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Re-feeding rapidly restores protection against Heligmosomoides bakeri (Nematoda) in protein-deficient mice

Published online by Cambridge University Press:  09 February 2007

T. TU ,
K. G. KOSKI ,
L. J. WYKES  and
M. E. SCOTT
T. TU
Affiliation:
School of Dietetics and Human NutritionMcGill University(Macdonald Campus), 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec H9X 3V9, Canada
K. G. KOSKI
Affiliation:
School of Dietetics and Human NutritionMcGill University(Macdonald Campus), 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec H9X 3V9, Canada
L. J. WYKES
Affiliation:
School of Dietetics and Human NutritionMcGill University(Macdonald Campus), 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec H9X 3V9, Canada
M. E. SCOTT*
Affiliation:
Institute of Parasitology, McGill University(Macdonald Campus), 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec H9X 3V9, Canada
*
*Corresponding author: Institute of Parasitology, McGill University(Macdonald Campus), 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec H9X 3V9, Canada. Tel: +514 398 7996. Fax: +514 398 7857. E-mail: marilyn.scott@mcgill.ca
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Summary

This study determined whether the timing of re-feeding of protein-deficient mice restored functional protection against the gastrointestinal nematode, Heligmosomoides bakeri. Balb/c mice were fed a 3% protein-deficient (PD) diet and then transferred to 24% protein-sufficient (PS) diet either on the day of primary infection, 10 days after the primary infection, on the day of challenge infection, or 7 days after the challenge infection. Control mice were fed either the PD or PS diet. Onset of challenge, but not primary, infection caused short-term body weight loss, anorexia and reduced feed efficiency. Weight gain was delayed in mice when re-feeding commenced on the day of challenge infection; alkaline phosphatase (ALP) was also elevated in these mice on day 28 post-challenge. In contrast, other re-feeding groups attained similar body weights to PS mice within 4 days and had similar ALP at day 28. Serum leptin was higher in PD than PS mice and positively associated with food intake. As expected, worm survival was prolonged in mice fed the PD diet. However, egg production and worm burdens were similar in all re-feeding groups to the PS mice, indicating that protein re-feeding during either the primary or challenge infection rapidly restored normal parasite clearance.

Keywords

protein deficiencyprotein re-feedingnutritional statusmousenematodeHeligmosomoides bakeriresistanceinfection-induced weight lossanorexia
Type
Research Article
Information
Parasitology , Volume 134 , Issue 6 , June 2007 , pp. 899 - 909
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Acra, S. A., Bulus, N., Bogatcheva, G., Coffey, R. J. and Barnard, J. A. (1998). Increased intestinal epithelial proliferation in metallothioneine-transforming growth factor alpha transgenic mice. Regulatory Peptides 30, 105–112.CrossRefGoogle Scholar
Arnalich, F., Lopez, J., Codoceo, R., Jim Nez, M., Madero, R. and Montiel, C. (1999). Relationship of plasma leptin to plasma cytokines and human survival in sepsis and septic shock. Journal of Infectious Diseases 180, 908–911.CrossRefGoogle ScholarPubMed
Barbier, M., Cherbut, C., Aube, A. C., Blottiere, H. M. and Galmiche, J. P. (1998). Elevated plasma leptin concentrations in early stages of experimental intestinal inflammation in rats. Gut 43, 783–790.CrossRefGoogle ScholarPubMed
