Different regulatory mechanisms in protozoan parasitic infections

International Journal for Parasitology

Volumn 43, Issue 6, 2013, Pages 417-425

  Kling, Jessica C ^a   Körner, Heinrich ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Alternatively activated macrophages; Arginase 1; INOS; Leishmania; Plasmodium; Regulatory T cells; Trypanosoma

Indexed keywords

ARGINASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 2; LEISHMANIA VACCINE; MALARIA VACCINE; NITRIC OXIDE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRYPANOSOMA VACCINE;

IMMUNE RESPONSE; PARASITE; PARASITIC DISEASE; PATHOGEN; PROTOZOAN;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; CYTOKINE PRODUCTION; HOST PARASITE INTERACTION; HUMAN; IMMUNE DEFICIENCY; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; LEISHMANIA; LEISHMANIASIS; MACROPHAGE ACTIVATION; MALARIA; NONHUMAN; PLASMODIUM; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; REVIEW; SUPPRESSOR CELL; TRYPANOSOMA; TRYPANOSOMIASIS; ZOONOSIS;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; LEISHMANIA; PARASITIC DISEASES; PLASMODIUM; TRYPANOSOMA;

PROTOZOA; TRYPANOSOMA;

EID: 84876314257     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.02.001     Document Type: Review

References (110)

1. + regulatory T cells and limited effect of T cell-derived IL-10 on pathogen clearance during Plasmodium yoelii infection. J. Immunol. 2012, 188:5467-5477.
2. Agnandji S.T., Lell B., Soulanoudjingar S.S., Fernandes J.F., Abossolo B.P., Conzelmann C., Methogo B.G., Doucka Y., Flamen A., Mordmuller B., Issifou S., Kremsner P.G., Sacarlal J., Aide P., Lanaspa M., Aponte J.J., Nhamuave A., Quelhas D., Bassat Q., Mandjate S., Macete E., Alonso P., Abdulla S., Salim N., Juma O., Shomari M., Shubis K., Machera F., Hamad A.S., Minja R., Mtoro A., Sykes A., Ahmed S., Urassa A.M., Ali A.M., Mwangoka G., Tanner M., Tinto H., D'Alessandro U., Sorgho H., Valea I., Tahita M.C., Kabore W., Ouedraogo S., Sandrine Y., Guiguemde R.T., Ouedraogo J.B., Hamel M.J., Kariuki S., Odero C., Oneko M., Otieno K., Awino N., Omoto J., Williamson J., Muturi-Kioi V., Laserson K.F., Slutsker L., Otieno W., Otieno L., Nekoye O., Gondi S., Otieno A., Ogutu B., Wasuna R., Owira V., Jones D., Onyango A.A., Njuguna P., Chilengi R., Akoo P., Kerubo C., Gitaka J., Maingi C., Lang T., Olotu A., Tsofa B., Bejon P., Peshu N., Marsh K., Owusu-Agyei S., Asante K.P., Osei-Kwakye K., Boahen O., Ayamba S., Kayan K., Owusu-Ofori R., Dosoo D., Asante I., Adjei G., Chandramohan D., Greenwood B., Lusingu J., Gesase S., Malabeja A., Abdul O., Kilavo H., Mahende C., Liheluka E., Lemnge M., Theander T., Drakeley C., Ansong D., Agbenyega T., Adjei S., Boateng H.O., Rettig T., Bawa J., Sylverken J., Sambian D., Agyekum A., Owusu L., Martinson F., Hoffman I., Mvalo T., Kamthunzi P., Nkomo R., Msika A., Jumbe A., Chome N., Nyakuipa D., Chintedza J., Ballou W.R., Bruls M., Cohen J., Guerra Y., Jongert E., Lapierre D., Leach A., Lievens M., Ofori-Anyinam O., Vekemans J., Carter T., Leboulleux D., Loucq C., Radford A., Savarese B., Schellenberg D., Sillman M., Vansadia P. First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. N. Engl. J. Med. 2011, 365:1863-1875.
