Splenic Damage during SIV Infection: Role of T-Cell Depletion and Macrophage Polarization and Infection

American Journal of Pathology

Volumn 186, Issue 8, 2016, Pages 2068-2087

  Williams, Dionna W ^a   Engle, Elizabeth L ^a   Shirk, Erin N ^a   Queen, Suzanne E ^a   Gama, Lucio ^a   Mankowski, Joseph L ^a   Zink, M Christine ^a   Clements, Janice E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CHEMOKINE RECEPTOR; CHLORDANE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 27;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD3+ T LYMPHOCYTE; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL POPULATION; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MACAQUE MODEL; MACROPHAGE; MONOCYTE; NONHUMAN; PATHOGENESIS; POLARIZATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SPLEEN INJURY; T CELL DEPLETION; T LYMPHOCYTE; TERMINAL DISEASE; UPREGULATION; ANIMAL; DNA MICROARRAY; IMMUNOLOGY; IN SITU HYBRIDIZATION; MACACA NEMESTRINA; PATHOLOGY; SPLEEN;

ANIMALS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA NEMESTRINA; MACROPHAGES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SPLEEN; T-LYMPHOCYTES;

EID: 84990063295     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2016.03.019     Document Type: Article

References (100)

1. 1 Nyberg, M., Suni, J., Haltia, M., Isolation of human immunodeficiency virus (HIV) at autopsy one to six days postmortem. Am J Clin Pathol 94 (1990), 422–425.
2. 2 Diaz, L.K., Murphy, R.L., Phair, J.P., Variakojis, D., The AIDS autopsy spleen: a comparison of the pre-anti-retroviral and highly active anti-retroviral therapy eras. Mod Pathol 15 (2002), 406–412.
3. 3 Jung, A., Maier, R., Vartanian, J.-P., Bocharov, G., Jung, V., Fischer, U., Meese, E., Wain-Hobson, S., Meyerhans, A., Recombination: multiply infected spleen cells in HIV patients. Nature, 418, 2002, 144.
4. 4 Deeks, S.G., Autran, B., Berkhout, B., Benkirane, M., Cairns, S., Chomont, N., Chun, T.-W., Churchill, M., Di Mascio, M., Katlama, C., Towards an HIV cure: a global scientific strategy. Nat Rev Immunol 12 (2012), 607–614.
5. 5 Costiniuk, C.T., Jenabian, M.-A., HIV reservoir dynamics in the face of highly active antiretroviral therapy. AIDS Patient Care STDs 29 (2015), 55–68.
6. 6 Di Mascio, M., Srinivasula, S., Bhattacharjee, A., Cheng, L., Martiniova, L., Herscovitch, P., Lertora, J., Kiesewetter, D., Antiretroviral tissue kinetics: in vivo imaging using positron emission tomography. Antimicrob Agents Chemother 53 (2009), 4086–4095.
7. 7 McElrath, M.J., Steinman, R.M., Cohn, Z.A., Latent HIV-1 infection in enriched populations of blood monocytes and T cells from seropositive patients. J Clin Invest, 87, 1991, 27.
8. 8 Doitsh, G., Galloway, N.L.K., Geng, X., Yang, Z., Monroe, K.M., Zepeda, O., Hunt, P.W., Hatano, H., Sowinski, S., Munoz-Arias, I., Greene, W.C., Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505 (2014), 509–514.
9. 9 Okoye, A.A., Picker, L.J., CD4+ T-cell depletion in HIV infection: mechanisms of immunological failure. Immunol Rev 254 (2013), 54–64.
10. 10 Doitsh, G., Cavrois, M., Lassen, K.G., Zepeda, O., Yang, Z., Santiago, M.L., Hebbeler, A.M., Greene, W.C., Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143 (2010), 789–801.
11. 11 Williams, K.C., Burdo, T.H., HIV and SIV infection: the role of cellular restriction and immune responses in viral replication and pathogenesis. APMIS 117 (2009), 400–412.
