The increased prevalence of allergy and the hygiene hypothesis: Missing immune deviation, reduced immune suppression, or both?

Immunology

Volumn 112, Issue 3, 2004, Pages 352-363

  Romagnani, Sergio ^a,b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b NONE   (Italy)

Author keywords

Hygiene hypothesis; Immune deviation; Immune suppression; Th1 Th2 cells; Treg cells

Indexed keywords

ALLERGEN; BCG VACCINE; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; OLIGODEOXYNUCLEOTIDE DERIVATIVE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ALLERGY; ASTHMA; ATOPIC DERMATITIS; BACTERIUM; BRONCHUS HYPERREACTIVITY; CELL ACTIVITY; CELL STIMULATION; CLINICAL TRIAL; CYTOKINE PRODUCTION; EOSINOPHILIA; HUMAN; HYGIENE; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; LIFESTYLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHINITIS; TH2 CELL;

ANIMALS; BACTERIAL INFECTIONS; CYTOKINES; DEVELOPED COUNTRIES; DISEASE OUTBREAKS; HUMANS; HYGIENE; HYPERSENSITIVITY; IMMUNE SYSTEM; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; TH1 CELLS; TH2 CELLS;

EID: 3042798442     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2004.01925.x     Document Type: Review

References (110)

1. Romagnani S. The role of lymphocytes in allergic disease. J Allergy Clin Immunol 2000; 105:399-408.
2. Larché M, Robinson DS, Kay AB. The role of T lymphocytes in the pathogenesis of asthma. J Allergy Clin Immunol 2003; 111:450-64.
3. Sperger JM, Paller AS. Atopic dermatitis and the atopic march. J Allergy Clin Immunol 2003; 112:s118-27.
4. Strachan DP. Hay fever, hygiene and household size. Br Med J 1989; 299:1259-60.
5. Matricardi PM, Rosmini F, Riondino S et al. Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: an epidemiological study. Br Med J 2000; 320:412-7.
6. Alm JS, Swartz J, Lilja G et al. Atopy in children with an anthroposophic style of life. Lancet 1999; 353:1484-8.
7. Braun-Fahrlander C, Riedler J, Herz U et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. New Engl J Med 2002; 347:869-77.
8. Romagnani S. Regulation of Th2 development in allergy. Curr Opin Immunol 1994; 6:838-46.
9. Martinez FD. The coming-of-age of the hygiene hypothesis. Respir Res 2001; 2:129-32.
10. Yazdanbakhah M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002; 296:490-4.
11. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. New Engl J Med 2002; 347:911-20.
12. Wills-Karp M, Santeliz J, Karp CL. The germless allergic disease: revisiting the hygiene hypothesis. Nature Rev Immunol 2001; 1:69-75.
13. Sabroe I, Read RC, Whyte MKB et al. Toll-like receptors in health and disease: complex questions remain. J Immunol 2003; 74:1630-5.
14. Manetti R, Parronchi P, Giudizi MG et al. Natural killer cell stimulatory factor (interleukin-12) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J Exp Med 1993; 177:1199-204.
15. Kaplan MH, Sun YL, Hoey T et al. Impaired IL-12 responses and enhanced development of Th2 cells in STAT-4-deficient mice. Science 1996; 382:174-7.
16. Szabo SJ, Kim ST, Costa GL et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000; 100:655-69.
17. Maggi E, Parronchi P, Manetti R et al. Reciprocal regulatory role of IFN-γ and IL-4 on the in vitro development of human Th1 and Th2 cells. J Immunol 1992; 148:2142-7.
18. Parronchi P, De Carli M, Manetti R et al. IL-4 and IFN (s) (alpha and gamma) exhibit opposite regulatory effects on the development of cytolytic potential by TH1 or TH2 human T cell clones. J Immunol 1992; 149:2977-82.
19. Rengarajan J, Szabo SJ, Glimcher LH. Transcriptional regulation of Th1/Th2 polarization. Immunol Today 2000; 21:479-83.
20. Agrawal S, Agrawal A, Doughty B et al. Different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos. J Immunol 2003; 171:4984-9.
