Type I Interferons Induce T Regulatory 1 Responses and Restrict Humoral Immunity during Experimental Malaria

PLoS Pathogens

Volumn 12, Issue 10, 2016, Pages

  Zander, Ryan A ^a   Guthmiller, Jenna J ^a   Graham, Amy C ^a   Pope, Rosemary L ^a   Burke, Bradly E ^a   Carr, Daniel J J ^a,b   Butler, Noah S ^a,b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; MONOCLONAL ANTIBODY; SULFAMETHOXAZOLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HELPER CELL; HUMORAL IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; MALARIA; MOUSE; NONHUMAN; PARASITE CONTROL; PARASITOSIS; PLASMODIUM YOELII; PROTEIN EXPRESSION; RADIATION CHIMERA; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; VIRUS INFECTION; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNITY, HUMORAL; INTERFERON TYPE I; MALARIA; MICE, INBRED C57BL; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84992698965     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005945     Document Type: Article

References (75)

1. Organization WHWorld Malaria Report 2015. (Geneva: World Health Organization); 2015.
2. Crompton PD, Moebius J, Portugal S, Waisberg M, Hart G, Garver LS, et al. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annual review of immunology. 2014;32:157–87. Epub 2014/03/25. doi: 10.1146/annurev-immunol-032713-12022024655294; PubMed Central PMCID: PMC4075043.
3. Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(15):6958–63. Epub 2010/03/31. doi: 10.1073/pnas.100132310720351286; PubMed Central PMCID: PMC2872454.
4. Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K, What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malaria journal. 2009;8:242. Epub 2009/10/29. doi: 10.1186/1475-2875-8-24219860926; PubMed Central PMCID: PMC2773787.
5. Kinyanjui SM, Conway DJ, Lanar DE, Marsh K, IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malaria journal. 2007;6:82. Epub 2007/06/30. doi: 10.1186/1475-2875-6-8217598897; PubMed Central PMCID: PMC1920526.
6. Langhorne J, Ndungu FM, Sponaas AM, Marsh K, Immunity to malaria: more questions than answers. Nature immunology. 2008;9(7):725–32. Epub 2008/06/20. doi: 10.1038/ni.f.20518563083.
7. Portugal S, Pierce SK, Crompton PD, Young lives lost as B cells falter: what we are learning about antibody responses in malaria. Journal of immunology. 2013;190(7):3039–46. Epub 2013/03/26. doi: 10.4049/jimmunol.120306723526829; PubMed Central PMCID: PMC3608210.
8. Kometani K, Kurosaki T, Differentiation and maintenance of long-lived plasma cells. Current opinion in immunology. 2015;33:64–9. Epub 2015/02/14. doi: 10.1016/j.coi.2015.01.01725677584.
9. Nutt SL, Hodgkin PD, Tarlinton DM, Corcoran LM, The generation of antibody-secreting plasma cells. Nature reviews Immunology. 2015;15(3):160–71. Epub 2015/02/24. doi: 10.1038/nri379525698678.
10. Crotty S, Follicular helper CD4 T cells (TFH). Annual review of immunology. 2011;29:621–63. Epub 2011/02/15. doi: 10.1146/annurev-immunol-031210-10140021314428.
11. Cubas RA, Mudd JC, Savoye AL, Perreau M, van Grevenynghe J, Metcalf T, et al. Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nature medicine. 2013;19(4):494–9. Epub 2013/03/12. doi: 10.1038/nm.310923475201; PubMed Central PMCID: PMC3843317.
12. Yamamoto T, Lynch RM, Gautam R, Matus-Nicodemos R, Schmidt SD, Boswell KL, et al. Quality and quantity of TFH cells are critical for broad antibody development in SHIVAD8 infection. Science translational medicine. 2015;7(298):298ra120. Epub 2015/08/01. doi: 10.1126/scitranslmed.aab396426223303.
13. Butler NS, Kulu DI, The regulation of T follicular helper responses during infection. Current opinion in immunology. 2015;34:68–74. Epub 2015/03/03. doi: 10.1016/j.coi.2015.02.00725726751; PubMed Central PMCID: PMC4444382.