12. 12 Nie, C., Sato, K., Misawa, N., Kitayama, H., Fujino, H., Hiramatsu, H., Heike, T., Nakahata, T., Tanaka, Y., Ito, M., Koyanagi, Y., Selective infection of CD4+ effector memory T lymphocytes leads to preferential depletion of memory T lymphocytes in R5 HIV-1-infected humanized NOD/SCID/IL-2Rγnull mice. Virology 394 (2009), 64–72.
13. 13 Sun, Z., Denton, P.W., Estes, J.D., Othieno, F.A., Wei, B.L., Wege, A.K., Melkus, M.W., Padgett-Thomas, A., Zupancic, M., Haase, A.T., Intrarectal transmission, systemic infection, and CD4+ T cell depletion in humanized mice infected with HIV-1. J Exp Med 204 (2007), 705–714.
14. 14 Boasso, A., Vaccari, M., Hryniewicz, A., Fuchs, D., Nacsa, J., Cecchinato, V., Andersson, J., Franchini, G., Shearer, G.M., Chougnet, C., Regulatory T-cell markers, indoleamine 2,3-dioxygenase, and virus levels in spleen and gut during progressive simian immunodeficiency virus infection. J Virol 81 (2007), 11593–11603.
15. 15 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 434 (2005), 1093–1097.
16. 16 Haase, A., Population biology of HIV-1 infection: viral and CD4+ T cell demographics and dynamics in lymphatic tissues. Annu Rev Immunol 17 (1999), 625–656.
17. 17 Cheynier, R., Henrichwark, S., Hadida, F., Pelletier, E., Oksenhendler, E., Autran, B., Wain-Hobson, S., HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-specific cytotoxic T lymphocytes. Cell 78 (1994), 373–387.
18. 18 Falk, S., Stutte, H.J., The spleen in HIV infection: morphological evidence of HIV-associated macrophage dysfunction. Res Virol 141 (1990), 161–169.
19. 19 Chun, T.-W., Carruth, L., Finzi, D., Shen, X., DiGiuseppe, J.A., Taylor, H., Hermankova, M., Chadwick, K., Margolick, J., Quinn, T.C., Kuo, Y.H., Brookmeyer, R., Zeiger, M.A., Barditch-Crovo, P., Siliciano, R.F., Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387 (1997), 183–188.
20. 20 Rappaport, J., Volsky, D., Role of the macrophage in HIV-associated neurocognitive disorders and other comorbidities in patients on effective antiretroviral treatment. J Neurovirol 21 (2015), 235–241.
21. 21 Matusali, G., Dereuddre Bosquet, N., Le Tortorec, A., Moreau, M., Satie, A.-P., Mahé, D., Roumaud, P., Bourry, O., Sylla, N., Bernard-Stoecklin, S., Pruvost, A., Le Grand, R., Dejucq-Rainsford, N., Detection of SIV in semen, urethra and male reproductive organs during efficient HAART. J Virol 89 (2015), 5772–5787.
22. 22 Abbas, W., Tariq, M., Iqbal, M., Kumar, A., Herbein, G., Eradication of HIV-1 from the macrophage reservoir: an uncertain goal?. Viruses 7 (2015), 1578–1598.
23. 23 Fischer, T., Wyatt, C.M., D'Agati, V.D., Croul, S., McCourt, L., Morgello, S., Rappaport, J., Mononuclear phagocyte accumulation in visceral tissue in HIV encephalitis: evidence for increased monocyte/macrophage trafficking and altered differentiation. Curr HIV Res, 12, 2014, 201.
24. 24 Hernandez-Vargas, E.A., Middleton, R.H., Modeling the three stages in HIV infection. J Theor Biol 320 (2013), 33–40.
25. 25 Pasternak, A.O., Lukashov, V.V., Berkhout, B., Cell-associated HIV RNA: a dynamic biomarker of viral persistence. Retrovirology, 10, 2013, 41.
