Hostname: page-component-848d4c4894-v5vhk Total loading time: 0 Render date: 2024-07-05T21:01:11.519Z Has data issue: false hasContentIssue false

Expansion of the humoral effector cell compartment of both systemic and mucosal immune systemsin a weanling murine model which duplicates critical features of human protein-energy malnutrition

Published online by Cambridge University Press:  09 March 2007

C.-L. Ha
Affiliation:
Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, ON NIG 2 W1, Canada
L.E. Paulino
Affiliation:
Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, ON NIG 2 W1, Canada
B.D. Woodward
Affiliation:
Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, ON NIG 2 W1, Canada
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A direct comparison of systemic (spleen) and mucosal (intestine) antibody-producing systems was made in weanling male C57BL/6J mice subjected to wasting protein-energy malnutrition (PEM) by means of a low-protein protocol known to duplicate immunological and physiological features of human malnutrition. ELISA revealed low concentrations of biliary and gut lumen immunoglobulin (Ig) A in malnourished mice concomitantly with a high concentration of blood IgA. The low-protein model, therefore, exhibited fidelity to human protein-energy malnutrition in its influence on the concentrations of the mucosal Ig, IgA, in critical biological fluids. The number of IgA-, IgM- and IgG-containing cells was estimated morphometrically on a per organ basis. The low-protein protocol supported expansion in numbers of mucosal IgA-containing cells (18 x relative to a zero-time control group) and of splenic IgG- containing cells (135 x ), albeit an attenuated expansion in comparison with that of well-nourished control animals (132x and 571x respectively relative to zero-time controls). Up to terminal differentiation of Ig-containing cells, systemic and mucosal antibody-producing systems exhibited similarly remarkable resistance to wasting malnutrition. Epithelial transport of IgA may be an aspect of the mucosal antibody response which is particularly sensitive to PEM.

Type
immune response in malnutrition
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Abbas, A.K., Lichtman, A. H. & Pober, J.S. (1991). Cellular and Molecular Immunology. Philadelphia: W.B. Sanunders.Google Scholar
Alverdy, J.A., Aoys, E., Weiss-Carrington, P. & Burke, D. A. (1992). The effect of glutamine-enriched TPN on gut immune cellularity. Journal of Surgical Research 52, 3438.CrossRefGoogle ScholarPubMed
Barry, W. S. & Pierce, N. F. (1979). Protein deprivation causes reversible impairment of mucosal immune response to cholera toxoid/toxin in rat gut. Nature 281, 6465.CrossRefGoogle ScholarPubMed
Beatty, D. W., Napier, B., Sinclair-Smith, C. C., McCabe, K. & Hughes, E. J. (1983). Secretory IgA synthesis in kwashiorkor. Journal of Clinical and Laboratory Immunology 12, 3136.Google ScholarPubMed
Bell, R. G., Turner, K. J., Gracey, M., Suharjono, & Sunoto, (1976). Serum and small intestinal immunoglobulin livels in undernourished children. American Journal of Clinical Nutrition 29, 392397.CrossRefGoogle Scholar
Brunser, O., Araya, M. & Espinoza, J. (1990). Gastrointestinal tract changes in the malnourished child. In The Malnourished Child, pp. 261276 [Suskind, R. M. and Lewinter-Suskind, L., editors]. New York: Vevey/Raven Press.Google Scholar
Chandra, R.K. (1975). Reduced secretory antibody response to live attenuated measles and poliovirus vaccines in malnourished children. British Medical Journal 2, 583585.CrossRefGoogle ScholarPubMed
Chandra, R. K. (1991). Nutrition and immunity: lessons from the past and new insights into the future. American Journal of Clinical Nutrition 53, 10871101,CrossRefGoogle ScholarPubMed
Chandra, R. K. & Wadhwa, M. (1993). Nutritional deficiencies and intestinal mucosal immunity. In Immunophysiology of the Gut, pp. 389399 [Walker, W. A., Harmatz, P. R. and Wershil, B. K., editors]. San Diego: Academic Press.CrossRefGoogle Scholar
Crabbe, P. A., Bazin, H., Eyssen, H. & Heremans, J. F. (1968). The normal microbial flora as a major stimulus for proliferation of plasma cells synthesizing IgA in the gut. International Archives of Allergy 34, 362375.CrossRefGoogle Scholar
Delacroix, D. L., Malburny, G. N. & Vaerman, J.-P. (1985). Hepatobiliary transport of plasma IgA in the mouse: contribution to clearance of intravascular IgA. European Journal of Immunology 15, 893899.CrossRefGoogle ScholarPubMed