21. Redecke V, Hacker H, Datta SK et al. Activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J Immunol 2004; 172:2729-43.
22. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick C, Bottomly K. Lipolysaccharide-enhanced, Toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med 2002; 196:1645-51.
23. Romagnani S. Lymphokine production by human T cells in disease states. Annu Rev Immunol 1994; 12:227-57.
24. Abbas AK, Murphy K, Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383:787-93.
25. Suri-Payer E, Amar AZ, Thornton AM et al. CD4+ CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J Immunol 1998; 160:1212-8.
26. Weiner HL. Induction and mechanism of action of transforming growth factor beta-secreting Th3 regulatory cells. Immunol Rev 2001; 182:207-14,
27. Roncarolo MG, Bacchetta R, Bordignon C et al. Type 1 T regulatory cells. Immunol Rev 2001; 182:68-79.
28. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 2003; 4:330-6.
29. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M, Byrne MC. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002; 6:311-23.
30. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nature Rev Immunol 2003; 3:253-7.
31. Netea MG, Sutmuller R, Hermann C et al. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 2004; 172:3712-8.
32. Platts-Mills T, Vaughan J, Squillace S et al. Sensitization, asthma and a modified Th2 response in children exposed to cat allergen: a population based cross-sectional study. Lancet 2001; 357:752-6.
33. Holt PG, Macaubas C, Strumbles PA, Sly PD. The role of allergy in the development of asthma. Nature 1999; 402 (6760 Suppl):12-7.
34. Lynch NR, Lopez RI, DiPrisco-Fuenmayor MC, Hagel I, Medouze L, Viana G, Ortega C, Prato G. Allergic reactivity and socioeconomic level in a tropical environment. Clin Allergy 1987; 17:199-207.
35. Pugliatti M, Sotgiu S, Solinas G et al. Multiple sclerosis epidemiology in Sardinia: evidence for a true increasing risk. Acta Neurol Scand 2001; 103:20-6.
36. Stefano S, Maura P, Alessandra S et al. Does the 'hygiene hypothesis' provide an explanation for the high prevelence of multiple sclerosis in Sardinia? Autoimmunity 2003; 36:257-60.
37. Cook SD, Cromarty JI, Tapp W et al. Declining incidence of multiple sclerosis in the Orkney Islands. Neurology 1985; 35:545-51.
38. Farrokyar F, Swarbrick ET, Levine EJ. A critical review of epidemiological studies in inflammatory bowel disease. Scan J Gastroenterol 2001; 36:2-15.
39. Sewell DL, Reinke EK, Logan LH et al. Immunoregulation of CNS autoimmunity by helminth and mycobacterial infections. Immunol Lett 2002; 82:101-10.
40. Hilliquin P, Allanore Y, Coste J et al. Reduced incidence and prevalence of atopy in rheumatoid arthritis. Results of a case-control study. Rheumatology 2000; 39:1020-6.
41. van Roon JAG, Bijlsma JWJ. Th2 mediated regulation in RA and spondyloarthropathies. Ann Rheum Dis 2002; 61:951-4.
42. Oro AM, Guarino TJ, Driver R et al. Regulation of disease susceptibility: decreased prevalence of IgE-mediated disease in patients with multiple sclerosis. J Allergy Clin Immunol 1996; 97:1402-8.
43. Tremlett HL, Evans J, Wiles CM et al. Asthma and multiple sclerosis: an inverse association in a case-control general practice population. QJM 2002; 95:753-6.
44. Tang L, Benjaponpitak S, DeKruyff RH et al. Reduced prevalence of allergic disease with multiple sclerosis is associated with enhanced IL-12 production. J Allergy Clin Immunol 1998; 102:428-35.
45. Johnson RJ, Hurtado A, Merszei J et al. Hypothesis: dysregulation of immunologic balance resulting from hygiene and socioeconomic factors may influence the epidemiology and cause of glomerulonephritis worldwide. Am J Kidney Dis 2003; 42:575-81.
46. Manetti R, Annunziato F, Tomasevic L et al. Polyinosinic acid: polycytidylic acid promotes T helper type 1-specific immune responses by stimulating macrophage production of interferon-alpha and interleukin-12. Eur J Immunol 1999; 25:2656-60.
