Abortive T Follicular Helper Development Is Associated with a Defective Humoral Response in Leishmania infantum-Infected Macaques

PLoS Pathogens

Volumn 10, Issue 4, 2014, Pages

  Rodrigues, Vasco ^a,b   Laforge, Mireille ^a   Campillo Gimenez, Laure ^a,g   Soundaramourty, Calaiselvy ^a   Correia de Oliveira, Ana ^c,d   Dinis Oliveira, Ricardo Jorge ^c,d,e   Ouaissi, Ali ^b   Cordeiro da Silva, Anabela ^b,e   Silvestre, Ricardo ^b   Estaquier, Jérôme ^a,f  

^a CNRS   (France)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSTITUTO DE INVESTIGAÇÃO E FORMAÇÃO AVANÇADA EM CIÊNCIAS E TECNOLOGIAS DA SAÚDE   (Portugal)

^d PORTUGUESE ONCOLOGY INSTITUTE   (Portugal)

^e UNIVERSITY OF PORTO   (Portugal)

^f LAVAL UNIVERSITY   (Canada)

^g PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; C REACTIVE PROTEIN; CD27 ANTIGEN; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CXCR5; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3D RECEPTOR; COMPLEMENT COMPONENT C4; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 4; KINETOPLAST DNA; L SELECTIN; PROTEIN BCL 6; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR;

ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MATURATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HELPER CELL; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LEISHMANIA INFANTUM; NONHUMAN; PARASITE LOAD; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RHESUS MONKEY; TH1 CELL; TH2 CELL; VISCERAL LEISHMANIASIS; ANIMAL; FEMALE; GENE EXPRESSION REGULATION; GERMINAL CENTER; IMMUNOLOGY; MALE; PARASITOLOGY; PATHOLOGY; SPLEEN;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; GERMINAL CENTER; IMMUNITY, HUMORAL; INTERLEUKIN-10; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; MACACA MULATTA; MALE; PROTO-ONCOGENE PROTEINS C-BCL-6; RECEPTORS, CXCR5; SPLEEN; TH1 CELLS;

EID: 84901321731     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004096     Document Type: Article

References (68)

