121: 228-241.
6. Rittling SR, Chambers AF (2004) Role of osteopontin in tumour progression. Br J Cancer 90: 1877-1881.
7. Wai PY, Kuo PC (2008) Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev 27: 103-118.
8. Oldberg A, Franzen A, Heinegard D (1986) Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc Natl Acad Sci U S A 83: 8819-8823.
9. Yokosaki Y, Tanaka K, Higashikawa F, Yamashita K, Eboshida A (2005) Distinct structural requirements for binding of the integrins alphavbeta6, alphavbeta3, alphavbeta5, alpha5beta1 and alpha9beta1 to osteopontin. Matrix Biol 24: 418-427.
10. Miyauchi A, Alvarez J, Greenfield EM, Teti A, Grano M, et al. (1991) Recognition of osteopontin and related peptides by an alpha v beta 3 integrin stimulates immediate cell signals in osteoclasts. J Biol Chem 266: 20369-20374.
11. Hu DD, Hoyer JR, Smith JW (1995) Characterization of the interaction between integrins and recombinant human osteopontin. Ann N Y Acad Sci 760: 312-314.
12. Hu DD, Lin EC, Kovach NL, Hoyer JR, Smith JW (1995) A biochemical characterization of the binding of osteopontin to integrins alpha v beta 1 and alpha v beta 5. J Biol Chem 270: 26232-26238.
13. Liaw L, Skinner MP, Raines EW, Ross R, Cheresh DA, et al. (1995) The adhesive and migratory effects of osteopontin are mediated via distinct cell surface integrins. Role of alpha v beta 3 in smooth muscle cell migration to osteopontin in vitro. J Clin Invest 95: 713-724.
14. Senger DR, Perruzzi CA, Papadopoulos-Sergiou A, Van de Water L (1994) Adhesive properties of osteopontin: regulation by a naturally occurring thrombin-cleavage in close proximity to the GRGDS cell-binding domain. Mol Biol Cell 5: 565-574.
15. Liaw L, Almeida M, Hart CE, Schwartz SM, Giachelli CM (1994) Osteopontin promotes vascular cell adhesion and spreading and is chemotactic for smooth muscle cells in vitro. Circ Res 74: 214-224.
16. Yue TL, McKenna PJ, Ohlstein EH, Farach-Carson MC, Butler WT, et al. (1994) Osteopontin-stimulated vascular smooth muscle cell migration is mediated by beta 3 integrin. Exp Cell Res 214: 459-464.
17. Philip S, Bulbule A, Kundu GC (2001) Osteopontin stimulates tumor growth and activation of promatrix metalloproteinase-2 through nuclear factor-kappa B-mediated induction of membrane type 1 matrix metalloproteinase in murine melanoma cells. J Biol Chem 276: 44926-44935.
18. Christensen B, Nielsen MS, Haselmann KF, Petersen TE, Sorensen ES (2005) Post-translationally modified residues of native human osteopontin are located in clusters: identification of 36 phosphorylation and five O-glycosylation sites and their biological implications. Biochem J 390: 285-292.
19. Christensen B, Kazanecki CC, Petersen TE, Rittling SR, Denhardt DT, et al. (2007) Cell type-specific post-translational modifications of mouse osteopontin are associated with different adhesive properties. J Biol Chem 282: 19463-19472.
20. Kazanecki CC, Uzwiak DJ, Denhardt DT (2007) Control of osteopontin signaling and function by post-translational phosphorylation and protein folding. J Cell Biochem 102: 912-924.
21. Rittling SR, Chen Y, Feng F, Wu Y (2002) Tumor-derived osteopontin is soluble, not matrix associated. J Biol Chem 277: 9175-9182.
22. Allan AL, George R, Vantyghem SA, Lee MW, Hodgson NC, et al. (2006) Role of the integrin-binding protein osteopontin in lymphatic metastasis of breast cancer. Am J Pathol 169: 233-246.
23. He B, Mirza M, Weber GF (2006) An osteopontin splice variant induces anchorage independence in human breast cancer cells. Oncogene 25: 2192-2202.
24. Mirza M, Shaughnessy E, Hurley JK, Vanpatten KA, Pestano GA, et al. (2008) Osteopontin-c is a selective marker of breast cancer. Int J Cancer 122: 889-897.
25. Ivanov SV, Ivanova AV, Goparaju CM, Chen Y, Beck A, et al. (2009) Tumorigenic properties of alternative osteopontin isoforms in mesothelioma. Biochem Biophys Res Commun 382: 514-518.
