A Novel CCR5 Mutation Common in Sooty Mangabeys Reveals SIVsmm Infection of CCR5-Null Natural Hosts and Efficient Alternative Coreceptor Use

1. GaoF

BailesE

RobertsonDL

ChenY

RodenburgCM

1999 Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397 436 441

2. BailesE

GaoF

Bibollet-RucheF

CourgnaudV

PeetersM

2003 Hybrid origin of SIV in chimpanzees. Science 300 1713

3. PeetersM

JanssensW

FransenK

BrandfulJ

HeyndrickxL

1994 Isolation of simian immunodeficiency viruses from two sooty mangabeys in Cote d'Ivoire: virological and genetic characterization and relationship to other HIV type 2 and SIVsm/mac strains. AIDS Res Hum Retroviruses 10 1289 1294

4. HirschVM

OlmstedRA

Murphey-CorbM

PurcellRH

JohnsonPR

1989 An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339 389 392

5. ApetreiC

KaurA

LercheNW

MetzgerM

PandreaI

2005 Molecular epidemiology of simian immunodeficiency virus SIVsm in U.S. primate centers unravels the origin of SIVmac and SIVstm. J Virol 79 8991 9005

6. SilvestriG

PaiardiniM

PandreaI

LedermanMM

SodoraDL

2007 Understanding the benign nature of SIV infection in natural hosts. J Clin Invest 117 3148 3154

7. SodoraDL

AllanJS

ApetreiC

BrenchleyJM

DouekDC

2009 Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 15 861 865

8. KeeleBF

JonesJH

TerioKA

EstesJD

RudicellRS

2009 Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460 515 519

9. Rey-CuilleMA

BerthierJL

Bomsel-DemontoyMC

ChaducY

MontagnierL

1998 Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. J Virol 72 3872 3886

10. BroussardSR

StapransSI

WhiteR

WhiteheadEM

FeinbergMB

2001 Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J Virol 75 2262 2275

11. SilvestriG

SodoraDL

KoupRA

PaiardiniM

O'NeilSP

2003 Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18 441 452

12. HolzammerS

HolznagelE

KaulA

KurthR

NorleyS

2001 High virus loads in naturally and experimentally SIVagm-infected African green monkeys. Virology 283 324 331

13. KootM

KeetIPM

RosAHV

de GoedeREY

RoosMTL

1993 Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. AnnInternMed 118 681 688

14. ScarlattiG

TresoldiE

BjorndalA

FredrikssonR

ColognesiC

1997 In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat Med 3 1259 1265

15. BlaakH

van't WoutAB

BrouwerM

HooibrinkB

HovenkampE

2000 In vivo HIV-1 infection of CD45RA+CD4+ T cells is established primarily by syncytium-inducing variants and correlates with the rate of CD4+ T cell decline. ProcNatlAcadSciUSA 97 1269 1274

16. Van RijRP

BlaakH

VisserJA

BrouwerM

RientsmaR

2000 Differential coreceptor expression allows for independent evolution of non-syncytium-inducing and syncytium-inducing HIV-1. JClinInvest 106 1039 1052

17. PandreaI

OnangaR

SouquiereS

Mouinga-OndemeA

BourryO

2008 Paucity of CD4+ CCR5+ T cells may prevent transmission of simian immunodeficiency virus in natural nonhuman primate hosts by breast-feeding. J Virol 82 5501 5509

18. PandreaI

ApetreiC

GordonS

BarbercheckJ

DufourJ

2007 Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109 1069 1076

19. RuckerJ

EdingerAL

SharronM

SamsonM

LeeB

1997 Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. J Virol 71 8999 9007

20. DengHK

UnutmazD

KewalRamaniVN

LittmanDR

1997 Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388 296 300

21. FarzanM

ChoeH

MartinK

MarconL

HofmannW

1997 Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. J Exp Med 186 405 411

22. PohlmannS

StolteN

MunchJ

Ten HaaftP

HeeneyJL

1999 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 180 1494 1502

23. MattapallilJJ

DouekDC

HillB

NishimuraY

MartinM

2005 Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434 1093 1097

24. GordonSN

KlattNR

BosingerSE

BrenchleyJM

MilushJM

2007 Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 179 3026 3034

25. McCuneJM

2001 The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410 974 979

26. GrossmanZ

Meier-SchellersheimM

PaulWE

PickerLJ

2006 Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat Med 12 289 295

27. OkoyeA

Meier-SchellersheimM

BrenchleyJM

HagenSI

WalkerJM

2007 Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 204 2171 2185

28. LiuZ

CumberlandWG

HultinLE

PrinceHE

DetelsR

1997 Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr Hum Retrovirol 16 83 92

