Advertisement

AGE

, Volume 17, Issue 1, pp 13–21 | Cite as

Effect of chronic caloric restriction: Physiological and behavioral response to alternate day feeding in old female B6C3F1 mice

  • Peter H. Duffy
  • Ritchie J. Feuers
  • James L. Pipkin
  • Ronald W. Hart
Article

Abstract

Physiological and behavioral performance was monitored in old (24 month) female B6C3F1 hybrid mice that were fed either a caloric restricted (CR) diet (60% of ad libitum) or fed ad libitum (AL). The CR group was fed (CR1) and then fasted (CR2) on alternate days starting at 12–14 weeks of age. The main objective of the study was to determine if the effects of intermittent feeding were different from those for daily CR feeding. The average daily body weight, body temperature, oxygen consumption per gram of lean body mass (LBM), and respiratory quotient were higher on the feed day (CR1) than on the fast day (CR2), whereas the average daily body weight, temperature, activity, and oxygen metabolism per gram of LBM were lower on CR1 than in AL. The daily range in temperature, oxygen metabolism per gram of LBM, and RQ was greater on CR1 and CR2 than in AL; the exception was RQ on CR1. No food was eaten on CR2, and water consumption was reduced by 60% compared to CR1. Average food consumption per meal, and average time eating and drinking per meal was greater in CR mice than in AL mice. The results of this study indicated that mice responded to alternate day CR by changing average daily metabolic output per gram of LBM in direct response to food consumption, whereas when CR mice were fed daily, no change was seen in average metabolism per gram of LBM. The fact that a significant reduction in energy output and temperature occurred in CR mice when metabolic pathways shifted from carbohydrate to fat metabolism may indicate that decreased glucose utilization may have triggered these CR-induced effects.

