TCR triggering transcriptionally downregulates CCR5 expression on rhesus macaque CD4+ T-cells with no measurable effect on susceptibility to SIV infection

Virology

Volumn 409, Issue 1, 2011, Pages 132-140

  Minang, Jacob T ^a   Trivett, Matthew T ^a   Barsov, Eugene V ^a   Del Prete, Gregory Q ^a   Trubey, Charles M ^a   Thomas, James A ^a   Gorelick, Robert J ^a   Piatak, Michael ^a   Ott, David E ^a   Ohlen, Claes ^a  

^a SAIC FREDERICK INC   (United States)

Author keywords

AIDS; CCR5; CD4; Rhesus macaques; SIV

Indexed keywords

CHEMOKINE RECEPTOR CCR5; MARAVIROC; MONOCLONAL ANTIBODY CD3; SHORT HAIRPIN RNA; T LYMPHOCYTE RECEPTOR; VIRUS DNA;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION REGULATION; IMMUNOSTIMULATION; INFECTION SENSITIVITY; LENTIVIRUS INFECTION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RHESUS MONKEY; RNA INTERFERENCE; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS INFECTION; TRANSCRIPTION REGULATION; VIRUS CELL INTERACTION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; DNA, VIRAL; DOWN-REGULATION; FEMALE; GENE PRODUCTS, GAG; HUMANS; MACACA MULATTA; MALE; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CCR5; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 78649449904     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.10.005     Document Type: Article

References (56)