26. 26 Wang, T., Xu, Y., Zhu, H., Andrus, T., Ivanov, S.B., Pan, C., Dolores, J., Dann, G.C., Zhou, M., Forte, D., Yang, Z., Holte, S., Corey, L., Zhu, T., Successful isolation of infectious and high titer human monocyte-derived HIV-1 from two subjects with discontinued therapy. PLoS One, 8, 2013, e65071.
27. 27 Kallianpur, K.J., Shikuma, C., Kirk, G.R., Shiramizu, B., Valcour, V., Chow, D., Souza, S., Nakamoto, B., Sailasuta, N., Peripheral blood HIV DNA is associated with atrophy of cerebellar and subcortical gray matter. Neurology 80 (2013), 1792–1799.
28. 28 Cummins, N., Badley, A., Anti-apoptotic mechanisms of HIV: lessons and novel approaches to curing HIV. Cell Mol Life Sci 70 (2012), 3355–3363.
29. 29 Zhu, T., HIV-1 in peripheral blood monocytes: an underrated viral source. J Antimicrob Chemother 50 (2002), 309–311.
30. 30 Meltzer, M.S., Nakamura, M., Hansen, B.D., Turpin, J.A., Kalter, D.C., Gendelman, H.E., Macrophages as susceptible targets for HIV infection, persistent viral reservoirs in tissue, and key immunoregulatory cells that control levels of virus replication and extent of disease. AIDS Res Hum Retroviruses 6 (1990), 967–971.
31. 31 Koenig, S., Gendelman, H.E., Orenstein, J.M., Dal Canto, M., Pezeshkpour, G.H., Yungbluth, M., Janotta, F., Aksamit, A., Martin, M.A., Fauci, A.S., Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233 (1986), 1089–1093.
32. 32 Ho, D.D., Rota, T.R., Hirsch, M.S., Infection of monocyte/macrophages by human T lymphotropic virus type III. J Clin Invest, 77, 1986, 1712.
33. 33 Gartner, S., Markovits, P., Markovitz, D.M., Kaplan, M.H., Gallo, R.C., Popovic, M., The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233 (1986), 215–219.
34. 34 Duncan, C.J., Williams, J.P., Schiffner, T., Gärtner, K., Ochsenbauer, C., Kappes, J., Russell, R.A., Frater, J., Sattentau, Q.J., High-multiplicity HIV-1 infection and neutralizing antibody evasion mediated by the macrophage-T cell virological synapse. J Virol 88 (2014), 2025–2034.
35. 35 Costiniuk, C.T., Jenabian, M.-A., Cell-to-cell transfer of HIV infection: implications for HIV viral persistence. J Gen Virol 95 (2014), 2346–2355.
36. 36 Alexaki, A., Liu, Y., Wigdahl, B., Cellular reservoirs of HIV-1 and their role in viral persistence. Curr HIV Res, 6, 2008, 388.
37. 37 Carr, J., Hocking, H., Li, P., Burrell, C., Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes. Virology 265 (1999), 319–329.
38. 38 Crowe, S.M., Mills, J., Elbeik, T., Lifson, J.D., Kosek, J., Marshall, J.A., Engleman, E.G., McGrath, M.S., Human immunodeficiency virus-infected monocyte-derived macrophages express surface gp120 and fuse with CD4 lymphoid cells in vitro: a possible mechanism of T lymphocyte depletion in vivo. Clin Immunol Immunopathol 65 (1992), 143–151.
39. 39 Crowe, S., Mills, J., Kirihara, J., Boothman, J., Marshall, J., McGrath, M., Full-length recombinant CD4 and recombinant gp120 inhibit fusion between HIV infected macrophages and uninfected CD4-expressing T-lymphoblastoid cells. AIDS Res Hum Retroviruses 6 (1990), 1031–1037.
40. 40 Bronte, V., Pittet Mikael, J., The spleen in local and systemic regulation of immunity. Immunity 39 (2013), 806–818.
