Immune evasion, immunopathology and the regulation of the immune system

Pathogens

Volumn 2, Issue 1, 2013, Pages 71-91

  Sorci, Gabriele ^a   Cornet, Stéphane ^b,c   Faivre, Bruno ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b University de Montpellier   (France)

^c CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Autoimmunity; Hygiene hypothesis; Immune evasion; Immune regulation; Immunosuppression; Molecular mimicry; T cells

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; BACTERIUM; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; DOWN REGULATION; HELMINTH; HUMAN; IMMUNE DEFICIENCY; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOLOGY; IMMUNOREGULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR MIMICRY; NONHUMAN; PARASITOSIS; PROTOZOON; REVIEW; VIRUS;

EID: 84929299274     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens2010071     Document Type: Review

References (153)

1. Frank, S.A. Immunology and Evolution of Infectious Diseases; Priceton University Press: Priceton, NJ, USA, 2002
2. Rolff, J.; Siva-Jothy, M.T. Invertebrate ecological immunology. Science 2003, 301, 472-475
3. Schmid-Hempel, P. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 357-366
4. Schmid-Hempel, P.; Ebert, D. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 2003, 18, 27-32
5. Schmid-Hempel, P. Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology and Genetics; Oxford University Press: New York, NY, USA, 2011
6. Sheldon, B.C.; Verhulst, S. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol. Evol. 1996, 11, 317-321
7. Viney, M.E.; Riley, E.M.; Buchanan, K.L. Optimal immune responses: immunocompetence revisited. Trends Ecol. Evol. 2005, 20, 665-669
8. Graham, A.L.; Shuker, D.M.; Pollitt, L.C.; Auld, S.; Wilson, A.J.; Little, T.J. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct. Ecol. 2011, 25, 5-17
9. Pedersen, A.B.; Babayan, S.A. Wild immunology. Mol. Ecol. 2011, 20, 872-880
10. Stearns, S.C. The Evolution of Life Histories; Oxford University Press: Oxford, England, 1992
11. Bonneaud, C.; Mazuc, J.; Guillermo, G.; Haussy, C.; Chastel, O.; Faivre, B.; Sorci, G. Assessing the cost of mounting an immune response. Am. Nat. 2003, 161, 367-379
12. Soler, J.J.; de Neve, L.; Pérez-Contreras, T.; Soler, M.; Sorci, G. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 341-248
13. Sadd, B.M.; Schmid-Hempel, P. Principles of ecological immunology. Evol. Appl. 2009, 2, 113-121
14. Demas, G.E.; Chefer, V.; Talan, M.I.; Nelson, R.J. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am. J. Physiol. 1997, 273, R1631-R1637
15. Svensson, E.; Råberg, L.; Koch, C.; Hasselquist, D. Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 1998, 12, 912-919
16. Ots, I.; Kerimov, A.B.; Ivankina, E.; Ilyina, T.A.; Hõrak, P. Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. Lond. B Biol. Sci. 2001, 268, 1175-1181
17. Råberg, L.; Vestberg, M.; Hasselquist, D.; Holmdahl, R.; Svensson, E.; Nilsson, J.-Å. Basal metabolic rate and the evolution of the adaptative immune system. Proc. R. Soc. Lond. B Biol. Sci. 2002, 260, 817-821
18. Ksiazek, A.; Konarzewski, M.; Chadzinska, M.; Cichon, M. Costs of immune response in cold-stressed laboratory mice selected for high and low basal metabolism rates. Proc. R. Soc. B Biol. Sci. 2003, 270, 2025-2031
19. Martin, L.B.; Scheuerlein, A.; Wikelski, M. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 153-158