Behnke, J. M. and Robinson, M. (1985). Genetic control of immunity to Nematospiroides dubius: a 9-day anthelminthic abbreviated immunizing regime which separated weak and strong responder strains of mice. Parasite Immunology 7, 235–253.CrossRefGoogle ScholarPubMed
Bell, R. G., Hazell, L. A. and Price, P. (1976). Influence of dietary protein restriction on immune competence. II. Effect on lymphoid tissue. Clinical and Experimental Immunology 26, 314–326.Google ScholarPubMed
Boulay, M., Scott, M. E., Conly, S. L., Stevenson, M. M. and Koski, K. G. (1998). Dietary protein and zinc restrictions independently modify a Heligmosomoides polygyrus (Nematoda) infection in mice. Parasitology 116, 449–462.CrossRefGoogle ScholarPubMed
Cummins, A. G., Kenny, A. L., Duncombe, V. M., Bolin, T. D. and Davis, A. E. (1987 a). The effect of protein deficiency on systemic release of rat mucosal mast cell protease II during Nippostrongylus brasiliensis infection and following systemic anaphylaxis. Immunology and Cell Biology 65, 357–363.CrossRefGoogle ScholarPubMed
Cummins, A. G., Duncombe, V. M., Bolin, T. D., Davis, A. E. and Yong, J. (1987 b). The response of the small intestine of protein-deficient rats to infection with Nippostrongylus brasiliensis. International Journal for Parasitology 17, 1445–1450.CrossRefGoogle ScholarPubMed
Cywinska, A., Czuminska, K. and Schollenberger, A. (2004). Granulomatous inflammation during Heligmosomoides polygyrus primary infections in FVB mice. Journal of Helminthology 78, 17–24.CrossRefGoogle ScholarPubMed
Darmon, N. (1993). Oxidative stress may contribute to the intestinal dysfunction of weanling rats fed a low protein diet. Journal of Nutrition 123, 1068–1075.Google Scholar
Deitch, E. A., Xu, D. Z., Qi, L., Specian, R. D. and Berg, R. D. (1992). Protein malnutrition alone and in combination with endotoxin impairs systemic and gut-associated immunity. Journal of Parenteral and Enteral Nutrition 16, 25–31.CrossRefGoogle ScholarPubMed
Doherty, J. F., Golden, M. H., Remick, D. G. and Griffin, G. E. (1994). Production of interleukin-6 and tumour necrosis factor-alpha in vitro is reduced in whole blood of severely malnourished children. Clinical Science (London) 86, 347–351.CrossRefGoogle ScholarPubMed
Ey, P. L. (1988). Heligmosomiodes polygyrus: retarded development and stunting of larvae by antibodies specific for excretory/secretory antigens. Experimental Parasitology 65, 232–243.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Morris, S. C., Orekhova, T., Mori, M., Donaldson, D., Reiner, S. L., Reilly, N. L., Schopf, L. and Urban, J. (2000). Stat6 regulation of in vivo IL-4 responses. Journal of Immunology 164, 2303–2310.CrossRefGoogle ScholarPubMed
Garcia, S., Disanto, J. and Stockinger, B. (1999). Following the development of a CD4 T cell response in vivo: from activation to memory formation. Immunity 11, 163–171.CrossRefGoogle ScholarPubMed
Gause, W. C., Urban, J. and Stadecker, M. J. (2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269–277.Google ScholarPubMed
Ha, C. L. and Woodward, B. (1997). Reduction in the quantity of the polymeric immunoglobulin receptor is sufficient to account for the low concentration of intestinal secretory immunoglobulin A in a weanling mouse model of wasting protein-energy malnutrition. Journal of Nutrition 127, 427–435.CrossRefGoogle Scholar
Haluzik, M., Kabrt, J., Nedvidkova, J., Svobodova, J., Kotrlikova, E. and Papezova, H. (1999). Relationship of serum leptin levels and selected nutritional parameters in patients with protein-caloric malnutrition. Nutrition 15, 829–833.CrossRefGoogle ScholarPubMed
Hong, S. T., Park, K. H., Seo, M., Choi, B. I., Chai, J. Y. and Lee, S. H. (1994). Correlation of sonographic findings with histopathological changes of the bile ducts in rabbits infected with Clonorchis sinensis. The Korean Journal of Parasitology 32, 223–230.CrossRefGoogle ScholarPubMed