26. Zhu Y, Denhardt DT, Cao H, Sutphin PD, Koong AC, et al. (2005) Hypoxia upregulates osteopontin expression in NIH-3T3 cells via a Ras-activated enhancer. Oncogene.
27. Loster K, Schuler C, Heidrich C, Horstkorte R, Reutter W (1997) Quantification of cell-matrix and cell-cell adhesion using horseradish peroxidase. Anal Biochem 244: 96-102.
28. Graves EE, Quon A, Loo BW, Jr. (2007) RT-Image: an open-source tool for investigating PET in radiation oncology. Technol Cancer Res Treat 6: 111-121.
29. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, et al. (2006) Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440: 1222-1226.
30. Le QT, Sutphin PD, Raychaudhuri S, Yu SC, Terris DJ, et al. (2003) Identification of osteopontin as a prognostic plasma marker for head and neck squamous cell carcinomas. Clin Cancer Res 9: 59-67.
31. Le QT, Kong C, Lavori PW, O'Byrne K, Erler JT, et al. (2007) Expression and Prognostic Significance of a Panel of Tissue Hypoxia Markers in Head-and-Neck Squamous Cell Carcinomas. Int J Radiat Oncol Biol Phys 69: 167-175.
32. Chakraborty G, Jain S, Kundu GC (2008) Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms. Cancer Res 68: 152-161.
33. Cui R, Takahashi F, Ohashi R, Gu T, Yoshioka M, et al. (2007) Abrogation of the interaction between osteopontin and alphavbeta3 integrin reduces tumor growth of human lung cancer cells in mice. Lung Cancer 57: 302-310.
34. Zhao J, Dong L, Lu B, Wu G, Xu D, et al. (2008) Down-regulation of osteopontin suppresses growth and metastasis of hepatocellular carcinoma via induction of apoptosis. Gastroenterology 135: 956-968.
35. Gong M, Lu Z, Fang G, Bi J, Xue X (2008) A small interfering RNA targeting osteopontin as gastric cancer therapeutics. Cancer Lett.
36. Furger KA, Allan AL, Wilson SM, Hota C, Vantyghem SA, et al. (2003) Beta(3) integrin expression increases breast carcinoma cell responsiveness to the malignancy-enhancing effects of osteopontin. Mol Cancer Res 1: 810-819.
37. Nasu K, Ishida T, Setoguchi M, Higuchi Y, Akizuki S, et al. (1995) Expression of wild-type and mutated rabbit osteopontin in Escherichia coli, and their effects on adhesion and migration of P388D1 cells. Biochem J 307(Pt 1): 257-265.
38. Tuck AB, Elliott BE, Hota C, Tremblay E, Chambers AF (2000) Osteopontin-induced, integrin-dependent migration of human mammary epithelial cells involves activation of the hepatocyte growth factor receptor (Met). J Cell Biochem 78: 465-475.
39. Mi Z, Guo H, Wai PY, Gao C, Kuo PC (2006) Integrin-linked kinase regulates osteopontin-dependent MMP-2 and uPA expression to convey metastatic function in murine mammary epithelial cancer cells. Carcinogenesis 27: 1134-1145.
40. Khan SA, Lopez-Chua CA, Zhang J, Fisher LW, Sorensen ES, et al. (2002) Soluble osteopontin inhibits apoptosis of adherent endothelial cells deprived of growth factors. J Cell Biochem 85: 728-736.
41. Geissinger E, Weisser C, Fischer P, Schartl M, Wellbrock C (2002) Autocrine stimulation by osteopontin contributes to antiapoptotic signalling of melanocytes in dermal collagen. Cancer Res 62: 4820-4828.
42. Gu T, Ohashi R, Cui R, Tajima K, Yoshioka M, et al. (2009) Osteopontin is involved in the development of acquired chemo-resistance of cisplatin in small cell lung cancer. Lung Cancer 66: 176-183.
43. Kim HJ, Lee HJ, Jun JI, Oh Y, Choi SG, et al. (2009) Intracellular cleavage of osteopontin by caspase-8 modulates hypoxia/reoxygenation cell death through p53. Proc Natl Acad Sci U S A 106: 15326-15331.
44. Hsieh YH, Juliana MM, Hicks PH, Feng G, Elmets C, et al. (2006) Papilloma development is delayed in osteopontin-null mice: implicating an antiapoptosis role for osteopontin. Cancer Res 66: 7119-7127.
