Interplay between αvβ3 integrin and nucleolin regulates human endothelial and glioma cell migration

Journal of Biological Chemistry

Volumn 288, Issue 1, 2013, Pages 343-354

  Koutsioumpa, Marina ^a   Polytarchou, Christos ^b,c,g   Courty, José ^d   Zhang, Yue ^e   Kieffer, Nelly ^e   Mikelis, Constantinos ^a,h   Skandalis, Spyros S ^a,f   Hellman, Ulf ^f   Iliopoulos, Dimitrios ^b,c,g   Papadimitriou, Evangelia ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Université Paris Est Créteil   (France)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

^f UPPSALA UNIVERSITY   (Sweden)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC GROWTH FACTORS; ANTI-CANCER AGENTS; CELL MIGRATION; CELL SURFACES; GLIOBLASTOMAS; GLIOMA CELLS; INTEGRINS; MULTIFUNCTIONAL PROTEIN; NUCLEOLIN; PLEIOTROPHIN; POSITIVE CORRELATIONS; PROTEIN-TYROSINE PHOSPHATASE; SIGNALING CASCADES; TUMOR CELLS;

AMINO ACIDS; CELL MEMBRANES; CYTOLOGY; PHOSPHORYLATION; PROTEINS; TUMORS;

ENDOTHELIAL CELLS;

BETA3 INTEGRIN; NUCLEOLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE P60; VITRONECTIN RECEPTOR;

ARTICLE; ASTROCYTOMA; CELL MIGRATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL MARKERS; CARRIER PROTEINS; CELL MEMBRANE; CELL MOVEMENT; CHO CELLS; CRICETINAE; CYTOKINES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; INTEGRIN ALPHAVBETA3; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOPROTEINS; PHOSPHORYLATION; RATS; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84872076844     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.387076     Document Type: Article

References (62)

