Seminars in Immunopathology

, Volume 34, Issue 6, pp 889–901 | Cite as

Helminth infection in populations undergoing epidemiological transition: a friend or foe?

  • Aprilianto Eddy Wiria
  • Yenny Djuardi
  • Taniawati Supali
  • Erliyani Sartono
  • Maria Yazdanbakhsh
Review

Abstract

Helminth infections are highly prevalent in developing countries, especially in rural areas. With gradual development, there is a transition from living conditions that are dominated by infection, poor sanitation, manual labor, and traditional diet to a situation where burden of infections is reduced, infrastructure is improved, sedentary lifestyle dominates, and processed food forms a large proportion of the calorie intake. The combinations of some of the changes in lifestyle and environment are expected to result in alteration of the landscape of diseases, which will become dominated by non-communicable disorders. Here we review how the major helminth infections affect a large proportion of the population in the developing world and discuss their impact on the immune system and the consequences of this for other infections which are co-endemic in the same areas. Furthermore, we address the issue of decreasing helminth infections in many parts of the world within the context of increasing inflammatory, metabolic, and cardiovascular diseases.

Keywords

Helminths Co-infection Allergy Metabolic syndrome Cardiovascular diseases Epidemiological transition Immune responses 

References

  1. 1.
    Hotez PJ, Mistry N, Rubinstein J, Sachs JD (2011) Integrating neglected tropical diseases into AIDS, tuberculosis, and malaria control. N Engl J Med 364:2086–2089PubMedCrossRefGoogle Scholar
  2. 2.
    Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367:1521–1532PubMedCrossRefGoogle Scholar
  3. 3.
    Gryseels B (2012) Schistosomiasis. Infect Dis Clin North Am 26:383–397PubMedCrossRefGoogle Scholar
  4. 4.
    Ross AG, McManus DP, Farrar J, Hunstman RJ, Gray DJ, Li YS (2012) Neuroschistosomiasis. J Neurol 259:22–32PubMedCrossRefGoogle Scholar
  5. 5.
    Ross AG, Vickers D, Olds GR, Shah SM, McManus DP (2007) Katayama syndrome. Lancet Infect Dis 7:218–224PubMedCrossRefGoogle Scholar
  6. 6.
    Taylor MJ, Hoerauf A, Bockarie M (2010) Lymphatic filariasis and onchocerciasis. Lancet 376:1175–1185PubMedCrossRefGoogle Scholar
  7. 7.
    Hoerauf A, Pfarr K, Mand S, Debrah AY, Specht S (2011) Filariasis in Africa—treatment challenges and prospects. Clin Microbiol Infect 17:977–985PubMedCrossRefGoogle Scholar
  8. 8.
    Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133:775–787PubMedCrossRefGoogle Scholar
  9. 9.
    Maizels RM, Yazdanbakhsh M (2008) T-cell regulation in helminth parasite infections: implications for inflammatory diseases. Chem Immunol Allergy 94:112–123PubMedCrossRefGoogle Scholar
  10. 10.
    Hussaarts L, van der Vlugt LE, Yazdanbakhsh M, Smits HH (2011) Regulatory B-cell induction by helminths: implications for allergic disease. J Allergy Clin Immunol 128:733–739PubMedCrossRefGoogle Scholar
  11. 11.
    Atochina O, Daly-Engel T, Piskorska D, McGuire E, Harn DA (2001) A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1(+) macrophages that suppress naive CD4(+) T cell proliferation via an IFN-gamma and nitric oxide-dependent mechanism. J Immunol 167:4293–4302PubMedGoogle Scholar
  12. 12.
    Everts B, Smits HH, Hokke CH, Yazdanbakhsh M (2010) Helminths and dendritic cells: sensing and regulating via pattern recognition receptors, Th2 and Treg responses. Eur J Immunol 40:1525–1537PubMedCrossRefGoogle Scholar
  13. 13.
    Broere F, du Pre MF, van Berkel LA, Garssen J, Schmidt-Weber CB, Lambrecht BN, Hendriks RW, Nieuwenhuis EE, Kraal G, Samsom JN (2009) Cyclooxygenase-2 in mucosal DC mediates induction of regulatory T cells in the intestine through suppression of IL-4. Mucosal Immunol 2:254–264PubMedCrossRefGoogle Scholar
  14. 14.
    Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969PubMedCrossRefGoogle Scholar
  15. 15.
    Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, Ouma JH, Capron A, Pierce RJ, Sturrock RF (1992) Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol 22:1483–1494PubMedCrossRefGoogle Scholar
  16. 16.
    Roberts M, Butterworth AE, Kimani G, Kamau T, Fulford AJ, Dunne DW, Ouma JH, Sturrock RF (1993) Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect Immun 61:4984–4993PubMedGoogle Scholar
  17. 17.
    Betts CJ, Wilson RA (1998) Th1 cytokine mRNA expression dominates in the skin-draining lymph nodes of C57BL/6 mice following vaccination with irradiated Schistosoma mansoni cercariae, but is down-regulated upon challenge infection. Immunology 93:49–54PubMedCrossRefGoogle Scholar
  18. 18.
    Hoffmann KF, James SL, Cheever AW, Wynn TA (1999) Studies with double cytokine-deficient mice reveal that highly polarized Th1- and Th2-type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni. J Immunol 163:927–938PubMedGoogle Scholar
  19. 19.
    Mwatha JK, Kimani G, Kamau T, Mbugua GG, Ouma JH, Mumo J, Fulford AJ, Jones FM, Butterworth AE, Roberts MB, Dunne DW (1998) High levels of TNF, soluble TNF receptors, soluble ICAM-1, and IFN-gamma, but low levels of IL-5, are associated with hepatosplenic disease in human schistosomiasis mansoni. J Immunol 160:1992–1999PubMedGoogle Scholar
  20. 20.
    Alves Oliveira LF, Moreno EC, Gazzinelli G, Martins-Filho OA, Silveira AM, Gazzinelli A, Malaquias LC, LoVerde P, Leite PM, Correa-Oliveira R (2006) Cytokine production associated with periportal fibrosis during chronic schistosomiasis mansoni in humans. Infect Immun 74:1215–1221PubMedCrossRefGoogle Scholar
  21. 21.
