1932

Abstract

In this review we discuss the effects of microbial exposure on the B cell repertoire. Neonatal exposure to conserved bacterial carbohydrates and phospholipids permanently reprograms the natural antibody repertoire directed toward these antigens by clonal expansion, alterations in clonal dominance, and increased serum antibody levels. These epitopes are present not only in bacterial cell walls, but also in common environmental allergens. Neonatal immunization with bacterial polysaccharide vaccines results in attenuated allergic airway responses to fungi-, house dust mite-, and cockroach-associated allergens in mouse models. The similarities between mouse and human natural antibody repertoires suggest that reduced microbial exposure in children may have the opposite effect, providing a potential mechanistic explanation for the hygiene hypothesis. We propose that understanding the effects of childhood infections on the natural antibody repertoire and the mechanisms of antibody-mediated immunoregulation observed in allergy models will lead to the development of prevention/interventional strategies for treatment of allergic asthma.

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2015-03-21
2024-03-28
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Literature Cited

  1. Strachan DP. 1.  1989. Hay fever, hygiene, and household size. BMJ 299:1259–60 [Google Scholar]
  2. Bach JF. 2.  2002. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347:911–20 [Google Scholar]
  3. Rook GA, Raison CL, Lowry CA. 3.  2014. Microbial ‘Old Friends’, immunoregulation and socioeconomic status. Clin. Exp. Immunol. 177:1–12 [Google Scholar]
  4. Boyden SV. 4.  1966. Natural antibodies and the immune response. Adv. Immunol. 5:1–28 [Google Scholar]
  5. Bos NA, Kimura H, Meeuwsen CG, De Visser H, Hazenberg MP. 5.  et al. 1989. Serum immunoglobulin levels and naturally occurring antibodies against carbohydrate antigens in germ-free BALB/c mice fed chemically defined ultrafiltered diet. Eur. J. Immunol. 19:2335–39 [Google Scholar]
  6. Choi YS, Baumgarth N. 6.  2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205:3053–64 [Google Scholar]
  7. Briles DE, Nahm M, Schroer K, Davie J, Baker P. 7.  et al. 1981. Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 streptococcus pneumoniae. J. Exp. Med. 153:694–705 [Google Scholar]
  8. Ballot DE, Nana T, Sriruttan C, Cooper PA. 8.  2012. Bacterial bloodstream infections in neonates in a developing country. ISRN Pediatr. 2012:508512 [Google Scholar]
  9. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M. 9.  et al. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374:893–902 [Google Scholar]
  10. 10. World Health Organ 2005. Group A streptococcal vaccine development: current status and issues of relevance to less developed countries WHO/FCH/CAH/05.09 Geneva, Switz. http://whqlibdoc.who.int/hq/2005/WHO_IVB_05.14_eng.pdf
  11. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH. 11.  et al. 2008. Epidemiology of invasive group B streptococcal disease in the United States, 1999–2005. JAMA 299:2056–65 [Google Scholar]
  12. Kearney JF, McCarthy MT, Stohrer R, Benjamin WH Jr, Briles DE. 12.  1985. Induction of germ-line anti-alpha 1-3 dextran antibody responses in mice by members of the Enterobacteriaceae family. J. Immunol. 135:3468–72 [Google Scholar]
  13. Foote JB, Kearney JF. 13.  2009. Generation of B cell memory to the bacterial polysaccharide alpha-1,3 dextran. J. Immunol. 183:6359–68 [Google Scholar]