1. Srivastava, M., and Pollard, H. B. (1999) Molecular dissection of nucleolin's role in growth and cell proliferation. New insights. FASEB J. 13, 1911-1922
2. Hovanessian, A. G., Puvion-Dutilleul, F., Nisole, S., Svab, J., Perret, E., Deng, J. S., and Krust, B. (2000) The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp. Cell Res. 261, 312-328
3. Destouches, D., El Khoury, D., Hamma-Kourbali, Y., Krust, B., Albanese, P., Katsoris, P., Guichard, G., Briand, J. P., Courty, J., and Hovanessian, A. G. (2008) Suppression of tumor growth and angiogenesis by a specific antagonist of the cell-surface expressed nucleolin. PLoS One 3, e2518
4. Di Segni, A., Farin, K., and Pinkas-Kramarski, R. (2008) Identification of nucleolin as new ErbB receptors-interacting protein. PLoS One 3, e2310
5. Hoja-Łukowicz, D., Przybyło, M., Pocheć, E., Drabik, A., Silberring, J., Kremser, M., Schadendorf, D., Laidler, P., and Lityńska, A. (2009) The new face of nucleolin in human melanoma. Cancer Immunol. Immunother. 58, 1471-1480
6. Christian, S., Pilch, J., Akerman, M. E., Porkka, K., Laakkonen, P., and Ruoslahti, E. (2003) Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J. Cell Biol. 163, 871-878
7. Fogal, V., Sugahara, K. N., Ruoslahti, E., and Christian, S. (2009) Cell surface nucleolin antagonist causes endothelial cell apoptosis and normalization of tumor vasculature. Angiogenesis 12, 91-100
8. Huang, Y., Shi, H., Zhou, H., Song, X., Yuan, S., and Luo, Y. (2006) The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin. Blood 107, 3564-3571
9. El Khoury, D., Destouches, D., Lengagne, R., Krust, B., Hamma-Kourbali, Y., Garcette, M., Niro, S., Kato, M., Briand, J. P., Courty, J., Hovanessian, A. G., and Prévost-Blondel, A. (2010) Targeting surface nucleolin with a multivalent pseudopeptide delays development of spontaneous melanoma in RET transgenic mice. BMC Cancer 10, 325
10. Krust, B., El Khoury, D., Nondier, I., Soundaramourty, C., and Hovanessian, A. G. (2011) Targeting surface nucleolin with multivalent HB-19 and related Nucant pseudopeptides results in distinct inhibitory mechanisms depending on the malignant tumor cell type. BMC Cancer 11, 333
11. Soundararajan, S., Wang, L., Sridharan, V., Chen, W., Courtenay-Luck, N., Jones, D., Spicer, E. K., and Fernandes, D. J. (2009) Plasma membrane nucleolin is a receptor for the anticancer aptamer AS1411 in MV4-11 leukemia cells. Mol. Pharmacol. 76, 984-991
12. Destouches, D., Page, N., Hamma-Kourbali, Y., Machi, V., Chaloin, O., Frechault, S., Birmpas, C., Katsoris, P., Beyrath, J., Albanese, P., Maurer, M., Carpentier, G., Strub, J. M., Van Dorsselaer, A., Muller, S., Bagnard, D., Briand, J. P., and Courty, J. (2011) A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res. 71, 3296-3305
13. Tate, A., Isotani, S., Bradley, M. J., Sikes, R. A., Davis, R., Chung, L. W., and Edlund, M. (2006) Met-independent hepatocyte growth factor-mediated regulation of cell adhesion in human prostate cancer cells. BMC Cancer 6, 197
14. Shi, H., Huang, Y., Zhou, H., Song, X., Yuan, S., Fu, Y., and Luo, Y. (2007) Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood 110, 2899-2906
15. Kibbey, M. C., Johnson, B., Petryshyn, R., Jucker, M., and Kleinman, H. K. (1995) A 110-kDa nuclear shuttling protein, nucleolin, binds to the neurite-promoting IKVAV site of laminin-1. J. Neurosci. Res. 42, 314-322
16. Reyes-Reyes, E. M., and Akiyama, S. K. (2008) Cell-surface nucleolin is a signal transducing P-selectin binding protein for human colon carcinoma cells. Exp. Cell Res. 314, 2212-2223
17. Said, E. A., Krust, B., Nisole, S., Svab, J., Briand, J. P., and Hovanessian, A. G. (2002) The anti-HIV cytokine midkine binds the cell surface-expressed nucleolin as a low affinity receptor. J. Biol. Chem. 277, 37492-37502
18. Koutsioumpa, M., Drosou, G., Mikelis, C., Theochari, K., Vourtsis, D., Katsoris, P., Giannopoulou, E., Courty, J., Petrou, C., Magafa, V., Cordopatis, P., and Papadimitriou, E. (2012) Pleiotrophin expression and role in physiological angiogenesis in vivo. Potential involvement of nucleolin. Vascular Cell 4, 4