29. BosingerSE

LiQ

GordonSN

KlattNR

DuanL

2009 Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119 3556 3572

30. JacquelinB

MayauV

TargatB

LiovatAS

KunkelD

2009 Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119 3544 3555

31. BrenchleyJM

PriceDA

SchackerTW

AsherTE

SilvestriG

2006 Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12 1365 1371

32. BrenchleyJM

SchackerTW

RuffLE

PriceDA

TaylorJH

2004 CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200 749 759

33. PandreaIV

GautamR

RibeiroRM

BrenchleyJM

ButlerIF

2007 Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 179 3035 3046

34. VeazeyRS

DeMariaM

ChalifouxLV

ShvetzDE

PauleyDR

1998 Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280 427 431

35. FavreD

LedererS

KanwarB

MaZM

ProllS

2009 Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 5 e1000295

36. RaffatelluM

SantosRL

VerhoevenDE

GeorgeMD

WilsonRP

2008 Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14 421 428

37. CecchinatoV

TrindadeCJ

LaurenceA

HeraudJM

BrenchleyJM

2008 Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal Immunol 1 279 288

38. BrenchleyJM

PaiardiniM

KnoxKS

AsherAI

CervasiB

2008 Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112 2826 2835

39. LiuR

PaxtonWA

ChoeS

CeradiniD

MartinSR

1996 Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86 367 377

40. SamsonM

LibertF

DoranzBJ

RuckerJ

LiesnardC

1996 Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382 722 725

41. HuangY

PaxtonW

WolinskySM

NeumannAU

ZhangL

1996 The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nature Med 2 1240 1243

42. DeanM

CarringtonM

WinklerC

HuttleyGA

SmithMW

1996 Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CCR5 structural gene. Science 273 1856 1862

43. ChenZ

KwonD

JinZ

MonardS

TelferP

1998 Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J Exp Med 188 2057 2065

44. PalaciosE

DigilioL

McClureHM

ChenZ

MarxPA

1998 Parallel evolution of CCR5-null phenotypes in humans and in a natural host of simian immunodeficiency virus. Curr Biol 8 943 946

45. SantiagoML

RangeF

KeeleBF

LiY

BailesE

2005 Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79 12515 12527

46. ApetreiC

GautamR

SumpterB

CarterAC

GaufinT

2007 Virus subtype-specific features of natural simian immunodeficiency virus SIVsmm infection in sooty mangabeys. J Virol 81 7913 7923

47. MilushJM

ReevesJD

GordonSN

ZhouD

MuthukumarA

2007 Virally induced CD4+ T cell depletion is not sufficient to induce AIDS in a natural host. J Immunol 179 3047 3056

48. SaitaY

KondoM

ShimizuY

2007 Species selectivity of small-molecular antagonists for the CCR5 chemokine receptor. Int Immunopharmacol 7 1528 1534

49. KetasTJ

KuhmannSE

PalmerA

ZuritaJ

HeW

2007 Cell surface expression of CCR5 and other host factors influence the inhibition of HIV-1 infection of human lymphocytes by CCR5 ligands. Virology 364 281 290

50. AlkhatibG

LiaoF

BergerEA

FarberJM

PedenKW

1997 A new SIV co-receptor, STRL33. Nature 388 238

51. ForteS

HarmonME

PinedaMJ

OverbaughJ

2003 Early- and intermediate-stage variants of simian immunodeficiency virus replicate efficiently in cells lacking CCR5. J Virol 77 9723 9727

52. LaurenA

VodrosD

ThorstenssonR

FenyoEM

2006 Comparative studies on mucosal and intravenous transmission of simian immunodeficiency virus (SIVsm): evolution of coreceptor use varies with pathogenic outcome. J Gen Virol 87 581 594