Ikeda, S., Saito, H., Kazuhiko, F., Inoue, T., Han, I., Furukawa, S., Matsuda, T. and Hidemura, A. (2001). Dietary restriction impairs neutrophil exudation by reducing CD11b/CD18 expression and chemokine production. Archives of Surgery 136, 297–304.CrossRefGoogle ScholarPubMed
Ing, R., Su, Z., Scott, M. E. and Koski, K. G. (2000). Suppressed T helper 2 immunity and prolonged survival of a nematode parasite in protein malnourished mice. Proceedings of the National Academy of Sciences, USA 97, 7078–7083.Google ScholarPubMed
Ingram, K. G., Crouch, D. A., Douez, D. L., Croy, B. A. and Woodward, B. (1995). Effects of triiodothyronine supplements on splenic natural killer cells in malnourished weanling mice. International Journal of Immunopharmacology 17, 21–32.CrossRefGoogle ScholarPubMed
Kamal, M., Dehlawi, M. S., Rosa Brunet, L. and Wakelin, D. (2002). Paneth and intermediate cell hyperplasia in mice by helminth infections. Parasitology 125, 275–281.CrossRefGoogle ScholarPubMed
Koski, K. G. and Scott, M. E. (2001). Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition 21, 297–321.CrossRefGoogle ScholarPubMed
Kristan, D. M. and Hammond, K. A. (2000). Combined effects of cold exposure and sub-lethal intestinal parasites on host morphology and physiology. Journal of Experimental Biology 203, 3495–3504.CrossRefGoogle ScholarPubMed
Li, M., Specian, R. D., Berg, R. D. and Deitch, E. A. (1989). Effects of protein malnutrition and endotoxin on the intestinal mucosal barrier to the translocation of indigenous flora in mice. Journal of Parenteral and Enteral Nutrition 13, 572–578.Google Scholar
Madden, K. B., Whitman, L., Sullivan, C., Gause, W. C., Urban, J., Katona, I. M., Finkelman, F. D. and Shea-Donohue, T. (2002). Role of STAT6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. Journal of Immunology 169, 4417–4422.CrossRefGoogle ScholarPubMed
Madi, K., Jervis, H. R., Anderson, P. R. and Zimmerman, M. R. (1970). A protein-deficient diet. Effect on the liver, pancreas, stomach, and small intestine of the rat. Archives of Pathology 89, 38–52.Google ScholarPubMed
Mansour, M. M., Farid, Z., Bassily, S., Salah, L. H. and Watten, R. H. (1982). Serum enzyme tests in hepatosplenic schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 109–111.CrossRefGoogle ScholarPubMed
Matarese, G., Carrieri, P. B., La Cava, A., Perna, F., Sanna, V., De Rosa, V., Aufiero, D., Fontana, S. and Zappacosta, S. (2005). Leptin increase in multiple sclerosis associates with reduced number of CD4(+)CD25+ regulatory T cells. Proceedings of the National Academy of Sciences, USA 102, 5150–5155.CrossRefGoogle ScholarPubMed
McDermott, M. R., Mark, D. A., Befus, A. D., Baliga, B. S. and Suskind, R. M. (1982). Impaired intestinal localization of mesenteric lymphoblasts associated with vitamin A deficiency and protein-calorie malnutrition. Immunology 45, 1–5.Google ScholarPubMed
Menaker, L. and Navia, J. M. (1973). Appetite regulation in the rat under various physiological conditions: the role of dietary protein and calories. Journal of Nutrition 103, 347–352.CrossRefGoogle ScholarPubMed
Mercer, L. P., Kelley, D. S., Humphries, L. L. and Dunn, J. D. (1994). Manipulation of central nervous system histamine or histaminergic receptors (H1) affects food intake in rats. Journal of Nutrition 124, 1029–1036.CrossRefGoogle ScholarPubMed
Mulivor, R. A., Boccelli, D. and Harris, H. (1985). Quantitative analysis of alkaline phosphatases in serum and amniotic fluid: comparison of biochemical and immunologic assays. The Journal of Laboratory and Clinical Medicine 105, 342–348.Google ScholarPubMed
