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Morphological changes of the rat intestinal lining in relation to body stores depletion during fasting and after refeeding

  • Gastrointestinal Function
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Abstract

Intestinal villus atrophy through prolonged fasting was studied according to two different metabolic phases reached by fasting animals and characterized by (a) the mobilization of fat stores as body fuel and (b) an increase in protein catabolism for energy expenditure. The mechanisms involved in the rapid jejunal restoration after refeeding were also determined. Mucosal structural atrophy during fasting proved to worsen over the two phases due mainly to the retraction of the lacteals in the lamina propria, as observed through the immunolocalization of aquaporin 1 in the endothelial cells of the lymphatic vessels and the detachment of the basal membrane of the epithelial lining at the tip of the villi. Microvilli surface area is preserved through fasting, and apical PepT1 expression increases during both metabolic fasting phases. Refeeding after both fasting phases induces an increase in FATP4 accompanied by a rapid lipid uptake by the enterocytes at the tip of the villi and a rapid extension of the lamina propria due to inflated lymphatic vessels. These mechanisms were more prevalent in animals refed after the phase III fast and could be considered as the major processes allowing complete morphological restoration of the jejunum within only 3 days after refeeding.

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References

  1. Aldewachi HS, Wright NA, Appleton DR, Watson AJ (1975) The effect of starvation and refeeding on cell population kinetics in the rat small bowel mucosa. J Anat 119:105–121

    PubMed  CAS  Google Scholar 

  2. Altmann GG (1972) Influence of starvation and refeeding on mucosal size and epithelial renewal in the rat small intestine. Am J Anat 133:391–400

    Article  PubMed  CAS  Google Scholar 

  3. Belkhou R, Cherel Y, Heitz A, Robin JP, Le Maho Y (1991) Energy contribution of protein and lipids during prolonged fasting in the rat. Nutr Res 11:365–374

    Article  CAS  Google Scholar 

  4. Blikslager AT, Roberts MC (1997) Mechanisms of intestinal mucosal repair. J Am Vet Med Assoc 211:1437–1441

    PubMed  CAS  Google Scholar 

  5. Boza JJ, Moennoz D, Vuichoud J, Jarret AR, Gaudard-de-Weck D, Fritsche R, Donnet A, Schiffrin EJ, Perruisseau G, Ballevre O (1999) Food deprivation and refeeding influence growth, nutrient retention and functional recovery of rats. J Nutr 129(7):1340–1346

    PubMed  CAS  Google Scholar 

  6. Brown HO, Levine ML, Lipkin M (1963) Inhibition of intestinal epithelial cell renewal and migration induced by starvation. Am J Physiol 205(5):868–872

    PubMed  CAS  Google Scholar 

  7. Buts JP, Vijverman V, Barudi C, De Keyser N, Maldague P, Dive C (1990) Refeeding after starvation in the rat: comparative effects of lipids, proteins and carbohydrates on jejunal and ileal mucosal adaptation. Eur J Clin Invest 20:441–452

    Article  PubMed  CAS  Google Scholar 

  8. Carey HV (1990) Seasonal changes in mucosal structure and function in ground squirrel intestine. Am J Physiol 259:R385–R392

    PubMed  CAS  Google Scholar 

  9. Challet E, Le Maho Y, Robin JP, Malan A, Cherel Y (1995) Involvement of corticosterone in the fasting-induced rise in protein utilization and locomotor activity. Pharmacol Biochem Behav 50:405–412

    Article  PubMed  CAS  Google Scholar 

  10. Cherel Y, Groscolas R (1999) Relationships between nutrient storage and nutrient utilization in long-term fasting birds and mammals. In: Adams NJ, Slotow RH (eds) Proceedings of the 22nd International Ornithology Congress, Durban, pp 17–34

  11. Cherel Y, Robin JP, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166

    CAS  Google Scholar 

  12. Clarke RM (1975) The time-course of changes in mucosal architecture and epithelial cell production and cell shedding in the small intestine of the rat fed after fasting. J Anat 120(2):321–327

    PubMed  CAS  Google Scholar 

  13. Cramp RL, Franklin CE (2003) Is re-feeding efficiency compromised by prolonged starvation during aestivation in the green striped burrowing frog, Cyclorana alboguttata? J Exp Zool 300:126–132

    Article  Google Scholar 

  14. Diaz JP, Guyot E, Vigier S, Connes R (1997) First events in lipid absorption during post-embryonic development of the anterior intestine in gilt-head sea bream. J Fish Biol 51(1):180–192

