Clinical severity of visceral leishmaniasis is associated with changes in immunoglobulin G Fc N-glycosylation

mBio

Volumn 5, Issue 6, 2014, Pages

  Gardinassi, Luiz Gustavo ^a   Dotz, Viktoria ^b   Ederveen, Agnes Hipgrave ^c   De Almeida, Roque Pacheco ^d   Costa, Carlos Henrique Nery ^e   Costa, Dorcas Lamounier ^e   De Jesus, Amélia Ribeiro ^d   Mayboroda, Oleg A ^c   Garcia, Gustavo Rocha ^a   Wuhrer, Manfred ^b,c,f   de Miranda Santos, Isabel Kinney Ferreira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^e FEDERAL UNIVERSITY OF PIAUÍ   (Brazil)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN FC FRAGMENT; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IMMUNOGLOBULIN G; PROTOZOON ANTIBODY;

ADULT; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENDEMIC DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; IMMUNOREGULATION; LEISHMANIA CHAGASI; MAJOR CLINICAL STUDY; MALE; MOLECULAR INTERACTION; NONHUMAN; PATHOGENESIS; PROTEIN BLOOD LEVEL; PROTEIN GLYCOSYLATION; VISCERAL LEISHMANIASIS; BLOOD; CHEMISTRY; GLYCOSYLATION; IMMUNOLOGY; METABOLISM; PATHOLOGY; PROTEIN PROCESSING;

LEISHMANIA INFANTUM;

ANTIBODIES, PROTOZOAN; C-REACTIVE PROTEIN; CYTOKINES; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; LEISHMANIASIS, VISCERAL; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84920911922     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01844-14     Document Type: Article

References (73)

1. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M. 2007. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat. Rev. Microbiol. 5:873–882. http://dx.doi.org/10.1038/nrmicro1748.
2. Peruhype-Magalhães V, Martins-Filho OA, Prata A, Silva LdeA, Rabello A, Teixeira-Carvalho A, Figueiredo RM, Guimarães-Carvalho SF, Ferrari TC, Van Weyenbergh J, Correa-Oliveira R. 2006. Mixed inflammatory /regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral leishmaniasis due to Leishmania chagasi infection. Clin. Exp. Immunol. 146:124–132. http://dx.doi.org/10.1111/j.1365-2249.2006.03171.x.
3. Duthie MS, Guderian J, Vallur A, Bhatia A, Lima Dos Santos P, Vieira de Melo E, Ribeiro de Jesus A, Todt M, Mondal D, Almeida R, Reed SG. 2014. Alteration of the serum biomarker profiles of visceral leishmaniasis during treatment. Eur. J. Clin. Microbiol. Infect. Dis. 33:639–649. http://dx.doi.org/10.1007/s10096-013-1999-1.
4. Costa DL, Rocha RL, Carvalho RMA, Lima-Neto AS, Harhay MO, Costa CHN, Barral-Neto M, Barral AP. 2013. Serum cytokines associated with severity and complications of kala-azar. Pathog. Glob. Health 107:78–87. http://dx.doi.org/10.1179/2047773213Y.0000000078.
5. White AC, Castes M, Garcia L, Trujillo D, Zambrano L. 1992. Leishmania chagasi antigens recognized in cured visceral leishmaniasis and asymptomatic infection. Am. J. Trop. Med. Hyg. 46:123–131.
6. Zijlstra EE, el-Hassan AM, Ismael A, Ghalib HW. 1994. Endemic kalaazar in eastern Sudan: a longitudinal study on the incidence of clinical and subclinical infection and post-kala-azar dermal leishmaniasis. Am. J. Trop. Med. Hyg. 51:826–836.
7. Badaró R, Jones TC, Lorenço R, Cerf BJ, Sampaio D, Carvalho EM, Rocha H, Teixeira R, Johnson WD.. 1986. A prospective study of visceral leishmaniasis in an endemic area of Brazil. J. Infect. Dis. 154: 639–649. http://dx.doi.org/10.1093/infdis/154.4.639.
8. McCall LI, Zhang WW, Matlashewski G. 2013. Determinants for the development of visceral leishmaniasis disease. PLoS Pathog. 9:e1003053. http://dx.doi.org/10.1371/journal.ppat.1003053.
