Studies of plasmacytoid dendritic cell dynamics in Simian immunodeficiency virus infection of nonhuman primates provide insights into HIV pathogenesis

Current HIV Research

Volumn 7, Issue 1, 2009, Pages 23-29

  Wijewardana, Viskam ^a,b   Brown, Kevin N ^a,b   Barratt Boyes, Simon M ^a,b  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; HIV; IFN ; Migration; Plasmacytoid dendritic cells; SIV

Indexed keywords

ALPHA INTERFERON; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CXCL9 CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN G; INTERFERON; INTERLEUKIN 12; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 7; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTIGEN SPECIFICITY; APOPTOSIS; BONE MARROW SUPPRESSION; BYSTANDER EFFECT; CD4+ T LYMPHOCYTE; CELL COUNT; CELL FUNCTION; CELL LOSS; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; INNATE IMMUNITY; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PATHOGENESIS; PRIMATE; PROTEIN EXPRESSION; PROTEIN SECRETION; RECEPTOR UPREGULATION; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS INFECTION; ANIMAL; IMMUNOLOGY; MONKEY DISEASE; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; DENDRITIC CELLS; HIV INFECTIONS; HUMANS; PRIMATES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 59649107088     PISSN: 1570162X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016209787048483     Document Type: Review

References (99)

1. Ueno H, Klechevsky E, Morita R, et al. Dendritic cell subsets in health and disease. Immunol Rev 2007; 219: 118-42.
2. Vollenweider R, Lennert K. Plasmacytoid T-cell clusters in nonspecific lymphadenitis. Virchows Arch B Cell Pathol Incl Mol Pathol 1983; 44: 1-14.
3. Facchetti F, de Wolf-Peeters C, Mason DY, Pulford K, van den Oord JJ, Desmet VJ. Plasmacytoid T cells. Immunohistochemical evidence for their monocyte/macrophage origin. Am J Pathol 1988; 133: 15-21.
4. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185: 1101-11.
5. Pulendran B, Banchereau J, Burkeholder S, et al. Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J Immunol 2000; 165: 566-72.
6. Nakano H, Yanagita M, Gunn MD. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001; 194: 1171-8.
7. O'Keeffe M, Hochrein H, Vremec D, et al. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 2002; 196: 1307-19.
8. Liu K, Waskow C, Liu X, Yao K, Hoh J, Nussenzweig M. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 2007; 8: 578-83.
9. Kabashima K, Banks TA, Ansel KM, Lu TT, Ware CF, Cyster JG. Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 2005; 22: 439-50.
10. Cella M, Jarrossay D, Facchetti F, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999; 5: 919-23.
11. Yoneyama H, Matsuno K, Zhang Y, et al. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int Immunol 2004; 16: 915-28.
12. Liu YJ. IPC: professional type I interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 2005; 23: 275-306.
13. Coates PT, Barratt-Boyes SM, Donnenberg AD, Morelli AE, Murphey-Corb M, Thomson AW. Strategies for preclinical evaluation of dendritic cell subsets for promotion of transplant tolerance in the nonhuman primate. Hum Immunol 2002; 63: 955-65.
14. Coates PT, Barratt-Boyes SM, Zhang L, et al. Dendritic cell subsets in blood and lymphoid tissue of rhesus monkeys and their mobilization with Flt3 ligand. Blood 2003; 102: 2513-21.
15. Brown KN, Trichel A, Barratt-Boyes SM. Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS. J Immunol 2007; 178: 6958-67.
16. Reeves RK, Fultz PN. Disparate effects of acute and chronic infection with SIVmac239 or SHIV-89.6P on macaque plasmacytoid dendritic cells. Virology 2007; 365: 356-68.
17. Reeves RK, Fultz PN. Characterization of plasmacytoid dendritic cells in bone marrow of pig-tailed macaques. Clin Vaccine Immunol 2008; 15: 35-41.
18. Chung E, Amrute SB, Abel K, et al. Characterization of virus-responsive plasmacytoid dendritic cells in the rhesus macaque. Clin Diagn Lab Immunol 2005; 12: 426-35.