20. Eraud, C.; Duriez, O.; Chastel, O.; Faivre, B. The energetic cost of humoral immunity in the Collared Dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs? Funct. Ecol. 2005, 19, 110-118
21. Christen, U.; von Herrath, M.G. Infections and autoimmunity - Good or bad? J. Immunol. 2005, 174, 7481-7486
22. Sell, S. Immunology, Immunopathology and Immunity; ASM Press: Washington, D.C., USA, 2001
23. Graham, A.L.; Allen, J.E.; Read, A.F. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 2005, 36, 373-397
24. Kobasa, D.; Jones, S.M.; Shinya, K.; Kash, J.C.; Copps, J.; Ebihara, H.; Hatta, Y.; Kim, J.H.; Halfmann, P.; Hatta, M.; Feldmann, F.; Alimonti, J.B.; Fernando, L.; Li, Y.; Katze, M.G.; Feldmann, H.; Kawaoka, Y. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007, 445, 319-323
25. Moore, M.L.; Brown, C.C.; Spindler, K.R. T cells cause acute immunopathology and are required for long-term survival in mouse adenovirus type 1-induced encephalomyelitis. J. Virol. 2003, 77, 10060-10070
26. Brandt, S.M.; Dionne, M.S.; Khush, R.S.; Pham, L.N.; Vigdal, T.J.; Schneider, D.S. Secreted bacterial effectors and host-produced eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol. 2004, 2, 2067-2075
27. Long, G.H.; Chan, B.H.K.; Allen, J.E.; Read, A.F.; Graham, A.L. Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evol. Biol. 2008, 8, 128
28. Sorci, G.; Faivre, B. Inflammation and oxidative stress in vertebrate host-parasite systems. Phil. Trans. R. Soc. B 2009, 364, 71-83
29. Kaufmann, S.H.E.; Sher, A.; Ahmed, A.M. Immunology of Infectious Diseases; ASM Press: Washington D.C., USA, 2002
30. Kim, J.M.; Rasmussen, J.P.; Rudensky, A.Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nature Immunol. 2007, 8, 191-197
31. Belkaid, Y. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 2007, 7, 875-888
32. Bach, J.F. Regulatory T cells under scrutiny. Nat. Rev. Immunol. 2003, 3, 189-198
33. Bergstrom, C.T.; Antia, R. How do adaptive immune systems control pathogens while avoiding autoimmunity? Trends Ecol. Evol. 2006, 21, 22-28
34. Shevach, E.M. Regulatory T cells in autoimmmunity. Annu. Rev. Immunol. 2000, 18, 423-449
35. Sakaguchi, S.; Sakaguchi, N.; Shimizu, J.; Yamazaki, S.; Sakihama, T.; Itoh, M.; Kuniyasu, Y.; Nomura, T.; Toda, M.; Takahashi, T. Immunologic tolerance maintained by CD25(+) CD4(+) regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 2001, 182, 18-32
36. Walker, L.S.K.; Abbas, A.K. The enemy within: Keeping self-reactive T cells at bay in the periphery. Nat. Rev. Immunol. 2002, 2, 11-19
37. Kronenberg, M.; Rudensky, A. Regulation of immunity by self-reactive T cells. Nature 2005, 435, 598-604
38. Bennett, C.L.; Christie, J.; Ramsdell, F.; Brunkow, M.E.; Ferguson, P.J.; Whitesell, L.; Kelly, T.E.; Saulsbury, F.T.; Chance, P.F.; Ochs, H.D. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nature Genet. 2001, 27, 20-21
39. Bach, J.F. Mechanisms of disease: The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 2002, 347, 911-920
40. Gale, E.A.M. The rise of childhood type 1 diabetes in the 20th century. Diabetes 2002, 51, 3353-3361
41. Cooke, A.; Zaccone, P.; Raine, T.; Phillips, J.M.; Dunne, D.W. Infection and autoimmunity: are we winning the war, only to lose the peace? Trends Parasitol. 2004, 20, 316-321
42. Zaccone, P.; Fehervari, Z.; Phillips, J.M.; Dunne, D.W.; Cooke, A. Parasitic worms and inflammatory diseases. Parasite Immunol. 2006, 28, 515-523