41. 41 Davies, L.C., Jenkins, S.J., Allen, J.E., Taylor, P.R., Tissue-resident macrophages. Nat Immunol 14 (2013), 986–995.
42. 42 Cesta, M.F., Normal structure, function, and histology of the spleen. Toxicol Pathol 34 (2006), 455–465.
43. 43 den Haan, J.M., Martinez-Pomares, L., Macrophage heterogeneity in lymphoid tissues. Semin Immunopathol 35 (2013), 541–552.
44. 44 Högger, P., Dreier, J., Droste, A., Buck, F., Sorg, C., Identification of the integral membrane protein RM3/1 on human monocytes as a glucocorticoid-inducible member of the scavenger receptor cysteine-rich family (CD163). J Immunol 161 (1998), 1883–1890.
45. 45 Gordon, S., Homeostasis: a scavenger receptor for haemoglobin. Curr Biol 11 (2001), R399–R401.
46. 46 Holness, C., Simmons, D., Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81 (1993), 1607–1613.
47. 47 Zwadlo, G., Voegeíi, R., Osthoff, K.S., Sorg, C., A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the down-regulatory phase of the inflammatory process. Pathobiology 55 (1987), 295–304.
48. 48 Porcheray, F., Viaud, S., Rimaniol, A.C., Leone, C., Samah, B., Dereuddre-Bosquet, N., Dormont, D., Gras, G., Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol 142 (2005), 481–489.
49. 49 Gordon, S., Plüddemann, A., Martinez Estrada, F., Macrophage heterogeneity in tissues: phenotypic diversity and functions. Immunol Rev 262 (2014), 36–55.
50. 50 Brandtzaeg, P., Flavell, D.J., Fagerhol, M.K., Mac 387 antibody and detection of formalin resistant myelomonocytic L1 antigen. J Clin Pathol 41 (1988), 963–970.
51. 51 Soulas, C., Conerly, C., Kim, W.-K., Burdo, T.H., Alvarez, X., Lackner, A.A., Williams, K.C., Recently infiltrating MAC387+ monocytes/macrophages. Am J Pathol 178 (2011), 2121–2135.
52. 52 Lichtnekert, J., Kawakami, T., Parks, W.C., Duffield, J.S., Changes in macrophage phenotype as the immune response evolves. Curr Opin Pharmacol 13 (2013), 555–564.
53. 53 Committee for the Update of the Guide for the Care and Use of Laboratory Animals, National Research Council. Guide for the Care and Use of Laboratory Animals: Eighth Edition. 2011, National Academies Press, Washington, DC.
54. 54 Zink, M.C., Suryanarayana, K., Mankowski, J.L., Shen, A., Piatak, M., Spelman, J.P., Carter, D.L., Adams, R.J., Lifson, J.D., Clements, J.E., High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 73 (1999), 10480–10488.
55. 55 Zink, M.C., Clements, J.E., A novel simian immunodeficiency virus model that provides insight into mechanisms of human immunodeficiency virus central nervous system disease. J Neurovirol 8 (2002), 42–48.
56. 56 Zink, M.C., Brice, A.K., Kelly, K.M., Queen, S.E., Gama, L., Li, M., Adams, R.J., Bartizal, C., Varrone, J., Rabi, S.A., Graham, D.R., Tarwater, P.M., Mankowski, J.L., Clements, J.E., Simian immunodeficiency virus-infected macaques treated with highly active antiretroviral therapy have reduced central nervous system viral replication and inflammation but persistence of viral DNA. J Infect Dis 202 (2010), 161–170.
57. 57 Dinoso, J.B., Rabi, S.A., Blankson, J.N., Gama, L., Mankowski, J.L., Siliciano, R.F., Zink, M.C., Clements, J.E., A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 83 (2009), 9247–9257.
58. 58 Ravimohan, S., Gama, L., Engle, E.L., Zink, M.C., Clements, J.E., Early emergence and selection of a SIV-LTR C/EBP site variant in SIV-infected macaques that increases virus infectivity. PLoS One, 7, 2012, e42801.