3. Agnandji S.T., Lell B., Fernandes J.F., Abossolo B.P., Methogo B.G., Kabwende A.L., Adegnika A.A., Mordmuller B., Issifou S., Kremsner P.G., Sacarlal J., Aide P., Lanaspa M., Aponte J.J., Machevo S., Acacio S., Bulo H., Sigauque B., Macete E., Alonso P., Abdulla S., Salim N., Minja R., Mpina M., Ahmed S., Ali A.M., Mtoro A.T., Hamad A.S., Mutani P., Tanner M., Tinto H., D'Alessandro U., Sorgho H., Valea I., Bihoun B., Guiraud I., Kabore B., Sombie O., Guiguemde R.T., Ouedraogo J.B., Hamel M.J., Kariuki S., Oneko M., Odero C., Otieno K., Awino N., McMorrow M., Muturi-Kioi V., Laserson K.F., Slutsker L., Otieno W., Otieno L., Otsyula N., Gondi S., Otieno A., Owira V., Oguk E., Odongo G., Woods J.B., Ogutu B., Njuguna P., Chilengi R., Akoo P., Kerubo C., Maingi C., Lang T., Olotu A., Bejon P., Marsh K., Mwambingu G., Owusu-Agyei S., Asante K.P., Osei-Kwakye K., Boahen O., Dosoo D., Asante I., Adjei G., Kwara E., Chandramohan D., Greenwood B., Lusingu J., Gesase S., Malabeja A., Abdul O., Mahende C., Liheluka E., Malle L., Lemnge M., Theander T.G., Drakeley C., Ansong D., Agbenyega T., Adjei S., Boateng H.O., Rettig T., Bawa J., Sylverken J., Sambian D., Sarfo A., Agyekum A., Martinson F., Hoffman I., Mvalo T., Kamthunzi P., Nkomo R., Tembo T., Tegha G., Tsidya M., Kilembe J., Chawinga C., Ballou W.R., Cohen J., Guerra Y., Jongert E., Lapierre D., Leach A., Lievens M., Ofori-Anyinam O., Olivier A., Vekemans J., Carter T., Kaslow D., Leboulleux D., Loucq C., Radford A., Savarese B., Schellenberg D., Sillman M., Vansadia P. A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. N. Engl. J. Med. 2012, 367:2284-2295.
4. Alarcon J.B., Waine G.W., McManus D.P. DNA vaccines: technology and application as anti-parasite and anti-microbial agents. Adv. Parasitol. 1999, 42:343-410.
5. - Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 2007, 204:285-297.
6. Auffray C., Sieweke M.H., Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009, 27:669-692.
7. Barrett M.P., Burchmore R.J.S., Stich A., Lazzari J.O., Frasch A.C., Cazzulo J.J., Krishna S. The trypanosomiases. Lancet 2003, 362:1469-1480.
8. + T cells for IL-2 and exploit it for the induction of IL-10 production. Int. Immunol. 2005, 17:279-288.
9. Belkaid Y., Hoffmann K.F., Mendez S., Kamhawi S., Udey M.C., Wynn T.A., Sacks D.L. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 2001, 194:1497-1506.
10. + regulatory T cells control Leishmania major persistence and immunity. Nature 2002, 420:502-507.
11. Beschin A., Brys L., Magez S., Radwanska M., De Baetselier P. Trypanosoma brucei infection elicits nitric oxide-dependent and nitric oxide-independent suppressive mechanisms. J. Leukoc. Biol. 1998, 63:429-439.
12. Bhatia V., Garg N. Current status and future prospects for a vaccine against American trypanosomiasis. Expert Rev. Vaccines 2005, 4:867-880.
13. Borowy N.K., Sternberg J.M., Schreiber D., Nonnengasser C., Overath P. Suppressive macrophages occurring in murine Trypanosoma brucei infection inhibit T-cell responses in vivo and in vitro. Parasite Immunol. 1990, 12:233-246.
14. + regulatory T cells. Nat. Rev. Immunol. 2011, 11:119-130.
15. Cazorla S.I., Frank F.M., Malchiodi E.L. Vaccination approaches against Trypanosoma cruzi infection. Expert Rev. Vaccines 2009, 8:921-935.