14. Obeng-Adjei N, Portugal S, Tran TM, Yazew TB, Skinner J, Li S, et al. Circulating Th1-Cell-type Tfh Cells that Exhibit Impaired B Cell Help Are Preferentially Activated during Acute Malaria in Children. Cell reports. 2015;13(2):425–39. Epub 2015/10/07. doi: 10.1016/j.celrep.2015.09.00426440897; PubMed Central PMCID: PMC4607674.
15. Zander RA, Obeng-Adjei N, Guthmiller JJ, Kulu DI, Li J, Ongoiba A, et al. PD-1 Co-inhibitory and OX40 Co-stimulatory Crosstalk Regulates Helper T Cell Differentiation and Anti-Plasmodium Humoral Immunity. Cell host & microbe. 2015;17(5):628–41. Epub 2015/04/22. doi: 10.1016/j.chom.2015.03.00725891357; PubMed Central PMCID: PMC4433434.
16. Ryg-Cornejo V, Ioannidis LJ, Ly A, Chiu CY, Tellier J, Hill DL, et al. Severe Malaria Infections Impair Germinal Center Responses by Inhibiting T Follicular Helper Cell Differentiation. Cell reports. 2016;14(1):68–81. Epub 2016/01/05. doi: 10.1016/j.celrep.2015.12.00626725120.
17. Haque A, Best SE, Ammerdorffer A, Desbarrieres L, de Oca MM, Amante FH, et al. Type I interferons suppress CD4(+) T-cell-dependent parasite control during blood-stage Plasmodium infection. European journal of immunology. 2011;41(9):2688–98. Epub 2011/06/16. doi: 10.1002/eji.20114153921674481.
18. Kim CC, Nelson CS, Wilson EB, Hou B, DeFranco AL, DeRisi JL, Splenic red pulp macrophages produce type I interferons as early sentinels of malaria infection but are dispensable for control. PloS one. 2012;7(10):e48126. Epub 2012/11/13. doi: 10.1371/journal.pone.004812623144737; PubMed Central PMCID: PMC3483282.
19. Luty AJ, Perkins DJ, Lell B, Schmidt-Ott R, Lehman LG, Luckner D, et al. Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infection and immunity. 2000;68(7):3909–15. Epub 2000/06/17. doi: 10.1128/IAI.68.7.3909-3915.200010858202; PubMed Central PMCID: PMC101666.
20. Rhodes-Feuillette A, Bellosguardo M, Druilhe P, Ballet JJ, Chousterman S, Canivet M, et al. The interferon compartment of the immune response in human malaria: II. Presence of serum-interferon gamma following the acute attack. Journal of interferon research. 1985;5(1):169–78. Epub 1985/01/01. doi: 10.1089/jir.1985.5.1693921628.
21. Sharma S, DeOliveira RB, Kalantari P, Parroche P, Goutagny N, Jiang Z, et al. Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity. 2011;35(2):194–207. Epub 2011/08/09. doi: 10.1016/j.immuni.2011.05.01621820332; PubMed Central PMCID: PMC3162998.
22. Wu J, Tian L, Yu X, Pattaradilokrat S, Li J, Wang M, et al. Strain-specific innate immune signaling pathways determine malaria parasitemia dynamics and host mortality. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(4):E511–20. Epub 2014/01/30. doi: 10.1073/pnas.131646711124474800; PubMed Central PMCID: PMC3910569.
23. Ray JP, Marshall HD, Laidlaw BJ, Staron MM, Kaech SM, Craft J, Transcription factor STAT3 and type I interferons are corepressive insulators for differentiation of follicular helper and T helper 1 cells. Immunity. 2014;40(3):367–77. Epub 2014/03/19. doi: 10.1016/j.immuni.2014.02.00524631156; PubMed Central PMCID: PMC3992517.