59. 59 Witwer, K.W., Gama, L., Li, M., Bartizal, C.M., Queen, S.E., Varrone, J.J., Brice, A.K., Graham, D.R., Tarwater, P.M., Mankowski, J.L., Zink, M.C., Clements, J.E., Coordinated regulation of SIV replication and immune responses in the CNS. PLoS One, 4, 2009, e8129.
60. 60 Zaritsky, L.A., Gama, L., Clements, J.E., Canonical type I IFN signaling in simian immunodeficiency virus-infected macrophages is disrupted by astrocyte-secreted CCL2. J Immunol 188 (2012), 3876–3885.
61. 61 Carruth, L.M., Christine Zink, M., Tarwater, P.M., Miller, M.D., Li, M., Queen, L.A., Mankowski, J.L., Shen, A., Siliciano, R.F., Clements, J.E., SIV-specific T lymphocyte responses in PBMC and lymphoid tissues of SIV-infected pigtailed macaques during suppressive combination antiretroviral therapy. J Med Primatol 34 (2005), 109–121.
62. 62 Gama, L., Shirk, E.N., Russell, J.N., Carvalho, K.I., Li, M., Queen, S.E., Kalil, J., Zink, M.C., Clements, J.E., Kallas, E.G., Expansion of a subset of CD14highCD16negCCR2low/neg monocytes functionally similar to myeloid-derived suppressor cells during SIV and HIV infection. J Leukoc Biol 91 (2012), 803–816.
63. 63 Shinoda, K., Tokoyoda, K., Hanazawa, A., Hayashizaki, K., Zehentmeier, S., Hosokawa, H., Iwamura, C., Koseki, H., Tumes, D.J., Radbruch, A., Type II membrane protein CD69 regulates the formation of resting T-helper memory. Proc Natl Acad Sci U S A 109 (2012), 7409–7414.
64. 64 Simms, P.E., Ellis, T.M., Utility of flow cytometric detection of CD69 expression as a rapid method for determining poly- and oligoclonal lymphocyte activation. Clin Diagn Lab Immunol 3 (1996), 301–304.
65. 65 Lindsey, W., Lowdell, M., Marti, G., Abbasi, F., Zenger, V., King, K., Lamb, L. Jr., CD69 expression as an index of T-cell function: assay standardization, validation and use in monitoring immune recovery. Cytotherapy 9 (2007), 123–132.
66. 66 Pitcher, C.J., Hagen, S.I., Walker, J.M., Lum, R., Mitchell, B.L., Maino, V.C., Axthelm, M.K., Picker, L.J., Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168 (2002), 29–43.
67. 67 Hosseini, I., Gama, L., Mac Gabhann, F., Multiplexed component analysis to identify genes contributing to the immune response during acute SIV infection. PLoS One, 10, 2015, e0126843.
68. 68 Chakrabarti, L., Isola, P., Cumont, M.-C., Claessens-Maire, M.-A., Hurtrel, M., Montagnier, L., Hurtrel, B., Early stages of simian immunodeficiency virus infection in lymph nodes: evidence for high viral load and successive populations of target cells. Am J Pathol, 144, 1994, 1226.
69. 69 Kumar, A., Abbas, W., Herbein, G., HIV-1 latency in monocytes/macrophages. Viruses 6 (2014), 1837–1860.
70. 70 Le Douce, V., Herbein, G., Rohr, O., Schwartz, C., Molecular mechanisms of HIV-1 persistence in the monocyte-macrophage lineage. Retrovirology, 7, 2010, 32.
71. 71 Buechler, C., Ritter, M., Orso, E., Langmann, T., Klucken, J., Schmitz, G., Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro-and antiinflammatory stimuli. J Leukoc Biol, 67, 2000, 97.