16. Chaudhry A., Samstein R.M., Treuting P., Liang Y., Pils M.C., Heinrich J.-M., Jack R.S., Wunderlich F.T., Brüning J.C., Müller W., Rudensky A. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 2011, 34:566-578.
17. Coler R.N., Reed S.G. Second-generation vaccines against leishmaniasis. Trends Parasitol. 2005, 21:244-249.
18. Conrad S.M., Strauss-Ayali D., Field A.E., Mack M., Mosser D.M. Leishmania-derived murine monocyte chemoattractant protein 1 enhances the recruitment of a restrictive population of CC chemokine receptor 2-positive macrophages. Infect. Immun. 2007, 75:653-665.
19. + regulatory T cells following anti-CD25 treatment in malaria-infected mice. J. Immunol. 2007, 178:4136-4146.
20. - adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog. 2008, 4:e1000004.
21. Cuervo H., Guerrero N.A., Carbajosa S., Beschin A., De Baetselier P., Gironès N., Fresno M. Myeloid-derived suppressor cells infiltrate the heart in acute Trypanosoma cruzi infection. J. Immunol. 2011, 187:2656-2665.
22. + regulatory T cells: more of the same or a division of labor?. Immunity 2009, 30:626-635.
23. + cells in chagasic patients with and without megacolon. Hum. Immunol. 2009, 70:65-67.
24. Diefenbach A., Schindler H., Donhauser N., Lorenz E., Laskay T., MacMicking J., Röllinghoff M., Gresser I., Bogdan C. Type 1 interferon (IFNα/β) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 1998, 8:77-87.
25. Ding L., Shevach E.M. IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function. J. Immunol. 1992, 148:3133-3139.
26. Dowling D.P., Ilies M., Olszewski K.L., Portugal S., Mota M.M., Llinás M., Christianson D.W. Crystal structure of arginase from Plasmodium falciparum and implications for l-arginine depletion in malarial infection. Biochemistry 2010, 49:5600-5608.
27. Feltquate D.M., Heaney S., Webster R.G., Robinson H.L. Different T helper cell types and antibody isotypes generated by saline and gene gun DNA immunization. J. Immunol. 1997, 158:2278-2284.
28. + regulatory T cells: differentiation, specification, subphenotypes. Nat. Immunol. 2009, 10:689-695.
29. Finney O.C., Riley E.M., Walther M. Regulatory T cells in malaria - friend or foe?. Trends Immunol. 2010, 31:63-70.
30. Fiorentino D.F., Zlotnik A., Vieira P., Mosmann T.R., Howard M., Moore K.W., O'Garra A. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 1991, 146:3444-3451.
31. + regulatory T cells. Nat. Immunol. 2003, 4:330-336.
32. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
33. Gaur U., Roberts S.C., Dalvi R.P., Corraliza I., Ullman B., Wilson M.E. An effect of parasite-encoded arginase on the outcome of murine cutaneous leishmaniasis. J. Immunol. 2007, 179:8446-8453.
34. Gerber J.S., Mosser D.M. Reversing lipopolysaccharide toxicity by ligating the macrophage Fcγ receptors. J. Immunol. 2001, 166:6861-6868.
35. + immature myeloid suppressor cells. Int. Immunol. 2002, 14:1125-1134.
36. Good M.F., Xu H., Wykes M., Engwerda C.R. Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 2005, 23:69-99.
37. Gordon S., Martinez F.O. Alternative activation of macrophages: mechanism and functions. Immunity 2010, 32:593-604.
38. Gramaglia I., Sobolewski P., Meays D., Contreras R., Nolan J.P., Frangos J.A., Intaglietta M., Van der Heyde H.C. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat. Med. 2006, 12:1417-1422.
39. Guilliams M., Bosschaerts T., Hérin M., Hünig T., Loi P., Flamand V., De Baetselier P., Beschin A. Experimental expansion of the regulatory T cell population increases resistance to African trypanosomiasis. J. Infect. Dis. 2008, 198:781-791.
