Skip to main content
SpringerLink
Log in

Aging and the Effect of Calorie Restriction in Rhesus Monkeys

  • Chapter
  • First Online:
Calorie Restriction, Aging and Longevity

Abstract

Calorie restriction (CR), defined as the consumption of fewer calories in the absence of malnutrition, has been shown to decelerate the rate of aging and result in several health benefits in many short-lived species. Beginning about 20 years ago, well-controlled long-term studies initiated at both the National Institute on Aging and the Wisconsin National Primate Research Center have been investigating the effect of CR in long-lived rhesus monkeys, an animal model that closely recapitulates human biology. The studies were uniquely designed but share a common hypothesis that 30% CR will delay age-related diseases and increase lifespan in a long-lived mammal. Results from both studies have established a beneficial effect of CR in terms of body weight, body composition, insulin sensitivity, oxidative stress, and several hormone profiles or no detrimental effect on reproduction and sensory systems. More recently, work has focused on both behavioral and immune function alterations and thus this review emphasizes some of these findings and provides an update on female reproductive studies and sarcopenia.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akira, S., Taga, T. and Kishimoto, T., 1993. Interleukin-6 in biology and medicine. Adv Immunol 54, 1–78.

    Article  PubMed  CAS  Google Scholar 

  • Albert, M., 1993. Neuropsychological and neurophysiological changes in healthy adult humans across the age range. Neurobiol Aging 14(6), 623–625.

    Article  PubMed  CAS  Google Scholar 

  • Arnsten, A. F., Cai, J. X., Steere, J. C. and Goldman-Rakic, P. S., 1995. Dopamine D2 receptor mechanisms contribute to age-related cognitive decline, the effects of quinpirole on memory and motor performance in monkeys. J Neurosci 15(5 Pt 1), 3429–3439.

    PubMed  CAS  Google Scholar 

  • Bachevalier, J., Landis, L. S., Walker, L. C., Brickson, M., Mishkin, M., Price, D. L. and Cork, L. C., 1991. Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiol Aging 12(2), 99–111.

    Article  PubMed  CAS  Google Scholar 

  • Bartus, R. T., Dean, R. L., III and Fleming, D. L., 1979. Aging in the rhesus monkey, effects on visual discrimination learning and reversal learning. J Gerontol 34(2), 209–219.

    Article  PubMed  CAS  Google Scholar 

  • Bodkin, N. L., Alexander, T. M., Ortmeyer, H. K., Johnson, E. and Hansen, B. C., 2003. Mortality and morbidity in laboratory-maintained Rhesus monkeys and effects of long-term dietary restriction. J Gerontol A Biol Sci Med Sci 58(3), 212–219.

    Article  PubMed  Google Scholar 

  • Bruunsgaard, H., 2002. Effects of tumor necrosis factor-alpha and interleukin-6 in elderly populations. Eur Cytokine Netw 13(4), 389–391.

    PubMed  CAS  Google Scholar 

  • Bua, E. A., McKiernan, S. H., Wanagat, J., McKenzie, D. and Aiken, J. M., 2002. Mitochondrial abnormalities are more frequent in muscles undergoing sarcopenia. J Appl Physiol 92(6), 2617–2624.

    PubMed  Google Scholar 

  • Buccafusco, J. J., Terry, A. V., Jr. and Murdoch, P. B., 2002. A computer-assisted cognitive test battery for aged monkeys. J Mol Neurosci 19(1–2), 179–185.

    Article  PubMed  CAS  Google Scholar 

  • Cass, W. A., Grondin, R., Andersen, A. H., Zhang, Z., Hardy, P. A., Hussey-Andersen, L. K., Rayens, W. S., Gerhardt, G. A. and Gash, D. M., 2007. Iron accumulation in the striatum predicts aging-related decline in motor function in rhesus monkeys. Neurobiol Aging 28(2), 258–271.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J., Astle, C. M. and Harrison, D. E., 1998. Delayed immune aging in diet-restricted B6CBAT6 F1 mice is associated with preservation of naive T cells. J Gerontol A Biol Sci Med Sci 53(5), B330–B337, discussion B338–339.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J., Astle, C. M. and Harrison, D. E., 2003. Hematopoietic senescence is postponed and hematopoietic stem cell function is enhanced by dietary restriction. Exp Hematol 31(11), 1097–1103.