19. Desgrosellier, J. S., and Cheresh, D. A. (2010) Integrins in cancer. Biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9-22
20. Falcioni, R., Antonini, A., Nisticò, P., Di Stefano, S., Crescenzi, M., Natali, P. G., and Sacchi, A. (1997) α6β4 and α6β1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp. Cell Res. 236, 76-85
21. Borges, E., Jan, Y., and Ruoslahti, E. (2000) Platelet-derived growth factor receptor β and vascular endothelial growth factor receptor 2 bind to the β3 integrin through its extracellular domain. J. Biol. Chem. 275, 39867-39873
22. Patsenker, E., Popov, Y., Wiesner, M., Goodman, S. L., and Schuppan, D. (2007) Pharmacological inhibition of the vitronectin receptor abrogates PDGF-BB-induced hepatic stellate cell migration and activation in vitro. J. Hepatol. 46, 878-887
23. Mahabeleshwar, G. H., Feng, W., Reddy, K., Plow, E. F., and Byzova, T. V. (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101, 570-580
24. 3 is a pleiotrophin receptor required for pleiotro-phin- induced endothelial cell migration through receptor protein tyrosine phosphatase β/ζ. FASEB J. 23, 1459-1469
25. Papadimitriou, E., Mikelis, C., Lampropoulou, E., Koutsioumpa, M., Theochari, K., Tsirmoula, S., Theodoropoulou, C., Lamprou, M., Sfaelou, E., Vourtsis, D., and Boudouris, P. (2009) Roles of pleiotrophin in tumor growth and angiogenesis. Eur. Cytokine Netw. 20, 180-190
26. Polykratis, A., Katsoris, P., Courty, J., and Papadimitriou, E. (2005) Characterization of heparin affin regulatory peptide signaling in human endothelial cells. J. Biol. Chem. 280, 22454-22461
27. Papadimitriou, E., Polykratis, A., Courty, J., Koolwijk, P., Heroult, M., and Katsoris, P. (2001) HARP induces angiogenesis in vivo and in vitro. Implication of N or C terminal peptides. Biochem. Biophys. Res. Commun. 282, 306-313
28. Héroult, M., Bernard-Pierrot, I., Delbé, J., Hamma-Kourbali, Y., Katsoris, P., Barritault, D., Papadimitriou, E., Plouet, J., and Courty, J. (2004) Heparin affin regulatory peptide binds to vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. Oncogene 23, 1745-1753
29. Schaffner-Reckinger, E., Gouon, V., Melchior, C., Plançon, S., and Kieffer, N. (1998) Distinct involvement of β3 integrin cytoplasmic domain tyrosine residues 747 and 759 in integrin mediated cytoskeletal assembly and phosphotyrosine signaling. J. Biol. Chem. 273, 12623-12632
30. o, and N-type calcium channel complex at a presynaptic nerve terminal. Analysis by quantitative immunocolocalization. J. Neurosci. 24, 4070-4081
31. Hellman, U. (2002) in Mass Spectrometry and Hyphenated Techniques in Neuropeptide Research (Silberring, J., and Ekman, R., eds) pp. 259-275, John Wiley & Sons, Inc., New York
32. Lapeyre, B., Amalric, F., Ghaffari, S. H., Rao, S. V., Dumbar, T. S., and Olson, M. O. (1986) Protein and cDNA sequence of a glycine-rich, dimethylarginine-containing region located near the carboxyl-terminal end of nucleolin (C23 and 100 kDa). J. Biol. Chem. 261, 9167-9173
33. Turck, N., Lefebvre, O., Gross, I., Gendry, P., Kedinger, M., Simon-Assmann, P., and Launay, J. F. (2006) Effect of laminin-1 on intestinal cell differentiation involves inhibition of nuclear nucleolin. J. Cell Physiol. 206, 545-555
34. 3 integrin, osteopontin, and thrombin. Am. J. Pathol. 149, 293-305
35. 3 and VEGFR2 in angiogenesis. Angiogenesis 12, 177-185
36. 3 integrin and promotes angiogenesis. Biochem. Biophys. Res. Commun. 347, 248-253
37. Oikawa, Y., Hansson, J., Sasaki, T., Rousselle, P., Domogatskaya, A., Rodin, S., Tryggvason, K., and Patarroyo, M. (2011) Melanoma cells produce multiple laminin isoforms and strongly migrate on α5 laminin (s) via several integrin receptors. Exp. Cell Res. 317, 1119-1133
38. Rahman, S., Patel, Y., Murray, J., Patel, K. V., Sumathipala, R., Sobel, M., and Wijelath, E. S. (2005) Novel hepatocyte growth factor (HGF) binding domains on fibronectin and vitronectin coordinate a distinct and amplified Met-integrin induced signalling pathway in endothelial cells. BMC Cell Biol. 6, 8
39. Rehn, M., Veikkola, T., Kukk-Valdre, E., Nakamura, H., Ilmonen, M., Lombardo, C., Pihlajaniemi, T., Alitalo, K., and Vuori, K. (2001) Interaction of endostatin with integrins implicated in angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 98, 1024-1029
