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Effects of three simultaneous demands on glucose transport, resting metabolism and morphology of laboratory mice

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Abstract

In nature, animals must successfully respond to many simultaneous demands from their environment in order to survive and reproduce. We examined physiological and morphological responses of mice given three demands: intestinal parasite infection with Heligmosomoides polygyrus followed by caloric restriction (70% of ad libitum food intake versus ad libitum for 10 days) and/or cold exposure (5°C vs. 23°C for 10 days). We found significant interactions between these demands as well as independent effects. Small intestine structure and function changed with demands in both independent and interactive ways. Body mass decreased during caloric restriction and this decrease was greater for cold-exposed than warm-exposed mice. In ad libitum fed mice, body mass did not change with either cold exposure or parasite infection but body composition (fat versus lean mass of whole body or organs) changed with both demands. Generally, organ masses decreased with caloric restriction (even after accounting for body mass effects) and increased with cold exposure and parasite infection whereas fat mass decreased with both caloric restriction and parasite infection. Mass adjusted resting metabolic rate (RMR) increased with cold exposure, decreased with caloric restriction but, unlike previous studies with laboratory mice, did not change with parasite infection. Our results demonstrate that the ability of mice to respond to a demand is influenced by other concurrent demands and that mice show phenotypic plasticity of morphological and physiological features ranging from the tissue level to the level of the whole organism when given three simultaneous demands.

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References

  • Au Yeung KJ, Smith A, Zhao A, Madden KB, Elfre J, Sullivan C, Levander O, Urban JF, Shea-Donohue T (2005) Impact of vitamin E or selenium deficiency on nematode-induced alterations in murine intestinal function. Exp Parasitol 109:201–208

    Article  PubMed  CAS  Google Scholar 

  • Bansemir AD, Sukhdeo MV (1996) Villus length influences habitat selection by Heligmosomoides polygyrus. Parasitol 113:311–316

    Google Scholar 

  • Bowman DD (1995) Georgis’ parasitology for veterinarians, 6th edn. W.B. Saunders Co., Philadelphia

    Google Scholar 

  • Berry RJ (1981) Town mouse, country mouse: adaptation and adaptability in Mus domesticus (M. musculus domesticus). Mamm Rev 11:91–136

    Google Scholar 

  • Berry RJ, Jakobson ME, Triggs GS (1973) Survival in wild-living mice. Mamm Rev 3:46–57

    Google Scholar 

  • Bronson FH, Heideman PD, Kerbeshian MC (1991). Lability of fat stores in peripubertal wild house mice. J Comp Physiol B 161:15–18

    Article  PubMed  CAS  Google Scholar 

  • Carlomagno MA, Riarte A, Moreno M, Segura EL (1987) Effects of caloric-restriction on the course of Trypanosoma cruzi infection. Nutr Res 7:1031–1040

    Article  Google Scholar 

  • Cheeseman CI (2002) Intestinal hexose absorption: transcellular or paracellular fluxes. J Physiol 544.2:336

    Article  CAS  Google Scholar 

  • Diamond JM, Karasov WH (1984) Effect of dietary carbohydrates on monosaccharide uptake by mouse small intestine in vitro. J Physiol Lond 349:419–440

    PubMed  CAS  Google Scholar 

  • Dobson C (1961) Certain aspects of the host-parasite relationship of Nematospiroides dubius (Baylis). I. Resistance of male and female mice to experimental infections. Parasitol 51:173–179

    Article  CAS  Google Scholar 

  • Dobson C, Owen ME (1978) Effect of host sex on passive immunity in mice infected with Nematospiroides dubius. Int J Parasitol 8:359–364

    Article  PubMed  CAS  Google Scholar 

  • Fakae BB, Harrison LJS, Sewell MMH (2000) The intensity and duration of primary Heligmosomoides polygyrus infection in TO mice modify acquired immunity to secondary challenge. J Helminthol 74:225–231

    PubMed  CAS  Google Scholar 

  • Ferraris RP (1997) Effect of aging and caloric restriction on intestinal sugar and amino acid transport. Front Biosci 2:e108–e115

    PubMed  CAS  Google Scholar 

  • Ferraris RP (2001) Dietary and developmental regulation of intestinal sugar transport. Biochem J 360:265–276

    Article  PubMed  CAS  Google Scholar 

  • Ferraris RP, Diamond J (1997) Regulation of intestinal sugar transport. Physiol Rev 77:257–302

    PubMed  CAS  Google Scholar 

  • Ferraris RP, Villenas SA, Hirayama BA, Diamond J (1992) Effect of diet on glucose transporter site density along the intestinal crypt-villus axis. Am J Physiol 262:G1060–G1068

    PubMed  CAS  Google Scholar 

  • Hall DM, Oberley TD, Moseley PM, Buettner GR, Oberley LW, Weindruch R, Kregel KC (2000) Caloric restriction improves thermal tolerance and reduces hyperthermia-induced cellular damage in old rats. FASEB J 14:78–86

