Malaria Parasite Infection Compromises Control of Concurrent Systemic Non-typhoidal Salmonella Infection via IL-10-Mediated Alteration of Myeloid Cell Function

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Lokken, Kristen L ^a   Mooney, Jason P ^a   Butler, Brian P ^a   Xavier, Mariana N ^a,b   Chau, Jennifer Y ^a   Schaltenberg, Nicola ^a   Begum, Ramie H ^a,c   Müller, Werner ^d   Luckhart, Shirley ^a   Tsolis, Renée M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c ASSAM UNIVERSITY   (India)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10;

ANIMAL; BONE MARROW CELL; C57BL MOUSE; CBA MOUSE; COMPLICATION; DRUG EFFECTS; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; MALARIA FALCIPARUM; MICROBIOLOGY; MIXED INFECTION; MOUSE; PHYSIOLOGY; PLASMODIUM FALCIPARUM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; SEPSIS;

ANIMALS; COINFECTION; FEMALE; INFLAMMATION; INTERLEUKIN-10; MALARIA, FALCIPARUM; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MYELOID CELLS; PLASMODIUM FALCIPARUM; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SEPSIS;

EID: 84901298804     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004049     Document Type: Article

References (69)

1. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA, (2012) Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379: 2489-2499.
2. Gordon MA, (2008) Salmonella infections in immunocompromised adults. J Infect 56: 413-422.
3. Bronzan RN, Taylor TE, Mwenechanya J, Tembo M, Kayira K, et al. (2007) Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J Infect Dis 195: 895-904.
4. Nielsen MV, Sarpong N, Krumkamp R, Dekker D, Loag W, et al. (2012) Incidence and characteristics of bacteremia among children in Rural Ghana. PLoS One 7: e44063.
5. Walsh AL, Phiri AJ, Graham SM, Molyneux EM, Molyneux ME, (2000) Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 19: 312-318.
6. Reddy EA, Shaw AV, Crump JA, (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10: 417-432.
7. Sigauque B, Roca A, Mandomando I, Morais L, Quinto L, et al. (2009) Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108-113.
8. Molyneux EM, Walsh AL, Malenga G, Rogerson S, Molyneux ME, (2000) Salmonella meningitis in children in Blantyre, Malawi, 1996-1999. Ann Trop Paediatr 20: 41-44.
9. Molyneux EM, Mankhambo LA, Phiri A, Graham SM, Forsyth H, et al. (2009) The outcome of non-typhoidal salmonella meningitis in Malawian children, 1997-2006. Ann Trop Paediatr 29: 13-22.
10. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, et al. (2006) Characterisation of community acquired non-typhoidal Salmonella from bacteraemia and diarrhoeal infections in children admitted to hospital in Nairobi, Kenya. BMC Microbiol 6: 101.
11. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, et al. (2009) Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19: 2279-2287.
12. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, et al. (2012) Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 44: 1215-1221.
13. Oundo JO, Muli F, Kariuki S, Waiyaki PG, Iijima Y, et al. (2002) Non-typhi salmonella in children with severe malaria. East Afr Med J 79: 633-639.
14. Perry JA, Olver CS, Burnett RC, Avery AC, (2005) Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation. J Immunol 174: 5921-5925.
15. Vazquez-Torres A, Vallance BA, Bergman MA, Finlay BB, Cookson BT, et al. (2004) Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J Immunol 172: 6202-6208.
16. Chau JY, Tiffany CM, Nimishakavi S, Lawrence JA, Pakpour N, et al. (2013) Malaria-associated L-arginine deficiency induces mast cell-associated disruption to intestinal barrier defenses against nontyphoidal Salmonella bacteremia. Infect Immun 81: 3515-3526.
17. Roux CM, Butler BP, Chau JY, Paixao TA, Cheung KW, et al. (2010) Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to Nontyphoidal Salmonella enterica serovar typhimurium infection in mice. Infect Immun 78: 1520-1527.
18. Nairz M, Fritsche G, Brunner P, Talasz H, Hantke K, et al. (2008) Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur J Immunol 38: 1923-1936.