1. Murray HW, Berman JD, Davies CR, Saravia NG, (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
2. Kaye P, Scott P, (2011) Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 9: 604-615.
3. Nylen S, Sacks D, (2007) Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol 28: 378-384.
4. Banerjee R, Kumar S, Sen A, Mookerjee A, Mukherjee P, et al. (2011) TGF-beta-regulated tyrosine phosphatases induce lymphocyte apoptosis in Leishmania donovani-infected hamsters. Immunol Cell Biol 89: 466-474.
5. Nieto A, Dominguez-Bernal G, Orden JA, De La Fuente R, Madrid-Elena N, et al. (2011) Mechanisms of resistance and susceptibility to experimental visceral leishmaniosis: BALB/c mouse versus syrian hamster model. Vet Res 42: 39.
6. Kenney RT, Sacks DL, Gam AA, Murray HW, Sundar S, (1998) Splenic cytokine responses in Indian kala-azar before and after treatment. J Infect Dis 177: 815-818.
7. Karp CL, el-Safi SH, Wynn TA, Satti MM, Kordofani AM, et al. (1993) In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J Clin Invest 91: 1644-1648.
8. Goto H, Prianti MG, (2009) Immunoactivation and immunopathogeny during active visceral leishmaniasis. Rev Inst Med Trop Sao Paulo 51: 241-246.
9. McCall LI, Zhang WW, Matlashewski G, (2013) Determinants for the development of visceral leishmaniasis disease. PLoS Pathog 9: e1003053.
10. Brenchley JM, Vinton C, Tabb B, Hao XP, Connick E, et al. (2012) Differential infection patterns of CD4+ T cells and lymphoid tissue viral burden distinguish progressive and nonprogressive lentiviral infections. Blood 120: 4172-4181.
11. Hurtrel B, Petit F, Arnoult D, Muller-Trutwin M, Silvestri G, et al. (2005) Apoptosis in SIV infection. Cell Death Differ 12 Suppl 1: 979-990.
12. Micci L, Cervasi B, Ende ZS, Iriele RI, Reyes-Aviles E, et al. (2012) Paucity of IL-21-producing CD4(+) T cells is associated with Th17 cell depletion in SIV infection of rhesus macaques. Blood 120: 3925-3935.
13. Porrozzi R, Pereira MS, Teva A, Volpini AC, Pinto MA, et al. (2006) Leishmania infantum-induced primary and challenge infections in rhesus monkeys (Macaca mulatta): a primate model for visceral leishmaniasis. Trans R Soc Trop Med Hyg 100: 926-937.
14. Grimaldi G Jr, (2008) The utility of rhesus monkey (Macaca mulatta) and other non-human primate models for preclinical testing of Leishmania candidate vaccines. Mem Inst Oswaldo Cruz 103: 629-644.
15. Evans TG, Krug EC, Wilson ME, Vasconcelos AW, de Alencar JE, et al. (1989) Evaluation of antibody responses in American visceral leishmaniasis by ELISA and immunoblot. Mem Inst Oswaldo Cruz 84: 157-166.
16. Smelt SC, Cotterell SE, Engwerda CR, Kaye PM, (2000) B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol 164: 3681-3688.
17. Deak E, Jayakumar A, Cho KW, Goldsmith-Pestana K, Dondji B, et al. (2010) Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. Eur J Immunol 40: 1355-1368.
18. Bankoti R, Gupta K, Levchenko A, Stager S, (2012) Marginal zone B cells regulate antigen-specific T cell responses during infection. J Immunol 188: 3961-3971.
19. Scott P, Natovitz P, Sher A, (1986) B lymphocytes are required for the generation of T cells that mediate healing of cutaneous leishmaniasis. J Immunol 137: 1017-1021.
20. Woelbing F, Kostka SL, Moelle K, Belkaid Y, Sunderkoetter C, et al. (2006) Uptake of Leishmania major by dendritic cells is mediated by Fcgamma receptors and facilitates acquisition of protective immunity. J Exp Med 203: 177-188.
21. Zotos D, Tarlinton DM, (2012) Determining germinal centre B cell fate. Trends Immunol 33: 281-288.
22. Luther SA, Maillard I, Luthi F, Scarpellino L, Diggelmann H, et al. (1997) Early neutralizing antibody response against mouse mammary tumor virus: critical role of viral infection and superantigen-reactive T cells. J Immunol 159: 2807-2814.
23. Ma CS, Deenick EK, Batten M, Tangye SG, (2012) The origins, function, and regulation of T follicular helper cells. J Exp Med 209: 1241-1253.