19. Teleshova N, Kenney J, Jones J, et al. CpG-C immunostimulatory oligodeoxyribonucleotide activation of plasmacytoid dendritic cells in rhesus macaques to augment the activation of IFN-gamma-secreting simian immunodeficiency virus-specific T cells. J Immunol 2004; 173: 1647-57.
20. Dzionek A, Inagaki Y, Okawa K, et al. Plasmacytoid dendritic cells: from specific surface markers to specific cellular functions. Hum Immunol 2002; 63: 1133-48.
21. Cervantes-Barragan L, Zust R, Weber F, et al. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood 2007; 109: 1131-7.
22. Lund JM, Linehan MM, Iijima N, Iwasaki A. Cutting Edge: Plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J Immunol 2006; 177: 7510-4.
23. Meyers JH, Justement JS, Hallahan CW, et al. Impact of HIV on cell survival and antiviral activity of plasmacytoid dendritic cells. PLoS ONE 2007; 2: e458.
24. Muller-Trutwin M, and Hosmalin A. Role for plasmacytoid dendritic cells in anti-HIV innate immunity. Immunol Cell Biol 2005; 83: 578-83.
25. Gurney KB, Colantonio AD, Blom B, Spits H, Uittenbogaart CH. Endogenous IFN-alpha production by plasmacytoid dendritic cells exerts an antiviral effect on thymic HIV-1 infection. J Immunol 2004; 173: 7269-76.
26. Lovgren T, Eloranta ML, Bave U, Alm GV, Ronnblom L. Induction of interferon-alpha production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum 2004; 50: 1861-72.
27. Beignon AS, McKenna K, Skoberne M, et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 2005; 115: 3265-75.
28. Seya T, Funami K, Taniguchi M, Matsumoto M. Antibodies against human Toll-like receptors (TLRs): TLR distribution and localization in human dendritic cells. J Endotoxin Res 2005; 11: 369-74.
29. Izaguirre A, Barnes BJ, Amrute S, et al. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 2003; 74: 1125-38.
30. Cox K, North M, Burke M, et al. Plasmacytoid dendritic cells (PDC) are the major DC subset innately producing cytokines in human lymph nodes. J Leukoc Biol 2005; 78: 1142-1152.
31. Decalf J, Fernandes S, Longman R, et al. Plasmacytoid dendritic cells initiate a complex chemokine and cytokine network and are a viable drug target in chronic HCV patients. J Exp Med 2007; 204: 2423-37.
32. McKenna K, Beignon AS, Bhardwaj N. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J Virol 2005; 79: 17-27.
33. Yoneyama H, Matsuno K, Toda E, et al. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J Exp Med 2005; 202: 425-35.
34. Krug A, French AR, Barchet W, et al. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 2004; 21: 107-19.
35. Poeck H, Wagner M, Battiany J, et al. Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help. Blood 2004; 103: 3058-64.
36. Bekeredjian-Ding IB, Wagner M, Hornung V, et al. Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN. J Immunol 2005; 174: 4043-50.
37. Hoeffel G, Ripoche AC, Matheoud D, et al. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 2007; 27: 481-92.
38. Duan XZ, Wang M, Li HW, Zhuang H, Xu D, Wang FS. Decreased frequency and function of circulating plasmocytoid dendritic cells (pDC) in hepatitis B virus infected humans. J Clin Immunol 2004; 24: 637-46.
39. Goutagny N, Vieux C, Decullier E, et al. Quantification and functional analysis of plasmacytoid dendritic cells in patients with chronic hepatitis C virus infection. J Infect Dis 2004; 189: 1646-55.
40. Zhang Z, Xu D, Li Y, et al. Longitudinal alteration of circulating dendritic cell subsets and its correlation with steroid treatment in patients with severe acute respiratory syndrome. Clin Immunol 2005; 116: 225-35.
41. Pichyangkul S, Endy TP, Kalayanarooj S, et al. A blunted blood plasmacytoid dendritic cell response to an acute systemic viral infection is associated with increased disease severity. J Immunol 2003; 171: 5571-8.