9. Galvão-Castro B, Sá Ferreira JA, Marzochi KF, Marzochi MC, Coutinho SG, Lambert PH. 1984. Polyclonal B cell activation, circulating immune complexes and autoimmunity in human American visceral leishmaniasis. Clin. Exp. Immunol. 56:58–66.
10. Evans TG, Krug EC, Wilson ME, Vasconcelos AW, de Alencar JE, Pearson RD. 1989. Evaluation of antibody responses in American visceral leishmaniasis by ELISA and immunoblot. Mem. Inst. Oswaldo Cruz 84: 157–166. http://dx.doi.org/10.1590/S0074-02761989000800031.
11. Ryan JR, Smithyman AM, Rajasekariah GH, Hochberg L, Stiteler JM, Martin SK. 2002. Enzyme-linked immunosorbent assay based on soluble promastigote antigen detects immunoglobulinM(IgM) and IgG antibodies in sera from cases of visceral and cutaneous leishmaniasis. J. Clin. Microbiol. 40:1037–1043. http://dx.doi.org/10.1128/JCM.40.3.1037-1043.2002.
12. Pearson RD, de Alencar JE, Romito R, Naidu TG, Young AC, Davis JS IV. 1983. Circulating immune complexes and rheumatoid factors in visceral leishmaniasis. J. Infect. Dis. 147:1102. http://dx.doi.org/10.1093/infdis/147.6.1102.
13. 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. http://dx.doi.org/10.4049/jimmunol.164.7.3681.
14. Deak E, Jayakumar A, Cho KW, Goldsmith-Pestana K, Dondji B, Lambris JD, McMahon-Pratt D. 2010. Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. Eur. J. Immunol. 40:1355–1368. http://dx.doi.org/10.1002/eji.200939455.
15. Nimmerjahn F, Ravetch JV. 2005. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310:1510–1512. http://dx.doi.org/10.1126/science.1118948.
16. Pincetic A, Bournazos S, DiLillo DJ, Maamary J, Wang TT, Dahan R, Fiebiger BM, Ravetch JV. 2014. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat. Immunol. 15:707–716. http://dx.doi.org/10.1038/ni.2939.
17. Chu N, Thomas BN, Patel SR, Buxbaum LU. 2010. IgG1 is pathogenic in Leishmania mexicana infection. J. Immunol. 185:6939-6946. http://dx.doi.org/10.4049/jimmunol.1002484.
18. Woelbing F, Kostka SL, Moelle K, Belkaid Y, Sunderkoetter C, Verbeek S, Waisman A, Nigg AP, Knop J, Udey MC, von Stebut E. 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. http://dx.doi.org/10.1084/jem.20052288.
19. Zauner G, Selman MHJ, Bondt A, Rombouts Y, Blank D, Deelder AM, Wuhrer M. 2013. Glycoproteomic analysis of antibodies. Mol. Cell. Proteomics 12:856–865. http://dx.doi.org/10.1074/mcp.R112.026005.
20. Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB. 1995. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat. Med. 1:237–243. http://dx.doi.org/10.1038/nm0395-237.
21. Shields RL, Lai J, Keck R, O’Connell LY, Hong K, Meng YG, Weikert SH, Presta LG. 2002. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibodydependent cellular toxicity. J. Biol. Chem. 277:26733–26740. http://dx.doi.org/10.1074/jbc.M202069200.
22. Zou G, Ochiai H, Huang W, Yang Q, Li C, Wang LX. 2011. Chemoenzymatic synthesis and Fc_ receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to Fc_IIIa receptor. J. Am. Chem. Soc. 133:18975–18991. http://dx.doi.org/10.1021/ja208390n.
23. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. 2011. Intravenous gamma globulin suppresses inflammation through a novel T(H)2 pathway. Nature 475:110–113. http://dx.doi.org/10.1038/nature10134.
24. Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, Rosas M, McDonald JU, Orr SJ, Berger M, Petzold D, Blanchard V, Winkler A, Hess C, Reid DM, Majoul IV, Strait RT, Harris NL, Köhl G, Wex E, Ludwig R, Zillikens D, Nimmerjahn F, Finkelman FD, Brown GD, Ehlers M, Köhl J. 2012. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of Fc_RIIB and dectin-1. Nat. Med. 18:1401–1406. http://dx.doi.org/10.1038/nm.2862.