24. Onabajo OO, George J, Lewis MG, Mattapallil JJ, (2013) Rhesus macaque lymph node PD-1(hi)CD4+ T cells express high levels of CXCR5 and IL-21 and display a CCR7(lo)ICOS+Bcl6+ T-follicular helper (Tfh) cell phenotype. PLoS One 8: e59758.
25. Crotty S, (2011) Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29: 621-663.
26. Montes CL, Acosta-Rodriguez EV, Merino MC, Bermejo DA, Gruppi A, (2007) Polyclonal B cell activation in infections: infectious agents' devilry or defense mechanism of the host? J Leukoc Biol 82: 1027-1032.
27. Mary C, Faraut F, Lascombe L, Dumon H, (2004) Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42: 5249-5255.
28. Krammer PH, Arnold R, Lavrik IN, (2007) Life and death in peripheral T cells. Nat Rev Immunol 7: 532-542.
29. Pagan AJ, Peters NC, Debrabant A, Ribeiro-Gomes F, Pepper M, et al. (2012) Tracking antigen-specific CD4(+) T cells throughout the course of chronic Leishmania major infection in resistant mice. Eur J Immunol 43 (2): 427-38.
30. Anderson CF, Oukka M, Kuchroo VJ, Sacks D, (2007) CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med 204: 285-297.
31. Nylen S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, et al. (2007) Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 204: 805-817.
32. Owens BM, Beattie L, Moore JW, Brown N, Mann JL, et al. (2012) IL-10-producing Th1 cells and disease progression are regulated by distinct CD11c(+) cell populations during visceral leishmaniasis. PLoS Pathog 8: e1002827.
33. Stager S, Maroof A, Zubairi S, Sanos SL, Kopf M, et al. (2006) Distinct roles for IL-6 and IL-12p40 in mediating protection against Leishmania donovani and the expansion of IL-10+ CD4+ T cells. Eur J Immunol 36: 1764-1771.
34. Mebius RE, Kraal G, (2005) Structure and function of the spleen. Nat Rev Immunol 5: 606-616.
35. Moir S, Fauci AS, (2009) B cells in HIV infection and disease. Nat Rev Immunol 9: 235-245.
36. Titanji K, Velu V, Chennareddi L, Vijay-Kumar M, Gewirtz AT, et al. (2010) Acute depletion of activated memory B cells involves the PD-1 pathway in rapidly progressing SIV-infected macaques. J Clin Invest 120: 3878-3890.
37. Caldwell CW, Marty LM, Feldbush TL, (1991) Expression of the low Mr isoform of CD45 (CD45RO) in B-cell non-Hodgkin's lymphomas. Clin Immunol Immunopathol 58: 377-384.
38. Jackson SM, Harp N, Patel D, Zhang J, Willson S, et al. (2007) CD45RO enriches for activated, highly mutated human germinal center B cells. Blood 110: 3917-3925.
39. Berkowska MA, Driessen GJ, Bikos V, Grosserichter-Wagener C, Stamatopoulos K, et al. (2011) Human memory B cells originate from three distinct germinal center-dependent and-independent maturation pathways. Blood 118: 2150-2158.
40. Cumont MC, Diop O, Vaslin B, Elbim C, Viollet L, et al. (2008) Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J Virol 82: 1175-1184.
41. Engwerda CR, Kaye PM, (2000) Organ-specific immune responses associated with infectious disease. Immunol Today 21: 73-78.
42. Eidsmo L, Wolday D, Berhe N, Sabri F, Satti I, et al. (2002) Alteration of Fas and Fas ligand expression during human visceral leishmaniasis. Clin Exp Immunol 130: 307-313.
43. Heinzel FP, Sadick MD, Mutha SS, Locksley RM, (1991) Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc Natl Acad Sci U S A 88: 7011-7015.
44. Ghalib HW, Piuvezam MR, Skeiky YA, Siddig M, Hashim FA, et al. (1993) Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 92: 324-329.
45. O'Garra A, Vieira P, (2007) T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 7: 425-428.
46. Colle JH, Truffa-Bachi P, Chedid L, Modabber F, (1983) Lack of general immunosuppression during visceral Leishmania tropica infection in BALB/c mice: augmented antibody response to thymus-independent antigens and polyclonal activation. J Immunol 131: 1492-1495.
47. Campos-Neto A, Bunn-Moreno MM, (1982) Polyclonal B cell activation in hamsters infected with parasites of the genus Leishmania. Infect Immun 38: 871-876.
