Eosinophils Are Important for Protection, Immunoregulation and Pathology during Infection with Nematode Microfilariae

English version České info

Eosinophil recruitment is a classic characteristic of both allergic and parasitic helminth diseases. Elucidation of the role of eosinophils in these diseases is of pivotal importance for understanding the mechanisms of protection and the development of pathology. In the last few years, the part played by eosinophils in helminth-defence has been dissected using in vivo models and their importance in protection has been shown to be highly specific to the host-parasite combination. This study dissects the role of eosinophils during infection with the human lymphatic filarial parasite, Brugia malayi, which causes the major neglected tropical disease, lymphatic filariasis. In particular, we study the role of the eosinophil as a double–edged sword in generating both protection and pathology. We definitively confirm the importance of eosinophils in protection against B. malayi microfilariae and show that protection is not mediated by release of the eosinophil granule proteins, major basic protein or eosinophil peroxidase alone. Overall, we reveal that during an infection with B. malayi microfilariae, eosinophils are critical for primary protective responses. However, eosinophils contribute to nematode-induced lung dysfunction, while additionally, eosinophil granules are important negative regulators of parasite-induced lung inflammatory and some adaptive immune responses.

Vyšlo v časopise: Eosinophils Are Important for Protection, Immunoregulation and Pathology during Infection with Nematode Microfilariae. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003988
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003988

Souhrn

Zdroje

1. LeeJJ, DiminaD, MaciasMP, OchkurSI, McGarryMP, et al. (2004) Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305 : 1773–1776.

2. HumblesAA, LloydCM, McMillanSJ, FriendDS, XanthouG, et al. (2004) A critical role for eosinophils in allergic airways remodeling. Science 305 : 1776–1779.

3. CadmanET, LawrenceRA (2010) Granulocytes: effector cells or immunomodulators in the immune response to helminth infection? Parasite Immunol 32 : 1–19.

4. KlionAD, NutmanTB (2004) The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol 113 : 30–37.

5. SimonsJE, RothenbergME, LawrenceRA (2005) Eotaxin-1-regulated eosinophils have a critical role in innate immunity against experimental Brugia malayi infection. Eur J Immunol 35 : 189–197.

6. RamalingamT, Ganley-LealL, PorteP, RajanTV (2003) Impaired clearance of primary but not secondary Brugia infections in IL-5 deficient mice. Exp Parasitol 105 : 131–139.

7. Le GoffL, LokeP, AliHF, TaylorDW, AllenJE (2000) Interleukin-5 is essential for vaccine-mediated immunity but not innate resistance to a filarial parasite. Infect Immun 68 : 2513–2517.

8. AbrahamD, LeonO, Schnyder-CandrianS, WangCC, GaliotoAM, et al. (2004) Immunoglobulin E and eosinophil-dependent protective immunity to larval Onchocerca volvulus in mice immunized with irradiated larvae. Infect Immun 72 : 810–817.

9. HerbertDR, LeeJJ, LeeNA, NolanTJ, SchadGA, et al. (2000) Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol 165 : 4544–4551.

10. GaliotoAM, HessJA, NolanTJ, SchadGA, LeeJJ, et al. (2006) Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval Strongyloides stercoralis in mice. Infect Immun 74 : 5730–5738.

11. KnottML, MatthaeiKI, GiacominPR, WangH, FosterPS, et al. (2007) Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. Int J Parasitol 37 : 1367–1378.

12. VallanceBA, MatthaeiKI, SanovicS, YoungIG, CollinsSM (2000) Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunol 22 : 487–492.

13. HamannKJ, GleichGJ, CheckelJL, LoegeringDA, McCallJW, et al. (1990) In vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. J Immunol 144 : 3166–3173.

14. SpechtS, SaeftelM, ArndtM, EndlE, DubbenB, et al. (2006) Lack of eosinophil peroxidase or major basic protein impairs defense against murine filarial infection. Infect Immun 74 : 5236–5243.

15. FabreV, BeitingDP, BlissSK, GebreselassieNG, GagliardoLF, et al. (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. J Immunol 182 : 1577–1583.

16. BabayanSA, ReadAF, LawrenceRA, BainO, AllenJE (2010) Filarial parasites develop faster and reproduce earlier in response to host immune effectors that determine filarial life expectancy. PLoS Biol 8: e1000525.

17. HallLR, MehlotraRK, HigginsAW, HaxhiuMA, PearlmanE (1998) An essential role for interleukin-5 and eosinophils in helminth-induced airway hyperresponsiveness. Infect Immun 66 : 4425–4430.

18. PinelliE, WithagenC, FonvilleM, VerlaanA, DormansJ, et al. (2005) Persistent airway hyper-responsiveness and inflammation in Toxocara canis-infected BALB/c mice. Clin Exp Allergy 35 : 826–832.

19. EnobeCS, AraujoCA, PeriniA, MartinsMA, MacedoMS, et al. (2006) Early stages of Ascaris suum induce airway inflammation and hyperreactivity in a mouse model. Parasite Immunol 28 : 453–461.

20. PegorierS, WagnerLA, GleichGJ, PretolaniM (2006) Eosinophil-derived cationic proteins activate the synthesis of remodeling factors by airway epithelial cells. J Immunol 177 : 4861–4869.