42. Donaghy H, Pozniak A, Gazzard B, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 2001; 98: 2574-6.
43. Chehimi J, Campbell DE, Azzoni L, et al. Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol 2002; 168: 4796-801.
44. Barron MA, Blyveis N, Palmer BE, MaWhinney S, Wilson CC. Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis 2003; 187: 26-37.
45. Finke JS, Shodell M, Shah K, Siegal FP, Steinman RM. Dendritic cell numbers in the blood of HIV-1 infected patients before and after changes in antiretroviral therapy. J Clin Immunol 2004; 24: 647-52.
46. Schmidt B, Fujimura SH, Martin JN, Levy JA. Variations in plasmacytoid dendritic cell (PDC) and myeloid dendritic cell (MDC) levels in HIV-infected subjects on and off antiretroviral therapy. J Clin Immunol 2006; 26: 55-64.
47. Zhang Z, Fu J, Zhao Q, et al. Differential restoration of myeloid and plasmacytoid dendritic cells in HIV-1-infected children after treatment with highly active antiretroviral therapy. J Immunol 2006; 176: 5644-51.
48. Malleret B, Karlsson I, Maneglier B, et al. Effect of SIVmac infection on plasmacytoid and CD1c+ myeloid dendritic cells in cynomolgus macaques. Immunology 2008; 124: 223-33.
49. Koopman G, Niphuis H, Haaksma AG, et al. Increase in plasmacytoid and myeloid dendritic cells by progenipoietin-1, a chimeric Flt-3 and G-CSF receptor agonist, in SIV-Infected rhesus macaques. Hum Immunol 2004; 65: 303-16.
50. Diop OM, Ploquin MJ, Mortara L, et al. Plasmacytoid dendritic cell dynamics and alpha interferon production during Simian immunodeficiency virus infection with a nonpathogenic outcome. J Virol 2008; 82: 5145-52.
51. Feldman S, Stein D, Amrute S, et al. Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin Immunol 2001; 101: 201-10.
52. Abb J, Kochen M, Deinhardt F. Interferon production in male homosexuals with the acquired immune deficiency syndrome (AIDS) or generalized lymphadenopathy. Infection 1984; 12: 240-2.
53. Howell DM, Feldman SB, Kloser P, Fitzgerald-Bocarsly P. Decreased frequency of functional natural interferon-producing cells in peripheral blood of patients with the acquired immune deficiency syndrome. Clin Immunol Immunopathol 1994; 71: 223-30.
54. Lopez C, Fitzgerald PA, Siegal FP. Severe acquired immune deficiency syndrome in male homosexuals: diminished capacity to make interferon-alpha in vitro associated with severe opportunistic infections. J Infect Dis 1983; 148: 962-6.
55. Yonezawa A, Morita R, Takaori-Kondo A, et al. Natural alpha interferon-producing cells respond to human immunodeficiency virus type I with alpha interferon production and maturation into dendritic cells. J Virol 2003; 77: 3777-84.
56. Del Corno M, Gauzzi MC, Penna G, Belardelli F, Adorini L, Gessani S. Human immunodeficiency virus type I gp120 and other activation stimuli are highly effective in triggering alpha interferon and CC chemokine production in circulating plasmacytoid but not myeloid dendritic cells. J Virol 2005; 79: 12597-601.
57. Garcia-Sastre A, Biron CA. Type I interferons and the virus-host relationship: a lesson in detente. Science 2006; 312: 879-82.
58. Martinson JA, Roman-Gonzalez A, Tenorio AR, et al. Dendritic cells from HIV-1 infected individuals are less responsive to toll-like receptor (TLR) ligands. Cell Immunol 2007; 250: 75-84.
59. Tilton JC, Manion MM, Luskin MR, et al. Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol 2008; 82: 3997-4006.
60. Abel K, Alegria-Hartman MJ, Rothaeusler K, Marthas M, Miller CJ. The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFNalpha/beta) and IFN-alpha/ beta-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. J Virol 2002; 76: 8433-45.