1. Albright A.V., Shieh J.T., Itoh T., Lee B., Pleasure D., O'Connor M.J., Doms R.W., Gonzalez-Scarano F. Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. J. Virol. 1999, 73(1):205-213.
2. Blanpain C., Lee B., Tackoen M., Puffer B., Boom A., Libert F., Sharron M., Wittamer V., Vassart G., Doms R.W., Parmentier M. Multiple nonfunctional alleles of CCR5 are frequent in various human populations. Blood 2000, 96(5):1638-1645.
3. Campillo-Gimenez L., Laforge M., Fay M., Brussel A., Cumont M.C., Monceaux V., Diop O., Levy Y., Hurtrel B., Zaunders J., Corbeil J., Elbim C., Estaquier J. Non pathogenesis of SIV infection is associated with reduced inflammation and recruitment of plasmacytoid dendritic cells to lymph nodes, not to lack of an interferon type I response, during the acute phase. J. Virol. 2010, 84(4):1838-1846.
4. Carroll R.G., Riley J.L., Levine B.L., Feng Y., Kaushal S., Ritchey D.W., Bernstein W., Weislow O.S., Brown C.R., Berger E.A., June C.H., St Louis D.C. Differential regulation of HIV-1 fusion cofactor expression by CD28 costimulation of CD4+ T cells. Science 1997, 276(5310):273-276.
5. Chen Z., Kwon D., Jin Z., Monard S., Telfer P., Jones M.S., Lu C.Y., Aguilar R.F., Ho D.D., Marx P.A. Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J. Exp. Med. 1998, 188(11):2057-2065.
6. Cline A.N., Bess J.W., Piatak M., Lifson J.D. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J. Med. Primatol. 2005, 34(5-6):303-312.
7. Connor R.I., Paxton W.A., Sheridan K.E., Koup R.A. Macrophages and CD4+ T lymphocytes from two multiply exposed, uninfected individuals resist infection with primary non-syncytium-inducing isolates of human immunodeficiency virus type 1. J. Virol. 1996, 70(12):8758-8764.
8. DeGottardi M.Q., Lew S.K., Piatak M., Jia B., Feng Y., Lee S.J., Brenchley J.M., Douek D.C., Kodama T., Lifson J.D., Evans D.T. Comparison of plasma viremia and antibody responses in macaques inoculated with envelope variants of single-cycle simian immunodeficiency virus differing in infectivity and cellular tropism. J. Virol. 2008, 82(1):321-334.
9. Del Prete G.Q., Haggarty B., Leslie G.J., Jordan A.P., Romano J., Wang N., Wang J., Holmes M.C., Montefiori D.C., Hoxie J.A. Derivation and characterization of a simian immunodeficiency virus SIVmac239 variant with tropism for CXCR4. J. Virol. 2009, 83(19):9911-9922.
10. Dickins R.A., Hemann M.T., Zilfou J.T., Simpson D.R., Ibarra I., Hannon G.J., Lowe S.W. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 2005, 37(11):1289-1295.
11. Douek D.C., Brenchley J.M., Betts M.R., Ambrozak D.R., Hill B.J., Okamoto Y., Casazza J.P., Kuruppu J., Kunstman K., Wolinsky S., Grossman Z., Dybul M., Oxenius A., Price D.A., Connors M., Koup R.A. HIV preferentially infects HIV-specific CD4+ T cells. Nature 2002, 417(6884):95-98.
12. Edinger A.L., Hoffman T.L., Sharron M., Lee B., O'Dowd B., Doms R.W. Use of GPR1, GPR15, and STRL33 as coreceptors by diverse human immunodeficiency virus type 1 and simian immunodeficiency virus envelope proteins. Virology 1998, 249(2):367-378.
13. Forte S., Harmon M.E., Pineda M.J., Overbaugh J. Early- and intermediate-stage variants of simian immunodeficiency virus replicate efficiently in cells lacking CCR5. J. Virol. 2003, 77(17):9723-9727.
14. Glushakova S., Yi Y., Grivel J.C., Singh A., Schols D., De Clercq E., Collman R.G., Margolis L. Preferential coreceptor utilization and cytopathicity by dual-tropic HIV-1 in human lymphoid tissue ex vivo. J. Clin. Invest. 1999, 104(5):R7-R11.
15. Granelli-Piperno A., Moser B., Pope M., Chen D., Wei Y., Isdell F., O'Doherty U., Paxton W., Koup R., Mojsov S., Bhardwaj N., Clark-Lewis I., Baggiolini M., Steinman R.M. Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors. J. Exp. Med. 1996, 184(6):2433-2438.
