HTLV-1 uses HSPG and neuropilin-1 for entry by molecular mimicry of VEGF165

Blood

Volumn 113, Issue 21, 2009, Pages 5176-5185

  Lambert, Sophie ^a   Bouttier, Manuella ^a   Vassy, Roger ^b   Seigneuret, Michel ^a   Petrow Sadowski, Cari ^c   Janvier, Sébastien ^d   Heveker, Nikolaus ^d   Ruscetti, Francis W ^e   Perret, Gérard ^b   Jones, Kathryn S ^c   Pique, Claudine ^a  

^a CNRS   (France)

^b UNIVERSITÉ PARIS 13   (France)

^c SAIC FREDERICK INC   (United States)

^d UNIVERSITY OF MONTREAL   (Canada)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN 1; PROTEIN SUBUNIT; PROTEOHEPARAN SULFATE; VASCULOTROPIN 165; VIRUS ENVELOPE PROTEIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN; VIRUS RECEPTOR;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; MOLECULAR MIMICRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; VIRUS ATTACHMENT; VIRUS ENTRY; BINDING COMPETITION; CELL CULTURE; HUMAN T CELL LEUKEMIA VIRUS INFECTION; METABOLISM; PATHOGENICITY; VIROLOGY;

BINDING, COMPETITIVE; CELLS, CULTURED; GENE PRODUCTS, ENV; HEPARAN SULFATE PROTEOGLYCANS; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MOLECULAR MIMICRY; NEUROPILIN-1; PROTEIN BINDING; RECEPTORS, VIRUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VIRUS ATTACHMENT;

EID: 65949101737     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-04-150342     Document Type: Article

References (46)

1. Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL. Global epidemiology of HTLV-I infection and associated diseases. Oncogene. 2005;24:6058-6068. (Pubitemid 43086123)
2. Macatonia SE, Cruickshank JK, Rudge P, Knight SC. Dendritic cells from patients with tropical spastic paraparesis are infected with HTLV-1 and stimulate autologous lymphocyte proliferation. AIDS Res Hum Retroviruses. 1992;8:1699-1706.
3. Koyanagi Y, Itoyama Y, Nakamura N, et al. In vivo infection of human T-cell leukemia virus type I in non-T cells. Virology. 1993;196:25-33.
4. Hanon E, Stinchcombe JC, Saito M, et al. Fratricide among CD8(+) T lymphocytes naturally infected with human T cell lymphotropic virus type I. Immunity. 2000;13:657-664.
5. Igakura T, Stinchcombe JC, Goon PK, et al. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science. 2003;299:1713-1716. (Pubitemid 36337193)
6. Jones KS, Petrow-Sadowski C, Huang YK, Bertolette DC, Ruscetti FW. Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(+) T cells. Nat Med. 2008;14:429-436.
7. Jin Q, Agrawal L, Vanhorn-Ali Z, Alkhatib G. Infection of CD4(+) T lymphocytes by the human T cell leukemia virus type 1 is mediated by the glucose transporter GLUT-1: evidence using antibodies specific to the receptor's large extracellular domain. Virology. 2006;349:184-196.
8. Manel N, Kim FJ, Kinet S, Taylor N, Sitbon M, Battini JL. The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell. 2003;115:449-459. (Pubitemid 37456807)
9. Jin Q, Agrawal L, Vanhorn-Ali Z, Alkhatib G. GLUT-1-independent infection of the glioblastoma/astroglioma U87 cells by the human T cell leukemia virus type 1. Virology. 2006;353:99-110. (Pubitemid 44291777)
10. Takenouchi N, Jones KS, Lisinski I, et al. GLUT1 is not the primary binding receptor but is associated with cell-to-cell transmission of human T-cell leukemia virus type 1. J Virol. 2007;81:1506-1510. (Pubitemid 46167872)
11. Jones KS, Fugo K, Petrow-Sadowski C, et al. Human T-cell leukemia virus type 1 (HTLV-1) and HTLV-2 use different receptor complexes to enter T cells. J Virol. 2006;80:8291-8302. (Pubitemid 44384843)
12. Ghez D, Lepelletier Y, Lambert S, et al. Neuropilin- 1 is involved in human T-cell lymphotropic virus type 1 entry. J Virol. 2006;80:6844-6854. (Pubitemid 44025184)
13. Jones KS, Petrow-Sadowski C, Bertolette DC, Huang Y, Ruscetti FW. Heparan sulfate proteoglycans mediate attachment and entry of human T-cell leukemia virus type 1 virions into CD4+ T cells. J Virol. 2005;79:12692-12702. (Pubitemid 41433189)
14. Pinon JD, Klasse PJ, Jassal SR, et al. Human T-cell leukemia virus type 1 envelope glycoprotein gp46 interacts with cell surface heparan sulfate proteoglycans. J Virol. 2003;77:9922-9930.
15. Tordjman R, Lepelletier Y, Lemarchandel V, et al. A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat Immunol. 2002;3:477-482. (Pubitemid 34520798)
16. Grage-Griebenow E, Loseke S, Kauth M, Gehlhar K, Zawatzky R, Bufe A. Anti-BDCA-4 (neuropilin- 1) antibody can suppress virus-induced IFN-alpha production of plasmacytoid dendritic cells. Immunol Cell Biol. 2007;85:383-390. (Pubitemid 47035609)
17. Nakamura F, Goshima Y. Structural and functional relation of neuropilins. Adv Exp Med Biol. 2002;515:55-69.
18. Vander Kooi CW, Jusino MA, Perman B, Neau DB, Bellamy HD, Leahy DJ. Structural basis for ligand and heparin binding to neuropilin B domains. Proc Natl Acad Sci U S A. 2007;104:6152-6157. (Pubitemid 47186064)
19. Soker S, Fidder H, Neufeld G, Klagsbrun M. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J Biol Chem. 1996;271:5761-5767. (Pubitemid 26083914)
20. Gitay-Goren H, Soker S, Vlodavsky I, Neufeld G. The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J Biol Chem. 1992;267:6093-6098.
21. Krilleke D, DeErkenez A, Schubert W, et al. Molecular mapping and functional characterization of the VEGF164 heparin-binding domain. J Biol Chem. 2007;282:28045-28056. (Pubitemid 47533565)
22. Mamluk R, Gechtman Z, Kutcher ME, Gasiunas N, Gallagher J, Klagsbrun M. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J Biol Chem. 2002;277:24818-24825. (Pubitemid 34952014)
23. Cebe-Suarez S, Grunewald FS, Jaussi R, et al. Orf virus VEGF-E NZ2 promotes paracellular NRP-1/VEGFR-2 coreceptor assembly via the peptide RPPR. FASEB J. 2008;22:3078-3086.
24. Starzec A, Ladam P, Vassy R, et al. Structure-function analysis of the antiangiogenic ATWLPPR peptide inhibiting VEGF(165) binding to neuropilin-1 and molecular dynamics simulations of the ATWLPPR/neuropilin-1 complex. Peptides. 2007;28:2397-2402.