61. Abel K, Rocke DM, Chohan B, Fritts L, Miller CJ. Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. J Virol 2005; 79: 12164-72.
62. Johansson C, Wetzel JD, He J, Mikacenic C, Dermody TS, Kelsall BL. Type I interferons produced by hematopoietic cells protect mice against lethal infection by mammalian reovirus. J Exp Med 2007; 204: 1349-58.
63. Diebold SS, Montoya M, Unger H, et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003; 424: 324-8.
64. Fonteneau JF, Larsson M, Beignon AS, et al. Human immunodeficiency virus type I activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol 2004; 78: 5223-32.
65. Schmidt B, Ashlock BM, Foster H, Fujimura SH, Levy JA. HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 2005; 343: 256-66.
66. Abel K, La Franco-Scheuch L, Rourke T, et al. Gamma interferon-mediated inflammation is associated with lack of protection from intravaginal simian immunodeficiency virus SIVmac239 challenge in simian-human immunodeficiency virus 89.6-immunized rhesus macaques. J Virol 2004; 78: 841-54.
67. LaFranco-Scheuch L, Abel K, Makori N, Rothaeusler K, Miller CJ. High beta-chemokine expression levels in lymphoid tissues of simian/human immunodeficiency virus 89.6-vaccinated rhesus macaques are associated with uncontrolled replication of simian immunodeficiency virus challenge inoculum. J Virol 2004; 78: 6399-408.
68. Reinhart TA, Fallert BA, Pfeifer ME, et al. Increased expression of the inflammatory chemokine CXC chemokine ligand 9/monokine induced by interferon-gamma in lymphoid tissues of rhesus macaques during simian immunodeficiency virus infection and acquired immunodeficiency syndrome. Blood 2002; 99: 3119-28.
69. Sarkar S, Kalia V, Murphey-Corb M, Montelaro RC, Reinhart TA. Expression of IFN-gamma induced CXCR3 agonist chemokines and compartmentalization of CXCR3+ cells in the periphery and lymph nodes of rhesus macaques during simian immunodeficiency virus infection and acquired immunodeficiency syndrome. J Med Primatol 2003; 32: 247-64.
70. Kornfeld C, Ploquin MJ, Pandrea I, et al. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 2005; 115: 1082-91.
71. Silvestri G, Sodora DL, Koup RA, et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 2003; 18: 441-52.
72. Smit JJ, Rudd BD, Lukacs NW. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J Exp Med 2006; 203: 1153-9.
73. Gill MA, Palucka AK, Barton T, et al. Mobilization of plasmacytoid and myeloid dendritic cells to mucosal sites in children with respiratory syncytial virus and other viral respiratory infections. J Infect Dis 2005; 191: 1105-15.
74. Fong L, Mengozzi M, Abbey NW, Herndier BG, Engleman EG. Productive infection of plasmacytoid dendritic cells with human immunodeficiency virus type I is triggered by CD40 ligation. J Virol 2002; 76: 11033-41.
75. Lore K, Smed-Sorensen A, Vasudevan J, Mascola JR, Koup RA. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells. J Exp Med 2005; 201: 2023-33.
76. Patterson S, Rae A, Hockey N, Gilmour J, Gotch F. Plasmacytoid dendritic cells are highly susceptible to human immunodeficiency virus type I infection and release infectious virus. J Virol 2001; 75: 6710-3.
77. Smed-Sorensen A, Lore K, Vasudevan J, et al. Differential susceptibility to human immunodeficiency virus type I infection of myeloid and plasmacytoid dendritic cells. J Virol 2005; 79: 8861-9.
78. Schmidt B, Scott I, Whitmore RG, et al. Low-level HIV infection of plasmacytoid dendritic cells: onset of cytopathic effects and cell death after PDC maturation. Virology 2004; 329: 280-8.
79. Donaghy H, Gazzard B, Gotch F, Patterson S. Dysfunction and infection of freshly isolated blood myeloid and plasmacytoid dendritic cells in patients infected with HIV-1. Blood 2003; 101: 4505-11.