Najera, O., Gonzalez, C., Toledo, G., Lopez, L., Cortes, E., Betancourt, M. and Ortiz, R. (2001). CD45RA and CD45RO isoforms in infected malnourished and infected well-nourished children. Clinical and Experimental Immunology 126, 461–465.CrossRefGoogle ScholarPubMed
NRC (1995). Nutrient Requirements of Laboratory Animals, 4th Edn. National Research Council, National Academy of Sciences, Washington, D.C.Google Scholar
Oarada, M., Nikawa, T. and Kurita, N. (2002). Effect of timing of food deprivation on host resistance to fungal infection in mice. British Journal of Nutrition 88, 151–158.CrossRefGoogle ScholarPubMed
Palacio, A. C., Perez-Bravo, F., Santos, J. L., Schlesinger, L. and Monckeberg, F. (2002). Leptin levels and IGF-binding proteins in malnourished children: effect of weight gain. Nutrition 18, 17–19.CrossRefGoogle ScholarPubMed
Pond, W. G., Ellis, K. J. and Schoknecht, P. (1992). Response of blood serum constituents to production of and recovery from a kwashiorkor-like syndrome in the young pig. Proceedings of the Society for Experimental Biology and Medicine 200, 555–561.CrossRefGoogle ScholarPubMed
Qu, Z., Ling, P. R., Tahan, S. R., Sierra, P., Onderdonk, A. B. and Bistrian, B. R. (1996). Protein and lipid refeeding changes protein metabolism and colonic but not small intestinal morphology in protein-depleted rats. Journal of Nutrition 126, 906–912.CrossRefGoogle Scholar
Rana, S., Gupta, D., Malik, A., Katyal, R. and Mehta, S. K. (1995). Mild-to-moderate malnutrition and small intestine of young rhesus monkeys. Nutrition 11, 292–295.Google ScholarPubMed
Rana, S., Gupta, D., Katyal, R. and Singh, K. (2003). Effect of malnutrition on the digestive enzymes of the upper gastrointestinal tract of young rhesus monkeys. Tropical Gastroenterology 24, 22–24.Google ScholarPubMed
Roberts, H. C., Hardie, L. J., Chappell, L. H. and Mercer, J. G. (1999). Parasite-induced anorexia: leptin, insulin and corticosterone responses to infection with the nematode, Nippostrongylus brasiliensis. Parasitology 118, 117–123.CrossRefGoogle ScholarPubMed
Rodriguez, P. (1996). Intestinal paracellular permeability during malnutrition in guinea pigs: effect of high dietary zinc. Gut 39, 416–422.CrossRefGoogle ScholarPubMed
Rogers, P. R., Dubey, C. and Swain, S. L. (2000). Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. Journal of Immunology 164, 2338–2346.CrossRefGoogle ScholarPubMed
Schwartz, R. (1956). Alkaline phosphatase activity of the serum in kwashiorkor. Journal of Clinical Pathology 9, 333–340.CrossRefGoogle ScholarPubMed
Scott, M. E. (1988). Predisposition of mice to Heligmosomoides polygyrus and Aspiculuris tetraptera (Nematoda). Parasitology 97, 101–114.CrossRefGoogle ScholarPubMed
Scrimshaw, N. S. and San Giovanni, J. P. (1997). Synergism of nutrition, infection and immunity: an overview. American Journal of Clinical Nutrition 66 (Suppl.), 464–477.CrossRefGoogle ScholarPubMed
Shea-Donohue, T., Sullivan, C., Finkelman, F. D., Madden, K. B., Morris, S. C., Goldhill, J., Pineiro-Carrero, V. and Urban, J. (2001). The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. Journal of Immunology 167, 2234–2239.CrossRefGoogle ScholarPubMed
Shi, H. N., Scott, M. E., Stevenson, M. M. and Koski, K. G. (1994). Zinc deficiency impairs T cell function in mice with primary infection of Heligmosomoides polygyrus (Nematoda). Parasite Immunology 16, 339–350.CrossRefGoogle ScholarPubMed
Sidhu, P., Garg, M. L., Morgenstern, P., Vogt, J., Butz, T. and Dhawan, D. K. (2005). Ineffectiveness of nickel in augmenting the hepatotoxicity in protein deficient rats. Nutrición Hospitalaria 20, 378–385.Google ScholarPubMed