    Rutitzky LI, Bazzone L, Shainheit MG, Joyce-Shaikh B, Cua DJ, Stadecker MJ (2008) IL-23 is required for the development of severe egg-induced immunopathology in schistosomiasis and for lesional expression of IL-17. J Immunol 180:2486–2495PubMedGoogle Scholar
  22. 22.
    Rutitzky LI, Stadecker MJ (2011) Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-gamma. Eur J Immunol 41:2677–2687PubMedCrossRefGoogle Scholar
  23. 23.
    Mbow M, Larkin BM, Meurs L, Wammes LJ, de Jong SE, Labuda L, Camara M, Smits HH, Polman K, Dieye TN, Mboup S, Stadecker MJ, Yazdanbakhsh M (2012) Th17 cells are associated with pathology in human schistosomiasis. J Infect Dis (in press)Google Scholar
  24. 24.
    Baumgart M, Tompkins F, Leng J, Hesse M (2006) Naturally occurring CD4+ Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. J Immunol 176:5374–5387PubMedGoogle Scholar
  25. 25.
    Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, Leeto M, Kirsch R, Hall P, Mossmann H, Claussen B, Forster I, Brombacher F (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20:623–635PubMedCrossRefGoogle Scholar
  26. 26.
    Turner JD, Jenkins GR, Hogg KG, Aynsley SA, Paveley RA, Cook PC, Coles MC, Mountford AP (2011) CD4+ CD25+ regulatory cells contribute to the regulation of colonic Th2 granulomatous pathology caused by schistosome infection. PLoS Negl Trop Dis 5:e1269PubMedCrossRefGoogle Scholar
  27. 27.
    van der Vlugt LE, Labuda LA, Ozir-Fazalalikhan A, Lievers E, Gloudemans AK, Liu KY, Barr TA, Sparwasser T, Boon L, Ngoa UA, Feugap EN, Adegnika AA, Kremsner PG, Gray D, Yazdanbakhsh M, Smits HH (2012) Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS One 7:e30883PubMedCrossRefGoogle Scholar
  28. 28.
    Barron L, Wynn TA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur J Immunol 41:2509–2514PubMedCrossRefGoogle Scholar
  29. 29.
    Hayes KS, Bancroft AJ, Grencis RK (2007) The role of TNF-alpha in Trichuris muris infection II: global enhancement of ongoing Th1 or Th2 responses. Parasite Immunol 29:583–594PubMedCrossRefGoogle Scholar
  30. 30.
    Artis D, Humphreys NE, Bancroft AJ, Rothwell NJ, Potten CS, Grencis RK (1999) Tumor necrosis factor alpha is a critical component of interleukin 13-mediated protective T helper cell type 2 responses during helminth infection. J Exp Med 190:953–962PubMedCrossRefGoogle Scholar
  31. 31.
    Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grencis RK, Else KJ, Kamgno J, Boussinesq M, Bradley JE (2004) T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect Dis 190:1804–1811PubMedCrossRefGoogle Scholar
  32. 32.
    Else KJ, Grencis RK (1991) Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology 72:508–513PubMedGoogle Scholar
  33. 33.
    Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK (2005) Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308:1463–1465PubMedCrossRefGoogle Scholar
  34. 34.
    Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN, Barron L, Dickey BF, Wilson MS, Wynn TA, Grencis RK, Thornton DJ (2011) Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med 208:893–900PubMedCrossRefGoogle Scholar
  35. 35.
    Maizels RM, Hewitson JP, Smith KA (2012) Susceptibility and immunity to helminth parasites. Curr Opin Immunol 24:459–466PubMedCrossRefGoogle Scholar
  36. 36.
    Artis D, Potten CS, Else KJ, Finkelman FD, Grencis RK (1999) Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma. Exp Parasitol 92:144–153PubMedCrossRefGoogle Scholar
  37. 37.
    Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM (2010) Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 78:3160–3167PubMedCrossRefGoogle Scholar
  38. 38.
    Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, Kamgno J, Boussinesq M, Bradley JE (2008) Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis 197:1204–1212PubMedCrossRefGoogle Scholar
  39. 39.
    Figueiredo CA, Alcantara-Neves NM, Amorim LD, Silva NB, Carvalho LC, Cooper PJ, Rodrigues LC, Barreto ML (2011) Evidence for a modulatory effect of IL-10 on both Th1 and Th2 cytokine production: the role of the environment. Clin Immunol 139:57–64PubMedCrossRefGoogle Scholar
  40. 40.
    Reina OM, Schreiber F, Benitez S, Broncano N, Chico ME, Vaca M, Alexander N, Lewis DJ, Dougan G, Cooper PJ (2011) Effects of chronic ascariasis and trichuriasis on cytokine production and gene expression in human blood: a cross-sectional study. PLoS Negl Trop Dis 5:e1157CrossRefGoogle Scholar
  41. 41.
    Andolfo I, De FL, Asci R, Russo R, Colucci S, Gorrese M, Zollo M, Iolascon A (2010) Regulation of divalent metal transporter 1 (DMT1) non-IRE isoform by the microRNA Let-7d in erythroid cells. Haematologica 95:1244–1252PubMedCrossRefGoogle Scholar
  42. 42.
    Pandit KV, Corcoran D, Yousef H, Yarlagadda M, Tzouvelekis A, Gibson KF, Konishi K, Yousem SA, Singh M, Handley D, Richards T, Selman M, Watkins SC, Pardo A, Ben-Yehudah A, Bouros D, Eickelberg O, Ray P, Benos PV, Kaminski N (2010) Inhibition and role of let-7d in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 182:220–229PubMedCrossRefGoogle Scholar
  43. 43.
    Jungmann P, Figueredo-Silva J, Dreyer G (1991) Bancroftian lymphadenopathy: a histopathologic study of fifty-eight cases from northeastern Brazil. AmJTrop Med Hyg 45:325–331Google Scholar
  44. 44.
    Babu S, Bhat SQ, Pavan KN, Lipira AB, Kumar S, Karthik C, Kumaraswami V, Nutman TB (2009) Filarial lymphedema is characterized by antigen-specific Th1 and th17 proinflammatory responses and a lack of regulatory T cells. PLoS Negl Trop Dis 3:e420PubMedCrossRefGoogle Scholar
  45. 45.