    Article  PubMed  CAS  Google Scholar 

  15. Dunel-Erb S, Chevalier C, Laurent P, Bach A, Decrock F, Le Maho Y (2001) Restoration of the jejunal mucosa in rats refed after prolonged fasting. Comp Biochem Physiol 129A:933–947

    CAS  Google Scholar 

  16. Elmes ME (1977) Apoptosis in the small intestine of zinc-deficient and fasted rats. J Pathol 123:219–223

    Article  PubMed  CAS  Google Scholar 

  17. Garcia Hernandez MP, Lozano MT, Elbal MT, Agulleiro B (2001) Development of the digestive tract of sea bass (Dicentrarchus labrax L). Light and electron microscopic studies. Anat Embryol (Berl) 204(1):39–57

    Article  CAS  Google Scholar 

  18. Goodlad RA, Plumb JA, Wright NA (1988) Epithelial cell proliferation and intestinal absorptive function during starvation and refeeding in the rat. Clin Sci (Lond) 74(3):301–306

    CAS  Google Scholar 

  19. Goodman MN, Larsen PR, Kaplan MN, Aoki TT, Young VR, Ruderman NB (1980) Starvation in the rat. II. Effect of age and obesity on protein sparing and fuel metabolism. Am J Physiol 239:E277–E286

    PubMed  CAS  Google Scholar 

  20. Groos S, Reale E, Hünefeld G, Luciano L (2003) Changes in epithelial cell turnover and extracellular matrix in human small intestine after TPN. J Surg Res 109(2):74–85

    Article  PubMed  CAS  Google Scholar 

  21. Groscolas R, Robin JP (2001) Long-term fasting and re-feeding in penguins. Comp Biochem Physiol 128A:645–655

    CAS  Google Scholar 

  22. Habold C, Chevalier C, Dunel-Erb S, Foltzer-Jourdainne C, Le Maho Y, Lignot JH (2004) Effects of fasting and refeeding on jejunal morphology and cellular activity in rats according to body stores depletion. Scand J Gastroenterol 39(6):531–539

    Article  PubMed  CAS  Google Scholar 

  23. Habold C, Foltzer-Jourdainne C, Le Maho Y, Lignot JH, Oudart H (2005) Intestinal gluconeogenesis and glucose transport according to body fuel availability in rats. J Physiol 566(Pt 2):575–586

    Article  PubMed  CAS  Google Scholar 

  24. Habold C, Foltzer-Jourdainne C, Le Maho Y, Lignot JH (2006) Intestinal apoptotic changes linked to metabolic status in fasted and refed rats. Pflugers Arch 451(6):749–759

    Article  PubMed  CAS  Google Scholar 

  25. Hopper AF, Wannemacher RW Jr, McGovern PA (1968) Cell population changes in the intestinal epithelium of the rat following starvation and protein-depletion. Proc Soc Exp Biol Med 128(3):695–698

    PubMed  CAS  Google Scholar 

  26. Ihara T, Tsujikawa T, Fujiyama Y, Ueyama H, Ohkubo I, Bamba T (2000) Enhancement of brush border membrane peptidase activity in rat jejunum induced by starvation. Pflugers Arch 440(1):75–83

    PubMed  CAS  Google Scholar 

  27. Iwakiri R, Gotoh Y, Noda T, Sugihara H, Fujimoto K, Fuseler J, Aw TY (2001) Programmed cell death in rat intestine: effect of feeding and fasting. Scand J Gastroenterol 36:39–47

    Article  PubMed  CAS  Google Scholar 

  28. Jin SY, Liu YL, Xu LN, Jiang Y, Wang Y, Yang BX, Yang H, Ma TH (2006) Cloning and characterization of porcine aquaporin 1 water channel expressed extensively in gastrointestinal system. World J Gastroenterol 12(7):1092–1097

    PubMed  CAS  Google Scholar 

  29. Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 61–84

    Google Scholar 

  30. Karasov WH, Pinshow B, Starck JM, Afik D (2004) Anatomical and histological changes in the alimentary tract of migrating blackcaps (Sylvia atricapilla): a comparison among fed, fasted, food-restricted, and refed birds. Physiol Biochem Zool 77(1):149–160

    Article  PubMed  Google Scholar 

  31. Koubi HE, Robin JP, Dewasmes G, Le Maho Y, Frutoso J, Minaire Y (1991) Fasting-induced rise in locomotor activity in rats coincides with increased protein utilization. Physiol Behav 50:337–343