16. Hanenberg H., Xiao X.L., Dilloo D., Hashino K., Kato I., Williams D.A. Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat. Med. 1996, 2(8):876-882.
17. Hoffman T.L., MacGregor R.R., Burger H., Mick R., Doms R.W., Collman R.G. CCR5 genotypes in sexually active couples discordant for human immunodeficiency virus type 1 infection status. J. Infect. Dis. 1997, 176(4):1093-1096.
18. Huang Y., Paxton W.A., Wolinsky S.M., Neumann A.U., Zhang L., He T., Kang S., Ceradini D., Jin Z., Yazdanbakhsh K., Kunstman K., Erickson D., Dragon E., Landau N.R., Phair J., Ho D.D., Koup R.A. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat. Med. 1996, 2(11):1240-1243.
19. Kestler H., Kodama T., Ringler D., Marthas M., Pedersen N., Lackner A., Regier D., Sehgal P., Daniel M., King N., et al. Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 1990, 248(4959):1109-1112.
20. Kutner R.H., Zhang X.Y., Reiser J. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat. Protoc. 2009, 4(4):495-505.
21. Lauren A., Vodros D., Thorstensson R., Fenyo E.M. Comparative studies on mucosal and intravenous transmission of simian immunodeficiency virus (SIVsm): evolution of coreceptor use varies with pathogenic outcome. J. Gen. Virol. 2006, 87(Pt 3):581-594.
22. Lay M.D., Petravic J., Gordon S.N., Engram J., Silvestri G., Davenport M.P. Is the gut the major source of virus in early simian immunodeficiency virus infection?. J. Virol. 2009, 83(15):7517-7523.
23. Levine B.L., Mosca J.D., Riley J.L., Carroll R.G., Vahey M.T., Jagodzinski L.L., Wagner K.F., Mayers D.L., Burke D.S., Weislow O.S., St Louis D.C., June C.H. Antiviral effect and ex vivo CD4+ T cell proliferation in HIV-positive patients as a result of CD28 costimulation. Science 1996, 272(5270):1939-1943.
24. Lin Y.L., Mettling C., Portales P., Reynes J., Clot J., Corbeau P. Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc. Natl Acad. Sci. U.S.A. 2002, 99(24):15590-15595.
25. Liu R., Paxton W.A., Choe S., Ceradini D., Martin S.R., Horuk R., MacDonald M.E., Stuhlmann H., Koup R.A., Landau N.R. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 1996, 86(3):367-377.
26. Mattapallil J.J., Douek D.C., Hill B., Nishimura Y., Martin M., Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434(7037):1093-1097.
27. Means R.E., Matthews T., Hoxie J.A., Malim M.H., Kodama T., Desrosiers R.C. Ability of the V3 loop of simian immunodeficiency virus to serve as a target for antibody-mediated neutralization: correlation of neutralization sensitivity, growth in macrophages, and decreased dependence on CD4. J. Virol. 2001, 75(8):3903-3915.
28. Meythaler M., Martinot A., Wang Z., Pryputniewicz S., Kasheta M., Ling B., Marx P.A., O'Neil S., Kaur A. Differential CD4+ T-lymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J. Virol. 2009, 83(2):572-583.
29. Minang J.T., Barsov E.V., Yuan F., Trivett M.T., Piatak M., Lifson J.D., Ott D.E., Ohlen C. Efficient inhibition of SIV replication in rhesus CD4+ T-cell clones by autologous immortalized SIV-specific CD8+ T-cell clones. Virology 2008, 372(2):430-441.
30. Minang J.T., Trivett M.T., Coren L.V., Barsov E.V., Piatak M., Ott D.E., Ohlen C. Nef-mediated MHC class I down-regulation unmasks clonal differences in virus suppression by SIV-specific CD8(+) T cells independent of IFN-gamma and CD107a responses. Virology 2009, 391(1):130-139.