53. ChenZ

ZhouP

HoDD

LandauNR

MarxPA

1997 Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J Virol 71 2705 2714

54. ZhangY

LouB

LalRB

GettieA

MarxPA

2000 Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. J Virol 74 6893 6910

55. ChenZ

GettieA

HoDD

MarxPA

1998 Primary SIVsm isolates use the CCR5 coreceptor from sooty mangabeys naturally infected in west Africa: a comparison of coreceptor usage of primary SIVsm, HIV-2, and SIVmac. Virology 246 113 124

56. OwenSM

MasciotraS

NovembreF

YeeJ

SwitzerWM

2000 Simian immunodeficiency viruses of diverse origin can use CXCR4 as a coreceptor for entry into human cells. J Virol 74 5702 5708

57. WolinskySM

VeazeyRS

KunstmanKJ

KlassePJ

DufourJ

2004 Effect of a CCR5 inhibitor on viral loads in macaques dual-infected with R5 and X4 primate immunodeficiency viruses. Virology 328 19 29

58. VeazeyRS

KlassePJ

KetasTJ

ReevesJD

PiatakMJr

2003 Use of a small molecule CCR5 inhibitor in macaques to treat simian immunodeficiency virus infection or prevent simian-human immunodeficiency virus infection. J Exp Med 198 1551 1562

59. UnutmazD

XiangW

SunshineMJ

CampbellJ

ButcherE

2000 The primate lentiviral receptor Bonzo/STRL33 is coordinately regulated with CCR5 and its expression pattern is conserved between human and mouse. J Immunol 165 3284 3292

60. SharronM

PohlmannS

PriceK

LolisE

TsangM

2000 Expression and coreceptor activity of STRL33/Bonzo on primary peripheral blood lymphocytes. Blood 96 41 49

61. ElbimC

MonceauxV

MuellerYM

LewisMG

FrancoisS

2008 Early divergence in neutrophil apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J Immunol 181 8613 8623

62. LiQ

EstesJD

DuanL

JessurunJ

PambuccianS

2008 Simian immunodeficiency virus-induced intestinal cell apoptosis is the underlying mechanism of the regenerative enteropathy of early infection. J Infect Dis 197 420 429

63. PickerLJ

HagenSI

LumR

Reed-InderbitzinEF

DalyLM

2004 Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 200 1299 1314

64. GiorgiJV

HultinLE

McKeatingJA

JohnsonTD

OwensB

1999 Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179 859 870

65. EstesJD

GordonSN

ZengM

ChahroudiAM

DunhamRM

2008 Early resolution of acute immune activation and induction of PD-1 in SIV-infected sooty mangabeys distinguishes nonpathogenic from pathogenic infection in rhesus macaques. J Immunol 180 6798 6807

66. LedererS

FavreD

WaltersKA

ProllS

KanwarB

2009 Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog 5 e1000296

67. BernsteinI

1971 The influence of introductory techniques on the formation of captive mangabey groups. Primates 12 33 44

68. Georges-CourbotMC

LuCY

MakuwaM

TelferP

OnangaR

1998 Natural infection of a household pet red-capped mangabey (Cercocebus torquatus torquatus) with a new simian immunodeficiency virus. J Virol 72 600 608

69. HummelS

SchmidtD

KremeyerB

HerrmannB

OppermannM

2005 Detection of the CCR5-Delta32 HIV resistance gene in Bronze Age skeletons. Genes Immun 6 371 374

70. HedrickPW

VerrelliBC

2006 “Ground truth” for selection on CCR5-Delta32. Trends Genet 22 293 296

71. ConnorRI

ChenBK

ChoeS

LandauNR

1995 Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206 935 944

72. RongR

LiB

LynchRM

HaalandRE

MurphyMK

2009 Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog 5 e1000594

73. BurioniR

PlaisantP

RiccioML

RossoliniGM

SantangeloR

1995 Engineering human monoclonal antibody fragments: a recombinant enzyme-linked Fab. New Microbiol 18 127 133

74. GautamR

CarterAC

KatzN

ButlerIF

BarnesM

2007 In vitro characterization of primary SIVsmm isolates belonging to different lineages. In vitro growth on rhesus macaque cells is not predictive for in vivo replication in rhesus macaques. Virology 362 257 270

75. TaaffeJ

ChahroudiA

EngramJ

SumpterB

MeekerT

A five-year longitudinal analysis of naturally SIV-infected sooty mangabeys reveals a slow but progressive CD4+ T-cell decline whose magnitude is not predicted by viral load or immune activation. J Virol