Integrin αvβ3 binds to the RGD motif of glycoprotein B of Kaposi's sarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor

Journal of Virology

Volumn 82, Issue 3, 2008, Pages 1570-1580

  Garrigues, H Jacques ^a   Rubinchikova, Yelena E ^a   DiPersio, C Michael ^b   Rose, Timothy M ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; CELL RECEPTOR; COMPLEMENTARY DNA; GLYCOPROTEIN B; VIRUS ANTIBODY; VITRONECTIN RECEPTOR; GLYCOPROTEIN B, HUMAN HERPESVIRUS 8; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HOST CELL; HUMAN HERPESVIRUS 8; INHIBITION KINETICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; TARGET CELL; VIRION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; ANIMAL; CELL LINE; CERCOPITHECUS; CRICETULUS; HAMSTER; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; VIRUS ATTACHMENT;

HUMAN HERPESVIRUS 8; MUS;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; CRICETULUS; HERPESVIRUS 8, HUMAN; HUMANS; INTEGRIN ALPHAVBETA3; MICE; RECEPTORS, VIRUS; VIRAL ENVELOPE PROTEINS; VIRUS ATTACHMENT;

EID: 38349134847     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01673-07     Document Type: Article

References (70)

1. Adang, L. A., C. H. Parsons, and D. H. Kedes. 2006. Asynchronous progression through the lytic cascade and variations in intracellular viral loads revealed by high-throughput single-cell analysis of Kaposi's sarcoma-associated herpesvirus infection. J. Virol. 80:10073-10082.
2. Akula, S. M., N. P. Pramod, F. Z. Wang, and B. Chandran. 2002. Integrin alpha3beta1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108:407-419.
3. Akula, S. M., F. Z. Wang, J. Vieira, and B. Chandran. 2001. Human herpesvirus 8 interaction with target cells involves heparan sulfate. Virology 282:245-255.
4. Antman, K., and Y. Chang. 2000. Kaposi's sarcoma. N. Engl. J. Med. 342:1027-1038.
5. Bechtel, J. T., Y. Liang, J. Hvidding, and D. Ganem. 2003. Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 77:6474-6481.
6. Belkin, A. M., and M. A. Stepp. 2000. Integrins as receptors for laminins. Microsc. Res. Tech. 51:280-301.
7. Borza, C. M., A. Pozzi, D. B. Borza, V. Pedchenko, T. Hellmark, B. G. Hudson, and R. Zent. 2006. Integrin alpha3beta1, a novel receptor for alpha3(IV) noncollagenous domain and a trans-dominant inhibitor for integrin alphavbeta3. J. Biol. Chem. 281:20932-20939.
8. Brooks, P. C., R. A. Clark, and D. A. Cheresh. 1994. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264:569-571.
9. Burnside, K. L., J. T. Ryan, H. Bielefeldt-Ohmann, A. Gregory Bruce, M. E. Thouless, C. C. Tsai, and T. M. Rose. 2006. RFHVMn ORF73 is structurally related to the KSHV ORF73 latency-associated nuclear antigen (LANA) and is expressed in retroperitoneal fibromatosis (RF) tumor cells. Virology 354:103-115.
10. Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. Turner. 1988. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487-525.
11. Carter, W. G., M. C. Ryan, and P. J. Gahr. 1991. Epiligrin, a new cell adhesion ligand for integrin alpha 3 beta 1 in epithelial basement membranes. Cell 65:599-610.
12. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
13. Critchley, D. R., M. R. Holt, S. T. Barry, H. Priddle, L. Hemmings, and J. Norman. 1999. Integrin-mediated cell adhesion: the cytoskeletal connection. Biochem. Soc. Symp. 65:79-99.
14. Delwel, G. O., A. A. de Melker, F. Hogervorst, L. H. Jaspars, D. L. Fles, I. Kuikman, A. Lindblom, M. Paulsson, R. Timpl, and A. Sonnenberg. 1994. Distinct and overlapping ligand specificities of the alpha 3A beta 1 and alpha 6A beta 1 integrins: recognition of laminin isoforras. Mol. Biol. Cell 5:203-215.
