Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-29T02:40:44.727Z Has data issue: false hasContentIssue false

Advances in mucosal vaccination

Published online by Cambridge University Press:  28 February 2007

Els N. T. Meeusen*
Affiliation:
Centre for Animal Biotechnology, School of Veterinary Science, The University of Melbourne, Australia
Jean-Pierre Y. Scheerlinck
Affiliation:
Centre for Animal Biotechnology, School of Veterinary Science, The University of Melbourne, Australia
Sean Wattegedera
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh, UK
Gary Entrican
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh, UK
*
*Centre for Animal Biotechnology, School of Veterinary Science, The University of Melbourne, Victoria 3010, Australia

Abstract

Pathogens that enter the body via mucosal surfaces face unique defense mechanisms that combine the innate barrier provided by the mucus layer with an adaptive response typified by the production and transepithelial secretion of pathogen-specific IgA. Both the measurement and induction of mucosal responses pose significant challenges for experimental and practical application and may need to be adapted to the species under study. In particular, for livestock, immunization procedures developed in small rodent models are not always effective in large animals or compatible with management practices. This paper reviews the latest advances in our understanding of the processes that lead to secretory IgA responses and how this relates to the development of mucosal immunization procedures and adjuvants for veterinary vaccines. In addition, it highlights the complex interactions that can take place between the pathogen and the host's immune response, with specific reference to Chlamydia/Chlamydophila infections in sheep.

