Fonte GL, Baldriche AJ, Sarracent PJ, Hernández BY, Fong GA

Language: Spanish
References: 102
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ABSTRACT

Introduction: The last two decades have witnessed a swift accumulation of knowledge about the immunology of helminthiases. The information now available allows to better understand human defense mechanisms against helminth infection. Another area of knowledge about the immunology of helminthiases which has also benefited from such recent expansion of knowledge is the regulation of host immune responses by the parasite, with its great variety of clinical and epidemiological implications.
Objectives: Review publications about the evidence, mechanisms and consequences of the regulation of host immune responses by helminths.
Methods: Using various search engines, a review was conducted of papers about helminths, helminthiasis and regulation of host immune responses published from 1995 to 2015. Several monographs and original papers dated before that period were also consulted.
Results: The information gathered about the topics selected is presented, analyzed and whenever possible systematized.
Conclusions: Epidemiological, clinical and experimental data show that helminths can modulate the immune responses of their hosts and thus survive within them. Additionally, modulation of host immune responses has important clinical and epidemiological consequences which should be known by professionals related to the diagnosis, treatment and control of these parasitic diseases in order to improve the quality of medical practice.

REFERENCES

1. Hotez PJ, Brindley PJ, Bethony JM. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008;118:1311-21.

2. Cox F. History of human parasitology. Clin Microbiol Rev. 2002;15:595-612.

3. Hotez P, Ottesen E, Fenwick A, Molyneux D. The neglected tropical diseases: the ancient afflictions of stigma and poverty and the prospects for their control and elimination. Adv Exp Med Biol. 2006;582:23-33.

4. Salgame P, Yap GS, Gause WC. Effect of helminth-induced immunity on infections with microbial pathogens. Nat immunol. 2013;14:1118-26.

5. Dickson JH. The omnivorous Tyrolean Iceman: colon contents (meat, cereals, pollen, moss and whipworm) and stable isotope analyses. Phil Trans R Soc Lond. 2000;355:1843-9.

6. Maddison SE. Serodiagnosis of parasitic diseases. Clin Microbiol Rev. 1991;4:457-9.

7. Bundy DAP. This wormy world then and now. Parasitology Today. 1997;13:407-8.

8. de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soiltransmitted helminth infections: updating the global picture. Trends Parasitol. 2003;19:547-51.

9. Moreau E, Chauvin A. Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotech. 2010; doi:10.1155/2010/428593.

10. Mc Sorley HJ, Maizels RM. Helminth Infections and Host Immune Regulation. Clin Microbiol Rev. 2012;25:585-608.

11. Mishra PK, Palma M, Bleich D, Loke P, Gause WC. Systemic impact of intestinal helminth infections. Mucosal Immunol. 2014;7:753-62.

12. Flamme LA. The platinum age of parasitology: harnessing the power of the parasite. Parasite Immunol. 2015;37:275-6.

13. Fleming JO, Weinstock JV. Clinical trials of helminth therapy in autoimmune diseases: rationale and findings. Parasite Immunol. 2015;6:277-92.

14. Shepherd C, Navarro S, Wangchuk P, Wilson D, Daly NL, Loukas A. Identifying the immunomodulatory component of helminths. Parasite Immunol. 2015;6:293-303.

15. Nutman T. Looking beyond the induction of Th2 responses to explain immunomodulation by helminths. Parasite Immunol. 2015;6:303-13.

16. Loke P, Lim YAL. Helminths and the microbiota: parts of the hygiene hypothesis. Parasite Immunol. 2015;6:314-23.

17. Ezenwa VO, Jolles AN. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science. 2015;347:175-7.

18. Anderson RM, May RM. Helminth infection of humans: mathematical model, population dynamics and control. Adv Parasitol. 1985;24:1-101.

19. Bethony JM. Vaccines to combat the neglected tropical diseases. Immunol Rev. 2011;239:237-70.

20. Mangan NE, van Rooijen N, McKenzie AN, Fallon PG. Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol. 2006;176:138-47.

21. Palm NW, Rosenstein RK, Medzhitov R. Allergic host defences. Nature. 2012;484:465-72.

22. Anthony RM, Rutitzky LI, Urban JF, Stadecker MJ, Gause WC. Protective immune mechanisms in helminth infection. Nat Rev Immunol. 2007;7:975-87.

23. Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011;11:375-88.

24. Chen F. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat Med. 2012;18:260-6.

25. García-Hernández MH. Regulatory T cells in children with intestinal parasite infection. Parasite Immunol. 2009;31:597-603.

26. Hagan P, Blumenthal UJ, Dunn D, Simpson AJG, Wilkins HA. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991;349:243-5.

27. Joseph S. Increases in human T helper 2 cytokine responses to Schistosoma mansoni worm and worm-tegument antigens are induced by treatment with praziquantel. J Infec Dis. 2004;190:835-42.