25. Parekh R, Isenberg D, Rook G, Roitt I, Dwek R, Rademacher T. 1989. A comparative analysis of disease-associated changes in the galactosylation of serum IgG. J. Autoimmun. 2:101–114. http://dx.doi.org/10.1016/0896-8411(89)90121-2.
26. Selman MH, Niks EH, Titulaer MJ, Verschuuren JJ, Wuhrer M, Deelder AM. 2011. IgG fc N-glycosylation changes in Lambert-Eaton myasthenic syndrome and myasthenia gravis. J. Proteome Res. 10:143–152. http://dx.doi.org/10.1021/pr1004373.
27. Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, Dugast AS, Heizen EL, Ercan A, Choi I, Streeck H, Nigrovic PA, Bailey-Kellogg C, Scanlan C, Alter G. 2013. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J. Clin. Invest. 123:2183–2192. http://dx.doi.org/10.1172/JCI65708.
28. Troelsen LN, Jacobsen S, Abrahams JL, Royle L, Rudd PM, Narvestad E, Heegaard NH, Garred P. 2012. IgG glycosylation changes and MBL2 polymorphisms: associations with markers of systemic inflammation and joint destruction in rheumatoid arthritis. J. Rheumatol. 39:463-469. http://dx.doi.org/10.3899/jrheum.110584.
29. Rombouts Y, Ewing E, van de Stadt LA, Selman MH, Trouw LA, Deelder AM, Huizinga TW, Wuhrer M, van Schaardenburg D, Toes RE, Scherer HU. 8 October 2013. Anti-citrullinated protein antibodies acquire a pro-inflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis-2013-203565.
30. van Zeben D, Rook GA, Hazes JM, Zwinderman AH, Zhang Y, Ghelani S, Rademacher TW, Breedveld FC. 1994. Early agalactosylation of IgG is associated with a more progressive disease course in patients with rheumatoid arthritis: results of a follow-up study. Br. J. Rheumatol. 33:36–43. http://dx.doi.org/10.1093/rheumatology/33.suppl_2.36.
31. Bakovic´ MP, Selman MH, Hoffmann M, Rudan I, Campbell H, Deelder AM, Lauc G, Wuhrer M. 2013. High-throughput IgG Fc N-glycosylation profiling by mass spectrometry of glycopeptides. J. Proteome Res. 12: 821–831. http://dx.doi.org/10.1021/pr300887z.
32. Stadlmann J, Pabst M, Kolarich D, Kunert R, Altmann F. 2008. Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8:2858-2871. http://dx.doi.org/10.1002/pmic.200700968.
33. Stadlmann J, Weber A, Pabst M, Anderle H, Kunert R, Ehrlich HJ, Peter Schwarz H, Altmann F. 2009. A close look at human IgG sialylation and subclass distribution after lectin fractionation. Proteomics 9:4143–4153. http://dx.doi.org/10.1002/pmic.200800931.
34. Wuhrer M, Stam JC, van de Geijn FE, Koeleman CA, Verrips CT, Dolhain RJ, Hokke CH, Deelder AM. 2007. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum. Proteomics 7:4070–4081. http://dx.doi.org/10.1002/pmic.200700289.
35. Yamada E, Tsukamoto Y, Sasaki R, Yagyu K, Takahashi N. 1997. Structural changes of immunoglobulin Goligosaccharides with age in healthy human serum. Glycoconj. J 14:401-405. http://dx.doi.org/10.1023/A:1018582930906.
36. Shikata K, Yasuda T, Takeuchi F, Konishi T, Nakata M, Mizuochi T. 1998. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj. J 15:683-689. http://dx.doi.org/10.1023/A:1006936431276.
37. Tudor D, Yu H, Maupetit J, Drillet AS, Bouceba T, Schwartz-Cornil I, Lopalco L, Tuffery P, Bomsel M. 2012. Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc. Natl. Acad. Sci. U. S. A. 109:12680–12685. http://dx.doi.org/10.1073/pnas.1200024109.