31. Minang J.T., Trivett M.T., Bolton D.L., Trubey C.M., Estes J.D., Li Y., Smedley J., Pung R., Rosati M., Jalah R., Pavlakis G.N., Felber B.K., Piatak M., Roederer M., Lifson J.D., Ott D.E., Ohlen C. Distribution, persistence, and efficacy of adoptively transferred central and effector memory-derived autologous simian immunodeficiency virus-specific CD8(+) T cell clones in rhesus macaques during acute infection. J. Immunol. 2010, 184(1):315-326.
32. Monceaux V., Viollet L., Petit F., Cumont M.C., Kaufmann G.R., Aubertin A.M., Hurtrel B., Silvestri G., Estaquier J. CD4+ CCR5+ T-cell dynamics during simian immunodeficiency virus infection of Chinese rhesus macaques. J. Virol. 2007, 81(24):13865-13875.
33. Mueller Y.M., Do D.H., Altork S.R., Artlett C.M., Gracely E.J., Katsetos C.D., Legido A., Villinger F., Altman J.D., Brown C.R., Lewis M.G., Katsikis P.D. IL-15 treatment during acute simian immunodeficiency virus (SIV) infection increases viral set point and accelerates disease progression despite the induction of stronger SIV-specific CD8+ T cell responses. J. Immunol. 2008, 180(1):350-360.
34. Mulherin S.A., O'Brien T.R., Ioannidis J.P., Goedert J.J., Buchbinder S.P., Coutinho R.A., Jamieson B.D., Meyer L., Michael N.L., Pantaleo G., Rizzardi G.P., Schuitemaker H., Sheppard H.W., Theodorou I.D., Vlahov D., Rosenberg P.S. Effects of CCR5-Delta32 and CCR2-64I alleles on HIV-1 disease progression: the protection varies with duration of infection. AIDS 2003, 17(3):377-387.
35. Oh D.Y., Jessen H., Kucherer C., Neumann K., Oh N., Poggensee G., Bartmeyer B., Jessen A., Pruss A., Schumann R.R., Hamouda O. CCR5Delta32 genotypes in a German HIV-1 seroconverter cohort and report of HIV-1 infection in a CCR5Delta32 homozygous individual. PLoS ONE 2008, 3(7):e2747.
36. Okoye A., Park H., Rohankhedkar M., Coyne-Johnson L., Lum R., Walker J.M., Planer S.L., Legasse A.W., Sylwester A.W., Piatak M., Lifson J.D., Sodora D.L., Villinger F., Axthelm M.K., Schmitz J.E., Picker L.J. Profound CD4+/CCR5+ T cell expansion is induced by CD8+ lymphocyte depletion but does not account for accelerated SIV pathogenesis. J. Exp. Med. 2009, 206(7):1575-1588.
37. Pandrea I., Apetrei C., Gordon S., Barbercheck J., Dufour J., Bohm R., Sumpter B., Roques P., Marx P.A., Hirsch V.M., Kaur A., Lackner A.A., Veazey R.S., Silvestri G. Paucity of CD4+ CCR5+ T cells is a typical feature of natural SIV hosts. Blood 2007, 109(3):1069-1076.
38. Paxton W.A., Martin S.R., Tse D., O'Brien T.R., Skurnick J., VanDevanter N.L., Padian N., Braun J.F., Kotler D.P., Wolinsky S.M., Koup R.A. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat. Med. 1996, 2(4):412-417.
39. Perez E.E., Wang J., Miller J.C., Jouvenot Y., Kim K.A., Liu O., Wang N., Lee G., Bartsevich V.V., Lee Y.L., Guschin D.Y., Rupniewski I., Waite A.J., Carpenito C., Carroll R.G., Orange J.S., Urnov F.D., Rebar E.J., Ando D., Gregory P.D., Riley J.L., Holmes M.C., June C.H. Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol. 2008, 26(7):808-816.
40. Picker L.J., Hagen S.I., Lum R., Reed-Inderbitzin E.F., Daly L.M., Sylwester A.W., Walker J.M., Siess D.C., Piatak M., Wang C., Allison D.B., Maino V.C., Lifson J.D., Kodama T., Axthelm M.K. Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 2004, 200(10):1299-1314.
41. Pohlmann S., Krumbiegel M., Kirchhoff F. Coreceptor usage of BOB/GPR15 and Bonzo/STRL33 by primary isolates of human immunodeficiency virus type 1. J. Gen. Virol. 1999, 80(Pt 5):1241-1251.
42. Pohlmann S., Stolte N., Munch J., Ten Haaft P., Heeney J.L., Stahl-Hennig C., Kirchhoff F. Co-receptor usage of BOB/GPR15 in addition to CCR5 has no significant effect on replication of simian immunodeficiency virus in vivo. J. Infect. Dis. 1999, 180(5):1494-1502.