    Article  PubMed  CAS  Google Scholar 

  • Cicin-Sain, L., Messaoudi, I., Park, B., Currier, N., Planer, S., Fischer, M., Tackitt, S., Nikolich-Zugich, D., Legasse, A., Axthelm, M. K., Picker, L. J., Mori, M. and Nikolich-Zugich, J., 2007. Dramatic increase in naive T cell turnover is linked to loss of naive T cells from old primates. Proc Natl Acad Sci USA 104(50), 19960–19965.

    Article  PubMed  CAS  Google Scholar 

  • Colman, R. J., Anderson R. M., Johnson, S. C., Kastman, E. K., Kosmatka, J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., and Weindruch, R., 2009. Calorie restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201–204.

    Google Scholar 

  • Colman, R. J., Beasley, T. M., Allison, D. B. and Weindruch, R., 2008. Attenuation of sarcopenia by dietary restriction in rhesus monkeys. J Gerontol A Biol Sci Med Sci 63(6), 556–559.

    Article  PubMed  Google Scholar 

  • Colman, R. J., McKiernan, S. H., Aiken, J. M. and Weindruch, R., 2005. Muscle mass loss in Rhesus monkeys, age of onset. Exp Gerontol 40(7), 573–581.

    Article  PubMed  Google Scholar 

  • Czesnikiewicz-Guzik, M., Lee, W. W., Cui, D., Hiruma, Y., Lamar, D. L., Yang, Z. Z., Ouslander, J. G., Weyand, C. M. and Goronzy, J. J., 2008. T cell subset-specific susceptibility to aging. Clin Immunol 127(1), 107–118.

    Article  PubMed  CAS  Google Scholar 

  • De Martinis, M., Franceschi, C., Monti, D. and Ginaldi, L., 2005. Inflamm-ageing and lifelong antigenic load as major determinants of ageing rate and longevity. FEBS Lett 579(10), 2035–2039.

    Article  PubMed  CAS  Google Scholar 

  • Downs, J. L. and Urbanski, H. F., 2006. Neuroendocrine changes in the aging reproductive axis of female rhesus macaques (Macaca mulatta). Biol Reprod 75(4), 539–546.

    Article  PubMed  CAS  Google Scholar 

  • Dutta, C., 1997. Significance of sarcopenia in the elderly. J Nutr 127, S992–S993.

    Google Scholar 

  • Effros, R. B., Svoboda, K. and Walford, R. L., 1991a. Influence of age and caloric restriction on macrophage IL-6 and TNF production. Lymphokine Cytokine Res 10(5), 347–351.

    PubMed  CAS  Google Scholar 

  • Effros, R. B., Walford, R. L., Weindruch, R. and Mitcheltree, C., 1991b. Influences of dietary restriction on immunity to influenza in aged mice. J Gerontol 46(4), B142–B147.

    Article  PubMed  CAS  Google Scholar 

  • Emborg, M. E., Ma, S. Y., Mufson, E. J., Levey, A. I., Taylor, M. D., Brown, W. D., Holden, J. E. and Kordower, J. H., 1998. Age-related declines in nigral neuronal function correlate with motor impairments in rhesus monkeys. J Comp Neurol 401(2), 253–265.

    Article  PubMed  CAS  Google Scholar 

  • Ershler, W. B. and Keller, E. T., 2000. Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu Rev Med 51, 245–270.

    Article  PubMed  CAS  Google Scholar 

  • Fagnoni, F. F., Vescovini, R., Passeri, G., Bologna, G., Pedrazzoni, M., Lavagetto, G., Casti, A., Franceschi, C., Passeri, M. and Sansoni, P., 2000. Shortage of circulating naive CD8(+) T cells provides new insights on immunodeficiency in aging. Blood 95(9), 2860–2868.