47. Koski GK, Kariko K, Xu S et al. Innate immunity system discriminates between RNA containing bacterial versus eukaryotic structural features that prime for high-level IL-12 secretion by dendritic cells. J Immunol 2004; 172:3989-93.
48. Parronchi P, Brugnolo F, Annunziato F et al. Phosphorothioate oligodeoxynucletides promote the in vitro development of human allergen-specific CD4+ T cells into Th1 effectors. J Immunol 1999; 163:5946-53.
49. Tighe H, Takabayashi K, Schwartw D et al. Conjugation of immunostimulatory DNA to the short ragweed allergen amb a 1 enhances its immunogenicity and reduces its allergenicity. J Allergy Clin Immunol 2000; 106:124-34.
50. Annunziato F, Cosmi L, Manetti R et al. Reversal of human allergen-specific CRTH2+ Th2 cells by IL-12 or the PS-DSP30 oligodeoxynucleotide. J Allergy Clin Immunol 2001; 108:815-21.
51. Brugnolo F, Sampognaro S, Fintoni T et al. The novel synthetic immune response modifier R-848 (Resiquimod) has a powerful effect on the in vitro switching of human allergen-specific CD4+ Th2 lymphocytes into IFN-γ-producing cells. J Allergy Clin Immunol 2003; 111:380-8.
52. Tournoy KG, Kips JC, Pauwels RA. Is Th1 the solution for Th2 in asthma? Clin Exp Allergy 2002; 31:17-29.
53. Lack G, Bradley KL, Hamelmann E et al. Nebulized but not parenteral IFN-gamma decreases IgE production and normalizes airway function in a murine model of allergen sensitization. J Immunol 1994; 152:2546-54.
54. Lack G, Bradley KL, Hamelmann E et al. Nebulized IFN-gamma inhibits the development of secondary allergen responses in mice. J Immunol 1996; 157:1432-9.
55. Dow SW, Schwartze J, Heath TD et al. Systemic and local interferon gamma gene delivery to the lungs for treatment of allergen-induced airway hyperresponsiveness in mice. Hum Gene Ther 1999; 10:1905-14.
56. Li XM, Chopra RK, Chou TY et al. Mucosal IFN-gamma gene transfer inhibits pulmonary allergic responses in mice. J Immunol 1996; 157:3216-9.
57. Martin RJ, Boguniewicz M, Henson JE et al. The effects of inhaled interferon-gamma in normal human airways. Am Rev Respir Dis 1993; 148:1677-82.
58. Boguniewicz M, Martin RJ, Martin D et al. The effects of nebulized interferon-gamma in asthmatic airways. J Allergy Clin Immunol 1995; 95:133-5.
59. Randolph DA, Carruthers CJL, Szabo SJ et al. Modulation of airway inflammation by passive transfer of allergen-specific Th1 and Th2 cells in a mouse model of asthma. J Immunol 1999; 162:1375-83.
60. Hansen G, Berry G, DeKruyff RH et al. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J Clin Invest 1999; 103:175-83.
61. Kips JC, Brusselle GJ, Joos JF et al. Interleukin-12 inhibits antigen-induced airway hyperresponsiveness in mice. Am J Respir Crit Care Med 1996; 153:535-9.
62. Gerhold K, Blumchen K, Bock A et al. Endotoxins prevent murine IgE production, Th2 immune responses and development of airway eosinophilia but not airway hyperreactivity. J Allergy Clin Immunol 2002; 110:110-6.
63. Walter DM, Womg CP, DeKruyff RH et al. IL-18 gene transfer by adenovius prevents the development of and reverses established allergen-induced airway hyperreactivity. J Immunol 2001; 166:6392-8.
64. Sugimoto T, Ishikawa Y, Yoshimoto T et al. Interleukin 18 acts on memory T helper cells type 1 to induce airway inflammation and hyperresponsiveness in a naïve host mouse. J Exp Med 2004; 199:535-45.
65. Klinman DM. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nature Rev Immunol 2004; 4:1-10.
66. Erb KJ, Holloway JW, Sobeck A et al. Infection of mice with Mycobacterium bovis-Bacillus Calmette Guerin (BCG) suppresses allergen-induced airway eosinophilia. J Exp Med 1998; 187:561-9.