    Babu S, Blauvelt CP, Kumaraswami V, Nutman TB (2006) Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J Immunol 176:3248–3256PubMedGoogle Scholar
  46. 46.
    Metenou S, Dembele B, Konate S, Dolo H, Coulibaly SY, Coulibaly YI, Diallo AA, Soumaoro L, Coulibaly ME, Sanogo D, Doumbia SS, Traore SF, Mahanty S, Klion A, Nutman TB (2010) At homeostasis filarial infections have expanded adaptive T regulatory but not classical Th2 cells. J Immunol 184:5375–5382PubMedCrossRefGoogle Scholar
  47. 47.
    Wammes LJ, Hamid F, Wiria AE, Wibowo H, Sartono E, Maizels RM, Smits HH, Supali T, Yazdanbakhsh M (2012) Regulatory T cells in human lymphatic filariasis: stronger functional activity in microfilaremics. PLoS Negl Trop Dis 6:e1655PubMedCrossRefGoogle Scholar
  48. 48.
    Korten S, Hoerauf A, Kaifi JT, Buttner DW (2011) Low levels of transforming growth factor-beta (TGF-beta) and reduced suppression of Th2-mediated inflammation in hyperreactive human onchocerciasis. Parasitology 138:35–45PubMedCrossRefGoogle Scholar
  49. 49.
    Hoerauf A, Kruse S, Brattig NW, Heinzmann A, Mueller-Myhsok B, Deichmann KA (2002) The variant Arg110Gln of human IL-13 is associated with an immunologically hyper-reactive form of onchocerciasis (sowda). Microbes Infect 4:37–42PubMedCrossRefGoogle Scholar
  50. 50.
    Satoguina J, Mempel M, Larbi J, Badusche M, Loliger C, Adjei O, Gachelin G, Fleischer B, Hoerauf A (2002) Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect 4:1291–1300PubMedCrossRefGoogle Scholar
  51. 51.
    Doetze A, Satoguina J, Burchard G, Rau T, Loliger C, Fleischer B, Hoerauf A (2000) Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol 12:623–630PubMedCrossRefGoogle Scholar
  52. 52.
    Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE (2004) Helminth parasites—masters of regulation. Immunol Rev 201:89–116PubMedCrossRefGoogle Scholar
  53. 53.
    Metenou S, Dembele B, Konate S, Dolo H, Coulibaly SY, Coulibaly YI, Diallo AA, Soumaoro L, Coulibaly ME, Sanogo D, Doumbia SS, Wagner M, Traore SF, Klion A, Mahanty S, Nutman TB (2009) Patent filarial infection modulates malaria-specific type 1 cytokine responses in an IL-10-dependent manner in a filaria/malaria-coinfected population. J Immunol 183:916–924PubMedCrossRefGoogle Scholar
  54. 54.
    Metenou S, Dembele B, Konate S, Dolo H, Coulibaly YI, Diallo AA, Soumaoro L, Coulibaly ME, Coulibaly SY, Sanogo D, Doumbia SS, Traore SF, Mahanty S, Klion A, Nutman TB (2011) Filarial infection suppresses malaria-specific multifunctional Th1 and Th17 responses in malaria and filarial coinfections. J Immunol 186:4725–4733PubMedCrossRefGoogle Scholar
  55. 55.
    Babu S, Bhat SQ, Kumar NP, Jayantasri S, Rukmani S, Kumaran P, Gopi PG, Kolappan C, Kumaraswami V, Nutman TB (2009) Human type 1 and 17 responses in latent tuberculosis are modulated by coincident filarial infection through cytotoxic T lymphocyte antigen-4 and programmed death-1. J Infect Dis 200:288–298PubMedCrossRefGoogle Scholar
  56. 56.
    Marin ND, Paris SC, Velez VM, Rojas CA, Rojas M, Garcia LF (2010) Regulatory T cell frequency and modulation of IFN-gamma and IL-17 in active and latent tuberculosis. Tuberculosis (Edinb) 90:252–261CrossRefGoogle Scholar
  57. 57.
    Bueno LL, Morais CG, Araujo FF, Gomes JA, Correa-Oliveira R, Soares IS, Lacerda MV, Fujiwara RT, Braga EM (2010) Plasmodium vivax: induction of CD4+ CD25+ FoxP3+ regulatory T cells during infection are directly associated with level of circulating parasites. PLoS One 5:e9623PubMedCrossRefGoogle Scholar
  58. 58.
    Scholzen A, Mittag D, Rogerson SJ, Cooke BM, Plebanski M (2009) Plasmodium falciparum-mediated induction of human CD25Foxp3 CD4 T cells is independent of direct TCR stimulation and requires IL-2, IL-10 and TGFbeta. PLoS Pathog 5:e1000543PubMedCrossRefGoogle Scholar
  59. 59.
    Wammes LJ, Hamid F, de GB Wiria AE, Sartono E, Maizels RM, Luty AJ, Fillie Y, Brice GT, Supali T, Smits HH, Yazdanbakhsh M (2010) Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur J Immunol 40:437–442PubMedCrossRefGoogle Scholar
  60. 60.
    Nacher M (2011) Interactions between worms and malaria: good worms or bad worms? Malar J 10:259PubMedCrossRefGoogle Scholar
  61. 61.
    Elliott A, Yazdanbakhsh M (2012) Troubles never come alone. Curr Opin HIV AIDS. doi:10.1097/COH.0b013e32835268ab
  62. 62.
    Elias D, Akuffo H, Thors C, Pawlowski A, Britton S (2005) Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol 139:398–404PubMedCrossRefGoogle Scholar
  63. 63.
    Dias AT, de Castro SB, Alves CC, Rezende AB, Rodrigues MF, Machado RR, Fernandes A, Negrao-Correa D, Teixeira HC, Ferreira AP (2011) Lower production of IL-17A and increased susceptibility to Mycobacterium bovis in mice coinfected with Strongyloides venezuelensis. Mem Inst Oswaldo Cruz 106:617–619PubMedGoogle Scholar
  64. 64.