Type
Research Article
Copyright
Copyright © CAB International 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ayabe, T, Satchell, DP, Wilson, CL, Parks, WC, Selsted, ME and Ouellette, AJ (2000). Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nature Immunology 1: 99100.CrossRefGoogle ScholarPubMed
Babiuk, LA, Pontarollo, R, Babiuk, S, Loehr, B and van Drunen Littel-van den Hurk, S (2003). Induction of immune responses by DNA vaccines in large animals. Vaccine 21: 649658.CrossRefGoogle ScholarPubMed
Berzofsky, JA, Ahlers, JD and Belyakov, IM (2001). Strategies for designing and optimizing new generation vaccines. Nature Reviews. Immunology 1: 209219.CrossRefGoogle ScholarPubMed
Bouvet, JP, Decroix, N and Pamonsinlapatham, P (2002). Stimulation of local antibody production: parenteral or mucosal vaccination? Trends in Immunology 23: 209213.CrossRefGoogle ScholarPubMed
Brown, J, Howie, SEM and Entrican, G (2001). A role for tryptophan in immune control of chlamydial abortion in sheep. Veterinary Immunology and Immunopathology 82 107119.CrossRefGoogle ScholarPubMed
Constant, S, Brogdon, J, Piggott, D, Herrick, C, Visintin, I, Ruddle, N and Bottomly, K (2002). Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ. Journal of Clinical Investigation 110: 14411448.CrossRefGoogle ScholarPubMed
Cotter, TW, Meng, Q, Shen, Z-L, Zhang,, Y-X, Su,, H and Caldwell, HD (1995). Protective efficacy of major outer protein-specific immunoglobulin A (IgA) and IgG monoclonal antibodies in a murine model of Chlamydia trachomatis genital tract infection. Infection and Immunity 63: 47044714.CrossRefGoogle Scholar
Crottet, P and Corthesy, B (1998). Secretory component delays the conversion of secretory IgA into antigen-binding competent F(ab')2: a possible implication for mucosal defense. Journal of Immunology 161: 54455453.CrossRefGoogle ScholarPubMed
Daynes, R, Enioutina, E, Butler, S, Mu, H-H, McGee, Z and Araneo, B (1996). Induction of common mucosal immunity by hormonally immunomodulated peripheral immunization. Infection and Immunity 64: 1199–1109.CrossRefGoogle ScholarPubMed
Enioutina, E, Visic, D and Daynes, R (2000). The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 18: 27532767.CrossRefGoogle ScholarPubMed
Entrican, G (2002). Immune control during pregnancy and host-pathogen interactions in infectious abortion. Journal of Comparative Pathology 126: 7994.CrossRefGoogle ScholarPubMed
Entrican, G, Brown, J and Graham, S (1998). Cytokines and the protective host immune response to Chlamydia psittaci. Comparative Immunology, Microbiology and Infectious Diseases 21: 1526.CrossRefGoogle ScholarPubMed
Entrican, G, Buxton, D and Longbottom, D (2001). Chlamydial infection in sheep: immune control versus fetal pathology. Journal of the Royal Society of Medicine 94: 272277.CrossRefGoogle ScholarPubMed
Entrican, G, Wattegedera, S, Chui, M, Oemar, L, Rocchi, M and McInnes, C (2002). IFN-γ fails to induce expression of indolamine 2, 3- dioxygenase and does not control the growth of Chlamydophila abortus in BeWo trophoblast cells. Infection and Immunity 70: 26902693.CrossRefGoogle Scholar
Fagarasan, S and Honjo, T (2003). Intestinal IgA synthesis: regulation of front-line body defences. Nature Reviews. Immunology 3: 6372.CrossRefGoogle ScholarPubMed
Fujioka, H, Emancipator, S, Aikawa, M, Huang, D, Blatnik, F, Karban, T, DeFife, K and Mazanec, M (1998). Immunocytochemical colocalization of specific immunoglobulin A with sendai virus protein in infected polarized epithelium. Journal of Experimental Medicine 188: 12231229.CrossRefGoogle ScholarPubMed
Grohmann, U, Fallarino, F and Puccetti, P (2003). Tolerance, DCs and tryptophan: much ado about IDO. Trends in Immunology 24: 242248.CrossRefGoogle ScholarPubMed
Guerrero, R, Ball, J, Krater, S, Pacheco, S, Clements, J and Estes, M (2001). Recombinant Norwalk virus-like particles administered intranasally to mice induce systemic and mucosal (fecal and vaginal) immune responses. Journal of Virology 75: 97139722.CrossRefGoogle ScholarPubMed
Harandi, A, Eriksson, K and Holmgren, J (2003). A protective role of locally administered immunostimulatory CpG oligodeoxynucleotide in a mouse model of genital herpes infection. Journal of Virology 77: 953962.CrossRefGoogle Scholar
Holmgren, J, Czerkinsky, C, Eriksson, K and Mharandi, A (2003). Mucosal immunisation and adjuvants: a brief overview of recent advances and challenges. Vaccine 21 (Supplement 2): S89S95.CrossRefGoogle ScholarPubMed
Jacobs, HJ, Wiltshire, C, Ashman, K and Meeusen, EN (1999). Vaccination against the gastrointestinal nematode, Haemonchus contortus, using a purified larval surface antigen. Vaccine 17: 362368.CrossRefGoogle ScholarPubMed
Kirman, J and Seder, R (2003). DNA vaccination: the answer to stable, protective T-cell memory. Current Opinion in Immunology 15: 471476.CrossRefGoogle ScholarPubMed
Kriesel, J and Spruance, J (1999). Calcitriol (125-dihydroxy-vitamin D3) coadministered with influenza vaccine does not enhance humoral immunity in human volunteers. Vaccine 17: 18831888.CrossRefGoogle Scholar