  14. Stohrer R, Lee MC, Kearney JF. 14.  1983. Analysis of the anti-alpha 1 leads to 3 dextran response with monoclonal anti-idiotype antibodies. J. Immunol. 131:1375–79 [Google Scholar]
  15. Masmoudi H, Motasantos T, Huetz F, Coutinho A, Cazenave PA. 15.  1990. All T15 Id-positive antibodies (but not the majority of VHT15+ antibodies) are produced by peritoneal CD5+ B lymphocytes. Int. Immunol. 2:515–20 [Google Scholar]
  16. Sigal NH, Pickard AR, Metcalf ES, Gearhart PJ, Klinman NR. 16.  1977. Expression of phosphorylcholine-specific B cells during murine development. J. Exp. Med. 146:933–48 [Google Scholar]
  17. Pritchard DG, Gray BM, Egan ML. 17.  1992. Murine monoclonal antibodies to type Ib polysaccharide of group B streptococci bind to human milk oligosaccharides. Infect. Immun. 60:1598–602 [Google Scholar]
  18. Martin F, Kearney JF. 18.  2000. Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity 12:39–49 [Google Scholar]
  19. Foote JB, Mahmoud TI, Vale AM, Kearney JF. 19.  2012. Long-term maintenance of polysaccharide-specific antibodies by IgM-secreting cells. J. Immunol. 188:57–67 [Google Scholar]
  20. Hayakawa K, Hardy RR, Honda M, Herzenberg LA, Steinberg AD, Herzenberg LA. 20.  1984. Ly-1 B cells: functionally distinct lymphocytes that secrete IgM autoantibodies. PNAS 81:2494–98 [Google Scholar]
  21. Wardemann H, Boehm T, Dear N, Carsetti R. 21.  2002. B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J. Exp. Med. 195:771–80 [Google Scholar]
  22. Kroese FG, Butcher EC, Stall AM, Lalor PA, Adams S, Herzenberg LA. 22.  1989. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int. Immunol. 1:75–84 [Google Scholar]
  23. Lalor PA, Stall AM, Adams S, Herzenberg LA. 23.  1989. Permanent alteration of the murine Ly-1 B repertoire due to selective depletion of Ly-1 B cells in neonatal animals. Eur. J. Immunol. 19:501–6 [Google Scholar]
  24. Jiang HQ, Thurnheer MC, Zuercher AW, Boiko NV, Bos NA, Cebra JJ. 24.  2004. Interactions of commensal gut microbes with subsets of B- and T-cells in the murine host. Vaccine 22:805–11 [Google Scholar]
  25. Choi YS, Dieter JA, Rothaeusler K, Luo Z, Baumgarth N. 25.  2012. B-1 cells in the bone marrow are a significant source of natural IgM. Eur. J. Immunol. 42:120–29 [Google Scholar]
  26. Reynolds AE, Kuraoka M, Kelsoe G. 25.  2015. Natural IgM is produced by CD5 plasma cells that occupy a distinct survival niche in bone marrow. J. Immunol. 194:231–42 [Google Scholar]
  27. Yang Y, Tung JW, Ghosn EE, Herzenberg LA, Herzenberg LA. 26.  2007. Division and differentiation of natural antibody-producing cells in mouse spleen. PNAS 104:4542–46 [Google Scholar]
  28. Kawahara T, Ohdan H, Zhao G, Yang YG, Sykes M. 27.  2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171:5406–14 [Google Scholar]
  29. Pihlgren M, Friedli M, Tougne C, Rochat AF, Lambert PH, Siegrist CA. 28.  2006. Reduced ability of neonatal and early-life bone marrow stromal cells to support plasmablast survival. J. Immunol. 176:165–72 [Google Scholar]
  30. Belnoue E, Pihlgren M, McGaha TL, Tougne C, Rochat AF. 29.  et al. 2008. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood 111:2755–64 [Google Scholar]
  31. Vakil M, Kearney JF. 30.  1991. Functional relationship between T15 and J558 idiotypes in BALB/c mice. Dev. Immunol. 1:213–24 [Google Scholar]
  32. Tarlinton D. 31.  2011. Memory B cell and plasma cell differentiation Presented at Keyst. Symp., Apr. 12–17, Whistler, Can.