    Erb KJ, Trujillo C, Fugate M, Moll H (2002) Infection with the helminth Nippostrongylus brasiliensis does not interfere with efficient elimination of Mycobacterium bovis BCG from the lungs of mice. Clin Diagn Lab Immunol 9:727–730PubMedGoogle Scholar
  65. 65.
    Frantz FG, Rosada RS, Peres-Buzalaf C, Perusso FR, Rodrigues V, Ramos SG, Kunkel SL, Silva CL, Faccioli LH (2010) Helminth coinfection does not affect therapeutic effect of a DNA vaccine in mice harboring tuberculosis. PLoS Negl Trop Dis 4:e700PubMedCrossRefGoogle Scholar
  66. 66.
    Segura M, Matte C, Thawani N, Su Z, Stevenson MM (2009) Modulation of malaria-induced immunopathology by concurrent gastrointestinal nematode infection in mice. Int J Parasitol 39:1525–1532PubMedCrossRefGoogle Scholar
  67. 67.
    Helmby H (2009) Gastrointestinal nematode infection exacerbates malaria-induced liver pathology. J Immunol 182:5663–5671PubMedCrossRefGoogle Scholar
  68. 68.
    Nacher M, Singhasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, Wuthisen R, Looareesuwan S (2002) Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol 88:55–58PubMedGoogle Scholar
  69. 69.
    Le Hesran JY, Akiana J, el HM N, Dia M, Senghor P, Konate L (2004) Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg 98:397–399PubMedCrossRefGoogle Scholar
  70. 70.
    Nacher M, Singhasivanon P, Traore B, Vannaphan S, Gay F, Chindanond D, Franetich JF, Mazier D, Looareesuwan S (2002) Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. AmJTrop Med Hyg 66:304–309Google Scholar
  71. 71.
    Magalhaes RJ, Clements AC (2011) Mapping the risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med 8:e1000438PubMedCrossRefGoogle Scholar
  72. 72.
    Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, Benzecry SG, Alecrim MG, Lacerda MV (2010) Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS One 5:e11206PubMedCrossRefGoogle Scholar
  73. 73.
    Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, Harrison LM, Bungiro RD, Benham-Pyle B, Bimi L, Edoh D, Bosompem K, Wilson M, Cappello M (2011) Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. AmJTrop Med Hyg 84:792–800CrossRefGoogle Scholar
  74. 74.
    Fernandez-Nino JA, Idrovo AJ, Cucunuba ZM, Reyes-Harker P, Guerra AP, Moncada LI, Lopez MC, Barrera SM, Cortes LJ, Olivera M, Nicholls RS (2012) Paradoxical associations between soil-transmitted helminths and Plasmodium falciparum infection. Trans R Soc Trop Med Hyg. doi:10.1016/j.trstmh.2012.07.012
  75. 75.
    Webb EL, Mawa PA, Ndibazza J, Kizito D, Namatovu A, Kyosiimire-Lugemwa J, Nanteza B, Nampijja M, Muhangi L, Woodburn PW, Akurut H, Mpairwe H, Akello M, Lyadda N, Bukusuba J, Kihembo M, Kizza M, Kizindo R, Nabulime J, Ameke C, Namujju PB, Tweyongyere R, Muwanga M, Whitworth JA, Elliott AM (2011) Effect of single-dose anthelmintic treatment during pregnancy on an infant's response to immunisation and on susceptibility to infectious diseases in infancy: a randomised, double-blind, placebo-controlled trial. Lancet 377:52–62PubMedCrossRefGoogle Scholar
  76. 76.
    Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, Bruce MC, Ranford-Cartwright L, O' Neill SM, Holland CV (2010) Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis 10:277PubMedCrossRefGoogle Scholar
  77. 77.
    Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M (2007) Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. AmJTrop Med Hyg 77:1091–1095Google Scholar
  78. 78.
    Tristao-Sa R, Ribeiro-Rodrigues R, Johnson LT, Pereira FE, Dietze R (2002) Intestinal nematodes and pulmonary tuberculosis. Rev Soc Bras Med Trop 35:533–535PubMedCrossRefGoogle Scholar
  79. 79.
    Elias D, Britton S, Aseffa A, Engers H, Akuffo H (2008) Poor immunogenicity of BCG in helminth infected population is associated with increased in vitro TGF-beta production. Vaccine 26:3897–3902PubMedCrossRefGoogle Scholar
  80. 80.
    Zevallos K, Vergara KC, Vergara A, Vidal C, Garcia HH, Evans CA (2010) Tuberculin skin-test reactions are unaffected by the severity of hyperendemic intestinal helminth infections and co-infections. AmJTrop Med Hyg 83:319–325CrossRefGoogle Scholar
  81. 81.
    Webb EL, Ekii AO, Pala P (2012) Epidemiology and immunology of helminth–HIV interactions. Curr Opin HIV AIDS 7:245–253PubMedCrossRefGoogle Scholar
  82. 82.
    Walson JL, Herrin BR, John-Stewart G (2009) Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev 3:CD006419PubMedGoogle Scholar
  83. 83.
    Webb EL, Kyosiimire-Lugemwa J, Kizito D, Nkurunziza P, Lule S, Muhangi L, Muwanga M, Kaleebu P, Elliott AM (2012) The effect of anthelmintic treatment during pregnancy on HIV plasma viral load: results from a randomized, double-blind, placebo-controlled trial in Uganda. J Acquir Immune Defic Syndr 60:307–313PubMedGoogle Scholar
  84. 84.
    Sangare LR, Herrin BR, John-Stewart G, Walson JL (2011) Species-specific treatment effects of helminth/HIV-1 co-infection: a systematic review and meta-analysis. Parasitology 138:1546–1558PubMedCrossRefGoogle Scholar
  85. 85.
    Pulendran B, Artis D (2012) New paradigms in type 2 immunity. Science 337:431–435PubMedCrossRefGoogle Scholar
  86. 86.
    Xu F, Yan S, Li F, Cai M, Chai W, Wu M, Fu C, Zhao Z, Kan H, Kang K, Xu J (2012) Prevalence of childhood atopic dermatitis: an urban and rural community-based study in Shanghai, China. PLoS One 7:e36174PubMedCrossRefGoogle Scholar
  87. 87.
