Glutathione depletion is linked with Th2 polarization in mice with a retrovirus-induced immunodeficiency syndrome, murine AIDS: Role of proglutathione molecules as immunotherapeutics

Journal of Virology

Volumn 90, Issue 16, 2016, Pages 7118-7130

  Brundu, Serena ^a   Palma, Linda ^a   Picceri, Giusi Giada ^a   Ligi, Daniela ^a   Orlandi, Chiara ^a   Galluzzi, Luca ^a   Chiarantini, Laura ^a   Casabianca, Anna ^a   Schiavano, Giuditta Fiorella ^a   Santi, Martina ^a   Mannello, Ferdinando ^a   Green, Kathy ^b   Smietana, Michaël ^c   Magnani, Mauro ^a   Fraternale, Alessandra ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ARGINASE 1; CELL PROTEIN; CYSTEINE; CYTOKINE; FIZZ1 PROTEIN; GAMMA INTERFERON; GLUTATHIONE; INTERLEUKIN 12P40; INTERLEUKIN 4; INTERLEUKIN 5; MESSENGER RNA; N (N ACETYL CYSTEINYL)ACETYLCYSTEAMINE; NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG; YM1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL ACTIVATION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DOWN REGULATION; GENE EXPRESSION; GENETIC MARKER; GLUTATHIONE DEPLETION; GLUTATHIONE METABOLISM; IMMUNOREGULATION; IN VITRO STUDY; LYMPH NODE; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; MURINE LEUKEMIA VIRUS; NONHUMAN; OXIDATION REDUCTION STATE; PANCREAS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; TH1 CELL; TH1 TH2 BALANCE; TISSUE LEVEL; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPLICATION; DEFICIENCY; EXPERIMENTAL LEUKEMIA; FEMALE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOGENICITY; PATHOLOGY; RETROVIRUS INFECTION; TH2 CELL; VIROLOGY; VIRUS INFECTION;

ANIMALS; CELLS, CULTURED; CYTOKINES; FEMALE; GLUTATHIONE; LEUKEMIA VIRUS, MURINE; LEUKEMIA, EXPERIMENTAL; LYMPHOCYTE ACTIVATION; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; RETROVIRIDAE INFECTIONS; SPLEEN; TH1 CELLS; TH2 CELLS; TUMOR VIRUS INFECTIONS;

EID: 84982238873     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00603-16     Document Type: Article

References (72)

1. Mosier DE. 1986. Animal models for retrovirus-induced immunodeficiency disease. Immunol Invest 15:233-261. http://dx.doi.org/10.3109 /08820138609026687.
2. Mosier DE, Yetter RA, Morse HC, III. 1985. Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J Exp Med 161:766-784. http://dx.doi.org/10.1084 /jem.161.4.766.
3. Hartley JW, Fredrickson TN, Hartley JW, Yetter RA, Morse HC, III. 1989. Retrovirus-induced murine acquired immunodeficiency syndrome: natural history of infection and differing susceptibility of inbred mouse strains. J Virol 63:1223-1231.
4. Klinken SP, Fredrickson TN, Hartley JW, Yetter RA, Morse HC, III. 1988. Evolution of B cell lineage lymphomas in mice with a retrovirusinduced immunodeficiency syndrome, MAIDS. J Immunol 140:1123- 1131.
5. Cao L, Butler MB, Tan L, Draleau KS, Koh WY. 2012. Murine immunodeficiency virus-induced peripheral neuropathy and associated cytokine responses. J Immunol 189:3724-3733. http://dx.doi.org/10.4049 /jimmunol.1201313.
6. Dias AS, Bester MJ, Britz RF, Apostolides Z. 2006. Animal models used for the evaluation of antiretroviral therapies. Curr HIV Res 4:431-446. http://dx.doi.org/10.2174/157016206778560045.