45. Nystrom T, Duner P, Hultgardh-Nilsson A (2007) A constitutive endogenous osteopontin production is important for macrophage function and differentiation. Exp Cell Res 313: 1149-1160.
46. Trikha M, Zhou Z, Nemeth JA, Chen Q, Sharp C, et al. (2004) CNTO 95, a fully human monoclonal antibody that inhibits alphav integrins, has antitumor and antiangiogenic activity in vivo. Int J Cancer 110: 326-335.
47. Martin PL, Jiao Q, Cornacoff J, Hall W, Saville B, et al. (2005) Absence of adverse effects in cynomolgus macaques treated with CNTO 95, a fully human anti-alphav integrin monoclonal antibody, despite widespread tissue binding. Clin Cancer Res 11: 6959-6965.
48. Ning S, Nemeth JA, Hanson RL, Forsythe K, Knox SJ (2008) Anti-integrin monoclonal antibody CNTO 95 enhances the therapeutic efficacy of fractionated radiation therapy in vivo. Mol Cancer Ther 7: 1569-1578.
49. Zohar R, Zhu B, Liu P, Sodek J, McCulloch CA (2004) Increased cell death in osteopontin-deficient cardiac fibroblasts occurs by a caspase-3-independent pathway. Am J Physiol Heart Circ Physiol 287: H1730-1739.
50. Da Silva AP, Pollett A, Rittling SR, Denhardt DT, Sodek J, et al. (2006) Exacerbated tissue destruction in DSS-induced acute colitis of OPN-null mice is associated with downregulation of TNF-alpha expression and non-programmed cell death. J Cell Physiol 208: 629-639.
51. Denhardt DT, Noda M, O'Regan AW, Pavlin D, Berman JS (2001) Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 107: 1055-1061.
52. Burdo TH, Wood MR, Fox HS (2007) Osteopontin prevents monocyte recirculation and apoptosis. J Leukoc Biol 81: 1504-1511.
53. Hur EM, Youssef S, Haws ME, Zhang SY, Sobel RA, et al. (2007) Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat Immunol 8: 74-83.
54. Fan K, Dai J, Wang H, Wei H, Cao Z, et al. (2008) Treatment of collagen-induced arthritis with an anti-osteopontin monoclonal antibody through promotion of apoptosis of both murine and human activated T cells. Arthritis Rheum 58: 2041-2052.
55. Cao Z, Dai J, Fan K, Wang H, Ji G, et al. (2008) A novel functional motif of osteopontin for human lymphocyte migration and survival. Mol Immunol 45: 3683-3692.
56. Scatena M, Almeida M, Chaisson ML, Fausto N, Nicosia RF, et al. (1998) NF-kappaB mediates alphavbeta3 integrin-induced endothelial cell survival. J Cell Biol 141: 1083-1093.
57. Philip S, Kundu GC (2003) Osteopontin induces nuclear factor kappa B-mediated promatrix metalloproteinase-2 activation through I kappa B alpha/ IKK signaling pathways, and curcumin (diferulolylmethane) down-regulates these pathways. J Biol Chem 278: 14487-14497.
58. Rice J, Courter DL, Giachelli CM, Scatena M (2006) Molecular mediators of alphavbeta3-induced endothelial cell survival. J Vasc Res 43: 422-436.
59. Hood JD, Cheresh DA (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2: 91-100.
60. Hehlgans S, Haase M, Cordes N (2007) Signalling via integrins: implications for cell survival and anticancer strategies. Biochim Biophys Acta 1775: 163-180.
61. Fong YC, Liu SC, Huang CY, Li TM, Hsu SF, et al. (2008) Osteopontin increases lung cancer cells migration via activation of the alphavbeta3 integrin/ FAK/Akt and NF-kappaB-dependent pathway. Lung Cancer.
62. Li JJ, Han M, Wen JK, Li AY (2007) Osteopontin stimulates vascular smooth muscle cell migration by inducing FAK phosphorylation and ILK dephosphorylation. Biochem Biophys Res Commun 356: 13-19.
63. Lin YH, Yang-Yen HF (2001) The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J Biol Chem 276: 46024-46030.
64. Blasberg JD, Goparaju CM, Pass HI, Donington JS (2009) Lung cancer osteopontin isoforms exhibit angiogenic functional heterogeneity. J Thorac Cardiovasc Surg.
65. Chae S, Jun HO, Lee EG, Yang SJ, Lee DC, et al. (2009) Osteopontin splice variants differentially modulate the migratory activity of hepatocellular carcinoma cell lines. Int J Oncol 35: 1409-1416.