38. Sela-Culang I, Kunik V, Ofran Y. 2013. The structural basis of antibodyantigen recognition. Front. Immunol. 4:302. http://dx.doi.org/10.3389/fimmu.2013.00302.
39. Huffman JE, Puic-Bakovic´ M, Klaric´ L, Hennig R, Selman MHJ, Vukovic´ F, Novokmet M, Krištic´ J, Borowiak M, Muth T, Polašek O, Razdorov G, Gornik O, Plomp R, Theodoratou E, Wright AF, Rudan I, Hayward C, Campbell H, Deelder AM, Reichl U, Aulchenko YS, Rapp E, Wuhrer M, Lauc G. 2014. Comparative performance of four methods for high-throughput glycosylation analysis of immunoglobulin G in genetic and epidemiological research. Mol. Cell. Proteomics 13:1598–1610. http://dx.doi.org/10.1074/mcp.M113.037465.
40. Mehta AS, Long RE, Comunale MA, Wang M, Rodemich L, Krakover J, Philip R, Marrero JA, Dwek RA, Block TM. 2008. Increased levels of galactose-deficient anti-Gal immunoglobulin G in the sera of hepatitis C virus-infected individuals with fibrosis and cirrhosis. J. Virol. 82: 1259–1270. http://dx.doi.org/10.1128/JVI.01600-07.
41. Ho CH, Chien RN, Cheng PN, Liu JH, Liu CK, Su CS, Wu IC, Li IC, Tsai HW, Wu SL, Liu WC, Chen SH, Chang TT. 10 July 2014. Aberrant serum IgG glycosylation in chronic hepatitis B is associated with histological liver damage and is reversible by antiviral therapy. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jiu388.
42. O’Regan NL, Steinfelder S, Schwedler C, Rao GB, Srikantam A, Blanchard V, Hartmann S. 13 August 2014. Filariasis asymptomatically infected donors have lower levels of disialylated IgG compared to endemic normals. Parasite Immunol. doi: http://dx.doi.org/10.1111/pim.12137.
43. Hess C, Winkler A, Lorenz AK, Holecska V, Blanchard V, Eiglmeier S, Schoen AL, Bitterling J, Stoehr AD, Petzold D, Schommartz T, Mertes MM, Schoen CT, Tiburzy B, Herrmann A, Köhl J, Manz RA, Madaio MP, Berger M, Wardemann H, Ehlers M. 2013. T cell-independent B cell activation induces immunosuppressive sialylated IgG antibodies. J. Clin. Invest. 123:3788–3796. http://dx.doi.org/10.1172/JCI65938.
44. Sibéril S, de Romeuf C, Bihoreau N, Fernandez N, Meterreau JL, Regenman A, Nony E, Gaucher C, Glacet A, Jorieux S, Klein P, Hogarth MP, Fridman WH, Bourel D, Béliard R, Teillaud JL. 2006. Selection of a human anti-RhD monoclonal antibody for therapeutic use: impact of IgG glycosylation on activating and inhibitory Fc gamma R functions. Clin. Immunol. 118:170-179. http://dx.doi.org/10.1016/j.clim.2005.10.008.
45. Nimmerjahn F, Ravetch JV. 2008. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8:34-47. http://dx.doi.org/10.1038/nri2206.
46. Jeddi P, Keusch J, Lydyard PM, Bodman-Smith KB, Chesnutt MS, Wofsy D, Hirota H, Taga T, Delves PJ. 1999. The effect on immunoglobulin glycosylation of altering in vivo production of immunoglobulin G. Immunology 98:475-480. http://dx.doi.org/10.1046/j.1365-2567.1999.00896.x.
47. Selman MH, de Jong SE, Soonawala D, Kroon FP, Adegnika AA, Deelder AM, Hokke CH, Yazdanbakhsh M, Wuhrer M. 2012. Changes in antigen-specific IgG1 Fc N-glycosylation upon influenza and tetanus vaccination. Mol. Cell. Proteomics 11:M111.014563. http://dx.doi.org/10.1074/mcp.M111.014563.
48. Velge P, Kusnierz JP, Ouaissi A, Marty B, Pham BN, Capron A. 1991. Trypanosoma cruzi: infection of T lymphocytes and their destruction by antibody-dependent cell-mediated cytotoxicity. Eur. J. Immunol. 21: 2145–2152. http://dx.doi.org/10.1002/eji.1830210924.