    PubMed  CAS  Google Scholar 

  • Faulkner, J. A., Larkin, L. M., Claflin, D. R. and Brooks, S. V., 2007. Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol 34(11), 1091–1096.

    Article  PubMed  CAS  Google Scholar 

  • Gardner, E. M., 2005. Caloric restriction decreases survival of aged mice in response to primary influenza infection. J Gerontol A Biol Sci Med Sci 60(6), 688–694.

    Article  PubMed  Google Scholar 

  • Gash, D. M., Zhang, Z., Umberger, G., Mahood, K., Smith, M., Smith, C. and Gerhardt, G. A., 1999. An automated movement assessment panel for upper limb motor functions in rhesus monkeys and humans. J Neurosci Methods 89(2), 111–117.

    Article  PubMed  CAS  Google Scholar 

  • Gilardi, K. V., Shideler, S. E., Valverde, C. R., Roberts, J. A. and Lasley, B. L., 1997. Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 57(2), 335–340.

    Article  PubMed  CAS  Google Scholar 

  • Ginaldi, L., Di Benedetto, M. C. and De Martinis, M., 2005. Osteoporosis, inflammation and ageing. Immun Ageing 2, 14.

    Article  PubMed  Google Scholar 

  • Grondin, R., Zhang, Z., Gerhardt, G. A. and Gash, D. M., 2000. Dopaminergic therapy improves upper limb motor performance in aged rhesus monkeys. Ann Neurol 48(2), 250–253.

    Article  PubMed  CAS  Google Scholar 

  • Grossmann, A., Maggio-Price, L., Jinneman, J. C., Wolf, N. S. and Rabinovitch, P. S., 1990. The effect of long-term caloric restriction on function of T-cell subsets in old mice. Cell Immunol 131(1), 191–204.

    Article  PubMed  CAS  Google Scholar 

  • Grossmann, A., Rabinovitch, P. S., Lane, M. A., Jinneman, J. C., Ingram, D. K., Wolf, N. S., Cutler, R. G. and Roth, G. S., 1995. Influence of age, sex, and dietary restriction on intracellular free calcium responses of CD4+ lymphocytes in rhesus monkeys (Macaca mulatta). J Cell Physiol 162(2), 298–303.

    Article  PubMed  CAS  Google Scholar 

  • Harper, J. M., Galecki, A. T., Burke, D. T. and Miller, R. A., 2004. Body weight, hormones and T cell subsets as predictors of life span in genetically heterogeneous mice. Mech Ageing Dev 125(5), 381–390.

    Article  PubMed  CAS  Google Scholar 

  • Hasbold, J., Gett, A. V., Rush, J. S., Deenick, E., Avery, D., Jun, J. and Hodgkin, P. D., 1999. Quantitative analysis of lymphocyte differentiation and proliferation in vitro using carboxyfluorescein diacetate succinimidyl ester. Immunol Cell Biol 77(6), 516–522.

    Article  PubMed  CAS  Google Scholar 

  • Hein, W. R. and Griebel, P. J., 2003. A road less travelled, large animal models in immunological research. Nat Rev Immunol 3(1), 79–84.

    Article  PubMed  CAS  Google Scholar 

  • Hilbert, D. M., Cancro, M. P., Scherle, P. A., Nordan, R. P., Van Snick, J., Gerhard, W. and Rudikoff, S., 1989. T cell derived IL-6 is differentially required for antigen-specific antibody secretion by primary and secondary B cells. J Immunol 143(12), 4019–4024.

    PubMed  CAS  Google Scholar 

  • Holloszy, J. O., 2000. The biology of aging. Mayo Clin Proc 75(Suppl), S3–S8, discussion S8–S9.