72. 72 Goebeler, M., Roth, J., Teigelkamp, S., Sorg, C., The monoclonal antibody MAC387 detects an epitope on the calcium-binding protein MRP14. J Leukoc Biol 55 (1994), 259–261.
73. 73 Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38 (2013), 79–91.
74. 74 Ito, S., Ansari, P., Sakatsume, M., Dickensheets, H., Vazquez, N., Donnelly, R.P., Larner, A.C., Finbloom, D.S., Interleukin-10inhibits expression of both interferon a– and interferon γ– induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93 (1999), 1456–1463.
75. 75 Wang, X.-F., Wang, H.-S., Wang, H., Zhang, F., Wang, K.-F., Guo, Q., Zhang, G., Cai, S.-H., Du, J., The role of indoleamine 2,3-dioxygenase (IDO) in immune tolerance: focus on macrophage polarization of THP-1 cells. Cell Immunol 289 (2014), 42–48.
76. 76 Martinez, F.O., Gordon, S., The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep, 6, 2014, 13.
77. 77 van der Lans, A.A., Boon, M.R., Haks, M.C., Quinten, E., Schaart, G., Ottenhoff, T.H., van Marken Lichtenbelt, W.D., Cold acclimation affects immune composition in skeletal muscle of healthy lean subjects. Physiol Rep, 3, 2015, e12394.
78. 78 Brown, B.N., Ratner, B.D., Goodman, S.B., Amar, S., Badylak, S.F., Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 33 (2012), 3792–3802.
79. 79 Buckner, C.M., Calderon, T.M., Eugenin, E.A., Carvallo, L., Williams, D., Lopez, L., Belbin, T., Berman, J.W., Characterization of stages of monocyte maturation/differentiation that facilitate their transmigration across the blood brain barrier and infection by HIV: implications for NeuroAIDS. Cell Immunol 267 (2011), 109–123.
80. 80 Williams, D.W., Calderon, T.M., Lopez, L., Carvallo-Torres, L., Gaskill, P.J., Eugenin, E.A., Morgello, S., Berman, J.W., Mechanisms of HIV entry into the CNS: increased sensitivity of HIV infected CD14+CD16+ monocytes to CCL2 and key roles of CCR2, JAM-A, and ALCAM in diapedesis. PLoS One, 8, 2013, e69270.
81. 81 Wang, X., Xu, H., Alvarez, X., Pahar, B., Moroney-Rasmussen, T., Lackner, A.A., Veazey, R.S., Distinct expression patterns of CD69 in mucosal and systemic lymphoid tissues in primary SIV infection of rhesus macaques. PLoS One, 6, 2011, e27207.
82. 82 Otani, I., Mori, K., Sata, T., Terao, K., Doi, K., Akari, H., Yoshikawa, Y., Accumulation of MAC387+ macrophages in paracortical areas of lymph nodes in rhesus monkeys acutely infected with simian immunodeficiency virus. Microbes Infect 1 (1999), 977–985.
83. 83 Lakritz, J.R., Bodair, A., Shah, N., O'Donnell, R., Polydefkis, M.J., Miller, A.D., Burdo, T.H., Monocyte traffic, dorsal root ganglion histopathology, and loss of intraepidermal nerve fiber density in SIV peripheral neuropathy. Am J Pathol 185 (2015), 1912–1923.
84. 84 Fischer-Smith, T., Tedaldi, E.M., Rappaport, J., CD163/CD16 coexpression by circulating monocytes/macrophages in HIV: potential biomarkers for HIV infection and AIDS progression. AIDS Res Hum Retroviruses 24 (2008), 417–421.
85. 85 Williams, D.W., Eugenin, E.A., Calderon, T.M., Berman, J.W., Monocyte maturation, HIV susceptibility, and transmigration across the blood brain barrier are critical in HIV neuropathogenesis. J Leukoc Biol 91 (2012), 401–415.
86. 86 Pretlow, T., Pretlow, T., Analysis and separation of stromal cells infiltrating tumors. Cell Separat Methods Selected Appl, 2, 2014, 63.