7. Eiseman JL, Yetter RA, Fredrickson TN, Shapiro SG, MacAuley C, Bilello JA. 1991. Effect of 3=azidothymidine administered in drinking water or by continuous infusion on the development of MAIDS. Antiviral Res 16:307-326. http://dx.doi.org/10.1016/0166-3542(91)90046-T.
8. Palamara AT, Garaci E, Rotilio G, Ciriolo MR, Casabianca A, Fraternale A, Rossi L, Schiavano GF, Chiarantini L, Magnani M. 1996. Inhibition of murine AIDS by reduced glutathione. AIDS Res Hum Retroviruses 12:1373-1381. http://dx.doi.org/10.1089/aid.1996.12.1373.
9. Fraternale A, Casabianca A, Tonelli A, Vallanti G, Chiarantini L, Brandi G, Celeste AG, Magnani M. 2000. Inhibition of murine AIDS by alternate administration of azidothymidine and fludarabine monophosphate. J Acquir Immune Defic Syndr 23:209-220.
10. Fraternale A, Casabianca A, Tonelli A, Chiarantini L, Brandi G, Magnani M. 2001. New drug combinations for the treatment of murine AIDS and macrophage protection. Eur J Clin Invest 31:248-252. http://dx.doi .org/10.1046/j.1365-2362.2001.00806.x.
11. + subset regulation in viral infection. Preferential activation of Th2 cells during progression of retrovirusinduced immunodeficiency in mice. J Immunol 148:182-188.
12. Morawetz RA, Gabriele L, Rizzo LV, Noben-Trauth N, Kühn R, Rajewsky K, Müller W, Doherty TM, Finkelman F, Coffman RL, Morse HC, III. 1996. Interleukin (IL)-4-independent immunoglobulin class switch to immunoglobulin (Ig)E in the mouse. J Exp Med 184:1651-1661. http://dx.doi.org/10.1084/jem.184.5.1651.
13. Morse HC, III, McCarty T, Giese NA, Taddesse-Heath L, Grusby MJ. 1999. STAT6-deficient mice exhibit normal induction of murine AIDS and expression of immunoglobulin E following infection with LP-BM5 murine leukemia viruses. J Virol 73:7093-7095.
14. Morawetz RA, Doherty TM, Giese NA, Hartley JW, Müller W, Kühn R, Rajewsky K, Coffman R, Morse HC, III. 1994. Resistance to murine acquired immunodeficiency syndrome (MAIDS). Science 265:264-266.
15. Sher A, Gazzinelli RT, Oswald IP, Clerici M, Kullberg M, Pearce EJ, Berzofsky JA, Mosmann TR, James SL, Morse HC, III. 1992. Role of T-cell derived cytokines in the downregulation of immune responses in parasitic and retroviral infection. Immunol Rev 127:183-204. http://dx .doi.org/10.1111/j.1600-065X.1992.tb01414.x.
16. Desmedt M, Rotiers P, Dooms H, Fiers W, Grooten J. 1998. Macrophages induce cellular immunity by activating Th1 cell responses and suppressing Th2 cell responses. J Immunol 160:5300-5308.
17. Dobashi K, Aihara M, Araki T, Shimizu Y, Utsugi M, Iizuka K, Murata Y, Hamuro J, Nakazawa T, Mori M. 2001. Regulation of LPS induced IL-12 production by IFN-γ and IL-4 through intracellular glutathione status in human alveolar macrophages. Clin Exp Immunol 124:290-296. http://dx.doi.org/10.1046/j.1365-2249.2001.01535.x.
18. Peterson JD, Herzenberg LA, Vasquez K, Waltenbaugh C. 1998. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc Natl Acad SciUSA95:3071-3076. http://dx.doi.org /10.1073/pnas.95.6.3071.
19. Romagnani S. 2000. T-cell subsets (Th1 versus Th2). Ann Allergy Asthma Immunol 85:9-18. http://dx.doi.org/10.1016/S1081-1206(10)62426-X.