80. Ahr B, Robert-Hebmann V, Devaux C, Biard-Piechaczyk M. Apoptosis of uninfected cells induced by HIV envelope glycoproteins. Retrovirology 2004; 1: 12.
81. Bell DJ, Dockrell DH. Apoptosis in HIV-1 infection. J Eur Acad Dermatol Venereol 2003; 17: 178-83.
82. Holm GH, Zhang C, Gorry PR, et al. Apoptosis of bystander T cells induced by human immunodeficiency virus type I with increased envelope/ receptor affinity and coreceptor binding site exposure. J Virol 2004; 78: 4541-51.
83. Kameoka M, Suzuki S, Kimura T, et al. Exposure of resting peripheral blood T cells to HIV-1 particles generates CD25+ killer cells in a small subset, leading to induction of apoptosis in bystander cells. Int Immunol 1997; 9: 1453-62.
84. Zhang M, Li X, Pang X, et al. Identification of a potential HIV-induced source of bystander-mediated apoptosis in T cells: upregulation of trail in primary human macrophages by HIV-1 tat. J Biomed Sci 2001; 8: 290-6.
85. Finkel TH, Tudor-Williams G, Banda NK, et al. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1995; 1: 129-34.
86. Salvato MS, Yin CC, Yagita H, et al. Attenuated disease in SIV-infected macaques treated with a monoclonal antibody against FasL. Clin Dev Immunol 2007; 2007: 93462.
87. Summers KL, Hock BD, McKenzie JL, Hart DN. Phenotypic characterization of five dendritic cell subsets in human tonsils. Am J Pathol 2001; 159: 285-95.
88. Herbeuval JP, Grivel JC, Boasso A, et al. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type I interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 2005; 106: 3524-31.
89. Hardy AW, Graham DR, Shearer GM, Herbeuval JP. HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-alpha. Proc Natl Acad Sci USA 2007; 104: 17453-8.
90. Ho J, Moir S, Malaspina A, et al. Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proc Natl Acad Sci USA 2006; 103: 19436-41.
91. Geissler RG, Ottmann OG, Kleiner K, et al. Decreased haematopoietic colony growth in long-term bone marrow cultures of HIV-positive patients. Res Virol 1993; 144: 69-73.
92. Marandin A, Katz A, Oksenhendler E, et al. Loss of primitive hematopoietic progenitors in patients with human immunodeficiency virus infection. Blood 1996; 88: 4568-78.
93. Steinberg HN, Crumpacker CS, Chatis PA. In vitro suppression of normal human bone marrow progenitor cells by human immunodeficiency virus. J Virol 1991; 65: 1765-9.
94. Beltz L, Narayan O, Adams RJ, Noga SJ, Donnenberg AD. Recovery of the simian immunodeficiency virus (SIV) and depression of colony formation in in vitro infected progenitor cell-enriched rhesus bone marrow (BM). J Med Primatol 1991; 20: 144-51.
95. Hillyer CD, Lackey DA 3rd, Villinger F, Winton EF, McClure HM, Ansari AA. CD34+ and CFU-GM progenitors are significantly decreased in SIVsmm9 infected rhesus macaques with minimal evidence of direct viral infection by polymerase chain reaction. Am J Hematol 1993; 43: 274-8.
96. Thiebot H, Vaslin B, Derdouch S, et al. Impact of bone marrow hematopoiesis failure on T-cell generation during pathogenic simian immunodeficiency virus infection in macaques. Blood 2005; 105: 2403-9.
97. Moses A, Nelson J, Bagby GC Jr. The influence of human immunodeficiency virus-1 on hematopoiesis. Blood 1998; 91: 1479-95.
98. Shen H, Cheng T, Preffer FI, et al. Intrinsic human immunodeficiency virus type I resistance of hematopoietic stem cells despite coreceptor expression. J Virol 1999; 73: 728-37.
99. Lee CI, Cowan MJ, Kohn DB, Tarantal AF. Simian immunodeficiency virus infection of hematopoietic stem cells and bone marrow stromal cells. J Acquir Immune Defic Syndr 2004; 36: 553-61.