28. Manoury B, Gregory WF, Maizels RM, Watts C . Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol. 2001;11:447-51.

29. Sartono E, Kruize YCM, Kurniawan-Atmadja A, Maizels RM, Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. J Infect Dis. 1997;175:1276-80.

30. Matisz CE, McDougall JJ, Sharkey KA, McKay D. Helminth parasites and the modulation of joint inflammation. J Parasitol Res. 2011:942616. doi:10.1155/2011/942616.

31. Saenz SA. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 2010;31:407-13.

32. Massacand JC. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc Natl Acad Sci USA. 2009;106:13968-73.

33. Taylor BC. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J. Exp Med. 2009;206:655-67.

34. Harris N. Advances in helminth immunology: optimism for future vaccine design? Trends Parasitol. 2011;27:288-93.

35. Fallon PG. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med. 2006;203:1105-16.

36. Moro K. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463:540-4.

37. Neill DR. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464:1367-70.

38. Price AE. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci USA. 2010;107:11489-94.

39. Martinez F, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451-83.

40. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723-37.

41. White RR, Artavanis-Tsakonas K. How helminths use excretory secretory fractions to modulate dendritic cells. Virulence. 2012;3:668-77.

42. Everts B. Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J Exp Med. 2012;209:1753-67.

43. Al-Riyami L, Harnett,W. Immunomodulatory properties of ES-62, a phosphorylcholine-containing glycoprotein secreted by Acanthocheilonema viteae. Endocr. Metab. Immune Disord. Drug Targets. 2012;12:45-52.

44. Klaver EJ. Trichuris suis-induced modulation of human dendritic cell function is glycan-mediated. Int J Parasitol. 2013;43:191-200.

45. Carvalho L. Mechanisms underlying helminth modulation of dendritic cell function. Immunology. 2009;126:28-34.

46. Everts B, Smits HH, Hokke CH, Yazdankbakhsh M. Sensing of helminth infections by dendritic cells via pattern recognition receptors and beyond: consequences for T helper 2 and regulatory T cell polarization. Eur J Immunol. 2010;40:1525-37.

47. Mahanty S. High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J Infect Dis. 1996;173:769-73.

48. Bancroft AJ, Else KJ, Humphreys NE, Grencis RK. The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. Int J Parasitol. 2001;31:1627-37.

49. Steinfelder S. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med. 2009;206:1681-90.

50. El Kasmi KC. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol. 2008;9:1399-406.

51. Harris J. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity. 2007;27:505-17.

52. Rausch S. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect Immun. 2008;76:1908-19.

53. Mosser DM, Edwards, JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8:958-69.

54. Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematodeinduced immunosuppression. Eur J Immunol. 2007;37:1887-904.

55. Setiawan T. Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine normal distal intestine. Infect Immun. 2007;75:4655-63.

56. Walsh KP, Brady MT, Finlay CM, Boon L, Mills KH. Infection with a helminth parasite attenuates autoimmunity through TGF-β-mediated suppression of Th17 and Th1 responses. J Immunol. 2009;183:1577-86.

57. Aranzamendi C. Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro. Parasite Immunol. 2012;34:210-23.

58. Elliott AM. Associations between helminth infection and CD4+ T cell count, viral load and cytokine responses in HIV-1-infected Ugandan adults. Trans R Soc Trop Med Hyg. 2003;97:103-8.

59. Li Z. The phenotype and function of naturally existing regulatory dendritic cells in nematode-infected mice. Int J Parasitol. 2011;41:1129-37.

60. Teixeira A. Cytokines, chemokine receptors, CD4+CD25HIGH+ T-cells and clinical forms of human schistosomiasis. Acta Trop. 2008;108:139-49.

61. Knowles SC. The effect of helminth co-infection on malaria in mice: a metaanalysis. Int J Parasitol. 2011;41:1041-51.

62. Schopf L. Differential modulation of allergic eye disease by chronic and acute Ascaris infection. Invest Ophthalmol Vis Sci. 2005;46:2772-80.

63. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008;133:775-87.

64. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton S. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3:944-50.

65. Yazdanbakhsh M. T cell responsiveness correlates differentially with antibody isotype levels in clinical and asymptomatic filariasis. J Infect Dis. 1993;167:925-31.

66. Su Z, Segura M, Stevenson MM. Reduced protective efficacy of a blood-stage malaria vaccine by concurrent nematode infection. Infect Immun. 2006;74:2138-44.

67. Correale J, Farez M, Razzitte G. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann Neurol. 2008;64:187-99.

68. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30:531-64.

69. MacDonald AS, Araujo MI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun. 2002;70:427-33.

70. Van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology. 2007;212:475-90.

71. Taylor B, Wadsworth J, Wadsworth M, Peckham M. Changes in the reported prevalence of childhood eczema since the 1939–45 war. The Lancet. 1984;2:1255-7.