40. Guilliams M., Oldenhove G., Noel W., Hérin M., Brys L., Loi P., Flamand V., Moser M., De Baetselier P., Beschin A. African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation. J. Immunol. 2007, 179:2748-2757.
41. Gupta S., Snow R., Donnelly C.A., Marsh K., Newbold C. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat. Med. 1999, 5:340-343.
42. Highfill S.L., Rodriguez P.C., Zhou Q., Goetz C.A., Koehn B.H., Veenstra R., Taylor P.A., Panoskaltsis-Mortari A., Serody J.S., Munn D.H., Tolar J., Ochoa A.C., Blazar B.R. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 2010, 116:5738-5747.
43. Hill A.V.S. Vaccines against malaria. Philos. Trans. R. Soc. B 2011, 366:2806-2814.
44. + regulatory T cells. Nat. Med. 2004, 10:29-30.
45. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
46. + immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 2006, 66:1123-1131.
47. ω-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 2001, 193:777-783.
48. Iniesta V., Gómez-Nieto L.C., Molano I., Mohedano A., Carcelén J., Mirón C., Alonso C., Corraliza I. Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol. 2002, 24:113-118.
49. Janeway C.A.J. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today 1992, 13:11-16.
50. Kaye P., Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat. Rev. Microbiol. 2011, 9:604-615.
51. + T regulatory cells. Nat. Immunol. 2003, 4:337-342.
52. + regulatory T cells suppressing Th2-mediated allergic asthma. Proc. Natl. Acad. Sci. 2010, 107:8742-8747.
53. + regulatory T cells have a limited role in the control of Trypanosoma cruzi infection in mice. Infect. Immun. 2007, 75:861-869.
54. Kropf P., Fuentes J.M., Fähnrich E., Arpa L., Herath S., Weber V., Soler G., Celada A., Modolell M., Müller I. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J. 2005, 19:1000-1002.
55. Kropf P., Herath S., Weber V., Modolell M., Müller I. Factors influencing Leishmania major infection in IL-4-deficient BALB/c mice. Parasite Immunol. 2003, 25:439-447.
56. + T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 2004, 172:989-999.
57. + regulatory T cells induces a scurfy-like disease. J. Exp. Med. 2007, 204:57-63.
58. Langhorne J., Ndungu F.M., Sponaas A.-M., Marsh K. Immunity to malaria: more questions than answers. Nat. Immunol. 2008, 9:725-732.
59. Li C., Corraliza I., Langhorne J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect. Immun. 1999, 67:4435-4442.
60. Li C., Seixas E., Langhorne J. Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Med. Microbiol. Immunol. 2001, 189:115-126.
61. Linke A., Kühn R., Müller W., Honarvar N., Li C., Langhorne J. Plasmodium chabaudi chabaudi: differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp. Parasitol. 1996, 84.
62. Longley R., Smith C., Fortin A., Berghout J., McMorran B., Burgio G., Foote S., Gros P. Host resistance to malaria: using mouse models to explore the host response. Mamm. Genome 2011, 22:32-42.
63. Mabbott N.A., Sutherland I.A., Sternberg J.M. Suppressor macrophages in Trypanosoma brucei infection: nitric oxide is related to both suppressive activity and lifespan in vivo. Parasite Immunol. 1995, 17:143-150.
64. Magez S., Caljon G., Tran T., Stijlemans B., Radwanska M. Current status of vaccination against African trypanosomiasis. Parasitology 2010, 137:2017-2027.
65. Mailloux A.W., Sugimori C., Komrokji R.S., Yang L., Maciejewski J.P., Sekeres M.A., Paquette R., Loughran T.P., List A.F., Epling-Burnette P.K. Expansion of effector memory regulatory T cells represents a novel prognostic factor in lower risk myelodysplastic syndrome. J. Immunol. 2012, 189:3198-3208.
66. + T cells in the acute phase of Trypanosoma cruzi infection. Microbes Infect. 2008, 10:825-833.
67. Martin D.L., Tarleton R.L. Antigen-specific T cells maintain an effector memory phenotype during persistent Trypanosoma cruzi infection. J. Immunol. 2005, 174:1594-1601.