  33. Briles DE, Nahm M, Marion TN, Perlmutter RM, Davie JM. 32.  1982. Streptococcal group A carbohydrate has properties of both a thymus-independent (TI-2) and a thymus-dependent antigen. J. Immunol. 128:2032–35 [Google Scholar]
  34. Rijkers GT, Sanders EA, Breukels MA, Zegers BJ. 33.  1998. Infant B cell responses to polysaccharide determinants. Vaccine 16:1396–400 [Google Scholar]
  35. Gray BM, Dillon HC Jr, Briles DE. 34.  1983. Epidemiological studies of Streptococcus pneumoniae in infants: development of antibody to phosphocholine. J. Clin. Microbiol. 18:1102–7 [Google Scholar]
  36. Carlsson L, Holmberg D. 35.  1990. Genetic basis of the neonatal antibody repertoire: germline V-gene expression and limited N-region diversity. Int. Immunol. 2:639–43 [Google Scholar]
  37. Feeney AJ. 36.  1990. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J. Exp. Med. 172:1377–90 [Google Scholar]
  38. Schroeder HW Jr, Mortari F, Shiokawa S, Kirkham PM, Elgavish RA, Bertrand FE 3rd. 37.  1995. Developmental regulation of the human antibody repertoire. Ann. N.Y. Acad. Sci. 764:242–60 [Google Scholar]
  39. Schroeder HW Jr, Zhang L, Philips JB 3rd. 38.  2001. Slow, programmed maturation of the immunoglobulin HCDR3 repertoire during the third trimester of fetal life. Blood 98:2745–51 [Google Scholar]
  40. Martin F, Chen X, Shu F, Kearney JF. 39.  1995. Development of the mouse B-cell repertoire. Ann. N.Y. Acad. Sci. 764:207–21 [Google Scholar]
  41. Timens W, Boes A, Poppema S. 40.  1989. Human marginal zone B cells are not an activated B cell subset: strong expression of CD21 as a putative mediator for rapid B cell activation. Eur. J. Immunol. 19:2163–66 [Google Scholar]
  42. Siegrist CA, Aspinall R. 41.  2009. B-cell responses to vaccination at the extremes of age. Nat. Rev. Immunol. 9:185–94 [Google Scholar]
  43. Zinkernagel RM. 42.  2003. On natural and artificial vaccinations. Annu. Rev. Immunol. 21:515–46 [Google Scholar]
  44. Zinkernagel RM. 43.  2001. Maternal antibodies, childhood infections, and autoimmune diseases. N. Engl. J. Med. 345:1331–35 [Google Scholar]
  45. Sigal NH, Gearhart PJ, Press JL, Klinman NR. 44.  1976. Late acquisition of a germ line antibody specificity. Nature 259:51–52 [Google Scholar]
  46. Snape MD, Kelly DF, Green B, Moxon ER, Borrow R, Pollard AJ. 45.  2005. Lack of serum bactericidal activity in preschool children two years after a single dose of serogroup C meningococcal polysaccharide-protein conjugate vaccine. Pediatr. Infect. Dis. J. 24:128–31 [Google Scholar]
  47. Kelly DF, Snape MD, Clutterbuck EA, Green S, Snowden C. 46.  et al. 2006. CRM197-conjugated serogroup C meningococcal capsular polysaccharide, but not the native polysaccharide, induces persistent antigen-specific memory B cells. Blood 108:2642–47 [Google Scholar]
  48. Snape MD, Kelly DF, Salt P, Green S, Snowden C. 47.  et al. 2006. Serogroup C meningococcal glycoconjugate vaccine in adolescents: persistence of bactericidal antibodies and kinetics of the immune response to a booster vaccine more than 3 years after immunization. Clin. Infect. Dis. 43:1387–94 [Google Scholar]
  49. Harris NL, Spoerri I, Schopfer JF, Nembrini C, Merky P. 48.  et al. 2006. Mechanisms of neonatal mucosal antibody protection. J. Immunol. 177:6256–62 [Google Scholar]
  50. Benedict CL, Kearney JF. 49.  1999. Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10:607–17 [Google Scholar]