20. Becker Y. 2004. The changes in the T helper 1 (Th1) and T helper 2 (Th2) cytokine balance during HIV-1 infection are indicative of an allergic response to viral proteins that may be reversed by Th2 cytokine inhibitors and immune response modifiers-a review and hypothesis. Virus Genes 28:5-18. http://dx.doi.org/10.1023/B:VIRU.0000012260.32578.72.
21. Dwivedi VP, Bhattacharya D, Chatterjee S, Prasad DV, Chattopadhyay D, Van Kaer L, Bishai WR, Das G. 2012. Mycobacterium tuberculosis directs T helper 2 cell differentiation by inducing interleukin-1β production in dendritic cells. J Biol Chem 287:33656-33663. http://dx.doi.org/10 .1074/jbc.M112.375154.
22. Piedrafita D, Proudfoot L, Nikolaev AV, Xu D, Sands W, Feng GJ, Thomas E, Brewer J, Ferguson MA, Alexander J, Liew FY. 1999. Regulation of macrophage IL-12 synthesis by Leishmania phosphoglycans. Eur J Immunol 29:235-244.
23. Venketaraman V, Millman A, Salman M, Swaminathan S, Goetz M, Lardizabal A, Hom D, Connell ND. 2008. Glutathione levels and immune responses in tuberculosis patients. Microb Pathog 44:255-261. http: //dx.doi.org/10.1016/j.micpath.2007.09.002.
24. Helbling B, von Overbeck J, Lauterburg BH. 1996. Decreased release of glutathione into the systemic circulation of patients with HIV infection. Eur J Clin Invest 26:38-44. http://dx.doi.org/10.1046/j.1365-2362.1996 .88237.x.
25. Morris D, Ly J, Chi PT, Daliva J, Nguyen T, Soofer C, Chen YC, Lagman M, Venketaraman V. 2014. Glutathione synthesis is compromised in erythrocytes from individuals with HIV. Front Pharmacol 5:73. http://dx.doi.org/10.3389/fphar.2014.00073.
26. Herzenberg LA, De Rosa SC, Dubs JG, Roederer M, Anderson MT, Ela SW, Deresinski SC, Herzenberg LA. 1997. Glutathione deficiency is associated with impaired survival in HIV disease. Proc Natl Acad SciUSA 94:1967-1972. http://dx.doi.org/10.1073/pnas.94.5.1967.
27. + T cells are required for development of a murine retrovirus-induced immunodeficiency syndrome (MAIDS). J Exp Med 168:623-635. http://dx.doi.org/10.1084/jem.168.2.623.
28. Kawauchi Y, Suzuki K, Watanabe S, Yamagiwa S, Yoneyama H, Han GD, Palaniyandi SS, Veeraveedu PT, Watanabe K, Kawachi H, Okada Y, Shimizu F, Asakura H, Aoyagi Y, Narumi S. 2006. Role of IP-10/ CXCL10 in the progression of pancreatitis-like injury in mice after murine retroviral infection. Am J Physiol Gastrointest Liver Physiol 291:G345- G354. http://dx.doi.org/10.1152/ajpgi.00002.2006.
29. Kustova Y, Espey MG, Sung EG, Morse D, Sei Y, Basile AS. 1998. Evidence of neuronal degeneration in C57B1/6 mice infected with the LP-BM5 leukemia retrovirus mixture. Mol Chem Neuropathol 35:39-59. http://dx.doi.org/10.1007/BF02815115.
30. Sei Y, Arora PK, Skolnick P, Paul IA. 1992. Spatial learning impairment in a murine model of AIDS. FASEB J 6:3008-3013.
31. Sei Y, Kustova Y, Li Y, Morse HC, III, Skolnick P, Basile AS. 1998. The encephalopathy associated with murine acquired immunodeficiency syndrome. Ann N Y Acad Sci 840:822-834. http://dx.doi.org/10.1111/j.1749 -6632.1998.tb09620.x.