19. Mohammed AO, Elghazali G, Mohammed HB, Elbashir MI, Xu S, et al. (2003) Human neutrophil lipocalin: a specific marker for neutrophil activation in severe Plasmodium falciparum malaria. Acta Trop 87: 279-285.
20. Zhao H, Konishi A, Fujita Y, Yagi M, Ohata K, et al. (2012) Lipocalin 2 bolsters innate and adaptive immune responses to blood-stage malaria infection by reinforcing host iron metabolism. Cell Host Microbe 12: 705-716.
21. Kossodo S, Monso C, Juillard P, Velu T, Goldman M, et al. (1997) Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology 91: 536-540.
22. Li C, Corraliza I, Langhorne J, (1999) A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun 67: 4435-4442.
23. Linke A, Kuhn R, Muller W, Honarvar N, Li C, et al. (1996) Plasmodium chabaudi chabaudi: differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp Parasitol 84: 253-263.
24. Kobayashi F, Morii T, Matsui T, Fujino T, Watanabe Y, et al. (1996) Production of interleukin 10 during malaria caused by lethal and nonlethal variants of Plasmodium yoelii yoelii. Parasitol Res 82: 385-391.
25. Ayimba E, Hegewald J, Segbena AY, Gantin RG, Lechner CJ, et al. (2011) Proinflammatory and regulatory cytokines and chemokines in infants with uncomplicated and severe Plasmodium falciparum malaria. Clin Exp Immunol 166: 218-226.
26. Mirghani HA, Eltahir HG, TM AE, Mirghani YA, Elbashir MI, et al. (2011) Cytokine profiles in children with severe Plasmodium falciparum malaria in an area of unstable malaria transmission in central Sudan. J Trop Pediatr 57: 392-395.
27. Luty AJ, Perkins DJ, Lell B, Schmidt-Ott R, Lehman LG, et al. (2000) Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect Immun 68: 3909-3915.
28. Walther M, Woodruff J, Edele F, Jeffries D, Tongren JE, et al. (2006) Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol 177: 5736-5745.
29. Graham SM, Walsh AL, Molyneux EM, Phiri AJ, Molyneux ME, (2000) Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 94: 310-314.
30. Mabey DC, Brown A, Greenwood BM, (1987) Plasmodium falciparum malaria and Salmonella infections in Gambian children. J Infect Dis 155: 1319-1321.
31. Lissner CR, Swanson RN, O'Brien AD, (1983) Genetic control of the innate resistance of mice to Salmonella typhimurium: expression of the Ity gene in peritoneal and splenic macrophages isolated in vitro. J Immunol 131: 3006-3013.
32. O'Brien AD, Rosenstreich DL, Taylor BA, (1980) Control of natural resistance to Salmonella typhimurium and Leishmania donovani in mice by closely linked but distinct genetic loci. Nature 287: 440-442.
33. Plant J, Glynn AA, (1976) Genetics of resistance to infection with Salmonella typhimurium in mice. J Infect Dis 133: 72-78.
34. Harrington KA, Hormaeche CE, (1986) Expression of the innate resistance gene Ity in mouse Kupffer cells infected with Salmonella typhimurium in vitro. Microb Pathog 1: 269-274.
35. Vidal S, Tremblay ML, Govoni G, Gauthier S, Sebastiani G, et al. (1995) The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med 182: 655-666.
36. Stevenson MM, Lyanga JJ, Skamene E, (1982) Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 38: 80-88.
37. Freitas do Rosario AP, Lamb T, Spence P, Stephens R, Lang A, et al. (2012) IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol 188: 1178-1190.
38. Richter-Dahlfors A, Buchan AM, Finlay BB, (1997) Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186: 569-580.
39. Friedman RL, Moon RJ, (1977) Hepatic clearance of Salmonella typhimurium in silica-treated mice. Infect Immun 16: 1005-1012.
40. Arai T, Hiromatsu K, Nishimura H, Kimura Y, Kobayashi N, et al. (1995) Effects of in vivo administration of anti-IL-10 monoclonal antibody on the host defence mechanism against murine Salmonella infection. Immunology 85: 381-388.
41. Eisele NA, Ruby T, Jacobson A, Manzanillo PS, Cox JS, et al. (2013) Persistent Salmonella infection is controlled by PPARd, a host regulator of fatty acid metabolism. Cell Host Microbe 14: 171-82 doi:10.1016/j.chom.2013.07.010.