Kutteh, W, Hatch, K, Blackwell, R and Mestecky, J (1988). Secretory immune system of the female reproductive tract: I. Immunoglobulin and secretory component-containing cells. Obstetrics and Gynecology 71: 5660.Google ScholarPubMed
Lamkhioued, B, Gounni, A, Gruart, V, Pierce, A, Capron, A and Capron, M (1995). Human eosinophils express a receptor for secretory component. Role in secretory IgA-dependent activation. European Journal of Immunology 25: 117125.CrossRefGoogle ScholarPubMed
Longbottom, D (2003). Chlamydial vaccine development. Journal of Medical Microbiology 52: 537540.CrossRefGoogle ScholarPubMed
Longbottom, D and Coulter, LJ (2003). Animal chlamydioses and zoonotic implications. Journal of Comparative Pathology 128: 217244.CrossRefGoogle ScholarPubMed
Macpherson, A, Lamarre, A, McCoy, K, Harriman, G, Odermatt, B, Dougan, G, Hengartner, H and Zinkernagel, R (2001). IgA production without mu or delta chain expression in developing B cells. Nature Immunology 2: 625631.CrossRefGoogle ScholarPubMed
McSorley, S, Asch, S, Costalonga, M, Reinhardt, R and Jenkins, M (2002). Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16: 365377.CrossRefGoogle ScholarPubMed
Meeusen, EN, Premier, RR and Brandon, MR (1996). Tissue-specific migration of lymphocytes: a key role for Th1 and Th2 cells? Immunology Today 17: 421–4.CrossRefGoogle ScholarPubMed
Meeusen, EN, Bischof, RJ and Lee, CS (2001). Comparative T-cell responses during pregnancy in large animals and humans. American Journal of Reproductive Immunology 46: 169–79.CrossRefGoogle Scholar
Mowat, A (2003). Anatomical basis of tolerance and immunity to intestinal antigens. Nature Reviews. Immunology 3: 331341.CrossRefGoogle ScholarPubMed
Munn, DH, Zhou, M, Attwood, JT, Bondarev, I, Conway, SJ, Marshall, B, Brown, C and Mellor, AL (1998). Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 11911193.CrossRefGoogle ScholarPubMed
Nagler-Anderson, C (2001). Man the barrier! Strategic defences in the intestinal mucosa. Nature Reviews. Immunology 1: 5967.CrossRefGoogle ScholarPubMed
Phalipon, A and Corthesy, B (2003). Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends in Immunology 24: 5558.CrossRefGoogle ScholarPubMed
Podolsky, DK (1999). Mucosal immunity and inflammation V. Innate mechanisms of mucosal defence and repair: the best offence is a good defense. American Journal of Physiology 277: G495G499.Google Scholar
Premier, RR and Meeusen, EN (1998). Lymphocyte surface marker and cytokine expression in peripheral and mucosal lymph nodes. Immunology 94: 363367.CrossRefGoogle ScholarPubMed
Premier, RR, Jacobs, HJ, Lofthouse, SA, Sedgmen, BJ and Meeusen, ENT (2004). Antibody isotype profiles in serum and circulating antibody-secreting cells following mucosal and peripheral immunisations of sheep. Veterinary Immunology and Immunopathology 98: 7784.CrossRefGoogle ScholarPubMed
Reinhardt, T, Stabel, J and Goff, J (1999). 125-dihydroxyvitamin D3 enhances milk antibody titers to Escherichia coli J5 vaccine. Journal of Dairy Science 82: 19041909.CrossRefGoogle Scholar
Reinhardt, R, Khoruts, A, Merica, R, Zell, T and Jenkins, M (2001). Visualizing the generation of memory CD4 T cells in the whole body. Nature 410: 101105.CrossRefGoogle ScholarPubMed
Rescigno, M, Urbano, M, Valzasina, B, Francolini, M, Rotta, G, Bonasio, R, Granucci, F, Kraehenbuhl, J and Ricciardi-Castagnoli, P (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunology 2: 361367.CrossRefGoogle ScholarPubMed
Rincheval-Arnold, A, Belair, L and Djiane, J (2002). Developmental expression of pIgR gene in sheep mammary gland and hormonal regulation. Journal of Dairy Research 69: 1326.CrossRefGoogle ScholarPubMed
Robinson, J, Blanchard, T, Levine, A, Emancipator, S and Lamm, M (2001). A mucosal IgA-mediated excretory immune system in vivo. Journal of Immunology 166: 36883692.CrossRefGoogle ScholarPubMed
Scheerlinck, J-PY (2001). Genetic adjuvants for DNA vaccines. Vaccine 19: 26472656.CrossRefGoogle ScholarPubMed
Sedgmen, BJ, Lofthouse, SA, Scheerlinck, JP and Meeusen, EN (2002). Cellular and molecular characterisation of the ovine rectal mucosal environment. Veterinary Immunology and Immunopathology 86: 215–20.CrossRefGoogle ScholarPubMed
Staats, HF and Ennis, FA Jr (1999). IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. Journal of Immunology 162: 61416147.CrossRefGoogle ScholarPubMed
Stanley, A, Huntley, J, Jeffrey, M and Buxton, D (2001). Characterization of ovine nasal-associated lymphoid tissue and identification of M cells in the overlying follicle- associated epithelium. Journal of Comparative Pathology 125: 262270.CrossRefGoogle ScholarPubMed
Stephens, RS (2003). The cellular paradigm of chlamydial pathogenesis. Trends in Microbiology 11: 4451.CrossRefGoogle ScholarPubMed
Van der Stede, Y, Cox, E, Van den Broeck, W and Goddeeris, B (2001). Enhanced induction of the IgA response in pigs by calcitriol after intramuscular immunization. Vaccine 19: 18701878.CrossRefGoogle ScholarPubMed
Vanrompay, D, Cox, E, Volckaert, G and Goddeeris, B (1999). Turkeys are protected from infection with Chlamydia psittaci by plasmid DNA vaccination against the major outer membrane protein. Clinical and Experimental Immunology 118: 4955.CrossRefGoogle ScholarPubMed