32. Fraternale A, Brundu S, Magnani M. 2015. Polarization and repolarization of macrophages. J Clin Cell Immunol 6:319.
33. Donnelly S, O'Neill SM, Sekiya M, Mulcahy G, Dalton JP. 2005. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 73:166-173. http://dx.doi .org/10.1128/IAI.73.1.166-173.2005.
34. Raes G, De Baetselier P, Noël W, Beschin A, Brombacher F, Hassanzadeh Gh G. 2002. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol 71:597-602.
35. Chang NC, Hung SI, Hwa KY, Kato I, Chen JE, Liu CH, Chang AC. 2001. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J Biol Chem 276:17497-17506. http: //dx.doi.org/10.1074/jbc.M010417200.
36. Oiry J, Mialocq P, Puy JY, Fretier P, Dereuddre-Bosquet N, Dormont D, Imbach JL, Clayette P. 2004. Synthesis and biological evaluation in human monocyte-derived macrophages of N-(N-acetyl-L-cysteinyl)-Sacetylcysteamine analogues with potent antioxidant and anti-HIV activities. J Med Chem 47:1789-1795. http://dx.doi.org/10.1021/jm030374d.
37. Fraternale A, Paoletti MF, Casabianca A, Orlandi C, Schiavano GF, Chiarantini L, Clayette P, Oiry J, Vogel J-U, Cinatl J, Jr, Magnani M. 2008. Inhibition of murine AIDS by pro-glutathione (GSH) molecules. Antiviral Res 77:120-127. http://dx.doi.org/10.1016/j.antiviral.2007.11 .004.
38. Fraternale A, Paoletti MF, Dominici S, Caputo A, Castaldello A, Millo E, Brocca-Cofano E, Smietana M, Clayette P, Oiry J, Benatti U, Magnani M. 2010. The increase in intra-macrophage thiols induced by new pro-GSH molecules directs the Th1 skewing in ovalbumin immunized mice. Vaccine 28:7676-7682. http://dx.doi.org/10.1016/j.vaccine.2010.09 .033.
39. Fraternale A, Paoletti MF, Dominici S, Buondelmonte C, Caputo A, Castaldello A, Tripiciano A, Cafaro A, Palamara AT, Sgarbanti R, Garaci E, Ensoli B, Magnani M. 2011. Modulation of Th1/Th2 immune responses to HIV-1 Tat by new pro-GSH molecules. Vaccine 29:6823-6829. http://dx.doi.org/10.1016/j.vaccine.2011.07.101.
40. Nucci C, Palamara AT, Ciriolo MR, Nencioni L, Savini P, D'Agostini C, Rotilio G, Cerulli L, Garaci E. 2000. Imbalance in corneal redox state during herpes simplex virus 1-induced keratitis in rabbits. Effectiveness of exogenous glutathione supply. Exp Eye Res 70:215-220.
41. Buhl R, Jaffe HA, Holroyd KJ, Wells FB, Mastrangeli A, Saltini C, Cantin AM, Crystal RG. 1989. Systemic glutathione deficiency in symptom- free HIV-seropositive individuals. Lancet ii:1294-1298.
42. Ciriolo MR, Palamara AT, Incerpi S, Lafavia E, Buè MC, De Vito P, Garaci E, Rotilio G. 1997. Loss of GSH, oxidative stress, and decrease of intracellular pH as sequential steps in viral infection. J Biol Chem 272: 2700-2708. http://dx.doi.org/10.1074/jbc.272.5.2700.
43. Price TO, Ercal N, Nakaoke R, Banks WA. 2005. HIV-1 viral proteins gp 120 and Tat induce oxidative stress in brain endothelial cells. Brain Res 1045:57-63. http://dx.doi.org/10.1016/j.brainres.2005.03.031.
44. Okuda M, Li K, Beard MR, Showalter LA, Scholle F, Lemon SM, Weinman SA. 2002. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 122:366-375. http://dx.doi.org/10.1053/gast.2002.30983.
45. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
46. Brundu S, Nencioni L, Celestino I, Coluccio P, Palamara AT, Magnani M, Fraternale A. 2016. Validation of a reversed-phase high performance liquid chromatography method for the simultaneous analysis of cysteine and reduced glutathione in mouse organs. Oxid Med Cell Longev 2016:1746985. http://dx.doi.org/10.1155/2016/1746985.
47. Fraternale A, Crinelli R, Casabianca A, Paoletti MF, Orlandi C, Carloni E, Smietana M, Palamara AT, Magnani M. 2013. Molecules altering the intracellular thiol content modulate NF- B and STAT-1/IRF-1 signalling pathways and IL-12 p40 and IL-27 p28 production in murine macrophages. PLoS One 8:e57866. http://dx.doi.org/10.1371/journal.pone .0057866.
48. Fiorani M, De Sanctis R, Menghinello P, Cucchiarini L, Cellini B, Dachà M. 2001. Quercetin prevents glutathione depletion induced by dehydroascorbic acid in rabbit red blood cells. Free Radic Res 34:639-648. http://dx.doi.org/10.1080/10715760100300531.
49. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, p E3-E4, 2nd ed, vol 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
50. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093 /nar/29.9.e45.
51. Casabianca A, Orlandi C, Fraternale A, Magnani M. 2004. Development of a real-time PCR assay using SYBR green I for provirus load quantification in a murine model of AIDS. J Clin Microbiol 42:4361-4364. http://dx .doi.org/10.1128/JCM.42.9.4361-4364.2004.
52. Beck MA, Handy J, Levander OA. 2000. The role of oxidative stress in viral infections. Ann N Y Acad Sci 917:906-912.
53. Palamara AT, Perno CF, Ciriolo MR, Dini L, Balestra E, D'Agostini C, Di Francesco P, Favalli C, Rotilio G, Garaci E. 1995. Evidence for antiviral activity of glutathione: in vitro inhibition of herpes simplex virus type 1 replication. Antiviral Res 27:237-253. http://dx.doi.org/10.1016 /0166-3542(95)00008-A.
54. Staal FJ, Roederer M, Herzenberg LA, Herzenberg LA. 1990. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci U S A 87:9943-9947. http://dx.doi.org/10.1073/pnas.87.24.9943.
55. Löhr JM, Faissner R, Koczan D, Bewerunge P, Bassi C, Brors B, Eils R, Frulloni L, Funk A, Halangk W, Jesenofsky R, Kaderali L, Kleeff J, Krüger B, Lerch MM, Lösel R, Magnani M, Neumaier M, Nittka S, Sahin-Tóth M, Sänger J, Serafini S, Schnölzer M, Thierse HJ, Wandschneider S, Zamboni G, Klöppel G. 2010. Autoantibodies against the exocrine pancreas in autoimmune pancreatitis: gene and protein expression profiling and immunoassays identify pancreatic enzymes as a major target of the inflammatory process. Am J Gastroenterol 105:2060-2071. http://dx.doi.org/10.1038/ajg.2010.141.
56. Saharan S, Mandal PK. 2014. The emerging role of glutathione in Alzheimer's disease. J Alzheimers Dis 40:519-529. http://dx.doi.org/10.3233 /JAD-132483.
57. Zeevalk GD, Manzino L, Sonsalla PK, Bernard LP. 2007. Characterization of intracellular elevation of glutathione (GSH) with glutathione monoethyl ester and GSH in brain and neuronal cultures: relevance to Parkinson's disease. Exp Neurol 203:512-520. http://dx.doi.org/10.1016/j .expneurol.2006.09.004.
58. O'Garra A, McEvoy LM, Zlotnik A. 1998. T-cell subsets: chemokine receptors guide the way. Curr Biol 8:R646-R649. http://dx.doi.org/10 .1016/S0960-9822(07)00413-7.