42. McCoy MW, Moreland SM, Detweiler CS, (2012) Hemophagocytic macrophages in murine typhoid fever have an anti-inflammatory phenotype. Infect Immun 80: 3642-3649.
43. Mosser DM, Edwards JP, (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969.
44. Siewe L, Bollati-Fogolin M, Wickenhauser C, Krieg T, Muller W, et al. (2006) Interleukin-10 derived from macrophages and/or neutrophils regulates the inflammatory response to LPS but not the response to CpG DNA. Eur J Immunol 36: 3248-3255.
45. Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, et al. (2008) IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog 4: e1000004.
46. Roers A, Siewe L, Strittmatter E, Deckert M, Schluter D, et al. (2004) T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med 200: 1289-1297.
47. Setiawan T, Metwali A, Blum AM, Ince MN, Urban JF Jr, et al. (2007) Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine normal distal intestine. Infect Immun 75: 4655-4663.
48. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686.
49. Cambos M, Bazinet S, Abed E, Sanchez-Dardon J, Bernard C, et al. (2010) The IL-12p70/IL-10 interplay is differentially regulated by free heme and hemozoin in murine bone-marrow-derived macrophages. Int J Parasitol 40: 1003-1012.
50. Deshpande P, Shastry P, (2004) Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC. Cytokine 28: 205-213.
51. Hand WL, King-Thompson NL, (1983) Effect of erythrocyte ingestion on macrophage antibacterial function. Infect Immun 40: 917-923.
52. Xavier MN, Winter MG, Spees AM, den Hartigh AB, Nguyen K, et al. (2013) PPARgamma-Mediated Increase in Glucose Availability Sustains Chronic Brucella abortus Infection in Alternatively Activated Macrophages. Cell Host Microbe 14: 159-170.
53. Xavier MN, Winter MG, Spees AM, Nguyen K, Atluri VL, et al. (2013) CD4+ T cell-derived IL-10 promotes Brucella abortus persistence via modulation of macrophage function. PLoS Pathog 9: e1003454.
54. O'Leary S, O'Sullivan MP, Keane J, (2011) IL-10 Blocks Phagosome Maturation in Mycobacterium tuberculosis-infected Human Macrophages. American Journal of Respiratory Cell and Molecular Biology 45: 172-180.
55. Nguyen T, Robinson N, Allison SE, Coombes BK, Sad S, et al. (2013) IL-10 produced by trophoblast cells inhibits phagosome maturation leading to profound intracellular proliferation of Salmonella enterica Typhimurium. Placenta 34: 765-774.
56. Cunnington AJ, Njie M, Correa S, Takem EN, Riley EM, et al. (2012) Prolonged Neutrophil Dysfunction after Plasmodium falciparum Malaria Is Related to Hemolysis and Heme Oxygenase-1 Induction. J Immunol 189: 5336-46 doi:10.4049/jimmunol.1201028.
57. Cunnington AJ, de Souza JB, Walther M, Riley EM, (2012) Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 18: 120-127.
58. Conlan JW, (1996) Neutrophils prevent extracellular colonization of the liver microvasculature by Salmonella typhimurium. Infect Immun 64: 1043-1047.
59. Broz P, Monack DM, (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev 243: 174-190.
60. Fink SL, Cookson BT, (2007) Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9: 2562-2570.
61. Miao EA, Rajan JV, Aderem A, (2011) Caspase-1-induced pyroptotic cell death. Immunol Rev 243: 206-214.
62. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136-1142.
63. Greenwood BM, Brueton MJ, (1974) Complement activation in children with acute malaria. Clin Exp Immunol 18: 267-272.
64. Krettli AU, Nussenzweig V, Nussenzweig RS, (1976) Complement alterations in rodent malaria. Am J Trop Med Hyg 25: 34-41.
65. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W, (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
66. Pils MC, Pisano F, Fasnacht N, Heinrich JM, Groebe L, et al. (2010) Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur J Immunol 40: 443-448.
67. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I, (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277.
68. Stojiljkovic I, Baumler AJ, Heffron F, (1995) Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357-1366.
69. Prentki P, Krisch HM, (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29: 303-313.