    PubMed  CAS  Google Scholar 

  • Hammond KA, Diamond J (1992) An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiol Zool 65:952–977

    Google Scholar 

  • Hammond KA, Konarzewski M, Torres RM, Diamond J (1994) Metabolic ceilings under a combination of peak energy demands. Physiol Zool 67:1479–1506

    Google Scholar 

  • Hammond KA, Kristan DM (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Zool 73:547–556

    Article  CAS  Google Scholar 

  • Helliwell PA, Kellett GL (2002) The active and passive components of glucose absorption in rat jejunum under low and high perfusion stress. J Physiol 544.2:579–589

    Article  CAS  Google Scholar 

  • Karasov WH, Diamond JM (1983) A simple method for measuring intestinal nutrient uptake in vivo. J Comp Physiol 152:105–116

    CAS  Google Scholar 

  • Konarzewski M, Diamond J (1994) Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiol Zool 67:1186–1212

    Google Scholar 

  • Krackow S (1989) Effect of food restriction on reproduction and lactation in house mice mated post partum. J Reprod Fert 86:341–347

    Article  CAS  Google Scholar 

  • Kristan DM (2002a) Effects of intestinal nematodes during lactation: consequences for host morphology, physiology and offspring mass. J Exp Biol 205:3955–3965

    PubMed  Google Scholar 

  • Kristan DM (2002b) Maternal and direct effects of the intestinal nematode Heligmosomoides polygyrus on offspring growth and susceptibility to infection. J Exp Biol 205:3967–3977

    PubMed  Google Scholar 

  • Kristan DM (2004) Intestinal nematode infection affects host life history and offspring susceptibility to parasitism. J Anim Ecol 73:227–238

    Article  Google Scholar 

  • Kristan DM, Hammond KA (2000) Combined effects of cold exposure and sub-lethal intestinal parasites on host morphology and physiology. J Exp Biol 203:3495–3504

    PubMed  CAS  Google Scholar 

  • Kristan DM, Hammond KA (2001) Parasite infection and caloric restriction induce physiological and morphological plasticity. Am J Physiol 281:R502–R510

    CAS  Google Scholar 

  • Kristan DM, Hammond KA (2004) Morphological plasticity varies with duration of infection: evidence from lactating and virgin wild-derived house mice (Mus musculus) infected with an intestinal parasite (Heligmosomoides polygyrus: Nematoda). J Exp Biol 207:2351–2360

    Article  PubMed  Google Scholar 

  • Lam MM, O’Connor TP, Diamond J (2002) Loads, capacities and safety factors of maltase and the glucose transporter SGLT1 in mouse intestinal brush border. J Physiol 542.2:493–500

    Article  CAS  Google Scholar 

  • Monroy FG, Enriquez FJ (1992) Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitol Today 8:49–54

    Article  PubMed  CAS  Google Scholar 

  • Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138

    Article  Google Scholar 

  • Severinsen T, Munch IC (1999) Body core temperature during food restriction in rats. Acta Physiol Scand 165:299–305

    Article  PubMed  CAS  Google Scholar 

  • Shea-Donohue T, Sullivan C, Finkelman FD, Madden KB, Morris SC, Goldhill J, Piñeiro-Carrero V, Urban JF Jr (2001) The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J Immunol 167:2234–2239

    PubMed  CAS  Google Scholar 

  • Withers PC (1977) Measurement of \( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{2} ,\;\ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{CO}}_{2} , \) and evaporative water loss with a flow-through mask. J Appl Physiol Respirat Environ Exercise Physiol 42:120–123

  • Zarling EJ, Mobarhan S (1987) Effect of restricting a balanced diet on rat intestinal disaccharidase activity and intestinal architecture. J Lab Clin Med 109:556–559

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Allejandra Herrara for assistance with glucose uptake experiments. The original stock of Heligmosomoides polygyrus was graciously provided by the laboratory of Dr. Michael Sukhdeo. The manuscript benefited from helpful comments of two anonymous reviewers. This project was supported by a Newell Award, Dept. Biology, and a Dissertation Research Grant, Graduate Division, UCR to D.M.K. and by NSF 111604 to K.A.H.

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  1. Deborah M. Kristan

    Present address: Department of Biological Sciences, California State University, 333 S Twin Oaks Valley Rd., San Marcos, CA, 92096, USA

Authors and Affiliations

  1. Department of Biology, University of California, Riverside, CA, 92521, USA

    Deborah M. Kristan & Kimberly A. Hammond

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  1. Deborah M. Kristan
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  2. Kimberly A. Hammond
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Correspondence to Deborah M. Kristan.

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Communicated by H. Carey

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Kristan, D.M., Hammond, K.A. Effects of three simultaneous demands on glucose transport, resting metabolism and morphology of laboratory mice. J Comp Physiol B 176, 139–151 (2006). https://doi.org/10.1007/s00360-005-0036-9

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  • DOI: https://doi.org/10.1007/s00360-005-0036-9

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