Keywords

Caloric Restriction Lean Body Mass Respiratory Quotient Oxygen Metabolism Time Eating 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Walford, R.L., Liu, R.K., Gerbase-Delima, M., Mathies, M., and Smith, G.S.: Long term dietary restriction in immune function in mice: response to sheet red blood cells and to mitogenic agents. Mech. Ageing. Dev., 2: 447–454, 1974.CrossRefGoogle Scholar
  2. 2.
    Maeda, H., Gleiser, C.A., Masoro, E.J., Murata, I., McMahan, C.A., and Yu, B.P.: Nutritional influences on aging of Fischer 344 rats. II. Pathology. J. Gerontol., 40: 671–688, 1985.PubMedGoogle Scholar
  3. 3.
    Sarkar, N.H., Fernandes, G., Telang, N.T., Kourides, I.A., and Good, R.: A low-calorie diet prevents the development of mammary tumors in C3H mice and reduces circulating prolactin level, murine mammary tumor virus expression, and proliferation of mammary alveolar cells. Proc. Natl. Acad. Sci. U.S.A., 79: 7758–7762, 1982.PubMedGoogle Scholar
  4. 4.
    Ruggeri, B.A., Klurfeld, D.M., and Kritchevsky, D.: Biochemical alterations in 7,12-dimethylbenz[a]-anthracene-induced mammary tumors from rats subjected to caloric restriction. Biochem. Biophys. Acta, 929: 239–246, 1987.PubMedCrossRefGoogle Scholar
  5. 5.
    Kritchevsky, D., Weber, M.M., and Klurfeld, D.M.: Dietary fat versus caloric content in initiation and promotion of 7,12-dimethylbenz(a)-anthracene-induced mammary tumorigenesis in rats. Cancer Res., 44: 3174–3177, 1984.PubMedGoogle Scholar
  6. 6.
    McCay, C.M., Crowell, M.F., and Maynard, L.A.: The effect of retarded growth upon the length of life span and upon the ultimate body size. J. Nutr., 10: 67–79, 1935.Google Scholar
  7. 7.
    Masoro, E.J.: Mini-review: food restriction in rodents: an evaluation of its role in the study of aging. J. Gerontol., 43: B.59–64, 1988.Google Scholar
  8. 8.
    Ross, M.H.: Length of life and caloric intake. Am. J. Clin. Nutr., 25: 834–838, 1972.PubMedGoogle Scholar
  9. 9.
    Weindruch, R. and Walford R.L.: Dietary restriction in mice beginning at one year of age: Effect on life span and spontaneous cancer incidence. Science, 215: 1415–1418, 1982.PubMedGoogle Scholar
  10. 10.
    Beauchene, R.E., Bales, C.W., Tucker, S.M., and Mason, R.L.: The effect of feed restriction on body composition and longevity. Physiologist, 22: 8a, 1979.Google Scholar
  11. 11.
    Goodrick, C.L., Ingram, D.K., Reynolds, M.A., Freeman, J.R., and Cider, N.L.: Effect of intermittent feeding upon growth and life span in rats. Gerontology, 28: 293, 1982.CrossRefGoogle Scholar
  12. 12.
    Goodrick, C.L., Ingram, D.K., Reynolds, M.A., Freeman, J.R., and Cider, N.L.: Effects of intermittent feeding upon growth, activity, and life span in rats allowed voluntary exercise. Exp. Aging Res., 9: 203, 1983.PubMedGoogle Scholar
  13. 13.
    Talan, M.I. and Ingram, D.K.: Effect of intermittent feeding on thermoregulatory abilities of young and aged C57BL/6J mice. Arch. Gerontol. Geriatrics 4: 251, 1985.CrossRefGoogle Scholar
  14. 14.
    Dulloo, A.G. and Girardier, L.: Adaptive changes in energy expenditure during refeeding following low-calorie intake: evidence for a specific metabolic component favoring fat storage. Am. J. Clin. Nutr., 52: 415–420, 1990.PubMedGoogle Scholar
  15. 15.
    Yang, M.U., Presta, E., and Bjorntorp, P.: Refeeding after fasting in rats: effects of duration of starvation and refeeding on food efficiency in diet-induced obesity. Am. J. Clin. Nutr., 51: 970–978, 1990.PubMedGoogle Scholar
  16. 16.
    Duffy, P.H., Feuers, R.J., Leakey, J.A., Nakamura, K.D., Turturro, A., and Hart, R.W.: Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat. Mech. Ageing Dev., 48: 117–133, 1989.PubMedCrossRefGoogle Scholar
  17. 17.
    Duffy, P.H., Feuers, R.J., and Hart, R.W.: Effect of chronic caloric restriction on the circadian regulation of physiological and behavioral variables in old male B6C3F1 mice. Chronobiol. Int., 7: 291–303. 1990.PubMedGoogle Scholar
  18. 18.
    Duffy, P.H., Feuers, R.J., Leakey, J.A., and Hart, R.W.: Chronic caloric restriction in old female mice: changes in the circadian rhythms of physiological and behavioral variables, Chapter 24, in Biological effects of dietary Restriction, edited by Fishbein, L., New York, Springer-Verlaq, 1991, pp. 245–263.Google Scholar