    Article  PubMed  CAS  Google Scholar 

  32. Le Maho Y, Vu Van Kha H, Koubi H, Dewasmes G, Girard J, Ferre P, Cagnard M (1981) Body composition, energy expenditure, and plasma metabolites in long-term fasting geese. Am J Physiol 41:E342–E354

  33. Lignot JH, Helmstetter C, Secor SM (2005) Postprandial morphological response of the intestinal epithelium of the Burmese python (Python molurus). Comp Biochem Physiol A 141(3):280–291

    Article  CAS  Google Scholar 

  34. Noaillac-Depeyre J, Gas N (1974) Fat absorption by the enterocytes of the carp (Cyprinus carpio L.). Cell Tissue Res 155(3):353–365

    Article  PubMed  CAS  Google Scholar 

  35. Ogihara H, Suzuki T, Nagamachi Y, Inui K, Takata K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochem J 31(3):169–174

    Article  PubMed  CAS  Google Scholar 

  36. Rigaud D, Hassid J, Meulemans A, Poupard AT, Boulier A (2000) A paradoxical increase in resting energy expenditure in malnourished patients near death: the king penguin syndrome. Am J Clin Nutr 72:355–360

    PubMed  CAS  Google Scholar 

  37. Robin JP, Boucontet L, Chillet P, Groscolas R (1998) Behavioral changes in fasting emperor penguins: evidence for a “refeeding signal” linked to a metabolic shift. Am J Physiol 274:R746–R753

    PubMed  CAS  Google Scholar 

  38. Secor SM, Stein ED, Diamond J (1994) Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation. Am J Physiol 266:G695–G705

    Google Scholar 

  39. Secor SM, Lane JS, Whang EE, Ashley SW, Diamond J (2002) Luminal nutrient signals for intestinal adaptation in pythons. Am J Physiol 283(6):G1298–1309

    Google Scholar 

  40. Sire MF, Lutton C, Vernier JM (1981) New views on intestinal absorption of lipids in teleostean fishes: an ultrastructural and biochemical study in the rainbow trout. J Lipid Res 22(1):81–94

    PubMed  CAS  Google Scholar 

  41. Sohma M (1983) Ultrastructure of the absorptive cells in the small intestine of the rat during starvation. Anat Embryol (Berl) 168(3):331–339

    Article  CAS  Google Scholar 

  42. Stahl A, Hirsch DJ, Gimeno RE, Punreddy S, Ge P, Watson N, Patel S, Kotler M, Raimondi A, Tartaglia LA, Lodish HF (1999) Identification of the major intestinal fatty acid transport protein. Mol Cell 4(3):299–308

    Article  PubMed  CAS  Google Scholar 

  43. Starck JM, Beese K (2001) Structural flexibility of the intestine of Burmese python in response to feeding. J Exp Biol 204(Pt 2):325–335

    PubMed  CAS  Google Scholar 

  44. Starck JM, Beese K (2002) Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting. J Exp Biol 205(Pt 10):1377–1388

    PubMed  Google Scholar 

  45. Tarachai P, Yamauchi K (2000) Effects of luminal nutrient absorption, intraluminal physical stimulation, and intravenous parenteral alimentation on the recovery responses of duodenal villus morphology following feed withdrawal in chickens. Poult Sci 79(11):1578–1585

    PubMed  CAS  Google Scholar 

  46. Wang T, Hung CC, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251

    Article  PubMed  CAS  Google Scholar 

  47. Yamauchi K, Kamisoyama H, Isshiki Y (1996) Effects of fasting and refeeding on structures of the intestinal villi and epithelial cells in White Leghorn hens. Br Poult Sci 37(5):909–921

    PubMed  CAS  Google Scholar 

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Acknowledgments

We wish to thank C. Arbiol for her skillful technical assistance. The work was supported by the CNRS Life Science Department and the Scientific Committee of the Louis Pasteur University. We are also thankful to the Bettencourt-Schueller Foundation and the Nestlé Foundation for financial assistance to C.H. The experiments were carried out according to the Centre National de la Recherche Scientifique (CNRS) “Guide for Care and Use of Laboratory Animals” and the National Guidelines for Animal Experimentation (National Committee on Animal Experimentation, France).

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Correspondence to Jean-Hervé Lignot.

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Habold, C., Reichardt, F., Foltzer-Jourdainne, C. et al. Morphological changes of the rat intestinal lining in relation to body stores depletion during fasting and after refeeding. Pflugers Arch - Eur J Physiol 455, 323–332 (2007). https://doi.org/10.1007/s00424-007-0289-0

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