  51. Benedict CL, Gilfillan S, Thai TH, Kearney JF. 50.  2000. Terminal deoxynucleotidyl transferase and repertoire development. Immunol. Rev. 175:150–57 [Google Scholar]
  52. Mahmoud TI, Kearney JF. 51.  2010. Terminal deoxynucleotidyl transferase is required for an optimal response to the polysaccharide α-1,3 dextran. J. Immunol. 184:851–58 [Google Scholar]
  53. Veenhoven R, Bogaert D, Uiterwaal C, Brouwer C, Kiezebrink H. 52.  et al. 2003. Effect of conjugate pneumococcal vaccine followed by polysaccharide pneumococcal vaccine on recurrent acute otitis media: a randomised study. Lancet 361:2189–95 [Google Scholar]
  54. Blanchard Rohner G, Snape MD, Kelly DF, John T, Morant A. 53.  et al. 2008. The magnitude of the antibody and memory B cell responses during priming with a protein-polysaccharide conjugate vaccine in human infants is associated with the persistence of antibody and the intensity of booster response. J. Immunol. 180:2165–73 [Google Scholar]
  55. Kelly DF, Snape MD, Perrett KP, Clutterbuck EA, Lewis S. 54.  et al. 2009. Plasma and memory B-cell kinetics in infants following a primary schedule of CRM 197-conjugated serogroup C meningococcal polysaccharide vaccine. Immunology 127:134–43 [Google Scholar]
  56. McVernon J, MacLennan J, Pollard AJ, Oster P, Wakefield MJ. 55.  et al. 2003. Immunologic memory with no detectable bactericidal antibody response to a first dose of meningococcal serogroup C conjugate vaccine at four years. Pediatr. Infect. Dis. J. 22:659–61 [Google Scholar]
  57. Siegrist CA. 56.  2008. Blame vaccine interference, not neonatal immunization, for suboptimal responses after neonatal diphtheria, tetanus, and acellular pertussis immunization. J. Pediatr. 153:305–7 [Google Scholar]
  58. Dagan R, Kayhty H, Wuorimaa T, Yaich M, Bailleux F. 57.  et al. 2004. Tolerability and immunogenicity of an eleven valent mixed carrier Streptococcus pneumoniae capsular polysaccharide-diphtheria toxoid or tetanus protein conjugate vaccine in Finnish and Israeli infants. Pediatr. Infect. Dis. J. 23:91–98 [Google Scholar]
  59. Hamilton AM, Kearney JF. 58.  1994. Effects of IgM allotype suppression on serum IgM levels, B-1 and B-2 cells, and antibody responses in allotype heterozygous F1 mice. Dev. Immunol. 4:27–41 [Google Scholar]
  60. Hamilton AM, Lehuen A, Kearney JF. 59.  1994. Immunofluorescence analysis of B-1 cell ontogeny in the mouse. Int. Immunol. 6:355–61 [Google Scholar]
  61. Gronwall C, Silverman GJ. 60.  2014. Natural IgM: beneficial autoantibodies for the control of inflammatory and autoimmune disease. J. Clin. Immunol. 34:Suppl. 1S12–21 [Google Scholar]
  62. Mahmoud TI, Schroeder HW Jr, Kearney JF. 61.  2011. Limiting CDR-H3 diversity abrogates the antibody response to the bacterial polysaccharide α 1→3 dextran. J. Immunol. 187:879–86 [Google Scholar]
  63. Barbar E, Martin TM, Brown M, Rittenberg MB, Peyton DH. 62.  1996. Binding of phenylphosphocholine-carrier conjugates to the combining site of antibodies maintains a conformation of the hapten. Biochemistry 35:2958–67 [Google Scholar]
  64. Chang SP, Brown M, Rittenberg MB. 63.  1982. Immunologic memory to phosphorylcholine. II. PC-KLH induces two antibody populations that dominate different isotypes. J. Immunol. 128:702–6 [Google Scholar]