43. Ploegh, H.L. Viral strategies of immune evasion. Science 1998, 280, 248-253
44. Sacks, D.; Sher, A. Evasion of innate immunity by parasitic protozoa. Nature Immunol. 2002, 3, 1041-1047
45. Hornef, M.W.; Wick, M.J.; Rhen, M.; Normark, S. Bacterial strategies for overcoming host innate and adaptive immune responses. Nature Immunol. 2002, 3, 1033-1040
46. Maizels, R.M.; Yazdanbakhsh, M. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat. Rev. Immunol. 2003, 3, 733-744
47. Finlay, B.B.; McFadden, G. Anti-immunology: Evasion of the host immune system by bacterial and viral pathogens. Cell 2006, 124, 767-782
48. Schmid-Hempel, P. Parasite immune evasion: a momentous molecular war. Trends Ecol. Evol. 2008, 23, 318-326
49. Young, D.; Hussell, T.; Dougan, G. Chronic bacterial infections: living with unwanted guests. Nature Immunol. 2002, 3, 1026-1032
50. Falkow, S. Is persistent bacterial infection good for your health? Cell 2006, 124, 699-702
51. Oldstone, M.B. Prevention of type I diabetes in non obese diabetic mice by virus infection. Science 1988, 239, 500-502
52. Oldstone, M.B. Viruses as therapeutic agents. I. Treatment of non obese insulin-dependent diabetic mice with virus prevents insulin-dependent diabetes mellitus while maintaining general immune competence. J. Exp. Med. 1990, 171, 2077-2089
53. Yazdanbakhsh, M.; Kremsner, P.G.; van Ree, R. Allergy, parasites, and the hygiene hypothesis. Science 2002, 296, 490-494
54. Zaccone, P.; Raine, T.; Sidobre, S.; Kronenberg, M.; Mastroeni, P.; Cooke, A. Salmonella typhimurium infection halts development of type 1 diabetes in NOD mice. Eur. J. Immunol. 2004, 34, 3246-3256
55. Bach, J.F. Infections and autoimmune diseases. J. Autoimmun. 2005, 25, 74-80
56. Maizels, R.M.; Balic, A.; Gomez-Escobar, N.; Nair, M.; Taylor, M.D.; Allen, J.E. Helminth parasites - masters of regulation. Immunol. Rev. 2004, 201, 89-116
57. Dunne, D.W.; Cooke, A. Opinion - A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol. 2005, 5, 420-426
58. Maizels, R.M. Infections and allergy - helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 2005, 17, 656-661
59. Cooke, A.; Tonks, P.; Jones, F.M.; O'Shea, H.; Hutchings, P.; Fulford, A.J.C.; Dunne, D.W. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 1999, 21, 169-176
60. La Flamme, A.C.; Ruddenklau, K.; Backstrom, B.T. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect. Immun. 2003, 71, 4996-5004
61. Nagayama, Y.; Watanabe, K.; Niwa, M.; McLachlan, S.M.; Rapoport, B. Schistosoma mansoni and alpha-galactosylceramide: Prophylactic effect of Th1 immune suppression in a mouse model of Graves' hyperthyroidism. J. Immunol. 2004, 173, 2167-2173
62. Wilson, M.S.; Taylor, M.D.; Balic, A.; Finney, C.A.M.; Lamb, J.R.; Maizels, R.M. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 2005, 202, 1199-1212
63. Bashir, M.E.H.; Andersen, P.; Fuss, I.J.; Shi, H.N.; Nagler-Anderson, C. An enteric helminth infection protects against an allergic response to dietary antigen. J. Immunol. 2002, 169, 3284-3292
64. Mosmann, T.R.; Fowell, D.J. The Th1/Th2 paradigm in infections. In Immunology of infectious diseases; Kaufmann, S.H.E., Sher, A., Ahmed, R., Eds.; ASM Press: Washington, D.C., USA, 2002; pp. 163-174
65. Iwashiro, M.; Messer, R.J.; Peterson, K.E.; Stromnes, I.M.; Sugie, T.; Hasenkrug, K.J. Immunosuppression by CD4(+) regulatory T cells induced by chronic retroviral infection. Proc. Natl Acad. Sci. USA 2001, 98, 9226-9230