15. Desrosiers, R. C., V. G. Sasseville, S. C. Czajak, X. Zhang, K. G. Mansfield, A. Kaur, R. P. Johnson, A. A. Lackner, and J. U. Jung. 1997. A herpesvirus of rhesus monkeys related to the human Kaposi's sarcoma-associated herpesvirus. J. Virol. 71:9764-9769.
16. DiPersio, C. M., M. Shao, L. Di Costanzo, J. A. Kreidberg, and R. O. Hynes. 2000. Mouse keratinocytes immortalized with large T antigen acquire alpha3beta1 integrin-dependent secretion of MMP-9/gelatinase B. J. Cell Sci. 113:2909-2921.
17. Eble, J. A., K. W. Wucherpfennig, L. Gauthier, P. Dersch, E. Krukonis, R. R. Isbeng, and M. E. Hemler. 1998. Recombinant soluble human alpha 3 beta 1 integrin: purification, processing, regulation, and specific binding to laminin-5 and invasin in a mutually exclusive manner. Biochemistry 37:10945-10955.
18. Ensoli, B., C. Sgadari, G. Barillari, M. C. Sirianni, M. Sturzl, and P. Monini. 2001. Biology of Kaposi's sarcoma. Eur. J. Cancer. 37:1251-1269.
19. Ford, T., J. Graham, and D. Rickwood. 1994. Iodixanol: a nonionic iso-osmotic centrifugation medium for the formation of self-generated gradients. Anal. Biochem. 220:360-366.
20. Gresham, H. D., I. L. Graham, G. L. Griffin, J. C. Hsieh, L. J. Dong, A. E. Chung, and R. M. Senior. 1996. Domain-specific interactions between entactin and neutrophil integrins. G2 domain ligation of integrin alpha3beta1 and E domain ligation of the leukocyte response integrin signal for different responses. J. Biol. Chem. 271:30587-30594.
21. Haubner, R., H. J. Wester, U. Reuning, R. Senekowitsch-Schmidtke, B. Diefenbach, H. Kessler, G. Stocklin, and M. Schwaiger. 1999. Radiolabeled alpha(v) beta3 integrin antagonists: a new class of tracers for tumor targeting. J. Nucl. Med. 40:1061-1071.
22. Hodivala-Dilke, K. M., C. M. DiPersio, J. A. Kreidberg, and R. O. Hynes. 1998. Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J. Cell Biol. 142:1357-1369.
23. Horton, M. A. 1997. The alpha v beta 3 integrin "vitronectin receptor." Int. J. Biochem. Cell Biol. 29:721-725.
24. Hynes, R. O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673-687.
25. Janssen, M. L., W. J. Oyen, I. Dijkgraaf, L. F. Massuger, C. Frielink, D. S. Edwards, M. Rajopadhye, H. Boonstra, F. H. Corstens, and O. C. Boerman. 2002. Tumor targeting with radiolabeled alpha(v) beta(3) integrin binding peptides in a nude mouse model. Cancer Res. 62:6146-6151.
26. Kaaya, E. E., E. Castanos-Velez, H. Amir, L. Lema, J. Luande, J. Kitinya, M. Patarroyo, and P. Biberfeld. 1996. Expression of adhesion molecules in endemic and epidemic Kaposi's sarcoma. Histopathology 29:337-346.
27. Kaleeba, J. A., and E. A. Berger. 2006. Kaposi's sarcoma-associated herpesvirus fusion-entry receptor: cystine transporter xCT. Science 311:1921-1924.
28. Kantlehner, M., P. Schaffner, D. Finsinger, J. Meyer, A. Jonczyk, B. Diefenbach, B. Nies, G. Holzemann, S. L. Goodman, and H. Kessler. 2000. Surface coating with cyclic RGD peptides stimulates osteoblast adhesion and proliferation as well as bone formation. Chembiochem 1:107-114.
29. Kikkawa, Y., N. Sanzen, and K. Sekiguchi. 1998. Isolation and characterization of laminin-10/11 secreted by human lung carcinoma cells. Laminin-10/11 mediates cell adhesion through integrin alpha3 beta1. J. Biol. Chem. 273:15854-15859.
30. Kikkawa, Y., M. Umeda, and K. Miyazaki. 1994. Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J. Biochem. (Tokyo) 116:862-869.
31. Kim, J. M., W. H. Park, and B. M. Min. 2005. The PPFLMLLKGSTR motif in globular domain 3 of the human laminin-5 alpha3 chain is crucial for integrin alpha3beta1 binding and cell adhesion. Exp. Cell Res. 304:317-327.