24. Nakayamada S, Poholek AC, Lu KT, Takahashi H, Kato M, Iwata S, et al. Type I IFN induces binding of STAT1 to Bcl6: divergent roles of STAT family transcription factors in the T follicular helper cell genetic program. Journal of immunology. 2014;192(5):2156–66. Epub 2014/02/04. doi: 10.4049/jimmunol.130067524489092; PubMed Central PMCID: PMC3967131.
25. Haque A, Best SE, Montes de Oca M, James KR, Ammerdorffer A, Edwards CL, et al. Type I IFN signaling in CD8- DCs impairs Th1-dependent malaria immunity. The Journal of clinical investigation. 2014;124(6):2483–96. Epub 2014/05/03. doi: 10.1172/JCI7069824789914; PubMed Central PMCID: PMC4038565.
26. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, Heutel JD, et al. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2006;26(11):804–19. Epub 2006/11/23. doi: 10.1089/jir.2006.26.80417115899.
27. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, Welch M, et al. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science. 2013;340(6129):207–11. Epub 2013/04/13. doi: 10.1126/science.123521423580529; PubMed Central PMCID: PMC3640797.
28. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, Cheng G, et al. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science. 2013;340(6129):202–7. Epub 2013/04/13. doi: 10.1126/science.123520823580528; PubMed Central PMCID: PMC3704950.
29. Nagai T, Devergne O, Mueller TF, Perkins DL, van Seventer JM, van Seventer GA, Timing of IFN-beta exposure during human dendritic cell maturation and naive Th cell stimulation has contrasting effects on Th1 subset generation: a role for IFN-beta-mediated regulation of IL-12 family cytokines and IL-18 in naive Th cell differentiation. Journal of immunology. 2003;171(10):5233–43. Epub 2003/11/11. 14607924.
30. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF, Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity. 2001;14(4):461–70. Epub 2001/05/05. doi: 10.1016/S1074-7613(01)00126-111336691.
31. Butler NS, Moebius J, Pewe LL, Traore B, Doumbo OK, Tygrett LT, et al. Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nature immunology. 2012;13(2):188–95. Epub 2011/12/14. doi: 10.1038/ni.218022157630; PubMed Central PMCID: PMC3262959.
32. Butler NS, Schmidt NW, Vaughan AM, Aly AS, Kappe SH, Harty JT, Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell host & microbe. 2011;9(6):451–62. Epub 2011/06/15. doi: 10.1016/j.chom.2011.05.00821669394; PubMed Central PMCID: PMC3117254.
33. Guthmiller JJ, Zander RA, Butler NS, Measurement of the T Cell Response to Preerythrocytic Vaccination in Mice. Methods Mol Biol. 2015;1325:19–37. Epub 2015/10/10. doi: 10.1007/978-1-4939-2815-6_2. 26450376. 26450376
34. McDermott DS, Varga SM, Quantifying antigen-specific CD4 T cells during a viral infection: CD4 T cell responses are larger than we think. Journal of immunology. 2011;187(11):5568–76. Epub 2011/11/02. doi: 10.4049/jimmunol.110210422043009; PubMed Central PMCID: PMC3221938.
35. Schmidt NW, Butler NS, Badovinac VP, Harty JT, Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS pathogens. 2010;6(7):e1000998. Epub 2010/07/27. doi: 10.1371/journal.ppat.100099820657824; PubMed Central PMCID: PMC2904779.
36. Kimura D, Miyakoda M, Kimura K, Honma K, Hara H, Yoshida H, et al. Interleukin-27-Producing CD4(+) T Cells Regulate Protective Immunity during Malaria Parasite Infection. Immunity. 2016;44(3):672–82. Epub 2016/03/13. doi: 10.1016/j.immuni.2016.02.01126968425.
37. Stone EL, Pepper M, Katayama CD, Kerdiles YM, Lai CY, Emslie E, et al. ICOS coreceptor signaling inactivates the transcription factor FOXO1 to promote Tfh cell differentiation. Immunity. 2015;42(2):239–51. Epub 2015/02/19. doi: 10.1016/j.immuni.2015.01.01725692700; PubMed Central PMCID: PMC4334393.