68. Mazzoni A., Bronte V., Visintin A., Spitzer J.H., Apolloni E., Serafini P., Zanovello P., Segal D.M. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 2002, 168:689-695.
69. + regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J. Exp. Med. 2004, 200:201-210.
70. Millar A.E., Sternberg J., McSharry C., Wei X.Q., Liew F.Y., Turner C.M.R. T-cell responses during Trypanosoma brucei infection in mice deficient in inducible nitric oxide synthase. Infect. Immun. 1999, 67:3334-3338.
71. Miyara M., Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 2007, 13:108-116.
72. Mosmann T., Coffman R. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 1989, 7:145-173.
73. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
74. Nahrevanian H., Dascombe M.J. Nitric oxide and reactive nitrogen intermediates during lethal and nonlethal strains of murine malaria. Parasite Immunol. 2001, 23:491-501.
75. Noazin S., Khamesipour A., Moulton L.H., Tanner M., Nasseri K., Modabber F., Sharifi I., Khalil E.A.G., Bernal I.D.V., Antunes C.M.F., Smith P.G. Efficacy of killed whole-parasite vaccines in the prevention of leishmaniasis - a meta-analysis. Vaccine 2009, 27:4747-4753.
76. Noël W., Hassanzadeh Gh G., Raes G., Namangala B., Daems I., Brys L., Brombacher F., De Baetselier P., Beschin A. Infection stage-dependent modulation of macrophage activation in Trypanosoma congolense-resistant and -susceptible mice. Infect. Immun. 2002, 70:6180-6187.
77. Okwor I., Uzonna J. Persistent parasites and immunologic memory in cutaneous leishmaniasis: implications for vaccine designs and vaccination strategies. Immunol. Res. 2008, 41:123-136.
78. Okwor I., Uzonna J. Vaccines and vaccination strategies against human cutaneous leishmaniasis. Hum. Vaccines 2009, 5:291-301.
79. Okwor I., Onyilagha C., Kuriakose S., Mou Z., Jia P., Uzonna J. Regulatory T cells enhance susceptibility to experimental Trypanosoma congolense infection independent of mouse genetic background. PLoS Negl. Trop. Dis. 2012, 6:e1761.
80. Olszewski K.L., Morrisey J.M., Wilinski D., Burns J.M., Vaidya A.B., Rabinowitz J.D., Llinás M. Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 2009, 5:191-199.
81. Omer F.M., Riley E.M. Transforming growth factor β production is inversely correlated with severity of murine malaria infection. J. Exp. Med. 1998, 188:39-48.
82. Pereira W.F., Ribeiro-Gomes F.L., Guillermo L.V.C., Vellozo N.S., Montalvão F., DosReis G.A., Lopes M.F. Myeloid-derived suppressor cells help protective immunity to Leishmania major infection despite suppressed T cell responses. J. Leukoc. Biol. 2011, 90:1191-1197.
83. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 1993, 5:1461-1471.
84. Prudêncio M., Rodriguez A., Mota M.M. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat. Rev. Microbiol. 2006, 4:849-856.
85. Ronet C., Torre Y.H., Revaz-Breton M., Mastelic B., Tacchini-Cottier F., Louis J., Launois P. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J. Immunol. 2010, 184:886-894.
86. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995, 155:1151-1164.
87. Sanchez A.M., Zhu J., Huang X., Yang Y. The development and function of memory regulatory T cells after acute viral infections. J. Immunol. 2012, 189.
88. Schleifer K.W., Mansfield J.M. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J. Immunol. 1993, 151:5492-5503.
89. Schmidt E.M., Wang C.J., Ryan G.A., Clough L.E., Qureshi O.S., Goodall M., Abbas A.K., Sharpe A.H., Sansom D.M., Walker L.S.K. CTLA-4 controls regulatory T cell peripheral homeostasis and is required for suppression of pancreatic islet autoimmunity. J. Immunol. 2009, 182:274-282.
90. Schuster J.P., Schaub G.A. Trypanosoma cruzi: skin-penetration kinetics of vector-derived metacyclic trypomastigotes. Int. J. Parasitol. 2000, 30:1475-1479.
