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To B or not to B: B cells and the Th2-type immune response to helminths

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Harris, Nicola, Gause, William C.·2011·Trends in Immunology
DOI 10.1016/j.it.2010.11.005PMC PMC3076625
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Abstract

Similar T helper (Th)2-type immune responses are generated against different helminth parasites, but the mechanisms that initiate Th2 immunity, and the specific immune components that mediate protection against these parasites, can vary greatly. B cells are increasingly recognized as important during the Th2-type immune response to helminths, and B cell activation might be a target for effective vaccine development. Antibody production is a function of B cells during helminth infection and understanding how polyclonal and antigen-specific antibodies contribute should provide important insights into how protective immunity develops. In addition, B cells might also contribute to the host response against helminths through antibody-independent functions including, antigen presentation, as well as regulatory and effector activity. In this review, we examine the role of B cells during Th2-type immune response to these multicellular parasites.

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  • The host B cell response is crucial for parasite ejection.

    “An equally important target for helminth parasites is the host B cell response, which is known to be crucial for parasite ejection (Harris and Gause, 2011).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Harris and Gause, 2011

    The Concluding remarks say B cells are essential for protective immunity in some mucosal helminth responses, supporting their importance in parasite clearance. But the same section says other helminths elicit protective responses without B cells, and Mechanisms of antibody-mediated protection specifically reports expulsion of N. brasiliensis in their absence. The claim overgeneralizes their necessity for parasite ejection. (LLM, conf=0.88)