  19. 19.
    Scott, D.F. and Potter, V.R.: Metabolic oscillation in lipid metabolism in rats on controlled feeding schedules. Fed. Proc., 29: 1553–1559, 1970.PubMedGoogle Scholar
  20. 20.
    Leveille, G.A.: A dipose tissue metabolism: Influence of periodicity of eating and diet composition. Fed. Proc., 29: 1294–1301, 1970.PubMedGoogle Scholar
  21. 21.
    Feuers, R.J., Duffy, P.H., Leakey, J.A., Turturro, A., Mittelstaedt, R.A., and Hart, R.W.: Effect of chronic caloric restriction on hepatic enzymes of intermediary metabolism in the male Fischer 344 rat. Mech. Ageing Dev., 48: 179–189, 1989.PubMedCrossRefGoogle Scholar
  22. 22.
    Leakey, J.E.A., Cunny, H.C., Bazare, J., Webb, P.J., Duffy, P.H., and Hart, R.W.: Effects of aging and caloric restriction on hepatic drug metabolizing enzymes in the Fischer 344 rat. I. The cytochrome p-450 dependent monooxygenase system. Mech. Ageing Dev., 48: 145–155, 1989.PubMedCrossRefGoogle Scholar
  23. 23.
    McCarter, R.J. and McGee, J.R.: Transient reduction of metabolic rate by food restriction. Am. J. Physiol., 257: E175–E179, 1989.PubMedGoogle Scholar
  24. 24.
    McCarter, R., Masoro, E.J., and Yu, B.P.: Does food restriction retard aging by reducing the metabolic rate? Am. J. Physiol., 248: E488–E490, 1985.PubMedGoogle Scholar
  25. 25.
    Gonzales-Pacheco, D.M., Buss, W.C., Koehler, K.M., Woodside, W.F., and Alpert, S.S.: Energy restriction reduces metabolic rate in adult male Fischer-344 rats. J. Nutr., 123: 90–97, 1993.PubMedGoogle Scholar
  26. 26.
    Lesser, G.T., Deutsd, S., and Markofsky, J.: The rat fat-free baby in middle life: continuing growth and histochemical changes., J. Gerontol., 25: 108–114, 1970.PubMedGoogle Scholar
  27. 27.
    Halberg, F., Johnson, E.A., Nelson, W., and Sothern, R.B.: Autorhythmometry procedures for physiological self-measurements and their analysis., Physio. Teacher, 1: 1–11, 1972.Google Scholar
  28. 28.
    Lyman, C.P.: Entering hibernation, in Hibernation and torpor in mammals and birds, edited by Lyman, C., Willis, J., Malan, A., and Wang, L., San Diego, Academic Press, 1982, pp 37–53.Google Scholar
  29. 29.
    Willis, J.S.: Is there cold adaptation of metabolism in hibernators?, in Hibernation and torpor in mammals and birds, edited by Lyman, C., Willis, J., Malan, A., and Wang, L., San Diego, Academic Press, 1982, pp 140–171.Google Scholar
  30. 30.
    Wang, L.C.: Hibernation and the endocrines, in Hibernation and torpor in mammals and birds, edited by Lyman, C., Willis, J., Malan, A., and Wang, L., San Diego, Academic Press, 1982, pp 206–236.Google Scholar
  31. 31.
    Williams, R.S. and Benjamin, I.J.: Stress proteins and cardiovascular disease., Mol. Biol. Med., 8: 197–206, 1991.PubMedGoogle Scholar
  32. 32.
    Morimoto, R.I., Tissieres, A., Georgopoulos, C., and Huey, R.B.: Stress proteins in biology and medicine, New York, Cold Springs Harbor Laboratory Press, 1990.Google Scholar
  33. 33.
    Hart, R.W., Leakey, J.E.A., Allaben, W.T., Chou, M., Duffy, P.H., Feuers, R.J., and Turturro, A.: Nutrition and diet in regenerative processes. Int. J. Toxicol., Occup. and Environ. Hlth., 1(2): 26–32, 1992.Google Scholar
  34. 34.
    Sabatino, F., Masoro, E.J., McMahan, C.A., and Kuhn, R.W.: Assessment of the role of the glucocorticoid system in the aging processes and in the action of food restriction. J. Gerontol., 46: B171–179, 1991.PubMedGoogle Scholar
  35. 35.
    Falk, J.L.: Production of polydipsia in normal rats by an intermittent food schedule. Science, 133: 195–196, 1961.PubMedGoogle Scholar
  36. 36.
    Falk, J.L.: Conditions producing psychogenic polydipsia in animals. In: Ann. NY. Acad. Sci., 157: 569–593, 1969.PubMedGoogle Scholar
  37. 37.
    Robbins, T.W., Roberts, D.C.S., and Koob, G.F.: Effects of d-amphetamine and apomorphine upon operant behavior and schedule-induced licking in rats with 6-hydroxydopamine-induced lesions of the nucleus accumbens. J. Pharmacol. Exp. Ther., 224: 662–673, 1983.PubMedGoogle Scholar
  38. 38.