38. Leavenworth JW, Verbinnen B, Yin J, Huang H, Cantor H, A p85alpha-osteopontin axis couples the receptor ICOS to sustained Bcl-6 expression by follicular helper and regulatory T cells. Nature immunology. 2015;16(1):96–106. Epub 2014/12/02. doi: 10.1038/ni.305025436971; PubMed Central PMCID: PMC4405167.
39. Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, et al. IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS pathogens. 2008;4(2):e1000004. Epub 2008/04/11. doi: 10.1371/journal.ppat.100000418401464; PubMed Central PMCID: PMC2291447.
40. Freitas do Rosario AP, Lamb T, Spence P, Stephens R, Lang A, Roers A, et al. IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. Journal of immunology. 2012;188(3):1178–90. Epub 2011/12/30. doi: 10.4049/jimmunol.110275522205023; PubMed Central PMCID: PMC3272378.
41. Jankovic D, Kullberg MC, Feng CG, Goldszmid RS, Collazo CM, Wilson M, et al. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. The Journal of experimental medicine. 2007;204(2):273–83. Epub 2007/02/07. doi: 10.1084/jem.2006217517283209; PubMed Central PMCID: PMC2118735.
42. Parish IA, Marshall HD, Staron MM, Lang PA, Brustle A, Chen JH, et al. Chronic viral infection promotes sustained Th1-derived immunoregulatory IL-10 via BLIMP-1. The Journal of clinical investigation. 2014;124(8):3455–68. Epub 2014/07/09. doi: 10.1172/JCI6610825003188; PubMed Central PMCID: PMC4109559.
43. Montes de Oca M, Kumar R, de Labastida Rivera F, Amante FH, Sheel M, Faleiro RJ, et al. Blimp-1-Dependent IL-10 Production by Tr1 Cells Regulates TNF-Mediated Tissue Pathology. PLoS pathogens. 2016;12(1):e1005398. Epub 2016/01/15. doi: 10.1371/journal.ppat.100539826765224; PubMed Central PMCID: PMC4713066.
44. Neumann C, Heinrich F, Neumann K, Junghans V, Mashreghi MF, Ahlers J, et al. Role of Blimp-1 in programing Th effector cells into IL-10 producers. The Journal of experimental medicine. 2014;211(9):1807–19. Epub 2014/07/31. doi: 10.1084/jem.2013154825073792; PubMed Central PMCID: PMC4144744.
45. Gagliani N, Magnani CF, Huber S, Gianolini ME, Pala M, Licona-Limon P, et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nature medicine. 2013;19(6):739–46. doi: 10.1038/nm.317923624599.
46. Choi YS, Yang JA, Yusuf I, Johnston RJ, Greenbaum J, Peters B, et al. Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. Journal of immunology. 2013;190(8):4014–26. Epub 2013/03/15. doi: 10.4049/jimmunol.120296323487426; PubMed Central PMCID: PMC3626566.
47. Starbeck-Miller GR, Xue HH, Harty JT, IL-12 and type I interferon prolong the division of activated CD8 T cells by maintaining high-affinity IL-2 signaling in vivo. The Journal of experimental medicine. 2014;211(1):105–20. Epub 2013/12/25. doi: 10.1084/jem.2013090124367005; PubMed Central PMCID: PMC3892973.
48. Ray JP, Staron MM, Shyer JA, Ho PC, Marshall HD, Gray SM, et al. The Interleukin-2-mTORc1 Kinase Axis Defines the Signaling, Differentiation, and Metabolism of T Helper 1 and Follicular B Helper T Cells. Immunity. 2015;43(4):690–702. Epub 2015/09/28. doi: 10.1016/j.immuni.2015.08.01726410627; PubMed Central PMCID: PMC4618086.
49. Anderson CF, Oukka M, Kuchroo VJ, Sacks D, CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. The Journal of experimental medicine. 2007;204(2):285–97. Epub 2007/02/07. doi: 10.1084/jem.2006188617283207; PubMed Central PMCID: PMC2118728.