Doherty, J. F., Golden, M.H.N., Remick, D.G. & Griffin, G. E. (1994). Production of interleukin-6 and tumour necrosis factor-α in vitro is reduced in whole blood of severely malnourished children. Clinical Science 86, 347351.CrossRefGoogle ScholarPubMed
Filteau, S. M., Berdusco, E., Perry, K. J. & Woodward, B. (1987). The effect of triiodothyronine on evanescent delayed hypersensitivity to sheep red blood cells and on the primary antibody response to trinitrophenylated Brucella abortus in severely undernourished weanling mice. International Journal of Immunopharmacology 9, 811816.CrossRefGoogle ScholarPubMed
Filteau, S. M. & Woodward, B. (1984). Relationship between serum zinc level and immunocompetence in proteindeficient and well-nourished weanling mice. Nutrition Research 4, 853866.CrossRefGoogle Scholar
Filteau, S. M. & Woodward, B. (1987). Influence of severe protein deficiency and of severe food intake restriction on serum levels of thyroid hormones in the weanling mouse. Nutrition Research 7, 101107.CrossRefGoogle Scholar
Foy, T. M., Shepherd, D. M., Durie, F.H., Aruffo, A., Ledbetter, J. A. & Noelle, R. J. (1993). In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity. II. Prolonged suppression of the humoral immune response by an antibody to the ligand for CD40, gp39. Journal of Experimental Medicine 178, 15671575.CrossRefGoogle Scholar
Green, F. & Heyworth, B. (1980). Immunoglobulin-containing cells in jejunal mucosa of children with Protein-energy malnutrition and gastroenteritis. Archives of Disease in Childhood 55, 380383.CrossRefGoogle ScholarPubMed
Gross, R. L. & Newberne, P. M. (1980). Role of nutrition in immunologic function. Physiological Reviews 60, 188302.CrossRefGoogle ScholarPubMed
Ha, C.-L. & Woodward, B. D. (1994). Reduced IgA in intestinal lumen and low hepatic secretory component (SC) in weanling malnutrition. Canadian Federation of bilological Societies 74, Abstr.Google Scholar
Harlow, E. & Lane, D. (1988). Antibodies: a Laboratory Manual. New York: Cold Spring Harbor Laboratory.Google Scholar
Horwitz, W. (1980). Official Methods of Analysis of the Association of Oficial Analytical Chemists, 13th ed. Washington, DC: Association of Official Analytical Chemists.Google Scholar
Ingram, K. G., Croy, B. A. & Woodward, B. D. (1995). Splenic natural killer cell activity in wasted, protein-energy malnourished weanling mice. Nutrition Research 15, 231243.CrossRefGoogle Scholar
Keet, M. P. & Thorn, H. (1969). Serum immunoglobulins in kwashiorkor. Archives of Disease in Childhood 44, 600603.CrossRefGoogle ScholarPubMed
Kroese, F. G. M., Ammerlaan, W. A. M. & Deenen, G. J. (1992). Location and function of B-cell lineages. Annals of the New York Academy of Sciences 651, 4458.Google Scholar
Lim, T. S., Messiha, N. & Watson, R. R. (1981). Immune components of the intestinal mucosae of ageing and protein deficient mice. Immunology 43, 401407.Google ScholarPubMed
Lopez, M. C. & Roux, M. E. (1989). Impaired differentiation of IgA-B cell precursors in the Peyer's patches of protein depleted rats. Developmental and Comparative Immunology 13, 253262.CrossRefGoogle Scholar
McGee, D. W. & McMurray, D. N. (1988 a). The effect of protein malnutrition on the IgA immune response in mice. Immunology 63, 2529.Google ScholarPubMed
McGee, D. W. & McMurray, D. N. (1988 b). Protein malnutrition reduces the IgA immune response to oral antigen by altering B-cell and suppressor T-cell functions. Immunology 64, 697702.Google ScholarPubMed
McMurray, D. N., Mintzer, C. L., Bartow, R. A. & Parr, R. L. (1989). Dietary protein deficiency and Mycobacterium bovis BCG affect interleukin-2 activity in experimental pulmonary tuberculosis. Infection and Immunity 57, 26062611.CrossRefGoogle ScholarPubMed
McMurray, D.N., Rey, H., Casazza, L. J. & Watson, R.R. (1977). Effect of moderate malnutrition on concentrations of immunoglobulins and enzymes in tears and saliva of young Colombian children. American Journal of Clinical Nutrition 30, 19441948.CrossRefGoogle ScholarPubMed
Mattioli, C. A. & Tomasi, T. B. Jr (1973). The life span of IgA plasma cells from the mouse intestine. Journal of Experimental Medicine 138, 452460.CrossRefGoogle ScholarPubMed
Mayhew, T. M. & Williams, M. A. (1974). A quantitative morphological analysis of macrophage stimulation. II. Changes in granule number, size and size distributions. Cell and Tissue Research 150, 529543.CrossRefGoogle ScholarPubMed