67. Major T, Wohlleben G, Reibetanz B et al. Application of heat killed Mycobacterium bovis-BCG into the lungs inhibits the development of allergen-induced Th2 response. Vaccine 2002; 20:1532-40.
68. Tsai JJ, Liu YH, Shen HD et al. Prevention of Der p2-induced airway inflammation by Mycobacterium-bacillus Calmette Guerin. J Microbiol Immunol Infect 2002; 35:152-8.
69. Shirikawa T, Enomoto T, Shimazu S et al. The inverse association between tuberculin responses and atopic disorders. Science 1997; 275:77-9.
70. Marks GB, Ng K, Zhou J et al. The effect of neonatal BCG vaccination on atopy and asthma at age 7-14 years: an historical cohort study in a community with a very low prevalence of tuberculosis infection and a high prevalence of atopic disease. J Allergy Clin Immunol 2003; 111:541-9.
71. Townley RG, Barna IB, Patino C et al. The effect of BCG vaccine at birth on the development of atopy or allergic disease in young children. Ann Allergy Asthma Immunol 2004; 92:350-5.
72. Pochard P, Gosset P, Grangette C et al. Lactic acid bacteria inhibit TH2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 2002; 110:617-23.
73. Culley FJ, Pollot J, Openshaw PJM. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J Exp Med 2002; 196:1381-6.
74. Wollheben G, Muller J, Tatsch U et al. Influenza A virus infection inhibits the efficient recruitment of Th2 cells into the airways and the development of airway eosinophilia. J Immunol 2003; 170:4601-11.
75. Dahl ME, Dabbagh K, Liggitt D et al. Viral induced T helper type 1 responses enhance allergic disease by effects on lung dendritic cells. Nat Immunol 2004; 5:337-43.
76. Mardsland BJ, Harris NL, Camberis M et al. Bystander suppression of allergic airway inflammation by lung resident memory CD8+ T cells. Proc Natl Acad Sci USA 2004; 101:6116-21.
77. Smart JM, Horak E, Kemp AS et al. Polyclonal and allergen-induced cytokine responses in adults with asthma: resolution of asthma is associated with normalization of IFN-γ responses. J Allergy Clin Immunol 2002; 110:450-6.
78. Shahid SK, Kharltonov SA, Wilson NM et al. Increased interleukin-4 and decreased IFN-γ in exhaled breath condensate of children with asthma. Am J Respir Crit Care Med 2002; 165:1290-3.
79. Wierenga EA, Snoek M, Jansen HM et al. Functional subsets of allergen-reactive human CD4+ T cells. Immunol Today 1991; 12:392-5.
80. Romagnani S. Immunologic influences on allergy and the TH1/TH2 balance. J Allergy Clin Immunol 2004; 113:395-400.
81. Turcanu V, Maleki SJ, Lack G. Characterization of lymphocyte responses to peanuts in normal children, peanut-allergic children, and allergic children who acquired tolerance to peanuts. J Clin Invest 2003; 111:1065-72.
82. Gangur V, Simons ER, Hayglass KT. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-γ over IL-4 responses. FASEB J 1998; 12:705-13.
83. Campbell JD, Gangur V, Simons FER et al. Allergic humans are hyporesponsive to a CXCR3 ligand-mediated Th1 immunity-promoting loop. FASEB J 2004; 18:329-31.
84. Prescott SL, Taylor A, King B et al. Neonatal interleukin-12 capacity is associated with variations in allergen-specific immune responses in the neonatal and postnatal periods. Clin Exp Allergy 2003; 33:566-72.
85. Reider N, Reider D, Ebner S. Dendritic cells contribute to the development of atopy by an insufficiency in IL-12 production. J Allergy Clin Immunol 2002; 109:89-95.
86. Hamid QA, Shotman E, Jacobson MR et al. Increases in IL-12 messenger RNA+ cells accompany inhibition of allergen-induced late skin responses after successful grass pollen immunotherapy. J Allergy Clin Immunol 1997; 99:254-60.
87. Nakamura Y, Ghaffar O, Olivenstein R et al. Gene expression of the GATA-3 transcription factor is increased in atopic asthma. J Allergy Clin Immunol 1999; 103:215-22.
88. Finotto S, Neurath MF, Glickman JM et al. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 2002; 295:336-8.