    Article  PubMed  Google Scholar 

  • Huang, H., Patel, D. D. and Manton, K. G., 2005. The immune system in aging, roles of cytokines, T cells and NK cells. Front Biosci 10, 192–215.

    Article  PubMed  CAS  Google Scholar 

  • Ingram, D. K., 1991. Effects of dietary restriction on brain and behavioral function in aging rodents. In Ingram, D. K., Baker, G. T. and Shock, N. W. (eds), The Potential for Nutritional Modulation of Aging Processes, Food and Nutrition Press, Westport, CT, pp. 289–310.

    Google Scholar 

  • Ingram, D. K., 2000. Age-related decline in physical activity, generalization to nonhumans. Med Sci Sports Exer 32(9), 1623–1629.

    CAS  Google Scholar 

  • Ingram, D. K., Cutler, R. G., Weindruch, R., Renquist, D. M., Knapka, J. J., April, M., Belcher, C. T., Clark, M. A., Hatcherson, C. D., Marriott, B. M. et al., 1990. Dietary restriction and aging, the initiation of a primate study. J Gerontol 45(5), B148–B163.

    Article  PubMed  CAS  Google Scholar 

  • Jankovic, V., Messaoudi, I. and Nikolich-Zugich, J., 2003. Phenotypic and functional T-cell aging in rhesus macaques (Macaca mulatta), differential behavior of CD4 and CD8 subsets. Blood 102(9), 3244–3251.

    Article  PubMed  CAS  Google Scholar 

  • Janssen, I., Shepard, D. S., Katzmarzyk, P. T. and Roubenoff, R., 2004. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52(1), 80–85.

    Article  PubMed  Google Scholar 

  • Jolly, C. A., 2004. Dietary restriction and immune function. J Nutr 134(8), 1853–1856.

    PubMed  CAS  Google Scholar 

  • Jolly, C. A. and Fernandes, G., 1999. Diet modulates Th-1 and Th-2 cytokine production in the peripheral blood of lupus-prone mice. J Clin Immunol 19(3), 172–178.

    Article  PubMed  CAS  Google Scholar 

  • Kemnitz, J. W., Weindruch, R., Roecker, E. B., Crawford, K., Kaufman, P. L. and Ershler, W. B., 1993. Dietary restriction of adult male rhesus monkeys, design, methodology, and preliminary findings from the first year of study. J Gerontol 48(1), B17–B26.

    Article  PubMed  CAS  Google Scholar 

  • Kim, M.-J., Aiken, J. M., Havighurst, T., Hollander, J., Ripple, M. O. and Weindruch, R., 1997. Adult-onset energy restriction of rhesus monkeys attenuates oxidative stress-induced cytokine expression by peripheral blood mononuclear cells. J Nutr 127(12), 2293–2301.

    PubMed  CAS  Google Scholar 

  • Kristan, D. M., 2007. Chronic calorie restriction increases susceptibility of laboratory mice (Mus musculus) to a primary intestinal parasite infection. Aging Cell 6(6), 817–825.

    Article  PubMed  CAS  Google Scholar 

  • Kubo, N., Koyama, T., Kawasaki, K., Tsuchida, J., Sankai, T., Terao, K. and Yoshikawa, Y., 2001. Behavioral compensations in a positional learning and memory task by aged monkeys. Behav Processes 56(1), 15–22.

    Article  PubMed  Google Scholar 

  • Lacreuse, A., 2006. Relationships among cognitive function, fine motor speed, and age in the rhesus monkey. Age 28, 255–264.

    Article  PubMed  Google Scholar 

  • Lacreuse, A., Diehl, M. M., Goh, M. Y., Hall, M. J., Volk, A. M., Chhabra, R. K. and Herndon, J. G., 2005. Sex differences in age-related motor slowing in the rhesus monkey, behavioral and neuroimaging data. Neurobiol Aging 26(4), 543–551.

    Article  PubMed  Google Scholar 

  • Lacreuse, A. and Herndon, J. G., 2003. Effects of estradiol and aging on fine manual performance in female rhesus monkeys. Horm Behav 43(3), 359–366.