  65. Robbins JB, Schneerson R, Szu SC. 64.  1995. Perspective: hypothesis: serum IgG antibody is sufficient to confer protection against infectious diseases by inactivating the inoculum. J. Infect. Dis. 171:1387–98 [Google Scholar]
  66. Granoff DM, Holmes SJ, Osterholm MT, McHugh JE, Lucas AH. 65.  et al. 1993. Induction of immunologic memory in infants primed with Haemophilus influenzae type b conjugate vaccines. J. Infect. Dis. 168:663–71 [Google Scholar]
  67. Granoff DM, Rathore MH, Holmes SJ, Granoff PD, Lucas AH. 66.  1993. Effect of immunity to the carrier protein on antibody responses to Haemophilus influenzae type b conjugate vaccines. Vaccine 11:Suppl. 1S46–51 [Google Scholar]
  68. Granoff DM, Shackelford PG, Holmes SJ, Lucas AH. 67.  1993. Variable region expression in the antibody responses of infants vaccinated with Haemophilus influenzae type b polysaccharide-protein conjugates: description of a new lambda light chain-associated idiotype and the relation between idiotype expression, avidity, and vaccine formulation. The Collaborative Vaccine Study Group. J. Clin. Invest. 91:788–96 [Google Scholar]
  69. Lucas AH, Azmi FH, Mink CM, Granoff DM. 68.  1993. Age-dependent V region expression in the human antibody response to the Haemophilus influenzae type b polysaccharide. J. Immunol. 150:2056–61 [Google Scholar]
  70. Reason DC, Lucas AH. 69.  1993. Content and dynamics of the human antibody variable region repertoire to the Haemophilus influenzae type b polysaccharide. Springer Semin. Immunopathol. 15:119–37 [Google Scholar]
  71. Chung GH, Scott MG, Kim KH, Kearney J, Siber GR. 70.  et al. 1993. Clonal characterization of the human IgG antibody repertoire to Haemophilus influenzae type b polysaccharide. V. In vivo expression of individual antibody clones is dependent on Ig CH haplotypes and the categories of antigen. J. Immunol. 151:4352–61 [Google Scholar]
  72. Vakil M, Briles DE, Kearney JF. 71.  1991. Antigen-independent selection of T15 idiotype during B-cell ontogeny in mice. Dev. Immunol. 1:203–12 [Google Scholar]
  73. Vakil M, Kearney JF. 72.  1986. Functional characterization of monoclonal auto-anti-idiotype antibodies isolated from the early B cell repertoire of BALB/c mice. Eur. J. Immunol. 16:1151–58 [Google Scholar]
  74. Greenspan NS, Fulton RJ, Davie JM. 73.  1986. Analysis of anti-streptococcal group A carbohydrate idiotope levels in sera: correlation of magnitude of expression with idiotope position and VK haplotype. J. Immunol. 137:228–33 [Google Scholar]
  75. Stohrer R, Kearney J. 74.  1984. Ontogeny of B cell precursors responding to alpha 1- greater than 3 dextran in BALB/c mice. J. Immunol. 133:2323–26 [Google Scholar]
  76. Huflejt ME, Vuskovic M, Vasiliu D, Xu H, Obukhova P. 75.  et al. 2009. Anti-carbohydrate antibodies of normal sera: findings, surprises and challenges. Mol. Immunol. 46:3037–49 [Google Scholar]
  77. Scott MG, Briles DE, Shackelford PG, Smith DS, Nahm MH. 76.  1987. Human antibodies to phosphocholine: IgG anti-PC antibodies express restricted numbers of V and C regions. J. Immunol. 138:3325–31 [Google Scholar]
  78. Emmrich F, Schilling B, Eichmann K. 77.  1985. Human immune response to group A streptococcal carbohydrate (A-CHO). I. Quantitative and qualitative analysis of the A-CHO-specific B cell population responding in vitro to polyclonal and specific activation. J. Exp. Med. 161:547–62 [Google Scholar]