Slater, A. F. G. and Keymer, A. E. (1986). Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society of London, B 229, 69–83.Google ScholarPubMed
Slater, A. F. G. and Keymer, A. E. (1988). The influence of protein deficiency on immunity to Heligmosomoides polygyrus (Nematoda) in mice. Parasite Immunology 10, 507–522.CrossRefGoogle ScholarPubMed
Soliman, A. T., Elzalabany, M. M., Salama, M. and Ansari, B. M. (2000). Serum leptin concentrations during severe protein-energy malnutrition: correlation with growth parameters and endocrine function. Metabolism 49, 819–825.CrossRefGoogle ScholarPubMed
Stankiewicz, M., Cabaj, W., Pernthaner, A., Jonas, W. and Rabel, B. (1996). Drug-abbreviated infections and development of immunity against Trichostrongylus colubriformis in sheep. International Journal for Parasitology 26, 97–103.CrossRefGoogle ScholarPubMed
Stapleton, P. P., Barden, C. B., McCarter, M. D., Mackrell, P. J., Freeman, T. A., Naama, H. A. and Daly, J. M. (2003). Serum leptin levels in acute protein deprivation. Journal of Parenteral and Enteral Nutrition 27, 132–136.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. and Mettrick, D. F. (1984). Heligmosomoides polygyrus (syn. Nematospiroides dubius) (Nematoda): distribution and net fluxes of glucose, H2O, Na+, K+, and Cl− in the mouse small intestine. Canadian Journal of Zoology 62, 37–40.CrossRefGoogle Scholar
Swick, R. W. and Gribskov, C. L. (1983). The effect of dietary protein levels on diet-induced thermogenesis in the rat. Journal of Nutrition 113, 2289–2294.CrossRefGoogle ScholarPubMed
Syme, G. (1982). The effect of protein-deficient isoenergetic diets on the growth of rat jejunal mucosa. British Journal of Nutrition 48, 25–36.CrossRefGoogle ScholarPubMed
Urban, J., Katona, I. M. and Finkelman, F. D. (1991 a). Heligmosomoides polygyrus: CD4+ but not CD8+ T cells regulate the IgE response and protective immunity in mice. Experimental Parasitology 73, 500–511.CrossRefGoogle Scholar
Urban, J., Katona, I. M., Paul, W. E. and Finkelman, F. D. (1991 b). Interleukin 4 is important in protective immunity to gastrointestinal nematode infection in mice. Proceedings of the National Academy of Sciences, USA 88, 5513–5517.CrossRefGoogle ScholarPubMed
Wells, P. D. (1962). Mast cell, eosinophil and histamine levels in Nippostrongylus brasiliensis infected rats. Experimental Parasitology 12, 82–101.CrossRefGoogle ScholarPubMed
Wells, P. D. (1963). Mucin secreting cells in rats infected with Nippostrongylus brasiliensis. Experimental Parasitology 14, 15–22.CrossRefGoogle ScholarPubMed
White, B. D., He, B., Dean, R. G. and Martin, R. J. (1994). Low protein diets increase neuropeptide Y gene expression in the basomedial hypothalamus of rats. Journal of Nutrition 124, 1152–1160.CrossRefGoogle ScholarPubMed
White, B. D., Porter, M. H. and Martin, R. J. (2000). Protein selection, food intake, and body composition in response to the amount of dietary protein. Physiology and Behavior 69, 383–389.CrossRefGoogle Scholar
Woodward, B. and 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, 1329–1335.CrossRefGoogle ScholarPubMed
Woodward, B., Hillyer, L. and Hunt, K. (1999). T cells with a quiescent phenotype (CD45RA+) are overabundant in the blood and involved lymphoid tissues in wasting protein and energy deficiencies. Immunology 96, 246–253.CrossRefGoogle Scholar
Zhao, A. P., McDermott, J., Urban, J., Gause, W., Madden, K. B., Yeung, K. A., Morris, S. C., Finkelman, F. D. and Shea-Donohue, T. (2003). Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. Journal of Immunology 171, 948–954.CrossRefGoogle ScholarPubMed