66. Belkaid, Y.; Piccirillo, C.A.; Mendez, S.; Shevach, E.M.; Sacks, D.L. CD4(+)CD25(+) regulatory T cells control Leishmania major persistence and immunity. Nature 2002, 420, 502-507
67. Mendez, S.; Reckling, S.K.; Piccirillo, C.A.; Sacks, D.; Belkaid, Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent Leishmaniasis and control of concomitant immunity. J. Exp. Med. 2004, 200, 201-210
68. Toka, F.N.; Suvas, S.; Rouse, B.T. CD4(+) CD25(+) T cells regulate vaccine-generated primary and memory CD8(+) T-cell responses against herpes simplex virus type 1. J. Virol. 2004, 78, 13082-13089
69. Dittmer, U.; He, H.; Messer, R.J.; Schimmer, S.; Olbrich, A.R.M.; Ohlen, C.; Greenberg, P.D.; Stromnes, I.M.; Iwashiro, M.; Sakaguchi, S.; Evans, L.H.; Peterson, K.E.; Yang, G.J.; Hasenkrug, K.J. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 2004, 20, 293-303
70. Hisaeda, H.; Maekawa, Y.; Iwakawa, D.; Okada, H.; Himeno, K.; Kishihara, K.; Tsukumo, S.; Yasutomo, K. Escape of malaria parasites from host immunity requires CD4(+)CD25(+) regulatory T cells. Nat. Med. 2004, 10, 29-30
71. Navarro, L.; Alto, N.M.; Dixon, J.E. Functions of the Yersinia effector proteins in inhibiting host immune responses. Curr. Opin. Microbiol. 2005, 8, 21-27
72. Redpath, S.; Ghazal, P.; Gascoigne, N.R.J. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 2001, 9, 86-92
73. Sozzani, S.; Ghezzi, S.; Iannolo, G.; Luini, W.; Borsatti, A.; Polentarutti, N.; Sica, A.; Locati, M.; Mackay, C.; Wells, T.N.C.; Biswas, P.; Vicenzi, E.; Poli, G.; Mantovani, A. Interleukin 10 increases CCR5 expression and HIV infection in human monocytes. J. Exp. Med. 1998, 187, 439-444
74. Redpath, S.; Angulo, A.; Gascoigne, N.R.J.; Ghazal, P. Murine cytomegalovirus infection down-regulates MHC class II expression on macrophages by induction of IL-10. J. Immunol. 1999, 162, 6701-6707
75. Vallance, B.A.; Deng, W.Y.; De Grado, M.; Chan, C.; Jacobson, K.; Finlay, B.B. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect. Immun. 2002, 70, 6424-6435
76. Summers, R.W.; Elliott, D.E.; Urban, J.F.; Thompson, R.; Weinstock, J.V. Trichuris suis therapy in Crohn's disease. Gut 2005, 54, 87-90
77. Summers, R.W.; Elliott, D.E.; Urban, J.F.; Thompson, R.A.; Weinstock, J.V. Trichuris suis therapy for active ulcerative colitis: A randomized controlled trial. Gastroenterology 2005, 128, 825-832
78. Kamradt, T.; Goggel, R.; Erb, K.J. Induction, exacerbation and inhibition of allergic and autoimmune diseases by infection. Trends Immunol. 2005, 26, 260-267
79. Damian, R.T. Molecular mimicry: antigen sharing by parasite and host and its consequences. Am. Nat. 1964, 98, 129-149
80. Albert, L.J.; Inman, R.D. Mechanisms of disease: Molecular mimicry and autoimmunity. N. Engl. J. Med. 1999, 341, 2068-2074
81. Amedei, A.; Bergman, M.P.; Appelmelk, B.J.; Azzurri, A.; Benagiano, M.; Tamburini, C.; van der Zee, R.; Telford, J.L.; Vandenbroucke-Grauls, C.; D'Elios, M.M.; Del Prete, G. Molecular mimicry between Helicobacter pylori antigens and H+,K+-adenosine triphosphatase in human gastric autoimmunity. J. Exp. Med. 2003, 198, 1147-1156
82. De Libero, G.; Moran, A.P.; Gober, H.J.; Rossy, E.; Shamshiev, A.; Chelnokova, O.; Mazorra, Z.; Vendetti, S.; Sacchi, A.; Prendergast, M.M.; Sansano, S.; Tonevitsky, A.; Landmann, R.; Mori, L. Bacterial infections promote T cell recognition of self-glycolipids. Immunity 2005, 22, 763-772