  79. Shackelford PG, Nelson SJ, Palma AT, Nahm MH. 78.  1988. Human antibodies to group A streptococcal carbohydrate: ontogeny, subclass restriction, and clonal diversity. J. Immunol. 140:3200–5 [Google Scholar]
  80. Newacheck PW, Taylor WR. 79.  1992. Childhood chronic illness: prevalence, severity, and impact. Am. J. Public Health 82:364–71 [Google Scholar]
  81. Hansen G, Berry G, DeKruyff RH, Umetsu DT. 80.  1999. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 103:175–83 [Google Scholar]
  82. Yamaya M. 81.  2012. Virus infection-induced bronchial asthma exacerbation. Pulm. Med. 2012:834826 [Google Scholar]
  83. Acevedo N, Erler A, Briza P, Puccio F, Ferreira F, Caraballo L. 82.  2011. Allergenicity of Ascaris lumbricoides tropomyosin and IgE sensitization among asthmatic patients in a tropical environment. Int. Arch. Allergy Immunol. 154:195–206 [Google Scholar]
  84. Lechner CJ, Komander K, Hegewald J, Huang X, Gantin RG. 83.  et al. 2013. Cytokine and chemokine responses to helminth and protozoan parasites and to fungus and mite allergens in neonates, children, adults, and the elderly. Immun. Ageing 10:29 [Google Scholar]
  85. Mizoguchi E, Mizoguchi A, Preffer FI, Bhan AK. 84.  2000. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int. Immunol. 12:597–605 [Google Scholar]
  86. Vargas MH. 85.  2006. Ecological association between scarlet fever and asthma. Respir. Med. 100:363–66 [Google Scholar]
  87. Schaub B, Liu J, Hoppler S, Schleich I, Huehn J. 86.  et al. 2009. Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J. Allergy Clin. Immunol. 123:774–82.e5 [Google Scholar]
  88. Ling EM, Smith T, Nguyen XD, Pridgeon C, Dallman M. 87.  et al. 2004. Relation of CD4+CD25+ regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 363:608–15 [Google Scholar]
  89. Akdis M, Verhagen J, Taylor A, Karamloo F, Karagiannidis C. 88.  et al. 2004. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J. Exp. Med. 199:1567–75 [Google Scholar]
  90. Bellinghausen I, Klostermann B, Knop J, Saloga J. 89.  2003. Human CD4+CD25+ T cells derived from the majority of atopic donors are able to suppress TH1 and TH2 cytokine production. J. Allergy Clin. Immunol. 111:862–68 [Google Scholar]
  91. McGuirk P, Mills KH. 90.  2002. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 23:450–55 [Google Scholar]
  92. Dimov VV, Stokes JR, Casale TB. 91.  2009. Immunomodulators in asthma therapy. Curr. Allergy Asthma Rep. 9:475–83 [Google Scholar]
  93. Schwarze J, Cieslewicz G, Joetham A, Sun LK, Sun WN. 92.  et al. 1998. Antigen-specific immunoglobulin-A prevents increased airway responsiveness and lung eosinophilia after airway challenge in sensitized mice. Am. J. Respir. Crit. Care Med. 158:519–25 [Google Scholar]
  94. Moerch U, Haahr Hansen M, Vest Hansen NJ, Rasmussen LK, Oleksiewicz MB. 93.  et al. 2006. Allergen-specific polyclonal antibodies reduce allergic disease in a mouse model of allergic asthma. Int. Arch. Allergy Immunol. 140:261–69 [Google Scholar]
  95. Murali PS, Kelly KJ, Fink JN, Kurup VP. 94.  1994. Investigations into the cellular immune responses in latex allergy. J. Lab Clin. Med. 124:638–43 [Google Scholar]
  96. Reisinger J, Horak F, Pauli G, van Hage M, Cromwell O. 95.  et al. 2005. Allergen-specific nasal IgG antibodies induced by vaccination with genetically modified allergens are associated with reduced nasal allergen sensitivity. J. Allergy Clin. Immunol. 116:347–54 [Google Scholar]