50. Aucan C, Walley AJ, Hennig BJ, Fitness J, Frodsham A, Zhang L, et al. Interferon-alpha receptor-1 (IFNAR1) variants are associated with protection against cerebral malaria in the Gambia. Genes and immunity. 2003;4(4):275–82. Epub 2003/05/23. doi: 10.1038/sj.gene.636396212761564.
51. Ball EA, Sambo MR, Martins M, Trovoada MJ, Benchimol C, Costa J, et al. IFNAR1 controls progression to cerebral malaria in children and CD8+ T cell brain pathology in Plasmodium berghei-infected mice. Journal of immunology. 2013;190(10):5118–27. Epub 2013/04/16. doi: 10.4049/jimmunol.130011423585679.
52. Palomo J, Fauconnier M, Coquard L, Gilles M, Meme S, Szeremeta F, et al. Type I interferons contribute to experimental cerebral malaria development in response to sporozoite or blood-stage Plasmodium berghei ANKA. European journal of immunology. 2013;43(10):2683–95. Epub 2013/06/20. doi: 10.1002/eji.20134332723780878.
53. Voisine C, Mastelic B, Sponaas AM, Langhorne J, Classical CD11c+ dendritic cells, not plasmacytoid dendritic cells, induce T cell responses to Plasmodium chabaudi malaria. International journal for parasitology. 2010;40(6):711–9. Epub 2009/12/09. doi: 10.1016/j.ijpara.2009.11.00519968996.
54. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 2009;458(7240):904–8. Epub 2009/02/13. doi: 10.1038/nature0781519212321.
55. Sato T, Onai N, Yoshihara H, Arai F, Suda T, Ohteki T, Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nature medicine. 2009;15(6):696–700. Epub 2009/06/02. doi: 10.1038/nm.197319483695.
56. Ng CT, Sullivan BM, Teijaro JR, Lee AM, Welch M, Rice S, et al. Blockade of interferon Beta, but not interferon alpha, signaling controls persistent viral infection. Cell host & microbe. 2015;17(5):653–61. Epub 2015/05/15. doi: 10.1016/j.chom.2015.04.00525974304; PubMed Central PMCID: PMC4432251.
57. Ryg-Cornejo V, Ly A, Hansen DS, Immunological processes underlying the slow acquisition of humoral immunity to malaria. Parasitology. 2016;143(2):199–207. Epub 2016/01/09. doi: 10.1017/S003118201500170526743747.
58. Yeo CJ, Fearon DT, T-bet-mediated differentiation of the activated CD8+ T cell. European journal of immunology. 2011;41(1):60–6. Epub 2010/12/25. doi: 10.1002/eji.20104087321182077; PubMed Central PMCID: PMC3130140.
59. Freitas do Rosario AP, Langhorne J, T cell-derived IL-10 and its impact on the regulation of host responses during malaria. International journal for parasitology. 2012;42(6):549–55. Epub 2012/05/03. doi: 10.1016/j.ijpara.2012.03.01022549022.
60. Riley EM, Wahl S, Perkins DJ, Schofield L, Regulating immunity to malaria. Parasite Immunol. 2006;28(1–2):35–49. doi: 10.1111/J.1365-3024.2006.00775.X. WOS:000234982300006. 16438675
61. Awasthi A, Carrier Y, Peron JP, Bettelli E, Kamanaka M, Flavell RA, et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nature immunology. 2007;8(12):1380–9. Epub 2007/11/13. doi: 10.1038/ni154117994022.
62. Fitzgerald DC, Zhang GX, El-Behi M, Fonseca-Kelly Z, Li H, Yu S, et al. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nature immunology. 2007;8(12):1372–9. Epub 2007/11/13. doi: 10.1038/ni154017994023.
63. Stumhofer JS, Silver JS, Laurence A, Porrett PM, Harris TH, Turka LA, et al. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nature immunology. 2007;8(12):1363–71. Epub 2007/11/13. doi: 10.1038/ni153717994025.