21. OchkurSI, KimJD, ProtheroeCA, ColbertD, MoqbelR, et al. (2012) The development of a sensitive and specific ELISA for mouse eosinophil peroxidase: assessment of eosinophil degranulation ex vivo and in models of human disease. J Immunol Methods 375 : 138–147.

22. MehlotraRK, HallLR, HaxhiuMA, PearlmanE (2001) Reciprocal Immunomodulatory Effects of Gamma Interferon and Interleukin-4 on Filaria-Induced Airway Hyperresponsiveness. Infect Immun 69 : 1463–1468.

23. LawrenceRA, AllenJE, OsborneJ, MaizelsRM (1994) Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and Ig isotype responses in BALB/c mice. J Immunol 153 : 1216–1224.

24. LawrenceRA, AllenJE, GrayCA (2000) Requirements for in vivo IFN-γ induction by live microfilariae of the parasitic nematode, Brugia malayi. Parasitology 120 : 631–640.

25. O'BryanL, PinkstonP, KumaraswamiV, VijayanV, YenokidaG, et al. (2003) Localized eosinophil degranulation mediates disease in tropical pulmonary eosinophilia. Infect Immun 71 : 1337–1342.

26. RamalingamT, PorteP, LeeJ, RajanTV (2005) Eosinophils, but not eosinophil peroxidase or major basic protein, are important for host protection in experimental Brugia pahangi infection. Infect Immun 73 : 8442–8443.

27. DenzlerKL, BorchersMT, CrosbyJR, CieslewiczG, HinesEM, et al. (2001) Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J Immunol 167 : 1672–1682.

28. DenzlerKL, FarmerSC, CrosbyJR, BorchersM, CieslewiczG, et al. (2000) Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J Immunol 165 : 5509–5517.

29. PearlmanE, HazlettFEJr, BoomWH, KazuraJW (1993) Induction of murine T-helper-cell responses to the filarial nematode Brugia malayi.. Infect Immun 61 : 1105–1112.

30. O'ConnellAE, HessJA, SantiagoGA, NolanTJ, LokJB, et al. (2011) Major basic protein from eosinophils and myeloperoxidase from neutrophils are required for protective immunity to Strongyloides stercoralis in mice. Infect Immun 79 : 2770–2778.

31. SimonsJE, GrayCA, LawrenceRA (2010) Absence of regulatory IL-10 enhances innate protection against filarial parasites by a neutrophil-independent mechanism. Parasite Immunol 32 : 473–478.

32. KitaH (2011) Eosinophils: multifaceted biological properties and roles in health and disease. Immunol Rev 242 : 161–177.

33. SpencerLA, WellerPF (2010) Eosinophils and Th2 immunity: contemporary insights. Immunol Cell Biol 88 : 250–256.

34. DoyleAD, JacobsenEA, OchkurSI, McGarryMP, ShimKG, et al. (2013) Expression of the secondary granule proteins major basic protein 1 (MBP-1) and eosinophil peroxidase (EPX) is required for eosinophilopoiesis in mice. Blood 122 : 781–790.

35. JacobsenEA, OchkurSI, PeroRS, TaranovaAG, ProtheroeCA, et al. (2008) Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J Exp Med 205 : 699–710.

36. FulkersonPC, FischettiCA, McBrideML, HassmanLM, HoganSP, et al. (2006) A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci US 103 : 16418–16423.

37. VoehringerD, ReeseTA, HuangX, ShinkaiK, LocksleyRM (2006) Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med 203 : 1435–1446.

38. SchroederJH, SimbiBH, FordL, ColeSR, TaylorMJ, et al. (2012) Live Brugia malayi microfilariae inhibit transendothelial migration of neutrophils and monocytes. PLoS Negl Trop Dis 6: e1914.

39. CarterT, SumiyaM, ReillyK, AhmedR, SobieszczukP, et al. (2007) Mannose-binding lectin A-deficient mice have abrogated antigen-specific IgM responses and increased susceptibility to a nematode infection. J Immunol 178 : 5116–5123.

40. LomaskM (2006) Further exploration of the Penh parameter. Experimental and toxicologic pathology : official journal of the Gesellschaft fur Toxikologische Pathologie 57(Suppl 2): 13–20.

41. MiltonPL, DickinsonH, JenkinG, LimR (2012) Assessment of respiratory physiology of C57BL/6 mice following bleomycin administration using barometric plethysmography. Respiration; international review of thoracic diseases 83 : 253–266.

42. WitzenrathM, AhrensB, KubeSM, BraunA, HoymannHG, et al. (2006) Detection of allergen-induced airway hyperresponsiveness in isolated mouse lungs. American journal of physiology Lung cellular and molecular physiology 291: L466–472.

43. MitznerW, TankersleyC (2003) Interpreting Penh in mice. Journal of applied physiology 94 : 828–831; author reply 831–822.

44. GrayCA, LawrenceRA (2002) A role for antibody and Fc receptor in the clearance of Brugia malayi microfilariae. Eur J Immunol 32 : 1114–1120.

45. GrayCA, LawrenceRA (2002) IFN-γ and nitric oxide production are not required for the immune-mediated clearance of Brugia malayi microfilariae in mice. Parasite Immunol 24 : 329–336.