83. Fujinami, R.S.; von Herrath, M.G.; Christen, U.; Whitton, J.L. Molecular mimicry, bystander activation, or viral persistence: Infections and autoimmune disease. Clin. Microbiol. Rev. 2006, 19, 80-94
84. Zhao, Z.S.; Granucci, F.; Yeh, L.; Schaffer, P.A.; Cantor, H. Molecular mimicry by herpes simplex virus type 1: autoimmune disease after viral infection. Science 1998, 279, 1344-1347
85. Moran, A.P.; Prendergast, M.M. Molecular mimicry in Campylobacter jejuni and Helicobacter pylori lipopolysaccharides: Contribution of gastrointestinal infections to autoimmunity. J. Autoimmun. 2001, 16, 241-256
86. Ang, C.W.; Jacobs, B.C.; Laman, J.D. The Guillain-Barre syndrome: a true case of molecular mimicry. Trends Immunol. 2004, 25, 61-66
87. Moran, A.P.; Rietschel, E.T.; Kosunen, T.U.; Zahringer, U. Chemical characterization of Campylobacter jejuni lipopolysaccharides containing N-acetylneuraminic acid and 2,3-diamino-2,3-dideoxy-D-glucose. J. Bacteriol. 1991, 173, 618-626
88. Powell, P.D.; DeMartini, J.C.; Azari, P.; Stargell, L.A.; Cordain, L.; Tucker, A. Evolutionary stable strategy: A test for theories of retroviral pathology which are based upon the concept of molecular mimicry. J. Theor. Biol. 2000, 202, 213-229
89. Dahl, M.E.; Dabbagh, K.; Liggitt, D.; Kim, S.; Lewis, D.B. Viral-induced T helper type 1 responses enhance allergic disease by effects on lung dendritic cells. Nature Immunol. 2004, 5, 337-343
90. Suzuki, S.; Suzuki, Y.; Yamamoto, N.; Matsumoto, Y.; Shirai, A.; Okubo, T. Influenza A virus infection increases IgE production and airway responsiveness in aerosolized antigen-exposed mice. J. Allergy Clin. Immunol. 1998, 102, 732-740
91. Schwarze, J.; Hamelmann, E.; Bradley, K.L.; Takeda, K.; Gelfand, E.W. Respiratory syncytial virus infection results in airway hyperresponsiveness and enhanced airway sensitization to allergen. J. Clin. Invest. 1997, 100, 226-233
92. Kondo, Y.; Matsuse, H.; Machida, I.; Kawano, T.; Saeki, S.; Tomari, S.; Obase, Y.; Fukushima, C.; Kohno, S. Effects of primary and secondary low-grade respiratory syncytial virus infections in a murine model of asthma. Clin. Exp. Allergy 2004, 34, 1307-1313
93. Lukacs, N.W.; Tekkanat, K.K.; Berlin, A.; Hogaboam, C.M.; Miller, A.; Evanoff, H.; Lincoln, P.; Maassab, H. Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms. J. Immunol. 2001, 167, 1060-1065
94. Rose, N.R.; Mackay, I.R. Molecular mimicry: a critical look at exemplary instances in human diseases. Cell. Mol. Life Sci. 2000, 57, 542-551
95. Herz, U.; Lacy, P.; Renz, H.; Erb, K. The influence of infections on the development and severity of allergic disorders. Curr. Opin. Immunol. 2000, 12, 632-640
96. Wilberz, S.; Partke, H.J.; Dagnaeshansen, F.; Herberg, L. Persistent MHV (mouse hepatitis-virus) infection reduces the incidence of diabetes-mellitus in nonobese diabetic mice. Diabetologia 1991, 34, 2-5
97. Sewell, D.L.; Reinke, E.K.; Co, D.O.; Hogan, L.H.; Fritz, R.B.; Sandor, M.; Fabry, Z. Infection with Mycobactetium bovis BCG diverts traffic of myelin oligodendroglial glycoprotein autoantigen-specific T cells away from the central nervous system and ameliorates experimental autoimmune encephalomyelitis. Clin. Diagn. Lab. Immunol. 2003, 10, 564-572
98. Ristori, G.; Buzzi, M.G.; Sabatini, U.; Giugni, E.; Bastianello, S.; Viselli, F.; Buttinelli, C.; Ruggieri, S.; Colonnese, C.; Pozzilli, C.; Salvetti, M. Use of Bacille Calmette-Guerin (BCG) in multiple sclerosis. Neurology 1999, 53, 1588-1589