    Cooper PJ, Chico ME, Rodrigues LC, Ordonez M, Strachan D, Griffin GE, Nutman TB (2003) Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol 111:995–1000PubMedCrossRefGoogle Scholar
  88. 88.
    Dagoye D, Bekele Z, Woldemichael K, Nida H, Yimam M, Hall A, Venn AJ, Britton JR, Hubbard R, Lewis SA (2003) Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia. Am J Respir Crit Care Med 167:1369–1373PubMedCrossRefGoogle Scholar
  89. 89.
    van den Biggelaar AH, van RR, Rodrigues LC, Lell B, Deelder AM, Kremsner PG, Yazdanbakhsh M (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356:1723–1727PubMedCrossRefGoogle Scholar
  90. 90.
    Yazdanbakhsh M, Kremsner PG, van RR (2002) Allergy, parasites, and the hygiene hypothesis. Science 296:490–494PubMedCrossRefGoogle Scholar
  91. 91.
    Cooper PJ, Mitre E, Moncayo AL, Chico ME, Vaca MG, Nutman TB (2008) Ascaris lumbricoides-induced interleukin-10 is not associated with atopy in schoolchildren in a rural area of the tropics. J Infect Dis 197:1333–1340PubMedCrossRefGoogle Scholar
  92. 92.
    Flohr C, Tuyen LN, Quinnell RJ, Lewis S, Minh TT, Campbell J, Simmons C, Telford G, Brown A, Hien TT, Farrar J, Williams H, Pritchard DI, Britton J (2010) Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. Clin Exp Allergy 40:131–142PubMedGoogle Scholar
  93. 93.
    Smits HH, Hammad H, van NM, Soullie T, Willart MA, Lievers E, Kadouch J, Kool M, Kos-van OJ, Deelder AM, Lambrecht BN, Yazdanbakhsh M (2007) Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120:932–940PubMedCrossRefGoogle Scholar
  94. 94.
    Santiago HC, Leevan E, Bennuru S, Ribeiro-Gomes F, Mueller E, Wilson M, Wynn T, Garboczi D, Urban J, Mitre E, Nutman TB (2012) Molecular mimicry between cockroach and helminth glutathione S-transferases promotes cross-reactivity and cross-sensitization. J Allergy Clin Immunol 130:248–256PubMedCrossRefGoogle Scholar
  95. 95.
    Acevedo N, Sanchez J, Erler A, Mercado D, Briza P, Kennedy M, Fernandez A, Gutierrez M, Chua KY, Cheong N, Jimenez S, Puerta L, Caraballo L (2009) IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy 64:1635–1643PubMedCrossRefGoogle Scholar
  96. 96.
    Weinmayr G, Genuneit J, Nagel G, Bjorksten B, van HM, Priftanji A, Cooper P, Rijkjarv MA, von ME, Tsanakas J, Forastiere F, Doekes G, Garrido JB, Suarez-Varela MM, Braback L, Strachan DP (2010) International variations in associations of allergic markers and diseases in children: ISAAC Phase Two. Allergy 65:766–775PubMedCrossRefGoogle Scholar
  97. 97.
    Vereecken K, Kanobana K, Wordemann M, Junco DR, Menocal HL, Ruiz EA, Nunez FA, Rojas RL, Bonet GM, Polman K (2012) Associations between atopic markers in asthma and intestinal helminth infections in Cuban schoolchildren. Pediatr Allergy Immunol 23:332–338PubMedCrossRefGoogle Scholar
  98. 98.
    Levin ME, Le Souef PN, Motala C (2008) Total IgE in urban Black South African teenagers: the influence of atopy and helminth infection. Pediatr Allergy Immunol 19:449–454PubMedCrossRefGoogle Scholar
  99. 99.
    Cooper PJ, Chico ME, Vaca MG, Moncayo AL, Bland JM, Mafla E, Sanchez F, Rodrigues LC, Strachan DP, Griffin GE (2006) Effect of albendazole treatments on the prevalence of atopy in children living in communities endemic for geohelminth parasites: a cluster-randomised trial. Lancet 367:1598–1603PubMedCrossRefGoogle Scholar
  100. 100.
    Bager P, Vinkel HA, Wohlfahrt J, Melbye M (2012) Helminth infection does not reduce risk for chronic inflammatory disease in a population-based cohort study. Gastroenterology 142:55–62PubMedCrossRefGoogle Scholar
  101. 101.
    Mpairwe H, Webb EL, Muhangi L, Ndibazza J, Akishule D, Nampijja M, Ngom-wegi S, Tumusime J, Jones FM, Fitzsimmons C, Dunne DW, Muwanga M, Rodrigues LC, Elliott AM (2011) Anthelminthic treatment during pregnancy is associated with increased risk of infantile eczema: randomised-controlled trial results. Pediatr Allergy Immunol 22:305–312PubMedCrossRefGoogle Scholar
  102. 102.
    Djuardi Y, Wammes LJ, Supali T, Sartono E, Yazdanbakhsh M (2011) Immunological footprint: the development of a child's immune system in environments rich in microorganisms and parasites. Parasitology 138:1508–1518PubMedCrossRefGoogle Scholar
  103. 103.
    Moncayo AL, Vaca M, Oviedo G, Erazo S, Quinzo I, Fiaccone RL, Chico ME, Barreto ML, Cooper PJ (2010) Risk factors for atopic and non-atopic asthma in a rural area of Ecuador. Thorax 65:409–416PubMedCrossRefGoogle Scholar
  104. 104.
    Croft AM, Bager P, Kumar S (2012) Helminth therapy (worms) for allergic rhinitis. Cochrane Database Syst Rev 4:CD009238PubMedGoogle Scholar
  105. 105.
    Bager P, Arnved J, Ronborg S, Wohlfahrt J, Poulsen LK, Westergaard T, Petersen HW, Kristensen B, Thamsborg S, Roepstorff A, Kapel C, Melbye M (2010) Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol 125:123–130PubMedCrossRefGoogle Scholar
  106. 106.
    Feary JR, Venn AJ, Mortimer K, Brown AP, Hooi D, Falcone FH, Pritchard DI, Britton JR (2010) Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin Exp Allergy 40:299–306PubMedCrossRefGoogle Scholar
  107. 107.