40. Chen, Y. Q., Trikha, M., Gao, X., Bazaz, R., Porter, A. T., Timar, J., and Honn, K. V. (1997) Ectopic expression of platelet integrin αIIb β3 in tumor cells from various species and histological origin. Int. J. Cancer 72, 642-648
41. Cain, R. J., and Ridley, A. J. (2009) Phosphoinositide 3-kinases in cell migration. Biol. Cell 101, 13-29
42. Wennström, S., Hawkins, P., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L., and Stephens, L. (1994) Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393
43. 4 integrin. Semin. Cancer Biol. 11, 129-141
44. Ginisty, H., Sicard, H., Roger, B., and Bouvet, P. (1999) Structure and functions of nucleolin. J. Cell Sci. 112, 761-772
45. Huddleson, J. P., Ahmad, N., and Lingrel, J. B. (2006) Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin. J. Biol. Chem. 281, 15121-15128
46. Lemmon, M. A., and Ferguson, K. M. (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem. J. 350, 1-18
47. Burks, D. J., Wang, J., Towery, H., Ishibashi, O., Lowe, D., Riedel, H., and White, M. F. (1998) IRS pleckstrin homology domains bind to acidic motifs in proteins. J. Biol. Chem. 273, 31061-31067
48. 3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J. Cell Biol. 140, 1255-1263
49. Inder, K. L., Hill, M. M., and Hancock, J. F. (2010) Nucleophosmin and nucleolin regulate K-Ras signaling. Commun. Integr. Biol. 3, 188-190
50. Dumler, I., Stepanova, V., Jerke, U., Mayboroda, O. A., Vogel, F., Bouvet, P., Tkachuk, V., Haller, H., and Gulba, D. C. (1999) Urokinase-induced mitogenesis is mediated by casein kinase 2 and nucleolin. Curr. Biol. 9, 1468-1476
51. Ko, M. H., Kim, S., Kang, W. J., Lee, J. H., Kang, H., Moon, S. H., Hwang do, W., Ko, H. Y., and Lee, D. S. (2009) In vitro derby imaging of cancer biomarkers using quantum dots. Small 5, 1207-1212
52. Losfeld, M. E., Khoury, D. E., Mariot, P., Carpentier, M., Krust, B., Briand, J. P., Mazurier, J., Hovanessian, A. G., and Legrand, D. (2009) The cell surface expressed nucleolin is a glycoprotein that triggers calcium entry into mammalian cells. Exp. Cell Res. 315, 357-369
53. Barel, M., Balbo, M., Le Romancer, M., and Frade, R. (2003) Activation of Epstein-Barr virus/C3d receptor (gp140, CR2, CD21) on human cell surface triggers pp60src and Akt-GSK3 activities upstream and downstream to PI 3-kinase, respectively. Eur. J. Immunol. 33, 2557-2566
54. Sadowski, L., Pilecka, I., and Miaczynska, M. (2009) Signaling from endosomes. Location makes a difference. Exp. Cell Res. 315, 1601-1609
55. Santos, S. C., Miguel, C., Domingues, I., Calado, A., Zhu, Z., Wu, Y., and Dias, S. (2007) VEGF and VEGFR-2 (KDR) internalization is required for endothelial recovery during wound healing. Exp. Cell Res. 313, 1561-1574
56. De Donatis, A., Comito, G., Buricchi, F., Vinci, M. C., Parenti, A., Caselli, A., Camici, G., Manao, G., Ramponi, G., and Cirri, P. (2008) Proliferation versus migration in platelet-derived growth factor signaling. The key role of endocytosis. J. Biol. Chem. 283, 19948-19956
57. Caswell, P., and Norman, J. (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 18, 257-263
58. Legrand, D., Vigié, K., Said, E. A., Elass, E., Masson, M., Slomianny, M. C., Carpentier, M., Briand, J. P., Mazurier, J., and Hovanessian, A. G. (2004) Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells. Eur. J. Biochem. 271, 303-317
59. 3 in gliomas correlates with tumor grade and is not restricted to tumor vasculature. Brain Pathol. 18, 378-386
60. Ding, Y., Song, N., Liu, C., He, T., Zhuo, W., He, X., Chen, Y., Song, X., Fu, Y., and Luo, Y. (2012) Heat shock cognate 70 regulates the translocation and angiogenic function of nucleolin. Arterioscler. Thromb. Vasc. Biol. 32, e126-134
61. Garcia, M. C., Williams, J., Johnson, K., Olden, K., and Roberts, J. D. (2011) Arachidonic acid stimulates formation of a novel complex containing nucleolin and RhoA. FEBS Lett. 585, 618-622
62. Guerrero, C. A., and Moreno, L. P. (2012) Rotavirus receptor proteins Hsc70 and integrin αvβ3 are located in the lipid microdomains of animal intestinal cells. Acta Virol. 56, 63-70