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  1. [1]Hotez PJ 2008 Helminth infections: the great neglected tropical diseases J Clin Invest 118 4 1311 1321 18382743 PMC2276811
  2. [2]Bethony J 2006 Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm Lancet 367 9521 1521 1532 16679166
  3. [3]Maizels RM 1999 Vaccination against helminth parasites--the ultimate challenge for vaccinologists? Immunol Rev 171 125 147 10582168
  4. [4]Lightowlers MW 2006 Cestode vaccines: origins, current status and future prospects Parasitology 133 Suppl S27 42 17274847
  5. [5]Diemert DJ 2008 Hookworm vaccines Clin Infect Dis 46 2 282 288 18171264
  6. [6]McManus DP Loukas A 2008 Current status of vaccines for schistosomiasis Clin Microbiol Rev 21 1 225 242 18202444 PMC2223839
  7. [7]Cable J 2006 Molecular evidence that Heligmosomoides polygyrus from laboratory mice and wood mice are separate species Parasitology 133 Pt 1 111 122 16536883
  8. [8]McCoy KD 2008 Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection Cell Host Microbe 4 4 362 373 18854240
  9. [9]Watanabe N 1988 Protective immunity and eosinophilia in IgE-deficient SJA/9 mice infected with Nippostrongylus brasiliensis and Trichinella spiralis Proc Natl Acad Sci U S A 85 12 4460 4462 3380800 PMC280449
  10. [10]El Ridi R 1998 Schistosoma mansoni infection in IgE-producing and IgE-deficient mice J Parasitol 84 1 171 174 9488359
  11. [11]Grencis RK 1993 The in vivo role of stem cell factor (c-kit ligand) on mastocytosis and host protective immunity to the intestinal nematode Trichinella spiralis in mice Parasite Immunol 15 1 55 59 7679484
  12. [12]Ha TY 1983 Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice Infect Immun 41 1 445 447 6345400 PMC264803
  13. [13]Lantz CS 1998 Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites Nature 392 6671 90 93 9510253
  14. [14]Gurish MF 2004 IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis J Immunol 172 2 1139 1145 14707089
  15. [15]Martin C 2001 B-cell deficiency suppresses vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection Infect Immun 69 11 7067 7073 11598082 PMC100087
  16. [16]Bickle QD 2009 Radiation-attenuated schistosome vaccination--a brief historical perspective Parasitology 136 12 1621 1632 19327194
  17. [17]Blackwell NM Else KJ 2001 B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode Trichuris muris Infect Immun 69 6 3860 3868 11349052 PMC98409
  18. [18]Liu Q 2010 B cells have distinct roles in host protection against different nematode parasites J Immunol 184 9 5213 5223 20357259 PMC3729113
  19. [19]Wojciechowski W 2009 Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus Immunity 30 3 421 433 19249230 PMC2745290
  20. [20]Rajan B 2005 Critical role for IgM in host protection in experimental filarial infection J Immunol 175 3 1827 1833 16034125
  21. [21]Ghosh K Hotez PJ 1999 Antibody-dependent reductions in mouse hookworm burden after vaccination with Ancylostoma caninum secreted protein 1 J Infect Dis 180 5 1674 1681 10515831
  22. [22]Lightowlers MW 2003 Vaccination against cestode parasites: anti-helminth vaccines that work and why Vet Parasitol 115 2 83 123 12878418
  23. [23]Khoury PB 1977 Immune mechanisms to Ascaris suum in inbred guinea-pigs. I. Passive transfer of immunity by cells or serum Immunology 32 4 405 411 608676 PMC1445497
  24. [24]Murrell KD 1981 Protective role of immunoglobulin G in immunity to Strongyloides ratti J Parasitol 67 2 167 173 7241275
  25. [25]Harrison GB 2008 Antibodies to surface epitopes of the carbohydrate larval antigen CarLA are associated with passive protection in strongylid nematode challenge infections Parasite Immunol 30 11–12 577 584 19067838
  26. [26]Behnke JM Parish HA 1979 Expulsion of Nematospiroides dubius from the intestine of mice treated with immune serum Parasite Immunol 1 1 13 26 551374
  27. [27]Behnke JM Parish HA 1981 Transfer of immunity to Nematospiroides dubius: cooperation between lymphoid cells and antibodies in mediating worm expulsion Parasite Immunol 3 3 249 259 7301409
  28. [28]Dobson C 1982 Passive transfer of immunity with serum in mice infected with Nematospiroides dubius: influence of quality and quantity of immune serum Int J Parasitol 12 2–3 207 213 7076392
  29. [29]Marcet R 2002 Passive protection against fasciolosis in mice by immunization with a monoclonal antibody (ES-78 MoAb) Parasite Immunol 24 2 103 108 11874565
  30. [30]Attallah AM 1999 Induction of resistance against Schistosoma mansoni infection by passive transfer of an IgG2a monoclonal antibody Vaccine 17 18 2306 2310 10403599
  31. [31]Parab PB 1988 Characterization of a monoclonal antibody against infective larvae of Brugia malayi Immunology 64 1 169 174 3384450 PMC1385203
  32. [32]McVay CS 2000 Antibodies to tyvelose exhibit multiple modes of interference with the epithelial niche of Trichinella spiralis Infect Immun 68 4 1912 1918 10722582 PMC97366
  33. [33]Ortega-Pierres G 1984 Protection against Trichinella spiralis induced by a monoclonal antibody that promotes killing of newborn larvae by granulocytes Parasite Immunol 6 3 275 284 6377201
