Viral attachment induces rapid recruitment of an innate immune sensor (TRIM5α) to the Plasma Membrane

Journal of Innate Immunity

Volumn 5, Issue 4, 2013, Pages 414-424

  Ohmine, Seiga ^a   Singh, Raman Deep ^b   Marks, David L ^b   Meyer, Melissa A ^a   Pagano, Richard E ^b   Ikeda, Yasuhiro ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

HIV; Innate immunity; Membrane rafts; Plasma membrane; Restriction factor; TRIM5

Indexed keywords

GLYCOSPHINGOLIPID; TRIPARTITE MOTIF PROTEIN 5;

ARTICLE; CELL MEMBRANE; CELL SUBPOPULATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INNATE IMMUNITY; LIPID ANALYSIS; LIPID FLOTATION ASSAY; PRIORITY JOURNAL; RETROVIRUS INFECTION; STEREOISOMERISM; VESICULOVIRUS; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS LIKE AGENT;

EID: 84879412219     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000346963     Document Type: Article

References (60)

1. Perron MJ, Stremlau M, Song B, Ulm W, Mulligan RC, Sodroski J: TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc Natl Acad Sci USA 2004; 101: 11827-11832.
2. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD: Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci USA 2004; 101: 10774-10779.
3. Yap MW, Nisole S, Lynch C, Stoye JP: Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci USA 2004; 101: 10786-10791.
4. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J: The cytoplasmic body component TRIM5alpha restricts HIV-infection in Old World monkeys. Nature 2004; 427: 848-853.
5. Nisole S, Stoye JP, Saib A: TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 2005; 3: 799-808.
6. Ozato K, Shin DM, Chang TH, Morse HC 3rd: TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol 2008; 8: 849-860.
7. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD: Human tripartite motif 5? domains responsible for retrovirus restriction activity and specificity. J Virol 2005; 79: 8969-8978.
8. Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J: Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J Virol 2005; 79: 3930-3937.
9. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J: Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5? restriction factor. Proc Natl Acad Sci USA 2006; 103: 5514-5519.
10. Yap MW, Nisole S, Stoye JP: A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 2005; 15: 73-78.
11. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Bieniasz PD: Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 2002; 99: 11914-11919.
12. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM: Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci USA 2003; 100: 1298-1303.
13. Münk C, Brant SM, Lucero G, Landau NR: A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc Natl Acad Sci USA 2002; 99: 13843-13848.
14. Owens CM, Song B, Perron MJ, Yang PC, Stremlau M, Sodroski J: Binding and susceptibility to postentry restriction factors in monkey cells are specified by distinct regions of the human immunodeficiency virus type 1 capsid. J Virol 2004; 78: 5423-5437.
15. Ganser-Pornillos BK, Chandrasekaran V, Pornillos O, Sodroski JG, Sundquist WI, Yeager M: Hexagonal assembly of a restricting TRIM5alpha protein. Proc Natl Acad Sci USA 2011; 108: 534-539.
16. Keckesova Z, Ylinen LM, Towers GJ: The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci USA 2004; 101: 10780-10785.
17. Chatterji U, Bobardt MD, Gaskill P, Sheeter D, Fox H, Gallay PA: Trim5alpha accelerates degradation of cytosolic capsid associated with productive HIV-1 entry. J Biol Chem 2006; 281: 37025-37033.
18. Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
19. Wilkins C, Gale M Jr: Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 2010; 22: 41-47.
20. Kang DC, Gopalkrishnan RV, Wu Q, Jankowsky E, Pyle AM, Fisher PB: mda-5: an interferoninducible putative RNA helicase with doublestranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci USA 2002; 99: 637-642.
21. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S: Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105.
22. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M: Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 2006; 103: 8459-8464.
23. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grutter MG, Luban J: TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011; 472: 361-365.
24. Simons K, Ikonen E: Functional rafts in cell membranes. Nature 1997; 387: 569-572.
25. Guyader M, Kiyokawa E, Abrami L, Turelli P, Trono D: Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J Virol 2002; 76: 10356-10364.
26. Nguyen DH, Taub D: CXCR4 function requires membrane cholesterol: implications for HIV infection. J Immunol 2002; 168: 4121-4126.
27. Popik W, Alce TM, Au WC: Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. J Virol 2002; 76: 4709-4722.
28. Manes S, del Real G, Lacalle RA, Lucas P, Gomez-Mouton C, Sanchez-Palomino S, Delgado R, Alcami J, Mira E, Martinez AC: Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep 2000; 1: 190-196.
29. Ablan S, Rawat SS, Viard M, Wang JM, Puri A, Blumenthal R: The role of cholesterol and sphingolipids in chemokine receptor function and HIV-1 envelope glycoprotein-mediated fusion. Virol J 2006; 3: 104.
30. Singer II, Scott S, Kawka DW, Chin J, Daugherty BL, DeMartino JA, DiSalvo J, Gould SL, Lineberger JE, Malkowitz L, Miller MD, Mitnaul L, Siciliano SJ, Staruch MJ, Williams HR, Zweerink HJ, Springer MS: CCR5, CXCR4, and CD4 are clustered and closely apposed on microvilli of human macrophages and T cells. J Virol 2001; 75: 3779-3790.