49. Gibson-Corley KN, Bockenstedt MM, Li H, Boggiatto PM, Phanse Y, Petersen CA, Bellaire BH, Jones DE. 2014. An in vitro model of antibody-enhanced killing of the intracellular parasite Leishmania amazonensis. PLoS One 9:e106426. http://dx.doi.org/10.1371/journal.pone.0106426.
50. Miles SA, Conrad SM, Alves RG, Jeronimo SM, Mosser DM. 2005. A role for IgG immune complexes during infection with the intracellular pathogen Leishmania. J. Exp. Med. 201:747–754. http://dx.doi.org/10.1084/jem.20041470.
51. Biburger M, Aschermann S, Schwab I, Lux A, Albert H, Danzer H, Woigk M, Dudziak D, Nimmerjahn F. 2011. Monocyte subsets responsible for immunoglobulin G-dependent effector functions in vivo. Immunity 35:932–944. http://dx.doi.org/10.1016/j.immuni.2011.11.009.
52. Xia Y, Janda A, Eryilmaz E, Casadevall A, Putterman C. 2013. The constant region affects antigen binding of antibodies to DNA by altering secondary structure. Mol. Immunol. 56:28-37. http://dx.doi.org/10.1016/j.molimm.2013.04.004.
53. Ahmed AA, Giddens J, Pincetic A, Lomino JV, Ravetch JV, Wang LX, Bjorkman PJ. 2014. Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J. Mol. Biol. 426:3166-3179. http://dx.doi.org/10.1016/j.jmb.2014.07.006.
54. Kaneko Y, Nimmerjahn F, Ravetch JV. 2006. Anti-inflammatory activity of immunoglobulinGresulting from Fc sialylation. Science 313:670–673. http://dx.doi.org/10.1126/science.1129594.
55. Lauc G, Huffman JE, Pu_ic´ M, Zgaga L, Adamczyk B, Mužinic´ A, Novokmet M, Polašek O, Gornik O, Krištic´ J, Keser T, Vitart V, Scheijen B, Uh HW, Molokhia M, Patrick AL, McKeigue P, Kol_ic´ I, Lukic´ IK, Swann O, van Leeuwen FN, Ruhaak LR, Houwing-Duistermaat JJ, Slagboom PE, Beekman M, de Craen AJ, Deelder AM, Zeng Q, Wang W, Hastie ND, Gyllensten U, Wilson JF, Wuhrer M, Wright AF, Rudd PM, Hayward C, Aulchenko Y, Campbell H, Rudan I. 2013. Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet. 9:e1003225. http://dx.doi.org/10.1371/journal.pgen.1003225.
56. Collins ES, Galligan MC, Saldova R, Adamczyk B, Abrahams JL, Campbell MP, Ng CT, Veale DJ, Murphy TB, Rudd PM, Fitzgerald O. 2013. Glycosylation status of serum in inflammatory arthritis in response to anti-TNF treatment. Rheumatology (Oxford) 52:1572–1582. http://dx.doi.org/10.1093/rheumatology/ket189.
57. Wang J, Balog CIA, Stavenhagen K, Koeleman CAM, Scherer HU, Selman MHJ, Deelder AM, Huizinga TWJ, Toes REM, Wuhrer M. 2011. Fc-glycosylation of IgG1 is modulated by B-cell stimuli. Mol. Cell. Proteomics 10:M110.004655. http://dx.doi.org/10.1074/mcp.M110.004655.
58. Nimmerjahn F, Anthony RM, Ravetch JV. 2007. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc. Natl. Acad. Sci. U. S. A. 104:8433-8437. http://dx.doi.org/10.1073/pnas.0702936104.
59. Santos IK, Costa CH, Krieger H, Feitosa MF, Zurakowski D, Fardin B, Gomes RB, Weiner DL, Harn DA, Ezekowitz RA, Epstein JE. 2001. Mannan-binding lectin enhances susceptibility to visceral leishmaniasis. Infect. Immun. 69:5212–5215. http://dx.doi.org/10.1128/IAI.69.8.5212-5215.2001.