    Wang CC, Nolan TJ, Schad GA, Abraham D (2001) Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin. Clin Exp Allergy 31:495–503PubMedCrossRefGoogle Scholar
  108. 108.
    Wohlleben G, Trujillo C, Muller J, Ritze Y, Grunewald S, Tatsch U, Erb KJ (2004) Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 16:585–596PubMedCrossRefGoogle Scholar
  109. 109.
    Pinelli E, Brandes S, Dormans J, Gremmer E, van LH (2008) Infection with the roundworm Toxocara canis leads to exacerbation of experimental allergic airway inflammation. Clin Exp Allergy 38:649–658PubMedCrossRefGoogle Scholar
  110. 110.
    Cooper PJ, Chico ME, Guadalupe I, Sandoval CA, Mitre E, Platts-Mills TA, Barreto ML, Rodrigues LC, Strachan DP, Griffin GE (2011) Impact of early life exposures to geohelminth infections on the development of vaccine immunity, allergic sensitization, and allergic inflammatory diseases in children living in tropical Ecuador: the ECUAVIDA birth cohort study. BMC Infect Dis 11:184PubMedCrossRefGoogle Scholar
  111. 111.
    Pritchard DI, Blount DG, Schmid-Grendelmeier P, Till SJ (2012) Parasitic worm therapy for allergy: is this incongruous or avant-garde medicine? Clin Exp Allergy 42:505–512PubMedCrossRefGoogle Scholar
  112. 112.
    Hamid F, Wiria AE, Wammes LJ, Kaisar MM, Lell B, Ariawan I, Uh HW, Wibowo H, Djuardi Y, Wahyuni S, Schot R, Verweij JJ, van RR, May L, Sartono E, Yazdanbakhsh M, Supali T (2011) A longitudinal study of allergy and intestinal helminth infections in semi urban and rural areas of Flores, Indonesia (ImmunoSPIN Study). BMC Infect Dis 11:83PubMedCrossRefGoogle Scholar
  113. 113.
    Endara P, Vaca M, Chico ME, Erazo S, Oviedo G, Quinzo I, Rodriguez A, Lovato R, Moncayo AL, Barreto ML, Rodrigues LC, Cooper PJ (2010) Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity. Clin Exp Allergy 40:1669–1677PubMedCrossRefGoogle Scholar
  114. 114.
    Weinstock JV, Elliott DE (2009) Helminths and the IBD hygiene hypothesis. Inflamm Bowel Dis 15:128–133PubMedCrossRefGoogle Scholar
  115. 115.
    Sewell D, Qing Z, Reinke E, Elliot D, Weinstock J, Sandor M, Fabry Z (2003) Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 15:59–69PubMedCrossRefGoogle Scholar
  116. 116.
    Stromnes IM, Cerretti LM, Liggitt D, Harris RA, Goverman JM (2008) Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat Med 14:337–342PubMedCrossRefGoogle Scholar
  117. 117.
    Kroenke MA, Carlson TJ, Andjelkovic AV, Segal BM (2008) IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J Exp Med 205:1535–1541PubMedCrossRefGoogle Scholar
  118. 118.
    Correale J, Farez MF (2011) The impact of parasite infections on the course of multiple sclerosis. J Neuroimmunol 233:6–11PubMedCrossRefGoogle Scholar
  119. 119.
    Correale J, Farez M (2009) Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms. J Immunol 183:5999–6012PubMedCrossRefGoogle Scholar
  120. 120.
    Correale J, Farez M, Razzitte G (2008) Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann Neurol 64:187–199PubMedCrossRefGoogle Scholar
  121. 121.
    Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV (2005) Trichuris suis therapy in Crohn's disease. Gut 54:87–90PubMedCrossRefGoogle Scholar
  122. 122.
    Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV (2005) Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128:825–832PubMedCrossRefGoogle Scholar
  123. 123.
    Fleming JO, Isaak A, Lee JE, Luzzio CC, Carrithers MD, Cook TD, Field AS, Boland J, Fabry Z (2011) Probiotic helminth administration in relapsing–remitting multiple sclerosis: a phase 1 study. Mult Scler 17:743–754PubMedCrossRefGoogle Scholar
  124. 124.
    Broadhurst MJ, Leung JM, Kashyap V, McCune JM, Mahadevan U, McKerrow JH, Loke P (2010) IL-22+ CD4+ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient. Sci Transl Med 2:60ra88PubMedCrossRefGoogle Scholar
  125. 125.
    Sugimoto K, Ogawa A, Mizoguchi E, Shimomura Y, Andoh A, Bhan AK, Blumberg RS, Xavier RJ, Mizoguchi A (2008) IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 118:534–544PubMedGoogle Scholar
  126. 126.
    Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, Benjamin WH, Orenstein JM, Smith PD (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115:66–75PubMedGoogle Scholar
  127. 127.
    Weng M, Huntley D, Huang IF, Foye-Jackson O, Wang L, Sarkissian A, Zhou Q, Walker WA, Cherayil BJ, Shi HN (2007) Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J Immunol 179:4721–4731PubMedGoogle Scholar
  128. 128.
    Hunter MM, Wang A, Parhar KS, Johnston MJ, Van RN, Beck PL, McKay DM (2010) In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138:1395–1405PubMedCrossRefGoogle Scholar
  129. 129.
    Wolff MJ, Broadhurst MJ, Loke P (2012) Helminthic therapy: improving mucosal barrier function. Trends Parasitol. doi:10.1016/j.pt.2012.02.008
  130. 130.
    Berry JD, Liu K, Folsom AR, Lewis CE, Carr JJ, Polak JF, Shea S, Sidney S, O'Leary DH, Chan C, Lloyd-Jones DM (2009) Prevalence and progression of subclinical atherosclerosis in younger adults with low short-term but high lifetime estimated risk for cardiovascular disease: the coronary artery risk development in young adults study and multi-ethnic study of atherosclerosis. Circulation 119:382–389PubMedCrossRefGoogle Scholar
  131. 131.
    Tsimikas S, Kiechl S, Willeit J, Mayr M, Miller ER, Kronenberg F, Xu Q, Bergmark C, Weger S, Oberhollenzer F, Witztum JL (2006) Oxidized phospholipids predict the presence and progression of carotid and femoral atherosclerosis and symptomatic cardiovascular disease: five-year prospective results from the Bruneck study. J Am Coll Cardiol 47:2219–2228PubMedCrossRefGoogle Scholar
  132. 132.
    Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685–1695PubMedCrossRefGoogle Scholar
  133. 133.
    Libby P, Ridker PM, Hansson GK (2011) Progress and challenges in translating the biology of atherosclerosis. Nature 473:317–325PubMedCrossRefGoogle Scholar
  134. 134.
    Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM (2011) Inflammation, immunity, and hypertension. Hypertension 57:132–140PubMedCrossRefGoogle Scholar
  135. 135.
    Jain MK, Ridker PM (2005) Anti-inflammatory effects of statins: clinical evidence and basic mechanisms. Nat Rev Drug Discov 4:977–987PubMedCrossRefGoogle Scholar
  136. 136.
    Nissen SE, Tuzcu EM, Schoenhagen P, Crowe T, Sasiela WJ, Tsai J, Orazem J, Magorien RD, O'Shaughnessy C, Ganz P (2005) Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease. N Engl J Med 352:29–38PubMedCrossRefGoogle Scholar
  137. 137.
    Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z (2006) Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 12:178–180PubMedCrossRefGoogle Scholar
  138. 138.
    Kassan M, Galan M, Partyka M, Trebak M, Matrougui K (2011) Interleukin-10 released by CD4(+)CD25(+) natural regulatory T cells improves microvascular endothelial function through inhibition of NADPH oxidase activity in hypertensive mice. Arterioscler Thromb Vasc Biol 31:2534–2542PubMedCrossRefGoogle Scholar
  139. 139.
    Ueshima H, Sekikawa A, Miura K, Turin TC, Takashima N, Kita Y, Watanabe M, Kadota A, Okuda N, Kadowaki T, Nakamura Y, Okamura T (2008) Cardiovascular disease and risk factors in Asia: a selected review. Circulation 118:2702–2709PubMedCrossRefGoogle Scholar
  140. 140.
    Chan JC, Malik V, Jia W, Kadowaki T, Yajnik CS, Yoon KH, Hu FB (2009) Diabetes in Asia: epidemiology, risk factors, and pathophysiology. JAMA 301:2129–2140PubMedCrossRefGoogle Scholar
  141. 141.
    Jex AR, Lim YA, Bethony JM, Hotez PJ, Young ND, Gasser RB (2011) Soil-transmitted helminths of humans in Southeast Asia—towards integrated control. Adv Parasitol 74:231–265PubMedCrossRefGoogle Scholar
  142. 142.
    Stanley RG, Jackson CL, Griffiths K, Doenhoff MJ (2009) Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice. Atherosclerosis 207:131–138PubMedCrossRefGoogle Scholar
  143. 143.
    Meir KS, Leitersdorf E (2004) Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress. Arterioscler Thromb Vasc Biol 24:1006–1014PubMedCrossRefGoogle Scholar
  144. 144.
    Doenhoff MJ, Stanley RG, Griffiths K, Jackson CL (2002) An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite-induced lowering of blood total cholesterol. Parasitology 125:415–421PubMedCrossRefGoogle Scholar
  145. 145.
    La Flamme AC, Harvie M, Kenwright D, Cameron K, Rawlence N, Low YS, McKenzie S (2007) Chronic exposure to schistosome eggs reduces serum cholesterol but has no effect on atherosclerotic lesion development. Parasite Immunol 29:259–266PubMedCrossRefGoogle Scholar
  146. 146.
    Innala L, Moller B, Ljung L, Magnusson S, Smedby T, Sodergren A, Ohman ML, Rantapaa-Dahlqvist S, Wallberg-Jonsson S (2011) Cardiovascular events in early RA are a result of inflammatory burden and traditional risk factors: a five year prospective study. Arthritis Res Ther 13:R131PubMedCrossRefGoogle Scholar
  147. 147.
    Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE (2005) Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis Rheum 52:722–732PubMedCrossRefGoogle Scholar
  148. 148.
    del Rincon ID, Williams K, Stern MP, Freeman GL, Escalante A (2001) High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum 44:2737–2745PubMedCrossRefGoogle Scholar
  149. 149.
    Hot A, Lenief V, Miossec P (2012) Combination of IL-17 and TNFalpha induces a pro-inflammatory, pro-coagulant and pro-thrombotic phenotype in human endothelial cells. Ann Rheum Dis 71:768–776PubMedCrossRefGoogle Scholar
  150. 150.
    Micha R, Imamura F, von Wyler BM, Solomon DH, Hernan MA, Ridker PM, Mozaffarian D (2011) Systematic review and meta-analysis of methotrexate use and risk of cardiovascular disease. Am J Cardiol 108:1362–1370PubMedCrossRefGoogle Scholar
  151. 151.
    Mira E, Leon B, Barber DF, Jimenez-Baranda S, Goya I, Almonacid L, Marquez G, Zaballos A, Martinez A, Stein JV, Ardavin C, Manes S (2008) Statins induce regulatory T cell recruitment via a CCL1 dependent pathway. J Immunol 181:3524–3534PubMedGoogle Scholar
  152. 152.
    Hot A, Lavocat F, Lenief V, Miossec P (2012) Simvastatin inhibits the pro-inflammatory and pro-thrombotic effects of IL-17 and TNF-alpha on endothelial cells. Ann Rheum Dis. doi:10.1136/annrheumdis-2012-201887
  153. 153.
    Rhee SG, Woo HA (2011) Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H(2)O(2), and protein chaperones. Antioxid Redox Signal 15:781–794PubMedCrossRefGoogle Scholar
  154. 154.
    Robinson MW, Hutchinson AT, Dalton JP, Donnelly S (2010) Peroxiredoxin: a central player in immune modulation. Parasite Immunol 32:305–313PubMedCrossRefGoogle Scholar
  155. 155.
    Kisucka J, Chauhan AK, Patten IS, Yesilaltay A, Neumann C, Van Etten RA, Krieger M, Wagner DD (2008) Peroxiredoxin1 prevents excessive endothelial activation and early atherosclerosis. Circ Res 103:598–605PubMedCrossRefGoogle Scholar
  156. 156.