32. Kim, J. P., K. Zhang, R. H. Kramer, T. J. Schall, and D. T. Woodley. 1992. Integrin receptors and RGD sequences in human keratinocyte migration: unique anti-migratory function of alpha 3 beta 1 epiligrin receptor. J. Investig. Dermatol. 98:764-770.
33. Koivunen, E., B. Wang, and E. Ruoslahti. 1995. Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Biotechnology (N. Y.) 13:265-270.
34. Kok, R. J., A. J. Schraa, E. J. Bos, H. E. Moorlag, S. A. Asgeirsdottir, M. Everts, D. K. Meijer, and G. Molema. 2002. Preparation and functional evaluation of RGD-modified proteins as alpha(v)beta(3) integrin directed therapeutics. Bioconjug. Chem. 13:128-135.
35. Kolesnikova, T. V., B. A. Mannion, F. Berditchevski, and M. E. Hemler. 2001. Beta1 integrins show specific association with CD98 protein in low density membranes. BMC Biochem. 2:10.
36. Krishnan, H. H., N. Sharma-Walla, D. N. Streblow, P. P. Naranatt, and B. Chandran. 2006. Focal adhesion kinase is critical for entry of Kaposi's sarcoma-associated herpesvirus into target cells. J. Virol. 80:1167-1180.
37. Krutzsch, H. C., B. J. Choe, J. M. Sipes, N. Guo, and D. D. Roberts. 1999. Identification of an alpha(3)beta(1) integrin recognition sequence in thrombospondin-1. J. Biol. Chem. 274:24080-24086.
38. Ly, D. P., K. M. Zazzali, and S. A. Corbett. 2003. De novo expression of the integrin alpha5beta1 regulates alphavbeta3-mediated adhesion and migration on fibrinogen. J. Biol. Chem. 278:21878-21885.
39. Naranatt, P. P., S. M. Akula, C. A. Zien, H. H. Krishnan, and B. Chandran. 2003. Kaposi's sarcoma-associated herpesvirus induces the phosphatidylinositol 3-kinase-PKC-ζ-MEK-ERK signaling pathway in target cells early during infection: implications for infectivity. J. Virol. 77:1524-1539.
40. Naranatt, P. P., H. H. Krishnan, M. S. Smith, and B. Chandran. 2005. Kaposi's sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J. Virol. 79:1191-1206.
41. Nishiuchi, R., O. Murayama, H. Fujiwara, J. Gu, T. Kawakami, S. Aimoto, Y. Wada, and K. Sekiguchi. 2003. Characterization of the ligand-binding specificities of integrin alpha3beta1 and alpha6beta1 using a panel of purified laminin isoforms containing distinct alpha chains. 1. Biochem. (Tokyo) 134:497-504.
42. Pereira, L. 1994. Function of glycoprotein B homologues of the family herpesviridae. Infect. Agents Dis. 3:9-28.
43. Pfaff, M., K. Tangemann, B. Muller, M. Gurrath, G. Muller, H. Kessler, R. Timpl, and J. Engel. 1994. Selective recognition of cyclic RGD peptides of NMR defined conformation by alpha IIb beta 3, alpha V beta 3, and alpha 5 beta 1 integrins. J. Biol. Chem. 269:20233-20238.
44. Pierschbacher, M. D., and E. Ruoslahti. 1987. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J. Biol. Chem. 262:17294-17298.
45. Plow, E. F., T. A. Haas, L. Zhang, J. Loftus, and J. W. Smith. 2000. Ligand binding to integrins. J. Biol. Chem. 275:21785-21788.
46. Rappocciolo, G., F. J. Jenkins, H. R. Hensler, P. Piazza, M. Jais, L. Borowski, S. C. Watkins, and C. R. Rinaldo, Jr. 2006. DC-SIGN is a receptor for human herpesvirus 8 on dendritic cells and macrophages. J. Immunol. 176:1741-1749.
47. Renne, R., D. Blackbourn, D. Whitby, J. Levy, and D. Ganem. 1998. Limited transmission of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 72:5182-5188.
48. Renne, R., W. Zhong, B. Herndier, M. McGrath, N. Abbey, D. Kedes, and D. Ganem. 1996. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat. Med. 2:342-346.
49. Rose, T. M., K. B. Strand, and M. L. Bosch. January 1999. Glycoprotein B of the RFHV/KSHV subfamily of herpesviruses. U.S. patent 6,015,565.
50. Russo, J. J., R. A. Bohenzky, M. C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14867.