91. Scott P., Natovitz P., Coffman R.L., Pearce E., Sher A. Immunoregulation of cutaneous leishmaniasis: T cell lines that transfer protective immunity or exacerbation belong to different T helper subsets and respond to distinct parasite antigens. J. Exp. Med. 1988, 168:1675-1684.
92. Snow R., Omumbo J.A., Lowe B., Molyneux C.S., Obiero J.O., Palmer A., Weber M.W., Pinder M., Nahlen M., Obonyo C., Newbold C., Gupta S., Marsh K. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 1997, 349:1650-1654.
93. Sobolewski P., Gramaglia I., Frangos J.A., Intaglietta M., van der Heyde H. Plasmodium berghei resists killing by reactive oxygen species. Infect. Immun. 2005, 73:6704-6710.
94. + regulatory T cells in the control of experimental cerebral malaria. J. Immunol. 2009, 183:7014-7022.
95. Stephens R., Langhorne J. Effector memory Th1 CD4 T cells are maintained in a mouse model of chronic malaria. PLoS Pathog. 2010, 6:e1001208.
96. Strober S. Natural suppressor (NS) cells, neonatal tolerance, and total lymphoid irradiation: Exploring obscure relationships. Annu. Rev. Immunol. 1984, 2:219-237.
97. Stober C.B., Lange U.G., Roberts M.T.M., Alcami A., Blackwell J.M. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J. Immunol. 2005, 175:2517-2524.
98. Tabbara K.S., Peters N.C., Afrin F., Mendez S., Bertholet S., Belkaid Y., Sacks D.L. Conditions influencing the efficacy of vaccination with live organisms against Leishmania major infection. Infect. Immun. 2005, 73:4714-4722.
99. Takeuchi M., Alard P., Streilein J.W. TGF-β promotes immune deviation by altering accessory signals of antigen-presenting cells. J. Immunol. 1998, 160:1589-1597.
100. Van der Heyde H.C., Gu Y., Zhang Q., Sun G., Grisham M.B. Nitric oxide is neither necessary nor sufficient for resolution of Plasmodium chabaudi malaria in mice. J. Immunol. 2000, 165:3317-3323.
101. Vespa G.N.R., Cunha F.Q., Silva J.S. Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro. Infect. Immun. 1994, 62:5177-5182.
102. high regulatory T lymphocytes. Scand. J. Immunol. 2005, 62:297-308.
103. Walker L.S.K., Abbas A.K. The enemy within: keeping self-reactive T cells at bay in the periphery. Nat. Rev. Immunol. 2002, 2:11-19.
104. + T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009, 5:e1000364.
105. Wang Q.-H., Liu Y.-J., Liu J., Chen G., Zheng W., Wang J.-C., Cao Y.-M. Plasmodium yoelii: assessment of production and role of nitric oxide during the early stages of infection in susceptible and resistant mice. Exp. Parasitol. 2009, 121:268-273.
106. Wei G., Tabel H. Regulatory T cells prevent control of experimental African trypanosomiasis. J. Immunol. 2008, 180:2514-2521.
107. Wellhausen S.R., Mansfield J.M. Lymphocyte function in experimental African trypanosomiasis II. Splenic suppressor cell activity. J. Immunol. 1979, 122:818-824.
108. Yanaba K., Bouaziz J.-D., Matsushita T., Tsubata T., Tedder T.F. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol. 2009, 182:7459-7472.
109. Yazdanbakhsh M., Sacks D. Why does immunity to parasites take so long to develop?. Nat. Rev. Immunol. 2010, 10:80-81.
110. Yeo T.W., Lampah D.A., Gitawati R., Tjitra E., Kenangalem E., McNeil Y.R., Darcy C.J., Granger D.L., Weinberg J.B., Lopansri B.K., Price R.N., Duffull S.B., Celermajer D.S., Anstey N.M. Impaired nitric oxide bioavailability and l-arginine-reversible endothelial dysfunction in adults with falciparum malaria. J. Exp. Med. 2007, 204:2693-2704.