    Park JG, Yoo JY, Jeong SJ, Choi JH, Lee MR, Lee MN, Hwa LJ, Kim HC, Jo H, Yu DY, Kang SW, Rhee SG, Lee MH, Oh GT (2011) Peroxiredoxin 2 deficiency exacerbates atherosclerosis in apolipoprotein E-deficient mice. Circ Res 109:739–749PubMedCrossRefGoogle Scholar
  157. 157.
    Guo X, Yamada S, Tanimoto A, Ding Y, Wang KY, Shimajiri S, Murata Y, Kimura S, Tasaki T, Nabeshima A, Watanabe T, Kohno K, Sasaguri Y (2012) Overexpression of peroxiredoxin 4 attenuates atherosclerosis in apolipoprotein E knockout mice. Antioxid Redox Signal. doi:10.1089/ars.2012.4549
  158. 158.
    Donnelly S, Stack CM, O'Neill SM, Sayed AA, Williams DL, Dalton JP (2008) Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J 22:4022–4032PubMedCrossRefGoogle Scholar
  159. 159.
    Ou X, Thomas GR, Chacon MR, Tang L, Selkirk ME (1995) Brugia malayi: differential susceptibility to and metabolism of hydrogen peroxide in adults and microfilariae. Exp Parasitol 80:530–540PubMedCrossRefGoogle Scholar
  160. 160.
    Kumagai T, Osada Y, Ohta N, Kanazawa T (2009) Peroxiredoxin-1 from Schistosoma japonicum functions as a scavenger against hydrogen peroxide but not nitric oxide. Mol Biochem Parasitol 164:26–31PubMedCrossRefGoogle Scholar
  161. 161.
    Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98–107PubMedCrossRefGoogle Scholar
  162. 162.
    Feinstein R, Kanety H, Papa MZ, Lunenfeld B, Karasik A (1993) Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J Biol Chem 268:26055–26058PubMedGoogle Scholar
  163. 163.
    Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259:87–91PubMedCrossRefGoogle Scholar
  164. 164.
    Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867PubMedCrossRefGoogle Scholar
  165. 165.
    Aravindhan V, Mohan V, Surendar J, Rao MM, Ranjani H, Kumaraswami V, Nutman TB, Babu S (2010) Decreased prevalence of lymphatic filariasis among subjects with type-1 diabetes. AmJTrop Med Hyg 83:1336–1339CrossRefGoogle Scholar
  166. 166.
    Aravindhan V, Mohan V, Surendar J, Muralidhara RM, Pavankumar N, Deepa M, Rajagopalan R, Kumaraswami V, Nutman TB, Babu S (2010) Decreased prevalence of lymphatic filariasis among diabetic subjects associated with a diminished pro-inflammatory cytokine response (CURES 83). PLoS Negl Trop Dis 4:e707PubMedCrossRefGoogle Scholar
  167. 167.
    Cooke A (2009) Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126:12–17PubMedCrossRefGoogle Scholar
  168. 168.
    Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM (2011) Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332:243–247PubMedCrossRefGoogle Scholar
  169. 169.
    Ricardo-Gonzalez RR, Red EA, Odegaard JI, Jouihan H, Morel CR, Heredia JE, Mukundan L, Wu D, Locksley RM, Chawla A (2010) IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity. Proc Natl Acad Sci U S A 107:22617–22622PubMedCrossRefGoogle Scholar
  170. 170.
    Hewitson JP, Grainger JR, Maizels RM (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 167:1–11PubMedCrossRefGoogle Scholar
  171. 171.
    van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, Espevik T, de Jong EC, Kapsenberg ML, Golenbock DT, Tielens AG, Yazdanbakhsh M (2002) A novel host–parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem 277:48122–48129PubMedCrossRefGoogle Scholar
  172. 172.
    Schramm G, Haas H (2010) Th2 immune response against Schistosoma mansoni infection. Microbes Infect 12:881–888PubMedCrossRefGoogle Scholar
  173. 173.
    Everts B, Hussaarts L, Driessen NN, Meevissen MH, Schramm G, van der Ham AJ, van der Hoeven B, Scholzen T, Burgdorf S, Mohrs M, Pearce EJ, Hokke CH, Haas H, Smits HH, Yazdanbakhsh M (2012) Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J Exp Med 209:1753–1767PubMedCrossRefGoogle Scholar
  174. 174.
    Schramm G, Mohrs K, Wodrich M, Doenhoff MJ, Pearce EJ, Haas H, Mohrs M (2007) Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J Immunol 178:6023–6027PubMedGoogle Scholar
  175. 175.
    Klotz C, Ziegler T, Figueiredo AS, Rausch S, Hepworth MR, Obsivac N, Sers C, Lang R, Hammerstein P, Lucius R, Hartmann S (2011) A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog 7:e1001248PubMedCrossRefGoogle Scholar
  176. 176.
    Robinson MW, Alvarado R, To J, Hutchinson AT, Dowdell SN, Lund M, Turnbull L, Whitchurch CB, O'Brien BA, Dalton JP, Donnelly S (2012) A helminth cathelicidin-like protein suppresses antigen processing and presentation in macrophages via inhibition of lysosomal vATPase. FASEB J. doi:10.1096/fj.12-213876
  177. 177.
    Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y, Filbey KJ, Finney CA, Greenwood EJ, Knox DP, Wilson MS, Belkaid Y, Rudensky AY, Maizels RM (2010) Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-beta pathway. J Exp Med 207:2331–2341PubMedCrossRefGoogle Scholar
  178. 178.
    Hewitson JP, Filbey KJ, Grainger JR, Dowle AA, Pearson M, Murray J, Harcus Y, Maizels RM (2011) Heligmosomoides polygyrus elicits a dominant nonprotective antibody response directed against restricted glycan and peptide epitopes. J Immunol 187:4764–4777PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Aprilianto Eddy Wiria
    • 1
    • 2
  • Yenny Djuardi
    • 1
    • 2
  • Taniawati Supali
    • 1
  • Erliyani Sartono
    • 2
  • Maria Yazdanbakhsh
    • 2
  1. 1.Department of Parasitology, Faculty of MedicineUniversity of IndonesiaJakartaIndonesia
  2. 2.Department of ParasitologyLeiden University Medical CenterLeidenThe Netherlands

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