43. Pohlmann S., Lee B., Meister S., Krumbiegel M., Leslie G., Doms R.W., Kirchhoff F. Simian immunodeficiency virus utilizes human and sooty mangabey but not rhesus macaque STRL33 for efficient entry. J. Virol. 2000, 74(11):5075-5082.
44. Rana S., Besson G., Cook D.G., Rucker J., Smyth R.J., Yi Y., Turner J.D., Guo H.H., Du J.G., Peiper S.C., Lavi E., Samson M., Libert F., Liesnard C., Vassart G., Doms R.W., Parmentier M., Collman R.G. Role of CCR5 in infection of primary macrophages and lymphocytes by macrophage-tropic strains of human immunodeficiency virus: resistance to patient-derived and prototype isolates resulting from the delta ccr5 mutation. J. Virol. 1997, 71(4):3219-3227.
45. Riddick N.E., Hermann E.A., Lamorris M.L., Elliot S.T., Wey W.C., Cervasi B., Taafe J., Engram J.C., Li B., Else J.G., Li Y., Hahn B.H., Derdeyn C.A., Sodora D.L., Apetrei C., Paiardini M., Silvestri G., Collman R.G. A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor Use In Vivo. PLoS Pathog. 2010, 6(8).
46. Sacha J.B., Watkins D.I. Synchronous infection of SIV and HIV in vitro for virology, immunology and vaccine-related studies. Nat. Protoc. 2010, 5(2):239-246.
47. Salkowitz J.R., Bruse S.E., Meyerson H., Valdez H., Mosier D.E., Harding C.V., Zimmerman P.A., Lederman M.M. CCR5 promoter polymorphism determines macrophage CCR5 density and magnitude of HIV-1 propagation in vitro. Clin. Immunol. 2003, 108(3):234-240.
48. Scarlatti G., Tresoldi E., Bjorndal A., Fredriksson R., Colognesi C., Deng H.K., Malnati M.S., Plebani A., Siccardi A.G., Littman D.R., Fenyo E.M., Lusso P. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 1997, 3(11):1259-1265.
49. Sharron M., Pohlmann S., Price K., Lolis E., Tsang M., Kirchhoff F., Doms R.W., Lee B. Expression and coreceptor activity of STRL33/Bonzo on primary peripheral blood lymphocytes. Blood 2000, 96(1):41-49.
50. Unutmaz D., Xiang W., Sunshine M.J., Campbell J., Butcher E., Littman D.R. The primate lentiviral receptor Bonzo/STRL33 is coordinately regulated with CCR5 and its expression pattern is conserved between human and mouse. J. Immunol. 2000, 165(6):3284-3292.
51. Vatakis D.N., Bristol G., Wilkinson T.A., Chow S.A., Zack J.A. Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4+ T cells. J. Virol. 2007, 81(7):3574-3582.
52. Vatakis D.N., Nixon C.C., Bristol G., Zack J.A. Differentially stimulated CD4+ T cells display altered human immunodeficiency virus infection kinetics: implications for the efficacy of antiviral agents. J. Virol. 2009, 83(7):3374-3378.
53. Veazey R.S., Mansfield K.G., Tham I.C., Carville A.C., Shvetz D.E., Forand A.E., Lackner A.A. Dynamics of CCR5 expression by CD4(+) T cells in lymphoid tissues during simian immunodeficiency virus infection. J. Virol. 2000, 74(23):11001-11007.
54. Weiler A., May G.E., Qi Y., Wilson N., Watkins D.I. Polymorphisms in eight host genes associated with control of HIV replication do not mediate elite control of viral replication in SIV-infected Indian rhesus macaques. Immunogenetics 2006, 58(12):1003-1009.
55. Xiao L., Rudolph D.L., Owen S.M., Spira T.J., Lal R.B. Adaptation to promiscuous usage of CC and CXC-chemokine coreceptors in vivo correlates with HIV-1 disease progression. AIDS 1998, 12(13):F137-F143.
56. Zimmerman P.A., Buckler-White A., Alkhatib G., Spalding T., Kubofcik J., Combadiere C., Weissman D., Cohen O., Rubbert A., Lam G., Vaccarezza M., Kennedy P.E., Kumaraswami V., Giorgi J.V., Detels R., Hunter J., Chopek M., Berger E.A., Fauci A.S., Nutman T.B., Murphy P.M. Inherited resistance to HIV-1 conferred by an inactivating mutation in CC chemokine receptor 5: studies in populations with contrasting clinical phenotypes, defined racial background, and quantified risk. Mol. Med. 1997, 3(1):23-36.