72. Ring J. Davos Declaration: allergy as a global problem. Allergy. 2012;67:141-3.

73. Bruschi F, Araujo MI, Harnett W, Pinelli E. Allergy and Parasites. J Parasitol Research. 2013;2013:502562. doi:10.1155/2013/502562.

74. Cooper PJ, Barreto ML, Rodríguez LC. 2006. Human allergy and geohelminth infections: a review of the literature and a proposed conceptual model to guide the investigation of possible causal associations. Br Med Bull. 2006;80:203-18.

75. Flohr C, Quinnell RJ, Britton J. Do helminth parasites protect against atopy and allergic disease? Clin Exp Allergy. 2009;39:20-32.

76. van den Biggelaar A. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet. 2000;356:1723-27.

77. Rujeni N. Atopy is inversely related to schistosome infection intensity: a comparative study in Zimbabwean villages with distinct levels of Schistosoma haematobium infection. Int Arch Allergy Immunol. 2012;158:288-98.

78. Araujo M. Inverse association between skin response to aeroallergen and Schistosoma mansoni infection. Int Arch Allergy Immunol. 2000;123:145-8.

79. Medeiros M. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol. 2003; 111:947-51.

80. Araujo MI, de Carvalho EM. Human schistosomiasis decreases immune responses to allergens and clinical manifestations of asthma. Chem Immunol Allergy. 2006;90:29-44.

81. van den Biggelaar AH. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J Infect Dis. 2004;189:892-900.

82. Flohr C. Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. Clin Exp Allergy. 2010;40:131-42.

83. Obihara CC, Beyers N, Gie RP. Respiratory atopic disease, Ascaris immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy. 2006;36:640-8.

84. Flohr C, Tuyen LN, Lewis S, et al. Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study. J Allergy Clin Immunol. 2006;118:1305-11.

85. Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection. Am J Respirat Crit Care Med. 2006;174:514-23.

86. McKay DM. The therapeutic helminth? Trends Parasitol. 2008;24:1-6.

87. Weinstock JV. The possible link between de-worming and the emergence of immunological disease. J Lab Clin Med. 2002;139:334-8.

88. Weinstock JV. The worm returns. Nature. 2012;491:183-5.

89. Sabin EA, Araujo MI, Carvalho EM, Pearce EJ. Impairment of tetanus toxoid- -specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis. 1996;173:269-72.

90. Cooper PJ, Espinel I, Paredes W, Guderian RH, Nutman TB. Impaired tetanus- -specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. J Infect Dis. 1998;178:1133-8.

91. He Y. The inhibitory effect against collagen-induced arthritis by Schistosoma japonicum infection is infection stage-dependent. BMC Immunol. 2010;11:28. doi:10.1186/1471-2172-11-28.

92. Cooper PJ, Chico M, Losonsky G, Espinel I, Sandoval C, Aguilar M. Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. J Infect Dis. 2000;182:1199-206.

93. Cooper PJ, Chico M, Espinel I, Sandoval C, Guevara A, Levine M. Human infection with Ascaris lumbricoides is associated with suppression of the IL-2 response to recombinant cholera toxin B-subunit following vaccination with the live oral cholera vaccine CVD 103 HgR. Infect Immun. 2001;69:1574-80.

94. Elias D, Wolday D, Akuffo H, Petros B, Bronner U, Britton S. Effect of deworming on human T cell responses to mycobacterial antigens in helminth- -exposed individuals before and after bacille Calmette-Guérin (BCG) vaccination. Clin Exp Immunol. 2001;123:219-25.

95. Macedo MS, Barbuto JAM. Murine delayed type hypersensitivity is suppressed by Ascaris suum extract. Braz J Med Biol Res. 1988;21:523-5.

96. Faqim-Mauro EL, Coffmann RL, Abrahamsohn IA, Macedo MS. Mouse IgG1 antibodies comprise two functionally distinct types that are differentially regulated by IL-4 and IL-12. J Immunol. 1999;163:3572-6.

97. Su Z, Segura M, Stevenson MM. Reduced protective efficacy of a blood-stage malaria vaccine by concurrent nematode infection. Infect Immun. 2006;74:2138-44.

98. Ghosh K, Wu W, Antoine A, Bottazzi ME, Valenzuela J. Hotez P, Mendez S. The impact of concurrent and treated Ancylostoma ceylanicum hookworm infections on the immunogenicity of a recombinant hookworm vaccine in hamsters. JID. 2006;193:155-62.

99. Haswell-Elkins MR. Cross-sectional study of Opisthorchis viverrini infection and cholangiocarcinoma in communities within a high-risk area in northeast Thailand. Int J Cancer. 1994;59:505-9.

100. Smout MJ. Infection with the carcinogenic human liver fluke, Opisthorchis viverrini. Mol Biosyst. 2011;7:1367-75.

101. Fried B, Reddy A, Mayer D. Helminths in human carcinogenesis. Cancer Lett. 2011;305:239-49.

102. Smout MJ. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog. 2009;5:e1000611. doi:10.1371/journal.ppat.1000611.