59. Fu Q, Schoenhoff FS, Savage WJ, Zhang P, Van Eyk JE. 2010. Multiplex assays for biomarker research and clinical application: translational science coming of age. Proteomics Clin Appl 4:271-284. http://dx.doi.org/10 .1002/prca.200900217.
60. Prabhakar U, Eirikis E, Reddy M, Silvestro E, Spitz S, Pendley C, II, Davis HM, Miller BE. 2004. Validation and comparative analysis of a multiplexed assay for the simultaneous quantitative measurement of Th1/ Th2 cytokines in human serum and human peripheral blood mononuclear cell culture supernatants. J Immunol Methods 291:27-38. http://dx .doi.org/10.1016/j.jim.2004.04.018.
61. Chatila TA. 2004. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol Med 10:493-499. http://dx.doi.org/10.1016/j .molmed.2004.08.004.
62. Cerny A, Hügin AW, Hardy RR, Hayakawa K, Zinkernagel RM, Makino M, Morse HC, III. 1990. B cells are required for induction of T cell abnormalities in a murine retrovirus-induced immunodeficiency syndrome. J Exp Med 171:315-320. http://dx.doi.org/10.1084/jem.171.1.315.
63. Gajewski TF, Pinnas M, Wong T, Fitch FW. 1991. Murine Th1 and Th2 clones proliferate optimally in response to distinct antigen-presenting cell populations. J Immunol 46:1750-1758.
64. Farrar JD, Asnagli H, Murphy KM. 2002. T helper subset development: roles of instruction, selection, and transcription. J Clin Invest 109:431-435. http://dx.doi.org/10.1172/JCI0215093.
65. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166-6173. http://dx.doi.org/10.4049/jimmunol.164.12.6166.
66. Hamza T, Barnett JB, Li B. 2010. Interleukin 12 a key immunoregulatory cytokine in infection applications. Int J Mol Sci 11:789-806. http://dx.doi .org/10.3390/ijms11030789.
67. Koike Y, Hisada T, Utsugi M, Ishizuka T, Shimizu Y, Ono A, Murata Y, Hamuro J, Mori M, Dobashi K. 2007. Glutathione redox regulates airway hyperresponsiveness and airway inflammation in mice. Am J Respir Cell Mol Biol 37:322-329. http://dx.doi.org/10.1165/rcmb.2006-0423OC.
68. Nelson SM, Lei X, Prabhu KS. 2011. Selenium levels affect the IL-4- induced expression of alternative activation markers in murine macrophages. J Nutr 141:1754-1761. http://dx.doi.org/10.3945/jn.111.141176.
69. Green KA, Cook WJ, Green WR. 2013. Myeloid-derived suppressor cells in murine retrovirus-induced AIDS inhibit T- and B-cell responses in vitro that are used to define the immunodeficiency. J Virol 87:2058-2071. http: //dx.doi.org/10.1128/JVI.01547-12.
70. O'Connor MA, Vella JL, Green WR. 2016. Reciprocal relationship of T regulatory cells and monocytic myeloid-derived suppressor cells in LPBM5 murine retrovirus-induced immunodeficiency. J Gen Virol 97:509-522. http://dx.doi.org/10.1099/jgv.0.000260.
71. Green KA, Wang L, Noelle RJ, Green WR. 2015. Selective involvement of the checkpoint regulator VISTA in suppression of B-cell, but not T-cell, responsiveness by monocytic myeloid-derived suppressor cells from mice infected with an immunodeficiency-causing retrovirus. J Virol 89:9693-9698. http://dx.doi.org/10.1128/JVI.00888-15.
72. O'Connor MA, Fu W, Green KA, Green WR. 2015. Subpopulations of M-MDSCs from mice infected by an immunodeficiency-causing retrovirus and their differential suppression of T- vs B-cell responses. Virology 485:263-273. http://dx.doi.org/10.1016/j.virol.2015.07.020.