Ojeda, J. L., Ros, M. A. & Icardo, J. M. (1989). A technique for fluorescence microscopy in semithin sections. Stain Technology 64, 243248.CrossRefGoogle ScholarPubMed
Ramsay, A. J., Husband, A. J., Ramshaw, I. A., Bao, S., Matthaei, K. I., Koehler, G. & Kopf, M. (1994). The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264, 561563.CrossRefGoogle ScholarPubMed
Reddy, V., Raghuramulu, N. & Bhaskaram, C. (1976). Secretory IgA in protein-calorie malnutrition. Archives of Disease in Childhood 51, 871874.CrossRefGoogle ScholarPubMed
Reeves, P.G., Nielsen, F. H. & Gahey, G.C. Jr (1993). AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformation of the AIN-76A rodent diet. Journal of Nutrition 132, 19391951.CrossRefGoogle Scholar
Rothman, D., Latham, M. C. & Walker, W. A. (1982). Transport of macromolecules in malnourished animals. I. Evidence for increased uptake of intestinal antigens. NutrisionResearch 2, 467473.Google Scholar
Sirisinha, S., Suskind, R., Edelman, L.T.C.R., Asvapaka, C. & Olson, R. E. (1975). Secretory and serum IgA in children with protein-calorie malnutrition. Pediatrics 55, 166170.CrossRefGoogle ScholarPubMed
Slobodianik, N.H., Cosarinsky, R.C., Langini, S.H., Roux, M.R., Rio, M.E. & Sanahuja, J.C. (1984). Effect of severe protein deficiency on surface and intracellular markers of growing rats' lymphoid organs. Nutrition Reports International 29, 957964.Google Scholar
Statistical Analysis Systems (1985). SAS User's Guide, Statistics. Cary, NC: SAS Institute Inc.Google Scholar
Steihm, E. R. (1980). Humoral immunity in malnutrition. Federation Proceedings 39, 30933097.Google Scholar
Sullivan, D. A., Vaerman, J.-P. & Soo, C. (1993). Influence of severe protein malnutrition on rat lacrimal, salivary and gastrointestinal immune expression during development, adulthood and ageing. Immunology 78, 308317.Google ScholarPubMed
Talmage, D. W., Freter, G. G. & Taliaferro, W. H. (1956). The effect of repeated injection of sheep red cells on the hemolytic and combining capacities of rabbit antiserums. Journal of Infectious Diseases 98, 293299.CrossRefGoogle ScholarPubMed
van Noorden, S. (1986) Tissue preparation and immunostaining techniques for light microscopy. In Immunocytochemistry: Modern Methods and Application, pp. 2653 [Polak, J. M. and van Noorden, S., editors]. Bristol: Wright.Google Scholar
Wade, S., Lemonnier, D., Alexiu, A. & Bocquet, L. (1982). Effect of early postnatal under- and overnutrition on the development of IgA plasma cells in mouse gut. Journal of Nutrition 112, 10471051.CrossRefGoogle ScholarPubMed
Watson, R. R. (1984). Nutritional stresses: alterations in mucosal immunity and secretory IgA. In Nutrition, Disease Resistance, and Immune Function, pp. 189204 [Watson, R. R., editor]. New York: Marcel Dekker.Google Scholar
Watson, R. R., McMurray, D. N., Martin, P. & Reyes, M. A. (1985). Effect of age, malnutrition and renutrition on free secretory component and IgA in secretions. American Journal of Clinical Nutrition 42, 281288.CrossRefGoogle ScholarPubMed
Watson, R. R., Reyes, M. A. & McMurray, D. N. (1978). Influence of malnutrition on the concentration of IgA, lysozyme, amylase, and aminopeptidase in children's tears. Proceedings of the Society.for Experimental Biology and Medicine 157, 215219.CrossRefGoogle ScholarPubMed
Weibel, E. R. & Bolender, R. P. (1973). Stereological techniques for electron microscopic morphometry. In Principles and Techniques of Electron Microscopy. Biological Applicutions, vol. 3, pp. 237296 [Hayat, M. A., editor]. New York: Van Nostrand Reinhold.Google Scholar
Wold, A. E., Dahlgren, U. I. H., Hanson, L. A., Mattsby-Baltazer, I. & Midvetdt, T. (1989). Difference between bacterial and food antigens in mncosal immunogenicity. Infection and Immunity 57, 26662673.CrossRefGoogle ScholarPubMed
Woods, J. W. & Woodward, B. D. (1991). Enhancement of primary systemic acquired immunity by exogenous triiodothyronine in wasted, protein-energy malnourished weanling mice. Journal of Nutrition 121, 14251432.CrossRefGoogle ScholarPubMed
Woodward, B. D. & Miller, R. G. (1991). Depression of thymus-dependent immunity in wasting protein-energy malnutrition does not depend on an altered ratio of helper(CD4+) to suppressor (CD8+) T cells or on a disproportionately large atrophy of the T-cell relative to the B-cell pool. American Journal of Clinical Nutrition 53, 13291335.CrossRefGoogle ScholarPubMed