  34. [34]Ellis LA 1994 Glycans as targets for monoclonal antibodies that protect rats against Trichinella spiralis Glycobiology 4 5 585 592 7881172
  35. [35]Inaba T 2003 Impeded establishment of the infective stage of Trichinella in the intestinal mucosa of mice by passive transfer of an IgA monoclonal antibody J Vet Med Sci 65 11 1227 1231 14665753
  36. [36]Inaba T 2003 Monoclonal IgA antibody-mediated expulsion of Trichinella from the intestine of mice Parasitology 126 Pt 6 591 598 12866798
  37. [37]Appleton JA McGregor DD 1987 Characterization of the immune mediator of rapid expulsion of Trichinella spiralis in suckling rats Immunology 62 3 477 484 3499383 PMC1454122
  38. [38]Harris NL 2006 Mechanisms of neonatal mucosal antibody protection J Immunol 177 9 6256 6262 17056555
  39. [39]Anthony RM 2006 Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites Nat Med 12 8 955 960 16892038 PMC1955764
  40. [40]Patel N 2009 Characterisation of effector mechanisms at the host:parasite interface during the immune response to tissue-dwelling intestinal nematode parasites Int J Parasitol 39 1 13 21 18804113 PMC2842902
  41. [41]Anthony RM 2007 Protective immune mechanisms in helminth infection Nat Rev Immunol 7 12 975 987 18007680 PMC2258092
  42. [42]Herbert DR 2002 The role of B cells in immunity against larval Strongyloides stercoralis in mice Parasite Immunol 24 2 95 101 11874564
  43. [43]Ligas JA 2003 Specificity and mechanism of immunoglobulin M (IgM)- and IgG-dependent protective immunity to larval Strongyloides stercoralis in mice Infect Immun 71 12 6835 6843 14638770 PMC308934
  44. [44]Kerepesi LA 2004 Human immunoglobulin G mediates protective immunity and identifies protective antigens against larval Strongyloides stercoralis in mice J Infect Dis 189 7 1282 1290 15031798
  45. [45]McVay CS 1998 Participation of parasite surface glycoproteins in antibody-mediated protection of epithelial cells against Trichinella spiralis Infect Immun 66 5 1941 1945 9573073 PMC108147
  46. [46]Nimmerjahn F Ravetch JV 2010 FcgammaRs in Health and Disease Curr Top Microbiol Immunol 20680807
  47. [47]Finkelman FD 2004 Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites Immunol Rev 201 139 155 15361238
  48. [48]Herbert DR 2009 Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection J Exp Med 206 13 2947 2957 19995957 PMC2806463
  49. [50]Labeaud AD 2009 Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3 5 e442 19478847 PMC2682196
  50. [51]Urban JF Jr 2007 Infection with parasitic nematodes confounds vaccination efficacy Vet Parasitol 148 1 14 20 17587500 PMC1959410
  51. [52]Cooper PJ 2000 Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR J Infect Dis 182 4 1199 1206 10979918
  52. [53]Cooper PJ 1998 Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10 J Infect Dis 178 4 1133 1138 9806045
  53. [54]Kilian HD Nielsen G 1989 Cell-mediated and humoral immune responses to BCG and rubella vaccinations and to recall antigens in onchocerciasis patients Trop Med Parasitol 40 4 445 453 2623427
  54. [55]Nookala S 2004 Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis Infect Immun 72 5 2598 2604 15102768 PMC387878
  55. [56]Steenhard NR 2009 Ascaris suum infection negatively affects the response to a Mycoplasma hyopneumoniae vaccination and subsequent challenge infection in pigs Vaccine 27 37 5161 5169 19524617
  56. [57]Haseeb MA Craig JP 1997 Suppression of the immune response to diphtheria toxoid in murine schistosomiasis Vaccine 15 1 45 50 9041665
  57. [58]Noland GS 2010 Helminth infection impairs the immunogenicity of a Plasmodium falciparum DNA vaccine, but not irradiated sporozoites, in mice Vaccine 28 17 2917 2923 20188676 PMC2846978
  58. [59]Kilian HD Nielsen G 1989 Cell-mediated and humoral immune response to tetanus vaccinations in onchocerciasis patients Trop Med Parasitol 40 3 285 291 2617034
  59. [60]Itano AA 2003 Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity Immunity 19 1 47 57 12871638
  60. [61]Ekkens MJ 2003 The role of OX40 ligand interactions in the development of the Th2 response to the gastrointestinal nematode parasite Heligmosomoides polygyrus J Immunol 170 1 384 393 12496423
  61. [62]Liu Z 2002 Nippostrongylus brasiliensis can induce B7-independent antigen-specific development of IL-4-producing T cells from naive CD4 T cells in vivo J Immunol 169 12 6959 6968 12471130
  62. [63]King IL Mohrs M 2009 IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells J Exp Med 206 5 1001 1007 19380638 PMC2715031
  63. [64]Linton PJ 2003 Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo J Exp Med 197 7 875 883 12668647 PMC2193894
  64. [65]Bradley LM 2002 Availability of antigen-presenting cells can determine the extent of CD4 effector expansion and priming for secretion of Th2 cytokines in vivo Eur J Immunol 32 8 2338 2346 12209647
  65. [66]Hernandez HJ 1997 In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation J Immunol 158 10 4832 4837 9144498
  66. [67]Lu P 1994 CTLA-4 ligands are required to induce an in vivo interleukin 4 response to a gastrointestinal nematode parasite J Exp Med 180 2 693 698 8046343 PMC2191583