    Article  PubMed  CAS  Google Scholar 

  • Lane, M. A., Black, A., Handy, A. M., Shapses, S. A., Tilmont, E. M., Kiefer, T. L., Ingram, D. K. and Roth, G. S., 2001. Energy restriction does not alter bone mineral metabolism or reproductive cycling and hormones in female rhesus monkeys. J Nutr 131(3), 820–827.

    PubMed  CAS  Google Scholar 

  • Lane, M. A., Ingram, D. K., Cutler, R. G., Knapka, J. J., Barnard, D. E. and Roth, G. S., 1992. Dietary restriction in nonhuman primates, progress report on the NIA study. Ann N Y Acad Sci 673, 36–45.

    Article  PubMed  CAS  Google Scholar 

  • Lane, M. A., Ingram, D. K. and Roth, G. S., 1999. Nutritional modulation of aging in nonhuman primates. J Nutr Health Aging 3(2), 69–76.

    PubMed  CAS  Google Scholar 

  • Lane, M. A., Reznick, A. Z., Tilmont, E. M., Lanir, A., Ball, S. S., Read, V., Ingram, D. K., Cutler, R. G. and Roth, G. S., 1995. Aging and food restriction alter some indices of bone metabolism in male rhesus monkeys (Macaca mulatta). J Nutr 125(6), 1600–1610.

    PubMed  CAS  Google Scholar 

  • Larbi, A., Franceschi, C., Mazzatti, D., Solana, R., Wikby, A. and Pawelec, G., 2008. Aging of the immune system as a prognostic factor for human longevity. Physiol 23(2), 64–74.

    Article  CAS  Google Scholar 

  • Levine, B., Svoboda, E., Hay, J. F., Winocur, G. and Moscovitch, M., 2002. Aging and autobiographical memory, dissociating episodic from semantic retrieval. Psychol Aging 17(4), 677–689.

    Article  PubMed  Google Scholar 

  • Lexell, J., Taylor, C. C. and Sjostrom, M., 1988. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole VL muscle from 15- to 83-year-old men. J Neurol Sco 84, 275–294.

    Article  CAS  Google Scholar 

  • Line, S. W., Morgan, K. N., Markowitz, H. and Strong, S., 1989. Heart rate and activity of rhesus monkeys in response to routine events. Lab Primate NewsLett 28(2), 9–12.

    Google Scholar 

  • Lujan, M. E., Krzemien, A. A., Reid, R. L. and Van Vugt, D. A., 2005. Caloric restriction inhibits steroid-induced gonadotropin surges in ovariectomized rhesus monkeys. Endocrine 27(1), 25–31.

    Article  PubMed  CAS  Google Scholar 

  • Lujan, M. E., Krzemien, A. A., Reid, R. L. and Van Vugt, D. A., 2006a. Developing a model of nutritional amenorrhea in rhesus monkeys. Endocrinol 147(1), 483–492.

    Article  CAS  Google Scholar 

  • Lujan, M. E., Krzemien, A. A., Reid, R. L. and Van Vugt, D. A., 2006b. Effect of leptin administration on ovulation in food-restricted rhesus monkeys. Neuroendocrinol 84(2), 103–114.

    Article  CAS  Google Scholar 

  • Mascarucci, P., Taub, D., Saccani, S., Paloma, M. A., Dawson, H., Roth, G. S., Lane, M. A. and Ingram, D. K., 2002. Cytokine responses in young and old rhesus monkeys, effect of caloric restriction. J Interfer Cyto Res 22(5), 565–571.

    Article  CAS  Google Scholar 

  • Masoro, E. J., 2005. Overview of caloric restriction and ageing. Mech Ageing Dev 126(9), 913–922.