87. 87 Pochedly, C.E., Disorders of the Spleen: Pathophysiology and Management. 1989, Taylor & Francis, Abingdon, UK.
88. 88 Connick, E., Folkvord, J.M., Lind, K.T., Rakasz, E.G., Miles, B., Wilson, N.A., Santiago, M.L., Schmitt, K., Stephens, E.B., Kim, H.O., Compartmentalization of simian immunodeficiency virus replication within secondary lymphoid tissues of rhesus macaques is linked to disease stage and inversely related to localization of virus-specific CTL. J Immunol 193 (2014), 5613–5625.
89. 89 Rainho, J.N., Martins, M.A., Cunyat, F., Watkins, I.T., Watkins, D.I., Stevenson, M., Nef is dispensable for resistance of SIV–infected macrophages to CD8+ T cell killing. J Virol 89 (2015), 10625–10636.
90. 90 D'Andrea, A., Aste-Amezaga, M., Valiante, N.M., Ma, X., Kubin, M., Trinchieri, G., Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178 (1993), 1041–1048.
91. 91 Zaritsky, L.A., Dery, A., Leong, W.Y., Gama, L., Clements, J.E., Tissue-specific interferon alpha subtype response to SIV infection in brain, spleen, and lung. J Interferon Cytokine Res 33 (2013), 24–33.
92. 92 Qin, H., Holdbrooks, A.T., Liu, Y., Reynolds, S.L., Yanagisawa, L.L., Benveniste, E.N., SOCS3 deficiency promotes M1 macrophage polarization and inflammation. J Immunol 189 (2012), 3439–3448.
93. 93 Mulder, R., Banete, A., Basta, S., Spleen-derived macrophages are readily polarized into classically activated (M1) or alternatively activated (M2) states. Immunobiology 219 (2014), 737–745.
94. 94 Tuluc, F., Meshki, J., Spitsin, S., Douglas, S.D., HIV infection of macrophages is enhanced in the presence of increased expression of CD163 induced by substance P. J Leukoc Biol 96 (2014), 143–150.
95. 95 Yearley, J.H., Pearson, C., Shannon, R.P., Mansfield, K.G., Phenotypic variation in myocardial macrophage populations suggests a role for macrophage activation in SIV-associated cardiac disease. AIDS Res Hum Retroviruses 23 (2007), 515–524.
96. 96 Nowlin, B.T., Burdo, T.H., Midkiff, C.C., Salemi, M., Alvarez, X., Williams, K.C., SIV encephalitis lesions are composed of CD163+ macrophages present in the central nervous system during early SIV infection and SIV-positive macrophages recruited terminally with AIDS. Am J Pathol 185 (2015), 1649–1665.
97. 97 Cassol, E., Cassetta, L., Rizzi, C., Alfano, M., Poli, G., M1 and M2a polarization of human monocyte-derived macrophages inhibits HIV-1 replication by distinct mechanisms. J Immunol 182 (2009), 6237–6246.
98. 98 Herbein, G., Varin, A., The macrophage in HIV-1 infection: from activation to deactivation. Retrovirology 7 (2010), 1–15.
99. 99 Swirski, F.K., Nahrendorf, M., Etzrodt, M., Wildgruber, M., Cortez-Retamozo, V., Panizzi, P., Figueiredo, J.-L., Kohler, R.H., Chudnovskiy, A., Waterman, P., Aikawa, E., Mempel, T.R., Libby, P., Weissleder, R., Pittet, M.J., Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325 (2009), 612–616.
100. 100 van der Laan, A.M., ter Horst, E.N., Delewi, R., Begieneman, M.P.V., Krijnen, P.A.J., Hirsch, A., Lavaei, M., Nahrendorf, M., Horrevoets, A.J., Niessen, H.W.M., Piek, J.J., Monocyte subset accumulation in the human heart following acute myocardial infarction and the role of the spleen as monocyte reservoir. Eur Heart J 35 (2014), 376–385.