60. Alonso DP, Ferreira AF, Ribolla PE, de Miranda Santos IK, do Socorro Pirese Cruz M, Aécio de Carvalho F, Abatepaulo AR, Lamounier Costa D, Werneck GL, Farias TJ, Soares MJ, Costa CH. 2007. Genotypes of the mannan-binding lectin gene and susceptibility to visceral leishmaniasis and clinical complications. J. Infect. Dis. 195:1212–1217. http://dx.doi.org/10.1086/512683.
61. Imafuku Y, Yoshida H, Yamada Y. 2003. Reactivity of agalactosyl IgG with rheumatoid factor. Clin. Chim. Acta 334:217–223. http://dx.doi.org/10.1016/S0009-8981(03)00245-6.
62. Costa CH, Werneck GL, Costa DL, Holanda TA, Aguiar GB, Carvalho AS, Cavalcanti JC, Santos LS. 2010. Is severe visceral leishmaniasis a systemic inflammatory response syndrome? A case control study. Rev. Soc. Bras. Med. Trop. 43:386-392. http://dx.doi.org/10.1590/S0037-86822010000400010.
63. Gautam S, Kumar R, Maurya R, Nylén S, Ansari N, Rai M, Sundar S, Sacks D. 2011. IL-10 neutralization promotes parasite clearance in splenic aspirate cells from patients with visceral leishmaniasis. J. Infect. Dis. 204: 1134–1137. http://dx.doi.org/10.1093/infdis/jir461.
64. Rousset F, Garcia E, Defrance T, Péronne C, Vezzio N, Hsu DH, Kastelein R, Moore KW, Banchereau J. 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. http://dx.doi.org/10.1073/pnas.89.5.1890.
65. Nylén S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, Sacks D. 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. http://dx.doi.org/10.1084/jem.20061141.
66. Owens BMJ, Beattie L, Moore JWJ, Brown N, Mann JL, Dalton JE, Maroof A, Kaye PM. 2012. IL-10-producing Th1 cells and disease progression are regulated by distinct CD11c_ cell populations during visceral leishmaniasis. PLoS Pathog. 8:e1002827. http://dx.doi.org/10.1371/journal.ppat.1002827.
67. Elshafie AI, Ahlin E, Mathsson L, ElGhazali G, Rönnelid J. 2007. Circulating immune complexes (IC) and IC-induced levels of GM-CSF are increased in Sudanese patients with acute visceral Leishmania donovani infection undergoing sodium stibogluconate treatment: implications for disease pathogenesis. J. Immunol. 178:5383–5389. http://dx.doi.org/10.4049/jimmunol.178.8.5383.
68. Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD, Theurich S, Hausen AC, Schmitz J, Brönneke HS, Estevez E, Allen TL, Mesaros A, Partridge L, Febbraio MA, Chawla A, Wunderlich FT, Brüning JC. 2014. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat. Immunol. 15:423–430. http://dx.doi.org/10.1038/ni.2865.
69. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, Nakanishi K, Yoshida N, Kishimoto T, Akira S. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380:627–630. http://dx.doi.org/10.1038/380627a0.
70. Osorio EY, Zhao W, Espitia C, Saldarriaga O, Hawel L, Byus CV, Travi BL, Melby PC. 2012. Progressive visceral leishmaniasis is driven by dominant parasite-induced. STAT6 activation and STAT6-dependent host arginase 1 expression. PLoS Pathog. 8:e1002417. http://dx.doi.org/10.1371/journal.ppat.1002417.
71. Ansar W, Mukhopadhyay S, Habib SK, Basu S, Saha B, Sen AK, Mandal CN, Mandal C. 2009. Disease-associated glycosylated molecular variants of human C-reactive protein activate complement-mediated hemolysis of erythrocytes in tuberculosis and Indian visceral leishmaniasis. Glycoconj. J 26:1151–1169. http://dx.doi.org/10.1007/s10719-009-9236-y.
72. Samuelsson A, Towers TL, Ravetch JV. 2001. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science 291: 484–486. http://dx.doi.org/10.1126/science.291.5503.484.
73. Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância Epidemiológica,. 2006. Manual de vigilância e controle da leishmaniose visceral.. Ministério da Sáude, Brasília, Brazil.