48. Agenor Araujo Lima Verde F, Araujo Lima Verde F, De Francesco Daher E, Martins Dos Santos G, Saboia Neto A, et al. (2009) Renal tubular dysfunction in human visceral leishmaniasis (Kala-azar). Clin Nephrol 71: 492-500.
49. Luthje K, Kallies A, Shimohakamada Y, Belz GT, Light A, et al. (2012) The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat Immunol 13: 491-498.
50. Jones JL, Phuah CL, Cox AL, Thompson SA, Ban M, et al. (2009) IL-21 drives secondary autoimmunity in patients with multiple sclerosis, following therapeutic lymphocyte depletion with alemtuzumab (Campath-1H). J Clin Invest 119: 2052-2061.
51. Louzir H, Belal-Kacemi L, Sassi A, Laouini D, Ben Ismail R, et al. (1994) Natural autoantibodies, IgG antibodies to tetanus toxoid and CD5+ B cells in patients with Mediterranean visceral leishmaniasis. The Leishmania Study Group. Clin Exp Immunol 95: 479-484.
52. Argov S, Jaffe CL, Krupp M, Slor H, Shoenfeld Y, (1989) Autoantibody production by patients infected with Leishmania. Clin Exp Immunol 76: 190-197.
53. Lee SK, Rigby RJ, Zotos D, Tsai LM, Kawamoto S, et al. (2011) B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J Exp Med 208: 1377-1388.
54. Kerfoot SM, Yaari G, Patel JR, Johnson KL, Gonzalez DG, et al. (2011) Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 34: 947-960.
55. Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D, et al. (2009) Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325: 1006-1010.
56. Cordeiro-Da-Silva A, Borges MC, Guilvard E, Ouaissi A, (2001) Dual role of the Leishmania major ribosomal protein S3a homologue in regulation of T- and B-cell activation. Infect Immun 69: 6588-6596.
57. Rico AI, Girones N, Fresno M, Alonso C, Requena JM, (2002) The heat shock proteins, Hsp70 and Hsp83, of Leishmania infantum are mitogens for mouse B cells. Cell Stress Chaperones 7: 339-346.
58. Bermejo DA, Amezcua Vesely MC, Khan M, Acosta Rodriguez EV, Montes CL, et al. (2011) Trypanosoma cruzi infection induces a massive extrafollicular and follicular splenic B-cell response which is a high source of non-parasite-specific antibodies. Immunology 132: 123-133.
59. Xu Y, Weatherall C, Bailey M, Alcantara S, De Rose R, et al. (2013) SIV Infects Follicular Helper CD4 T cells in Lymphoid Tissues During Pathogenic Infection of Pigtail Macaques. J Virol 87: 3760-73.
60. Petrovas C, Yamamoto T, Gerner MY, Boswell KL, Wloka K, et al. (2012) CD4 T follicular helper cell dynamics during SIV infection. J Clin Invest 122: 3281-3294.
61. Lindqvist M, van Lunzen J, Soghoian DZ, Kuhl BD, Ranasinghe S, et al. (2012) Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J Clin Invest 122: 3271-3280.
62. Chacon-Salinas R, Limon-Flores AY, Chavez-Blanco AD, Gonzalez-Estrada A, Ullrich SE, (2011) Mast cell-derived IL-10 suppresses germinal center formation by affecting T follicular helper cell function. J Immunol 186: 25-31.
63. Rousset F, Garcia E, Defrance T, Peronne C, Vezzio N, et al. (1992) Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A 89: 1890-1893.
64. Silvestre R, Cordeiro-Da-Silva A, Santarem N, Vergnes B, Sereno D, et al. (2007) SIR2-deficient Leishmania infantum induces a defined IFN-gamma/IL-10 pattern that correlates with protection. J Immunol 179: 3161-3170.
65. Gibson-Corley KN, Boggiatto PM, Bockenstedt MM, Petersen CA, Waldschmidt TJ, et al. (2012) Promotion of a functional B cell germinal center response after Leishmania species co-infection is associated with lesion resolution. Am J Pathol 180: 2009-2017.
66. Silvestre R, Santarem N, Cunha J, Cardoso L, Nieto J, et al. (2008) Serological evaluation of experimentally infected dogs by LicTXNPx-ELISA and amastigote-flow cytometry. Vet Parasitol 158: 23-30.
67. Laforge M, Campillo-Gimenez L, Monceaux V, Cumont MC, Hurtrel B, et al. (2011) HIV/SIV infection primes monocytes and dendritic cells for apoptosis. PLoS Pathog 7: e1002087.
68. Preibisch S, Saalfeld S, Tomancak P, (2009) Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25: 1463-1465.