64. Pot C, Jin H, Awasthi A, Liu SM, Lai CY, Madan R, et al. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. Journal of immunology. 2009;183(2):797–801. Epub 2009/07/03. doi: 10.4049/jimmunol.090123319570826; PubMed Central PMCID: PMC2768608.
65. Villegas-Mendez A, Shaw TN, Inkson CA, Strangward P, de Souza JB, Couper KN, Parasite-Specific CD4+ IFN-gamma+ IL-10+ T Cells Distribute within Both Lymphoid and Nonlymphoid Compartments and Are Controlled Systemically by Interleukin-27 and ICOS during Blood-Stage Malaria Infection. Infection and immunity. 2015;84(1):34–46. Epub 2015/10/16. doi: 10.1128/IAI.01100-1526459508; PubMed Central PMCID: PMC4693994.
66. Axtell RC, de Jong BA, Boniface K, van der Voort LF, Bhat R, De Sarno P, et al. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nature medicine. 2010;16(4):406–12. Epub 2010/03/30. doi: 10.1038/nm.211020348925; PubMed Central PMCID: PMC3042885.
67. Sun J, Dodd H, Moser EK, Sharma R, Braciale TJ, CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nature immunology. 2011;12(4):327–34. Epub 2011/02/08. doi: 10.1038/ni.199621297642; PubMed Central PMCID: PMC3079402.
68. Bryant VL, Ma CS, Avery DT, Li Y, Good KL, Corcoran LM, et al. Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells. Journal of immunology. 2007;179(12):8180–90. Epub 2007/12/07. doi: 10.4049/jimmunol.179.12.818018056361.
69. Cai G, Nie X, Zhang W, Wu B, Lin J, Wang H, et al. A regulatory role for IL-10 receptor signaling in development and B cell help of T follicular helper cells in mice. Journal of immunology. 2012;189(3):1294–302. Epub 2012/07/04. doi: 10.4049/jimmunol.110294822753938.
70. Chacon-Salinas R, Limon-Flores AY, Chavez-Blanco AD, Gonzalez-Estrada A, Ullrich SE, Mast cell-derived IL-10 suppresses germinal center formation by affecting T follicular helper cell function. Journal of immunology. 2011;186(1):25–31. Epub 2010/11/26. doi: 10.4049/jimmunol.100165721098222; PubMed Central PMCID: PMC3059502.
71. Rousset F, Garcia E, Defrance T, Peronne C, Vezzio N, Hsu DH, et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proceedings of the National Academy of Sciences of the United States of America. 1992;89(5):1890–3. Epub 1992/03/01. doi: 10.1073/pnas.89.5.18901371884; PubMed Central PMCID: PMC48559.
72. Sun K, Torres L, Metzger DW, A detrimental effect of interleukin-10 on protective pulmonary humoral immunity during primary influenza A virus infection. Journal of virology. 2010;84(10):5007–14. Epub 2010/03/05. doi: 10.1128/JVI.02408-0920200252; PubMed Central PMCID: PMC2863832.
73. Jagannathan P, Eccles-James I, Bowen K, Nankya F, Auma A, Wamala S, et al. IFNgamma/IL-10 co-producing cells dominate the CD4 response to malaria in highly exposed children. PLoS pathogens. 2014;10(1):e1003864. Epub 2014/01/15. doi: 10.1371/journal.ppat.100386424415936; PubMed Central PMCID: PMC3887092.
74. Saraiva M, O'Garra A, The regulation of IL-10 production by immune cells. Nature reviews Immunology. 2010;10(3):170–81. Epub 2010/02/16. doi: 10.1038/nri271120154735.
75. Malleret B, Claser C, Ong AS, Suwanarusk R, Sriprawat K, Howland SW, et al. A rapid and robust tri-color flow cytometry assay for monitoring malaria parasite development. Scientific reports. 2011;1:118. Epub 2012/02/23. doi: 10.1038/srep0011822355635; PubMed Central PMCID: PMC3216599.