#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


Non-typhoidal Salmonella serotypes (NTS) most frequently cause diarrheal disease, which is self-limiting. However, in sub-Saharan Africa, NTS is one of the most common causes of life-threatening bloodstream infections. Individuals with these bloodstream infections frequently have an underlying condition such as HIV in adults or malaria in children. We used a mouse model to investigate why malaria predisposes children to invasive NTS infections. Our results implicate an anti-inflammatory response induced by malaria parasites via the cytokine IL-10 in promoting increased growth of bacteria that have disseminated from the intestine to other organs of the body. This response is beneficial in that it prevents death from malaria, but has an adverse effect on phagocytic cells, blocking their ability to control growth of bacteria that have disseminated from the intestine to other organs of the body.


Vyšlo v časopise: Malaria Parasite Infection Compromises Control of Concurrent Systemic Non-typhoidal Infection via IL-10-Mediated Alteration of Myeloid Cell Function. PLoS Pathog 10(5): e32767. doi:10.1371/journal.ppat.1004049
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004049

Souhrn

Non-typhoidal Salmonella serotypes (NTS) most frequently cause diarrheal disease, which is self-limiting. However, in sub-Saharan Africa, NTS is one of the most common causes of life-threatening bloodstream infections. Individuals with these bloodstream infections frequently have an underlying condition such as HIV in adults or malaria in children. We used a mouse model to investigate why malaria predisposes children to invasive NTS infections. Our results implicate an anti-inflammatory response induced by malaria parasites via the cytokine IL-10 in promoting increased growth of bacteria that have disseminated from the intestine to other organs of the body. This response is beneficial in that it prevents death from malaria, but has an adverse effect on phagocytic cells, blocking their ability to control growth of bacteria that have disseminated from the intestine to other organs of the body.


Zdroje

1. FeaseyNA, DouganG, KingsleyRA, HeydermanRS, GordonMA (2012) Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379: 2489–2499.

2. GordonMA (2008) Salmonella infections in immunocompromised adults. J Infect 56: 413–422.

3. BronzanRN, TaylorTE, MwenechanyaJ, TemboM, KayiraK, et al. (2007) Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J Infect Dis 195: 895–904.

4. NielsenMV, SarpongN, KrumkampR, DekkerD, LoagW, et al. (2012) Incidence and characteristics of bacteremia among children in Rural Ghana. PLoS One 7: e44063.

5. WalshAL, PhiriAJ, GrahamSM, MolyneuxEM, MolyneuxME (2000) Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 19: 312–318.

6. ReddyEA, ShawAV, CrumpJA (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10: 417–432.

7. SigauqueB, RocaA, MandomandoI, MoraisL, QuintoL, et al. (2009) Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108–113.

8. MolyneuxEM, WalshAL, MalengaG, RogersonS, MolyneuxME (2000) Salmonella meningitis in children in Blantyre, Malawi, 1996–1999. Ann Trop Paediatr 20: 41–44.

9. MolyneuxEM, MankhamboLA, PhiriA, GrahamSM, ForsythH, et al. (2009) The outcome of non-typhoidal salmonella meningitis in Malawian children, 1997–2006. Ann Trop Paediatr 29: 13–22.

10. KariukiS, RevathiG, KariukiN, KiiruJ, MwituriaJ, 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. KingsleyRA, MsefulaCL, ThomsonNR, KariukiS, HoltKE, 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. OkoroCK, KingsleyRA, ConnorTR, HarrisSR, ParryCM, et al. (2012) Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 44: 1215–1221.

13. OundoJO, MuliF, KariukiS, WaiyakiPG, IijimaY, et al. (2002) Non-typhi salmonella in children with severe malaria. East Afr Med J 79: 633–639.

14. PerryJA, OlverCS, BurnettRC, AveryAC (2005) Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation. J Immunol 174: 5921–5925.

15. Vazquez-TorresA, VallanceBA, BergmanMA, FinlayBB, CooksonBT, 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. ChauJY, TiffanyCM, NimishakaviS, LawrenceJA, PakpourN, 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. RouxCM, ButlerBP, ChauJY, PaixaoTA, CheungKW, 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. NairzM, FritscheG, BrunnerP, TalaszH, HantkeK, et al. (2008) Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur J Immunol 38: 1923–1936.

19. MohammedAO, ElghazaliG, MohammedHB, ElbashirMI, XuS, et al. (2003) Human neutrophil lipocalin: a specific marker for neutrophil activation in severe Plasmodium falciparum malaria. Acta Trop 87: 279–285.

20. ZhaoH, KonishiA, FujitaY, YagiM, OhataK, 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. KossodoS, MonsoC, JuillardP, VeluT, GoldmanM, et al. (1997) Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology 91: 536–540.

22. LiC, CorralizaI, LanghorneJ (1999) A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun 67: 4435–4442.

23. LinkeA, KuhnR, MullerW, HonarvarN, LiC, 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. KobayashiF, MoriiT, MatsuiT, FujinoT, WatanabeY, 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. AyimbaE, HegewaldJ, SegbenaAY, GantinRG, LechnerCJ, 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. MirghaniHA, EltahirHG, TMAE, MirghaniYA, ElbashirMI, 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. LutyAJ, PerkinsDJ, LellB, Schmidt-OttR, LehmanLG, et al. (2000) Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect Immun 68: 3909–3915.