99. Baxter, A.G.; Horsfall, A.C.; Healey, D.; Ozegbe, P.; Day, S.; Williams, D.G.; Cooke, A. Mycobacteria precipitate an SLE-like syndrome in diabetes-prone NOD mice. Immunology 1994, 83, 227-231
100. Moudgil, K.D.; Kim, E.; Yun, O.J.; Chi, H.H.; Brahn, E.; Sercarz, E.E. Environmental modulation of autoimmune arthritis involves the spontaneous microbial induction of T cell responses to regulatory determinants within heat shock protein 65. J. Immunol. 2001, 166, 4237-4243
101. Bras, A.; Aguas, A.P. Diabetes-prone NOD mice are resistant to Mycobacterium avium and the infection prevents autoimmune disease. Immunology 1996, 89, 20-25
102. Castro, A.P.; Esaguy, N.; Aguas, A.P. Effect of mycobacterial infection in the lupus-prone MRL/Lpr Mice - Enhancement of life-span of autoimmune mice, amelioration of kidney-disease and transient decrease in host-resistance. Autoimmunity 1993, 16, 159-166
103. Adams, V.C.; Hunt, J.R.F.; Martinelli, R.; Palmer, R.; Rook, G.A.W.; Brunet, L.R. Mycobacterium vaccae induces a population of pulmonary CD11c(+) cells with regulatory potential in allergic mice. Eur. J. Immunol. 2004, 34, 631-638
104. Han, X.B.; Fan, Y.J.; Wang, S.H.; Yang, J.; Bilenki, L.; Qiu, H.Y.; Jiao, L.; Yang, X. Dendritic cells from Chlamydia-infected mice show altered Toll-like receptor expression and play a crucial role in inhibition of allergic responses to ovalbumin. Eur. J. Immunol. 2004, 34, 981-989
105. Benoist, C.; Mathis, D. Autoimmunity provoked by infection: how good is the case for T cell epitope mimicry? Nature Immunol. 2001, 2, 797-801
106. Ennis, D.P.; Cassidy, J.P.; Mahon, B.P. Prior Bordetella pertussis infection modulates allergen priming and the severity of airway pathology in a murine model of allergic asthma. Clin. Exp. Allergy 2004, 34, 1488-1497
107. Lehmann, D.; Ben-Nun, A. Bacterial agents protect against autoimmune disease. I. Mice pre-exposed to Bordetella pertussis or Mycobacterium tuberculosis are highly refractory to induction of experimental autoimmune encephalomyelitis. J. Autoimmun. 1992, 5, 675-690
108. Hardy, R.D.; Jafri, H.S.; Olsen, K.; Hatfield, J.; Iglehart, J.; Rogers, B.B.; Patel, P.; Cassell, G.; McCracken, G.H.; Ramilo, O. Mycoplasma pneumoniae induces chronic respiratory infection, airway hyperreactivity, and pulmonary inflammation: a murine model of infection-associated chronic reactive airway disease. Infect. Immun. 2002, 70, 649-654
109. Costalonga, M.; Hodges, J.S.; Herzberg, M.C. Streptococcus sanguis modulates type II collagen-induced arthritis in DBA/1J mice. J. Immunol. 2002, 169, 2189-2195
110. Guilherme, L.; Oshiro, S.E.; Fae, K.C.; Cunha-Neto, E.; Renesto, G.; Goldberg, A.C.; Tanaka, A.C.; Pomerantzeff, P.M.A.; Kiss, M.H.; Silva, C.; Guzman, F.; Patarroyo, M.E.; Southwood, S.; Sette, A.; Kalil, J. T-cell reactivity against streptococcal antigens in the periphery mirrors reactivity of heart-infiltrating T lymphocytes in rheumatic heart disease patients. Infect. Immun. 2001, 69, 5345-5351
111. Kirvan, C.A.; Swedo, S.E.; Heuser, J.S.; Cunningham, M.W. Mimicry and auto antibody-mediated neuronal cell signaling in Sydenham chorea. Nat. Med. 2003, 9, 914-920
112. Mattsson, L.; Larsson, P.; Erlandsson-Harris, H.; Klareskog, L.; Harris, R.A. Parasite-mediated down-regulation of collagen-induced arthritis (CIA) in DA rats. Clin. Exp. Immunol. 2000, 122, 477-483
113. Reardon, C.; Sanchez, A.; Hogaboam, C.M.; McKay, D.M. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect. Immun. 2001, 69, 4417-4423