    Article  PubMed  CAS  Google Scholar 

  • Maswood, N., Young, J., Tilmont, E., Zhang, Z., Gash, D. M., Gerhardt, G. A., Grondin, R., Roth, G. S., Mattison, J., Lane, M. A., Carson, R. E., Cohen, R. M., Mouton, P. R., Quigley, C., Mattson, M. P. and Ingram, D. K., 2004. Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson’s disease. Proc Natl Acad Sci USA 101(52), 18171–18176.

    Article  PubMed  CAS  Google Scholar 

  • Mattison, J. A., Black, A., Huck, J., Moscrip, T., Handy, A., Tilmont, E., Roth, G. S., Lane, M. A. and Ingram, D. K., 2005. Age-related decline in caloric intake and motivation for food in rhesus monkeys. Neurobiol Aging 26(7), 1117–1127.

    Article  PubMed  Google Scholar 

  • McKiernan, S. H., Bua, E., McGorray, J. and Aiken, J., 2004. Early-onset calorie restriction conserves fiber number in aging rat skeletal muscle. FASEB J 18(3), 580–581.

    PubMed  Google Scholar 

  • Melton, L. J., III, Khosla, S., Crowson, C. S., O’Connor, M. K., O’Fallon, W. M. and Riggs, B. L., 2000. Epidemiology of sarcopenia. J Am Geriatr Soc 48(6), 625–630.

    PubMed  Google Scholar 

  • Messaoudi, I., Fischer, M., Warner, J., Park, B., Mattison, J., Ingram, D. K., Totonchy, T., Mori, M. and Nikolich-Zugich, J., 2008. Optimal window of caloric restriction onset limits its beneficial impact on T-cell senescence in primates. Aging Cell 7(6), 908–919.

    Article  PubMed  CAS  Google Scholar 

  • Messaoudi, I., Lemaoult, J., Guevara-Patino, J. A., Metzner, B. M. and Nikolich-Zugich, J., 2004. Age-related CD8 T cell clonal expansions constrict CD8 T cell repertoire and have the potential to impair immune defense. J Exp Med 200(10), 1347–1358.

    Article  PubMed  CAS  Google Scholar 

  • Messaoudi, I., Warner, J., Fischer, M., Park, B., Hill, B., Mattison, J., Lane, M. A., Roth, G. S., Ingram, D. K., Picker, L. J., Douek, D. C., Mori, M. and Nikolich-Zugich, J., 2006a. Delay of T cell senescence by caloric restriction in aged long-lived nonhuman primates. Proc Natl Acad Sci USA 103(51), 19448–19453.

    Article  PubMed  CAS  Google Scholar 

  • Messaoudi, I., Warner, J., Nikolich-Zugich, D., Fischer, M. and Nikolich-Zugich, J., 2006b. Molecular, cellular, and antigen requirements for development of age-associated T cell clonal expansions in vivo. J Immunol 176(1), 301–308.

    PubMed  CAS  Google Scholar 

  • Miller, R. A., 1996. The aging immune system, primer and prospectus. Science 273(5271), 70–74.

    Article  PubMed  CAS  Google Scholar 

  • Moscrip, T. D., Ingram, D. K., Lane, M. A., Roth, G. S. and Weed, J. L., 2000. Locomotor activity in female rhesus monkeys, assessment of age and calorie restriction effects. J Gerontol A Biol Sci Med Sci 55(8), B373–B380.

    Article  PubMed  CAS  Google Scholar 

  • Naylor, K., Li, G., Vallejo, A. N., Lee, W. W., Koetz, K., Bryl, E., Witkowski, J., Fulbright, J., Weyand, C. M. and Goronzy, J. J., 2005. The influence of age on T cell generation and TCR diversity. J Immunol 174(11), 7446–7452.

    PubMed  CAS  Google Scholar 

  • Nichols, S. M., Bavister, B. D., Brenner, C. A., Didier, P. J., Harrison, R. M. and Kubisch, H. M., 2005. Ovarian senescence in the rhesus monkey (Macaca mulatta). Hum Reprod 20(1), 79–83.