31. Carter GC, Bernstone L, Sangani D, Bee JW, Harder T, James W: HIV entry in macrophages is dependent on intact lipid rafts. Virology 2009; 386: 192-202.
32. del Real G, Jimenez-Baranda S, Lacalle RA, Mira E, Lucas P, Gomez-Mouton C, Carrera AC, Martinez AC, Manes S: Blocking of HIV-infection by targeting CD4 to nonraft membrane domains. J Exp Med 2002; 196: 293-301.
33. Kozak SL, Heard JM, Kabat D: Segregation of CD4 and CXCR4 into distinct lipid microdomains in T lymphocytes suggests a mechanism for membrane destabilization by human immunodeficiency virus. J Virol 2002; 76: 1802-1815.
34. Hwang CY, Holl J, Rajan D, Lee Y, Kim S, Um M, Kwon KS, Song B: Hsp70 interacts with the retroviral restriction factor TRIM5alpha and assists the folding of TRIM5alpha. J Biol Chem 2010; 285: 7827-7837.
35. Ohmine S, Sakuma R, Sakuma T, Thatava T, Solis GP, Ikeda Y: Cytoplasmic body component TRIM5? requires lipid-enriched microdomains for efficient HIV-1 restriction. J Biol Chem 2011; 285: 34508-34517.
36. Kim SY, Wang TK, Singh RD, Wheatley CL, Marks DL, Pagano RE: Proteomic identification of proteins translocated to membrane microdomains upon treatment of fibroblasts with the glycosphingolipid, C8-beta-D-lactosylceramide. Proteomics 2009; 9: 4321-4328.
37. Sakuma R, Noser JA, Ohmine S, Ikeda Y: Rhesus monkey TRIM5alpha restricts HIV-1 production through rapid degradation of viral Gag polyproteins. Nat Med 2007; 13: 631-635.
38. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D: Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997; 15: 871-875.
39. Noser JA, Towers GJ, Sakuma R, Dumont JM, Collins MK, Ikeda Y: Cyclosporine increases human immunodeficiency virus type 1 vector transduction of primary mouse cells. J Virol 2006; 80: 7769-7774.
40. Sakuma R, Mael AA, Ikeda Y: Alpha interferon enhances TRIM5alpha-mediated antiviral activities in human and rhesus monkey cells. J Virol 2007; 81: 10201-10206.
41. Freed EO, Myers DJ, Risser R: Mutational analysis of the cleavage sequence of the human immunodeficiency virus type 1 envelope glycoprotein precursor gp160. J Virol 1989; 63: 4670-4675.
42. Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, Leissner P, Winter AJ, Rabourdin-Combe C, Mehtali M, Moullier P, Darlix JL, Cosset FL: Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 2000; 7: 1613-1623.
43. Wang Z, Tiruppathi C, Minshall RD, Malik AB: Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. ACS Nano 2009; 3: 4110-4116.
44. Macdonald JL, Pike LJ: A simplified method for the preparation of detergent-free lipid rafts. J Lipid Res 2005; 46: 1061-1067.
45. Simm M, Shahabuddin M, Chao W, Allan JS, Volsky DJ: Aberrant Gag protein composition of a human immunodeficiency virus type vif mutant produced in primary lymphocytes. J Virol 1995; 69: 4582-4586.
46. Chesebro B, Wehrly K, Nishio J, Perryman S: Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual v3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J Virol 1992; 66: 6547-6554.
47. Axelrod D: Cell-substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 1981; 89: 141-145.
48. Aiken C: Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J Virol 1997; 71: 5871-5877.
49. Luo T, Douglas JL, Livingston RL, Garcia JV: Infectivity enhancement by HIV-1 Nef is dependent on the pathway of virus entry: implications for HIV-based gene transfer systems. Virology 1998; 241: 224-233.
50. Sharma DK, Brown JC, Cheng Z, Holicky EL, Marks DL, Pagano RE: The glycosphingolipid, lactosylceramide, regulates beta1-integrin clustering and endocytosis. Cancer Res 2005; 65: 8233-8241.
51. Singh RD, Holicky EL, Cheng ZJ, Kim SY, Wheatley CL, Marks DL, Bittman R, Pagano RE: Inhibition of caveolar uptake, SV40 infection, and beta1-integrin signaling by a nonnatural glycosphingolipid stereoisomer. J Cell Biol 2007; 176: 895-901.
52. Campbell EM, Dodding MP, Yap MW, Wu X, Gallois-Montbrun S, Malim MH, Stoye JP, Hope TJ: TRIM5 alpha cytoplasmic bodies are highly dynamic structures. Mol Biol Cell 2007; 18: 2102-2111.
53. Luban J: TRIM5 and the regulation of HIV-1 infectivity. Mol Biol Int 2012; 2012: 426840.
54. Nakayama EE, Shioda T: Role of human TRIM5alpha in intrinsic immunity. Front Microbiol 2012; 3: 97.
55. Rold CJ, Aiken C: Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog 2008; 4:e1000074.
56. Besnier C, Takeuchi Y, Towers G: Restriction of lentivirus in monkeys. Proc Natl Acad Sci USA 2002; 99: 11920-11925.
57. Shi J, Aiken C: Saturation of TRIM5 alphamediated restriction of HIV-1 infection depends on the stability of the incoming viral capsid. Virology 2006; 350: 493-500.
58. Campbell EM, Perez O, Anderson JL, Hope TJ: Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5alpha. J Cell Biol 2008; 180: 549-561.
59. Diaz-Griffero F, Qin XR, Hayashi F, Kigawa T, Finzi A, Sarnak Z, Lienlaf M, Yokoyama S, Sodroski J: A B-box 2 surface patch important for TRIM5alpha self-Association, capsid binding avidity, and retrovirus restriction. J Virol 2009; 83: 10737-10751.
60. Battivelli E, Migraine J, Lecossier D, Yeni P, Clavel F, Hance AJ: Gag cytotoxic T lymphocyte escape mutations can increase sensitivity of HIV-1 to human TRIM5alpha, linking intrinsic and acquired immunity. J Virol 2012; 85: 11846-11854.