114. Elliott, D.E.; Setiawan, T.; Metwali, A.; Blum, A.; Urban, J.F.; Weinstock, J.V. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur. J. Immunol. 2004, 34, 2690-2698
115. Zaccone, P.; Fehervari, Z.; Jones, F.M.; Sidobre, S.; Kronenberg, M.; Dunne, D.W.; Cooke, A. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur. J. Immunol. 2003, 33, 1439-1449
116. Moreels, T.G.; Nieuwendijk, R.J.; De Man, J.G.; De Winter, B.Y.; Herman, A.G.; Van Marck, E.A.; Pelckmans, P.A. Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut 2004, 53, 99-107
117. Summers, R.W.; Elliott, D.E.; Qadir, K.; Urban, J.F.; Thompson, R.; Weinstock, J.V. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am. J. Gastroenterol. 2003, 98, 2034-2041
118. Khan, W.I.; Blennerhasset, P.A.; Varghese, A.K.; Chowdhury, S.K.; Omsted, P.; Deng, Y.; Collins, S.M. Intestinal nematode infection ameliorates experimental colitis in mice. Infect. Immun. 2002, 70, 5931-5937
119. Wohlleben, G.; Trujillo, C.; Muller, J.; Ritze, Y.; Grunewald, S.; Tatsch, U.; Erb, K.J. Helminth infection modulates the development of allergen-induced airway inflammation. Int. Immunol. 2004, 16, 585-596
120. Coyle, A.J.; Kohler, G.; Tsuyuki, S.; Brombacher, F.; Kopf, M. Eosinophils are not required to induce airway hyperresponsiveness after nematode infection. Eur. J. Immunol. 1998, 28, 2640-2647
121. Wang, C.C.; Nolan, T.J.; Schad, G.A.; Abraham, D. Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin. Clin. Exp. Allergy 2001, 31, 495-503
122. Hall, L.R.; Mehlotra, R.K.; Higgins, A.W.; Haxhiu, M.A.; Pearlman, E. An essential role for interleukin-5 and eosinophils in helminth-induced airway hyperresponsiveness. Infect. Immun. 1998, 66, 4425-4430
123. Wills-Karp, M.; Santeliz, J.; Karp, C.L. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat. Rev. Immunol. 2001, 1, 69-75
124. Viskari, H.; Ludvigsson, J.; Uibo, R.; Salur, L.; Marciulionyte, D.; Hermann, R.; Soltesz, G.; Fuchtenbusch, M.; Ziegler, A.G.; Kondrashova, A.; Romanov, A.; Knip, M.; Hyoty, H. Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: Results from the EPIVIR project. J. Med. Vir. 2004, 72, 610-617
125. Strachan, D.P. Hay fever, hygiene and household size. Br. Med. J. 1989, 299, 1259-1260
126. Romagnani, S. The increased prevalence of allergy and the hygiene hypothesis: missing immune deviation, reduced immune suppression, or both? Immunology 2004, 112, 352-363
127. Falcone, F.H.; Pritchard, D.I. Parasite role reversal: worms on trial. Trends Parasitol. 2005, 21, 157-160
128. Downs, S.H.; Marks, G.B.; Mitakakis, T.Z.; Leuppi, J.D.; Car, N.G.; Peat, J.K. Having lived on a farm and protection against allergic diseases in Australia. Clin. Exp. Allergy 2001, 31, 570-575
129. Kilpelainen, M.; Terho, E.O.; Helenius, H.; Koskenvuo, M. Farm environment in childhood prevents the development of allergies. Clin. Exp. Allergy 2000, 30, 201-208
130. Kabesch, M.; Lauener, R.P. Why Old McDonald had a farm but no allergies: genes, environments, and the hygiene hypothesis. J. Leukoc. Biol. 2004, 75, 383-387
131. Hampe, J.; Heymann, K.; Krawczak, M.; Schreiber, S. Association of inflammatory bowel disease with indicators for childhood antigen and infection exposure. Int. J. Colorectal Dis. 2003, 18, 413-417
132. Gent, A.E.; Hellier, M.D.; Grace, R.H.; Swarbrick, E.T.; Coggon, D. Inflammatory bowel-disease and domestic hygiene in infancy. Lancet 1994, 343, 766-767