  97. Kurup VP, Choi H, Murali PS, Resnick A, Fink JN, Coffman RL. 96.  1997. Role of particulate antigens of Aspergillus in murine eosinophilia. Int. Arch. Allergy Immunol. 112:270–78 [Google Scholar]
  98. Hamelmann E, Oshiba A, Schwarze J, Bradley K, Loader J. 97.  et al. 1997. Allergen-specific IgE and IL-5 are essential for the development of airway hyperresponsiveness. Am. J. Respir. Cell Mol. Biol. 16:674–82 [Google Scholar]
  99. Tsitoura DC, Yeung VP, DeKruyff RH, Umetsu DT. 98.  2002. Critical role of B cells in the development of T cell tolerance to aeroallergens. Int. Immunol. 14:659–67 [Google Scholar]
  100. Wills-Karp M, Nathan A, Page K, Karp CL. 99.  2010. New insights into innate immune mechanisms underlying allergenicity. Mucosal Immunol. 3:104–10 [Google Scholar]
  101. Harnett W, Harnett MM. 100.  2008. Parasitic nematode modulation of allergic disease. Curr. Allergy Asthma Rep. 8:392–97 [Google Scholar]
  102. Cywes-Bentley C, Skurnik D, Zaidi T, Roux D, Deoliveira RB. 101.  et al. 2013. Antibody to a conserved antigenic target is protective against diverse prokaryotic and eukaryotic pathogens. PNAS 110:E2209–18 [Google Scholar]
  103. Kung TT, Jones H, Adams GK 3rd, Umland SP, Kreutner W. 102.  et al. 1994. Characterization of a murine model of allergic pulmonary inflammation. Int. Arch. Allergy Immunol. 105:83–90 [Google Scholar]
  104. Shah A, Panjabi C. 103.  2002. Allergic bronchopulmonary aspergillosis: a review of a disease with a worldwide distribution. J. Asthma 39:273–89 [Google Scholar]
  105. Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC. 104.  1993. Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. PNAS 90:4266–70 [Google Scholar]
  106. Shibata Y, Metzger WJ, Myrvik QN. 105.  1997. Chitin particle-induced cell-mediated immunity is inhibited by soluble mannan: mannose receptor-mediated phagocytosis initiates IL-12 production. J. Immunol. 159:2462–67 [Google Scholar]
  107. Kin NW, Stefanov EK, Dizon BL, Kearney JF. 106.  2012. Antibodies generated against conserved antigens expressed by bacteria and allergen-bearing fungi suppress airway disease. J. Immunol. 189:2246–56 [Google Scholar]
  108. 107. Quest Diagn 2011. The largest study of allergy testing in the United States Quest Diagn. Health Trends, Quest Diagn., Madison, NJ. http://www.questdiagnostics.com/dms/Documents/Other/2011_QD_AllergyReport.pdf
  109. Baldo BA, Krilis S, Fletcher TC. 108.  1979. Phosphorylcholine-containing allergens. Naturwissenschaften 66:623–25 [Google Scholar]
  110. Baldo BA, Fletcher TC, Uhlenbeuck G. 109.  1977. Reaction of house dust mite extracts with mouse anti-phosphorylcholine and anti-galactan myeloma proteins. Naturwissenschaften 64:594–95 [Google Scholar]
  111. Holt PG, Sly PD. 110.  2007. Prevention of allergic respiratory disease in infants: current aspects and future perspectives. Curr. Opin. Allergy Clin. Immunol. 7:547–55 [Google Scholar]
  112. Yazdanbakhsh M, Kremsner PG, van Ree R. 111.  2002. Allergy, parasites, and the hygiene hypothesis. Science 296:490–94 [Google Scholar]
  113. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. 112.  2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 107:129–34 [Google Scholar]
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