    Canon, H. and Lippa, A. Effects of clozapine, chlorpromazine and diazepam upon adjunctive and schedule controlled behaviors. Pharmacol. Biochem. Behav., 6: 581–587, 1977.PubMedCrossRefGoogle Scholar
  39. 39.
    Levine, R. and Levine, S.: Role of the pituitary-adrenal hormones in the acquisition of schedule-induced polydipsid. Behav. Neurosci., 103(3): 621–637, 1989.PubMedCrossRefGoogle Scholar
  40. 40.
    Hennessy, J. and Levine, S.: Stress, arousal and the pituitary-adrenal system: a psychoendocrine model, edited by Sprague, J., and Epstein, A., New York, Academic Press, pp 133–179, 1979.Google Scholar
  41. 41.
    Hiroshige, T.: Hormonal rhythm and feeding behavior. J. Auton. Nerv. Syst., 10(3–4): 337–346, 1984.PubMedCrossRefGoogle Scholar
  42. 42.
    Brett, L.P. and Levine, S.: The pituitary-adrenal response to “minimized” schedule-induced drinking. Physiol. Behav., 26: 153–158, 1981.PubMedCrossRefGoogle Scholar
  43. 43.
    Jazi, A., Dantzer, R., and LeMoal, M.: Schedule-induced polydipsid experience decreases locomotor response to amphetamines. Brain Res., 445: 211–215, 1988.CrossRefGoogle Scholar
  44. 44.
    Winn, P., Clark, J.M., Clark, A.J., and Parker, G.C.: NMDA lesions of lateral hypothalamus enhance the acquisition of schedule-induced polydipsid. Physiol. Behav., 52(6): 1069–1075, 1992.PubMedCrossRefGoogle Scholar
  45. 45.
    Beckman, A.L.: Hypothalamic and midbrain function during hibernation, in Current studies of hypothalamid function, edited by Veale, W.L. and Lederis, K., Basel, Karger, 1978, pp 29–43.Google Scholar
  46. 46.
    Nakamura, K.D., Duffy, P.H., Turturro, A., and Hart, R.W.: The effect of dietary restriction on MYC protooncogene expression in mice: A preliminary study., Mech. Ageing Dev., 48: 199–205, 1989.PubMedCrossRefGoogle Scholar
  47. 47.
    Lipman, J.M., Turturro, A., and Hart, R.W.: The influence of dietary restriction on DNA repair in rodents: A preliminary study., Mech. Ageing Dev., 48: 135–143, 1989.PubMedCrossRefGoogle Scholar
  48. 48.
    Lindahl, T. and Nyberg, B.: Rate of depurination of native deoxyribonucleic acid., Biochem., 11: 3610–3618, 1972.CrossRefGoogle Scholar
  49. 49.
    Joplin, K.H., Yocum, G.D., and Denlinger, D.L.: Cold shock elicits expression of heat shock proteins in the fresh fly, Sacraphaga crassipalpij. J. Insect Physiol., 36: 825–834, 1990.CrossRefGoogle Scholar
  50. 50.
    Worden, S.K., Kapor, R.P., and Lee, A.S.: The organization of the rat GRP78 gene and A23187-induced expression of fusion gene products targeted intracellularly., Expt. Cell Res., 178: 84–92, 1988.CrossRefGoogle Scholar
  51. 51.
    Chiag, H.L., Terlecky, S.R., Plant, C.P., and Dice, J.F.: A role for a 70-kilodalton heat shock protein in liposomal degradation of intracellular proteins., Science, 246: 382–385, 1989.Google Scholar
  52. 52.
    Riaborool, K.T., Mizzen, L.A., and Welch, W.J.: Heat shock is lethal to fibroblasts microinjected with antibodies against HSP70., Science, 242: 433–436, 1988.Google Scholar
  53. 53.
    Sanchez, Y. and Lindquist, S.L.: HSP104 required for induced thermotolerance., Science, 248: 1112–1115, 1990.PubMedGoogle Scholar
  54. 54.
    Picard, P., Khinsheed, B., Garabedian, M.J., Tortin, M.G., Lindquist, S., and Yamamoto, K.R.: Reduced levels of HSP90 compromise steroid receptor action in vivo, Nature (London), 348: 166–168, 1990.CrossRefGoogle Scholar
  55. 55.
    Boulos, Z., Rosenwasser, A.M., and Terman, M.: Feeding schedules and the circadian organization of behavior in the rat. Behav. Brain. Res., 1: 39–65, 1980.PubMedCrossRefGoogle Scholar
  56. 56.
    Rosenwasser, A.M., Boulos, Z., and Terman, M.: Circadian feeding and drinking rhythms in the rat under complete and skeleton photoperiods. Physiol. Behav., 30: 353–359, 1983.PubMedCrossRefGoogle Scholar

Copyright information

© American Aging Association, Inc. 1994

Authors and Affiliations

  • Peter H. Duffy
    • 1
  • Ritchie J. Feuers
    • 1
  • James L. Pipkin
    • 1
  • Ronald W. Hart
    • 1
  1. 1.Department of Health and Human Services, Food and Drug AdministrationNational Center for Toxicological Research, Division of Biometry and Risk AssessmentJeffersonUSA

Personalised recommendations