    Article  PubMed  CAS  Google Scholar 

  • Nikolich-Zugich, J. and Messaoudi, I., 2005. Mice and flies and monkeys too, caloric restriction rejuvenates the aging immune system of non-human primates. Exp Gerontol 40(11), 884–893.

    Article  PubMed  CAS  Google Scholar 

  • Papailiou, A., Sullivan, E. and Cameron, J. L., 2008. Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured by accelerometer. Am J Primatol 70(2), 185–190.

    Article  PubMed  Google Scholar 

  • Pawelec, G., Adibzadeh, M., Pohla, H. and Schaudt, K., 1995. Immunosenescence, ageing of the immune system. Immunol Today 16(9), 420–422.

    Article  PubMed  CAS  Google Scholar 

  • Peters, A., Rosene, D. L., Moss, M. B., Kemper, T. L., Abraham, C. R., Tigges, J. and Albert, M. S., 1996. Neurobiological bases of age-related cognitive decline in the rhesus monkey. J Neuropathol Exp Neurol 55(8), 861–874.

    PubMed  CAS  Google Scholar 

  • Pitcher, C. J., Hagen, S. I., Walker, J. M., Lum, R., Mitchell, B. L., Maino, V. C., Axthelm, M. K. and Picker, L. J., 2002. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168(1), 29–43.

    PubMed  CAS  Google Scholar 

  • Posnett, D. N., Sinha, R., Kabak, S. and Russo, C., 1994. Clonal populations of T cells in normal elderly humans, the T cell equivalent to “benign monoclonal gammapathy”. J Exp Med 179(2), 609–618.

    Article  PubMed  CAS  Google Scholar 

  • Ramsey, J. J., Colman, R. J., Binkley, N. C., Christensen, J. D., Gresl, T. A., Kemnitz, J. W. and Weindruch, R., 2000. Dietary restriction and aging in rhesus monkeys, the University of Wisconsin study. Exp Gerontol 35(9–10), 1131–1149.

    Article  PubMed  CAS  Google Scholar 

  • Ramsey, J. J., Roecker, E. B., Weindruch, R. and Kemnitz, J. W., 1997. Energy expenditure of adult male rhesus monkeys during the first 30 mo of dietary restriction. Am J Physiol 272(5 Pt 1), E901–E907.

    PubMed  CAS  Google Scholar 

  • Rapp, P. R., 1990. Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behav Neurosci 104(6), 876–884.

    Article  PubMed  CAS  Google Scholar 

  • Rapp, P. R. and Amaral, D. G., 1989. Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 9(10), 3568–3576.

    PubMed  CAS  Google Scholar 

  • Rink, L., Cakman, I. and Kirchner, H., 1998. Altered cytokine production in the elderly. Mech Ageing Dev 102(2–3), 199–209.

    Article  PubMed  CAS  Google Scholar 

  • Roecker, E. B., Kemnitz, J. W., Ershler, W. B. and Weindruch, R., 1996. Reduced immune responses in rhesus monkeys subjected to dietary restriction. J Gerontol A Biol Sci Med Sci 51(4), B276–B279.

    Article  PubMed  CAS  Google Scholar 

  • Roth, G. S., Ingram, D. K. and Lane, M. A., 1999. Calorie restriction in primates, will it work and how will we know? J Am Geriatr Soc 47(7), 896–903.

    PubMed  CAS  Google Scholar 

  • Roubenoff, R. and Castaneda, C., 2001. Sarcopenia-understanding the dynamics of aging muscle. JAMA 286(10), 1230–1231.

    Article  PubMed  CAS  Google Scholar 

  • Roy, A. C., Paulignan, Y., Farne, A., Jouffrais, C. and Boussaoud, D., 2000. Hand kinematics during reaching and grasping in the macaque monkey. Behav Brain Res 117(1–2), 75–82.

    Article  PubMed  CAS  Google Scholar 

  • Salamone, J. D. and Correa, M., 2002. Motivational views of reinforcement, implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 137(1–2), 3–25.