133. Blanchard, J.F.; Bernstein, C.N.; Wajda, A.; Rawsthorne, P. Small-area variations and sociodemographic correlates for the incidence of Crohn's disease and ulcerative colitis. Am. J. Epidemiol. 2001, 154, 328-335
134. Liu, A.H.; Murphy, J.R. Hygiene hypothesis: Fact or fiction? J. Allergy Clin. Immunol. 2003, 111, 471-478
135. van Schayck, C.P.; Knottnerus, J.A. Can the 'hygiene hypothesis' be explained by confounding by behavior? J. Clin. Epidemiol. 2004, 57, 435-437
136. Zuk, M.; Stoehr, A.M. Immune defense and host life history. Am. Nat. 2002, 160, S9-S22
137. Belloni, V.; Faivre, B.; Guerreiro, R.; Arnoux, E.; Bellenger, J.; Sorci, G. Suppressing an anti-inflammatory cytokine reveals a strong age-dependent survival cost in mice. PLoS One 2010, 5, e12940
138. Guerreiro, R.; Besson, A.A.; Bellenger, J.; Ragot, K.; Lizard, G.; Faivre, B.; Sorci, G. Correlational selection on pro- and anti-inflammatory effectors. Evolution 2012, 66, 3615-3623
139. Cornet, S.; Sorci, G. Parasite virulence when the infection reduces the host immune response. Proc. R. Soc. B Biol. Sci. 2010, 277, 1929-1935
140. Day, T.; Graham, A.L.; Read, A.F. Evolution of parasite virulence when host responses cause disease. Proc. R. Soc. B Biol. Sci. 2007, 274, 2685-2692
141. Best, A.; Long, G.; White, A.; Boots, M. The implications of immunopathology for parasite evolution. Proc. R. Soc. B Biol. Sci., 279, 3234-3240
142. Frank, S.A.; Schmid-Hempel, P. Mechanisms of pathogenesis and the evolution of parasite virulence. J. Evol. Biol. 2008, 21, 396-404
143. Bertrand, S.; Faivre, B.; Sorci, G. Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants? J. Exp. Biol. 2006, 209, 4414-4419
144. Sadd, B.M.; Siva-Jothy, M.T. Self-harm caused by an insect's innate immunity. Proc. R. Soc. B 2006, 273, 2571-2574
145. Rhiannon, E.; Rolff, J. Immunopathology in Ecological Immunology. In Ecoimmunology; Demas, G.E.; Nelson R.J., Eds.; Oxford University Press: New York, NY, USA, 2012; pp. 530-547
146. McIntire, J.J.; Umetsu, S.E.; Macaubas, C.; Hoyte, E.G.; Cinnioglu, C.; Cavalli-Sforza, L.L.; Barsh, G.S.; Hallmayer, J.F.; Underhill, P.A.; Risch, N.J.; Freeman, G.J.; DeKruyff, R.H.; Umetsu, D.T. Hepatitis A virus link to atopic disease. Nature 2003, 425, 576-576
147. Rioux, J.D.; Abbas, A.K. Paths to understanding the genetic basis of autoimmune disease. Nature 2005, 435, 584-589
148. Banting, F.G.; Best, C.H. The internal secretion of the pancreas. J. Lab. Clin. Med. 1922, 7, 465-480
149. Licastro, F.; Candore, G.; Lio, D.; Porcellini, E.; Colonna-Romano, G.; Franceschi, G.; Caruso, C. Innate immunity and inflammation in ageing: a key for understanding age-related diseases. Immun. Ageing 2005, 2, 2-8
150. Charlesworth, B. Evolution in age-structured populations; Cambridge University Press: Cambridge, England, 1994
151. Nacher, M.; Gay, F.; Singhasivanon, P.; Krudsood, S.; Treeprasertsuk, S.; Mazier, D.; Vouldoukis, I.; Looareesuwan, S. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol. 2000, 22, 107-113
152. Liesenfeld, O.; Dunay, I.R.; Erb, K.J. Infection with Toxoplasma gondii reduces established and developing Th2 responses induced by Nippostrongylus brasiliensis infection. Infect. Immun. 2004, 72, 3812-3822
153. Barton, E.S.; White, D.W.; Cathelyn, J.S.; Brett-McClellan, K.A.; Engle, M.; Diamond, M.S.; Miller, V.L.; Virgin, H.W. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 2007, 447, 326-329.