28. WaltherM, WoodruffJ, EdeleF, JeffriesD, TongrenJE, 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. GrahamSM, WalshAL, MolyneuxEM, PhiriAJ, MolyneuxME (2000) Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 94: 310–314.

30. MabeyDC, BrownA, GreenwoodBM (1987) Plasmodium falciparum malaria and Salmonella infections in Gambian children. J Infect Dis 155: 1319–1321.

31. LissnerCR, SwansonRN, O'BrienAD (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'BrienAD, RosenstreichDL, TaylorBA (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. PlantJ, GlynnAA (1976) Genetics of resistance to infection with Salmonella typhimurium in mice. J Infect Dis 133: 72–78.

34. HarringtonKA, HormaecheCE (1986) Expression of the innate resistance gene Ity in mouse Kupffer cells infected with Salmonella typhimurium in vitro. Microb Pathog 1: 269–274.

35. VidalS, TremblayML, GovoniG, GauthierS, SebastianiG, 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. StevensonMM, LyangaJJ, SkameneE (1982) Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 38: 80–88.

37. Freitas do RosarioAP, LambT, SpenceP, StephensR, LangA, 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-DahlforsA, BuchanAM, FinlayBB (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. FriedmanRL, MoonRJ (1977) Hepatic clearance of Salmonella typhimurium in silica-treated mice. Infect Immun 16: 1005–1012.

40. AraiT, HiromatsuK, NishimuraH, KimuraY, KobayashiN, 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. EiseleNA, RubyT, JacobsonA, ManzanilloPS, CoxJS, 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. McCoyMW, MorelandSM, DetweilerCS (2012) Hemophagocytic macrophages in murine typhoid fever have an anti-inflammatory phenotype. Infect Immun 80: 3642–3649.

43. MosserDM, EdwardsJP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958–969.

44. SieweL, Bollati-FogolinM, WickenhauserC, KriegT, MullerW, 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. CouperKN, BlountDG, WilsonMS, HafallaJC, BelkaidY, et al. (2008) IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog 4: e1000004.

46. RoersA, SieweL, StrittmatterE, DeckertM, SchluterD, 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. SetiawanT, MetwaliA, BlumAM, InceMN, UrbanJFJr, et al. (2007) Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine normal distal intestine. Infect Immun 75: 4655–4663.

48. MantovaniA, SicaA, SozzaniS, AllavenaP, VecchiA, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677–686.

49. CambosM, BazinetS, AbedE, Sanchez-DardonJ, BernardC, 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. DeshpandeP, ShastryP (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. HandWL, King-ThompsonNL (1983) Effect of erythrocyte ingestion on macrophage antibacterial function. Infect Immun 40: 917–923.

52. XavierMN, WinterMG, SpeesAM, den HartighAB, NguyenK, 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. XavierMN, WinterMG, SpeesAM, NguyenK, AtluriVL, et al. (2013) CD4+ T cell-derived IL-10 promotes Brucella abortus persistence via modulation of macrophage function. PLoS Pathog 9: e1003454.

54. O'LearyS, O'SullivanMP, KeaneJ (2011) IL-10 Blocks Phagosome Maturation in Mycobacterium tuberculosis-infected Human Macrophages. American Journal of Respiratory Cell and Molecular Biology 45: 172–180.

55. NguyenT, RobinsonN, AllisonSE, CoombesBK, SadS, 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. CunningtonAJ, NjieM, CorreaS, TakemEN, RileyEM, 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. CunningtonAJ, de SouzaJB, WaltherM, RileyEM (2012) Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 18: 120–127.

58. ConlanJW (1996) Neutrophils prevent extracellular colonization of the liver microvasculature by Salmonella typhimurium. Infect Immun 64: 1043–1047.

59. BrozP, MonackDM (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev 243: 174–190.

60. FinkSL, CooksonBT (2007) Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9: 2562–2570.

61. MiaoEA, RajanJV, AderemA (2011) Caspase-1-induced pyroptotic cell death. Immunol Rev 243: 206–214.

62. MiaoEA, LeafIA, TreutingPM, MaoDP, DorsM, et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136–1142.

63. GreenwoodBM, BruetonMJ (1974) Complement activation in children with acute malaria. Clin Exp Immunol 18: 267–272.

64. KrettliAU, NussenzweigV, NussenzweigRS (1976) Complement alterations in rodent malaria. Am J Trop Med Hyg 25: 34–41.

65. KuhnR, LohlerJ, RennickD, RajewskyK, MullerW (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263–274.

66. PilsMC, PisanoF, FasnachtN, HeinrichJM, GroebeL, 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. ClausenBE, BurkhardtC, ReithW, RenkawitzR, ForsterI (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265–277.

68. StojiljkovicI, BaumlerAJ, HeffronF (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. PrentkiP, KrischHM (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29: 303–313.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#