25. Soker S, Gollamudi-Payne S, Fidder H, Charmahelli H, Klagsbrun M. Inhibition of vascular endothelial growth factor (VEGF)-induced endothelial cell proliferation by a peptide corresponding to the exon 7-encoded domain of VEGF165. J Biol Chem. 1997;272:31582-31588. (Pubitemid 28013301)
26. Jia H, Bagherzadeh A, Hartzoulakis B, et al. Characterization of a bicyclic peptide neuropilin-1 (NP-1) antagonist (EG3287) reveals importance of vascular endothelial growth factor exon 8 for NP-1 binding and role of NP-1 in KDR signaling. J Biol Chem. 2006;281:13493-13502. (Pubitemid 43855262)
27. Starzec A, Vassy R, Martin A, et al. Antiangiogenic and antitumor activities of peptide inhibiting the vascular endothelial growth factor binding to neuropilin-1. Life Sci. 2006;79:2370-2381. (Pubitemid 44772930)
28. von Wronski MA, Raju N, Pillai R, et al. Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J Biol Chem. 2006;281:5702-5710. (Pubitemid 43847668)
29. Barr MP, Byrne AM, Duffy AM, et al. A peptide corresponding to the neuropilin-1-binding site on VEGF(165) induces apoptosis of neuropilin-1- expressing breast tumour cells. Br J Cancer. 2005;92:328-333.
30. Nasr R, Chiari E, El-Sabban M, et al. Tax ubiquitylation and sumoylation control critical cytoplasmic and nuclear steps of NF-kappaB activation. Blood. 2006;107:4021-4029. (Pubitemid 43726810)
31. Delamarre L, Rosenberg AR, Pique C, Pham D, Dokhelar MC. A novel human T-leukemia virus type 1 cell-to-cell transmission assay permits definition of SU glycoprotein amino acids important for infectivity. J Virol. 1997;71:259-266. (Pubitemid 26412287)
32. Jones KS, Nath M, Petrow-Sadowski C, et al. Similar regulation of cell surface human T-cell leukemia virus type 1 (HTLV-1) surface binding proteins in cells highly and poorly transduced by HTLV-1-pseudotyped virions. J Virol. 2002;76:12723-12734. (Pubitemid 35386957)
33. Pique C, Connan F, Levilain JP, Choppin J, Dokhelar MC. Among all human T-cell leukemia virus type 1 proteins, tax, polymerase, and envelope proteins are predicted as preferential targets for the HLA-A2-restricted cytotoxic T-cell response. J Virol. 1996;70:4919-4926. (Pubitemid 26240658)
34. Grange MP, Rosenberg AR, Horal P, Desgranges C. Identification of exposed epitopes on the envelope glycoproteins of human T-cell lymphotropic virus type I (HTLV-I). Int J Cancer. 1998;75:804-813. (Pubitemid 28145831)
35. Riboldi E, Musso T, Moroni E, et al. Cutting edge: proangiogenic properties of alternatively activated dendritic cells. J Immunol. 2005;175:2788-2792. (Pubitemid 41170494)
36. Oh H, Takagi H, Otani A, et al. Selective induction of neuropilin-1 by vascular endothelial growth factor (VEGF): a mechanism contributing to VEGF-induced angiogenesis. Proc Natl Acad Sci U S A. 2002;99:383-388. (Pubitemid 34060370)
37. Gu C, Limberg BJ, Whitaker GB, et al. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J Biol Chem. 2002;277:18069-18076. (Pubitemid 34967620)
38. Giger RJ, Urquhart ER, Gillespie SK, Levengood DV, Ginty DD, Kolodkin AL. Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity. Neuron. 1998;21:1079-1092. (Pubitemid 29018077)
39. Pique C, Pham D, Tursz T, Dokhelar MC. Human T-cell leukemia virus type I envelope protein maturation process: requirements for syncytium formation. J Virol. 1992;66:906-913.
40. de Graffenried CL, Bertozzi CR. The roles of enzyme localisation and complex formation in glycan assembly within the Golgi apparatus. Curr Opin Cell Biol. 2004;16:356-363.
41. Sommerfelt MA, Weiss RA. Receptor interference groups of 20 retroviruses plating on human cells. Virology. 1990;176:58-69.
42. Cebe Suarez S, Pieren M, Cariolato L, et al. A VEGF-A splice variant defective for heparan sulfate and neuropilin-1 binding shows attenuated signaling through VEGFR-2. Cell Mol Life Sci. 2006;63:2067-2077. (Pubitemid 44359746)
43. Palker TJ, Riggs ER, Spragion DE, et al. Mapping of homologous, amino-terminal neutralizing regions of human T-cell lymphotropic virus type I and II gp46 envelope glycoproteins. J Virol. 1992;66:5879-5889.
44. Inoue Y, Kuroda N, Shiraki H, Sato H, Maeda Y. Neutralizing activity of human antibodies against the structural protein of human T-cell lymphotropic virus type I. Int J Cancer. 1992;52:877-880. (Pubitemid 23009502)
45. Soker S, Miao HQ, Nomi M, Takashima S, Klagsbrun M. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J Cell Biochem. 2002;85:357-368. (Pubitemid 34274903)
46. Freeman MR, Schneck FX, Gagnon ML, et al. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res. 1995;55:4140-4145.