  67. [68]Liu Z 2004 Requirements for the development of IL-4-producing T cells during intestinal nematode infections: what it takes to make a Th2 cell in vivo Immunol Rev 201 57 74 15361233
  68. [69]Liu Q 2007 The role of B cells in the development of CD4 effector T cells during a polarized Th2 immune response J Immunol 179 6 3821 3830 17785819 PMC2258088
  69. [70]Harris DP 2000 Reciprocal regulation of polarized cytokine production by effector B and T cells Nat Immunol 1 6 475 482 11101868
  70. [71]Massacand JC 2009 Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function Proc Natl Acad Sci U S A 106 33 13968 13973 19666528 PMC2729004
  71. [72]Neill DR 2010 Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity Nature 464 7293 1367 1370 20200518 PMC2862165
  72. [73]Moro K 2010 Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells Nature 463 7280 540 544 20023630
  73. [74]Jankovic D 1998 CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling J Exp Med 187 4 619 629 9463412 PMC2212140
  74. [75]Lundy SK Boros DL 2002 Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10 Infect Immun 70 2 812 819 11796615 PMC127725
  75. [76]Smelt SC 2000 B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology J Immunol 164 7 3681 3688 10725726
  76. [77]Smits HH 2010 Chronic helminth infections protect against allergic diseases by active regulatory processes Curr Allergy Asthma Rep 10 1 3 12 20425508 PMC2816799
  77. [78]Amu S 2010 Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model J Allergy Clin Immunol 125 5 1114 1124 e1118 20304473
  78. [79]Mangan NE 2004 Helminth infection protects mice from anaphylaxis via IL-10-producing B cells J Immunol 173 10 6346 6356 15528374
  79. [80]Smits HH 2007 Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection J Allergy Clin Immunol 120 4 932 940 17689595
  80. [81]Velupillai P Harn DA 1994 Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsets Proc Natl Acad Sci U S A 91 1 18 22 7904066 PMC42877
  81. [82]Velupillai P 1997 B-1 cell (CD5+B220+) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars J Immunol 158 1 338 344 8977208
  82. [83]Wilson MS 2010 Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation Eur J Immunol 40 6 1682 1696 20306466 PMC3179601
  83. [84]Weinstock JV Elliott DE 2009 Helminths and the IBD hygiene hypothesis Inflamm Bowel Dis 15 1 128 133 18680198
  84. [85]Correale J 2008 Helminth infections associated with multiple sclerosis induce regulatory B cells Ann Neurol 64 2 187 199 18655096
  85. [86]Correale J Farez M 2007 Association between parasite infection and immune responses in multiple sclerosis Ann Neurol 61 2 97 108 17230481
  86. [87]Fleming J Fabry Z 2007 The hygiene hypothesis and multiple sclerosis Ann Neurol 61 2 85 89 17315205
  87. [88]Islam MK 2005 Vaccination with recombinant Ascaris suum 24-kilodalton antigen induces a Th1/Th2-mixed type immune response and confers high levels of protection against challenged Ascaris suum lung-stage infection in BALB/c mice Int J Parasitol 35 9 1023 1030 15998515
  88. [89]Rolink A 1996 The SCID but not the RAG-2 gene product is required for S mu-S epsilon heavy chain class switching Immunity 5 4 319 330 8885865
  89. [90]Perona-Wright G 2008 Cutting edge: Helminth infection induces IgE in the absence of mu- or delta-chain expression J Immunol 181 10 6697 6701 18981085 PMC3066072
  90. [91]DiLillo DJ 2010 B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer Ann N Y Acad Sci 1183 38 57 20146707
  91. [92]Mizoguchi A Bhan AK 2006 A case for regulatory B cells J Immunol 176 2 705 710 16393950
  92. [93]Schroppel B Heeger PS 2010 Gazing into a crystal ball to predict kidney transplant outcome J Clin Invest 120 6 1803 1806 20501950 PMC2877963
  93. [94]Fillatreau S 2008 Not always the bad guys: B cells as regulators of autoimmune pathology Nat Rev Immunol 8 5 391 397 18437156
  94. [95]Couper KN 2008 IL-10: the master regulator of immunity to infection J Immunol 180 9 5771 5777 18424693

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Authors
Harris, N., & Gause, W. C.
Affiliations
  • Swiss Vaccine Research Institute (CH)
  • Rutgers New Jersey Medical School (US)
Corresponding author
Gause, William C.
ORCID
Venue
Trends in Immunology
Publisher
Elsevier BV
Published
2011-02
Volume
32
Issue
2
Pages
80-88
ISSN
1471-4906 (ISSN-L)
DOI
10.1016/j.it.2010.11.005
PMC
PMC3076625
OpenAlex
W2044198861
Cited by
166
References
1
Citations by year
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FWCI
1.64
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Trends in Immunology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders
National Institute of Allergy and Infectious Diseases (R01AI031678, R01AI066188, R01AI069395, R01AI66188)
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Mollusks and Parasites Studies
Keywords
B cells, Th2 immune response, helminthiasis, humoral immunity, B cell activation, helminth vaccines, antigen presentation, regulatory B cells, effector B cells, protective immunity
MeSH terms
Animals, Antibodies, Helminth, B-Lymphocytes, Helminthiasis, Helminths, Humans, Vaccination, Th2 Cells

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