89. Shapenko A, Leipe J, Niesner U et al. GATA-3 in human T cell helper type 2 development. J Exp Med 2004; 199:423-8.
90. Renz H, von Mutius E, Illi S, Wolkers F, Hirsch T, Weiland SK. Th1/Th2 immune responses profiles differ between atopic children in eastern and western Germany. J Allergy Clin Immunol 2002; 109:338-42.
91. Gehring U, Bischoff W, Fahlbusch B et al. House dust endotoxin and allergic sensitization in children. Am J Respir Crit Care Med 2002; 166:939-44.
92. Lauener RP, Birchler T, Adamaski J et al. Expression of CD14 and Toll-like receptor 2 in farmers' and non-farmers' children. Lancet 2002; 360:465-6.
93. Gambineri E, Torgerson TR, Ochs HD. Immune dysregulation, poliendocrinopathy, enteropathy, and X-linked inheritance (IPEX) a syndrome of systemic autoimmunity caused by mutations of Foxp3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol 2003; 15:430-8.
94. Cosmi L, Lotta F, Lazzeri E et al. Th2 cells are less susceptible than ThI cells to the suppressive activity of CD25+ regulatory thymocytes because of their responsiveness to different cytokines. Blood 2004; 103:3117-21.
95. Suto A, Nakajima H, Kagami S-I et al. Role of CD4+ CD25+ regulatory T cells in T helper 2 cell-mediated allergic inflammation in the airways. Am J Respir Care Med 2001; 164:680-7.
96. Jaffar Z, Sivakuru T, Roberts K. CD4+ CD25+ T cells regulate airway eosinophilic inflammation by modulating the Th2 cell phenotype. J Immunol 2004; 172:3842-9.
97. Tiemessen MM, Van Hoffen E, Knulst AC et al. CD4+ CD25+ regulatory T cells are not functionally impaired in adult patients with IgE-mediated cow's milk allergy. J Allergy Clin Immunol 2002; 110:934-6.
98. Ling EM, Smith T, Nguyen XD et al. Relation of CD4+ CD25+ regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 2004; 363:608-15.
99. Hansen G, McIntire JJ, Yeung VP et al. CD4+ T helper cells engineered to produce latent TGF-beta reverse allergen-induced airway hyperreactivity and inflammation. J Clin Invest 2000; 105:61-70.
100. Stampfli MR, Cwiartka M, Gajewska BU et al. Interleukin-10 gene transfer to the airways regulates allergic mucosal sensitization in mice. Am J Respir Cell Mol Biol 1999; 21:586-96.
101. Oh W-J, Seroogy CM, Meyer EH et al. CD4 T-helper cells engineered to produce IL-10 prevent allergen-induced airway hyperreactivity and inflammation. J Allergy Clin Immunol 2002; 110:460-8.
102. Zuani-Amorim C, Sawicka E, Manlius C et al. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nature Med 2002; 8: 625-9.
103. Smitt JJ, Van Loveren H, Hoekstra MO et al. Mycobacterium vaccae administration during allergen sensitization or challenge suppresses asthmatic features. Clin Exp Allergy 2003; 33:1083-9.
104. Cottrez F, Hurst SD, Coffman RL et al. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000; 165:4848-53.
105. Blaser K, Akdis CA. Interleukin-10 T regulatory cells and specific allergy treatment. Clin Exp Allergy 2004; 34:328-31.
106. Jutel M, Akdis M, Budak F et al. IL-10 and TGF-beta cooperate in the regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy. Eur J Immunol 2003; 33:1205-14.
107. Nouri-Aria KT, Wackholz PA, Francis JM et al. Grass pollen immunotherapy induces mucosal and peripheral IL-10 responses and blocking IgG activity. J Immunol 2004; 172:3252-9.
108. Chatelain R, Mauze S, Coffman RL. Experimental Leishmania major infection in mice: role of IL-10. Parasite Immunol 1999; 21:211-8.
109. Laouini D, Alenius H, Tsitsikov E, Geha RS. IL-10 skews the immune response to Th2 and is critical for skin eosinophilia in a murine model of allergic dermatitis. J Clin Invest 2003; 112:1058-66.
110. Shapenko A, Niedobitek GU, Kalden JR et al. Generation and regulation of human Th1-biased immune responses in vivo: a critical role for IL-4 and IL-10. J Immunol 2004; 172:6427-34.