51. Salcedo, R., and M. Patarroyo. 1995. Constitutive alpha V beta 3 integrin-mediated adhesion of human lymphoid B cells to vitronectin substrate. Cell. Immunol. 160:165-172.
52. Schulz, T. F. 1998. Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8). J. Gen. Virol. 79:1573-1591.
53. Searles, R. P., E. P. Bergquam, M. K. Axthelm, and S. W. Wong. 1999. Sequence and genomic analysis of a Rhesus macaque rhadinovirus with similarity to Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J. Virol. 73:3040-3053.
54. Sharma-Walia, N., H. H. Krishnan, P. P. Naranatt, L. Zeng, M. S. Smith, and B. Chandran. 2005. ERK1/2 and MEK1/2 induced by Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) early during infection of target cells are essential for expression of viral genes and for establishment of infection. J. Virol. 79:10308-10329.
55. Sharma-Walia, N., P. P. Naranatt, H. H. Krishnan, L. Zeng, and B. Chandran. 2004. Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Src-phosphatidylinositol 3-kinase-Rho GTPase signal pathways and cytoskeletal rearrangements. J. Virol. 78:4207-4223.
56. Smith, J. W., and D. A. Cheresh. 1988. The Arg-Gly-Asp binding domain of the vitronectin receptor. Photoaffinity cross-linking implicates amino acid residues 61-203 of the beta subunit. J. Biol. Chem. 263:18726- 18731.
57. Smith, J. W., and D. A. Cheresh. 1990. Integrin (alpha v beta 3)-ligand interaction. Identification of a heterodimeric RGD binding site on the vitronectin receptor. J. Biol. Chem. 265:2168-2172.
58. Smith, J. W., R. S. Piotrowicz, and D. Mathis. 1994. A mechanism for divalent cation regulation of beta 3-integrins. J. Biol. Chem. 269:960-967.
59. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
60. Symington, B. E., Y. Takada, and W. G. Carter. 1993. Interaction of integrins alpha 3 beta 1 and alpha 2 beta 1: potential role in keratinocyte intercellular adhesion. J. Cell Biol. 120:523-535.
61. Takagi, J., T. Kamata, J. Meredith, W. Puzon-McLaughlin, and Y. Takada. 1997. Changing ligand specificities of alphavbeta1 and alphavbeta3 integrins by swapping a short diverse sequence of the beta subunit. J. Biol. Chem. 272:19794-19800.
62. Uccini, S., L. P. Ruco, F. Monarde, A. Stoppacciaro, E. Dejana, I. L. La Parola, D. Cerimele, and C. D. Baroni. 1994. Co-expression of endothelial cell and macrophage antigens in Kaposi's sarcoma cells. J. Pathol. 173:23-31.
63. Wang, F. Z., S. M. Akula, N. P. Pramod, L. Zeng, and B. Chandran. 2001. Human herpesvirus 8 envelope glycoprotein K8.1A interaction with the target cells involves heparan sulfate. J. Virol. 75:7517-7527.
64. Wang, F. Z., S. M. Akula, N. Sharma-Walia, L. Zeng, and B. Chandran. 2003. Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J. Virol. 77:3131-3147.
65. Wayner, E. A., and W. G. Carter. 1987. Identification of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J. Cell Biol. 105:1873-1884.
66. Weitzman, J. B., R. Pasqualini, Y. Takada, and M. E. Hemler. 1993. The function and distinctive regulation of the integrin VLA-3 in cell adhesion, spreading, and homotypic cell aggregation. J. Biol. Chem. 268:8651-8657.
67. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
68. Wozniak, M. A., K. Modzelewska, L. Kwong, and P. J. Keely. 2004. Focal adhesion regulation of cell behavior. Biochim. Biophys. Acta 1692:103-119.
69. Wu, C., A. E. Chung, and J. A. McDonald. 1995. A novel role for alpha 3 beta 1 integrins in extracellular matrix assembly. J. Cell Sci. 108:2511-2523.
70. Xue, W., I. Mizukami, R. F. Todd III, and H. R. Petty. 1997. Urokinase-type plasminogen activator receptors associate with beta1 and beta3 integrins of fibrosarcoma cells: dependence on extracellular matrix components. Cancer Res. 57:1682-1689.