    Article  PubMed  CAS  Google Scholar 

  • Sallis, J. F., 2000. Age-related decline in physical activity, a synthesis of human and animal studies. Med Sci Sports Exer 32(9), 1598–1600.

    CAS  Google Scholar 

  • Schwab, R., Szabo, P., Manavalan, J. S., Weksler, M. E., Posnett, D. N., Pannetier, C., Kourilsky, P. and Even, J., 1997. Expanded CD4+ and CD8+ T cell clones in elderly humans. J Immunol 158(9), 4493–4499.

    PubMed  CAS  Google Scholar 

  • Small, S. A., Stern, Y., Tang, M. and Mayeux, R., 1999. Selective decline in memory function among healthy elderly. Neurology 52(7), 1392–1396.

    Article  PubMed  CAS  Google Scholar 

  • Smith, C. D., Umberger, G. H., Manning, E. L., Slevin, J. T., Wekstein, D. R., Schmitt, F. A., Markesbery, W. R., Zhang, Z., Gerhardt, G. A., Kryscio, R. J. and Gash, D. M., 1999. Critical decline in fine motor hand movements in human aging. Neurology 53(7), 1458–1461.

    Article  PubMed  CAS  Google Scholar 

  • Smith, C. D., Walton, A., Loveland, A. D., Umberger, G. H., Kryscio, R. J. and Gash, D. M., 2005. Memories that last in old age, motor skill learning and memory preservation. Neurobiol Aging 26(6), 883–890.

    Article  PubMed  CAS  Google Scholar 

  • Spaulding, C. C., Walford, R. L. and Effros, R. B., 1997a. The accumulation of non-replicative, non-functional, senescent T cells with age is avoided in calorically restricted mice by an enhancement of T cell apoptosis. Mech Ageing Dev 93(1–3), 25–33.

    Article  PubMed  CAS  Google Scholar 

  • Spaulding, C. C., Walford, R. L. and Effros, R. B., 1997b. Calorie restriction inhibits the age-related dysregulation of the cytokines TNF-alpha and IL-6 in C3B10RF1 mice. Mech Ageing Dev 93(1–3), 87–94.

    Article  PubMed  CAS  Google Scholar 

  • Strindhall, J., Nilsson, B.-O., Lofgren, S., Ernerudh, J., Pawelec, G., Johansson, B. and Wikby, A., 2007. No Immune Risk Profile among individuals who reach 100 years of age, findings from the Swedish NONA immune longitudinal study. Exp Gerontol 42(8), 753–761.

    Article  PubMed  CAS  Google Scholar 

  • Tsuchida, J., Kubo, N. and Kojima, S., 2002. Position reversal learning in aged Japanese macaques. Behav Brain Res 129(1–2), 107–112.

    Article  PubMed  Google Scholar 

  • Vallejo, A. N., 2005. CD28 extinction in human T cells, altered functions and the program of T-cell senescence. Immunol Rev 205, 158–169.

    Article  PubMed  CAS  Google Scholar 

  • Volk, M. J., Pugh, T. D., Kim, M., Frith, C. H., Daynes, R. A., Ershler, W. B. and Weindruch, R., 1994. Dietary restriction from middle age attenuates age-associated lymphoma development and interleukin 6 dysregulation in C57BL/6 mice. Cancer Res 54(11), 3054–3061.

    PubMed  CAS  Google Scholar 

  • Voytko, M. L., 1999. Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys. Neurobiol Aging 20(6), 617–627.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, W. M., Ouyang, Q., Sekeri-Pataryas, K., Sourlingas, T. G. and Pawelec, G., 2004. Basic biology and clinical impact of immunosenescence. Biogerontol 5(1), 63–66.

    Article  CAS  Google Scholar 

  • Walford, R. L., Liu, R. K., Gerbase-Delima, M., Mathies, M. and Smith, G. S., 1973. Longterm dietary restriction and immune function in mice, response to sheep red blood cells and to mitogenic agents. Mech Ageing Dev 2(6), 447–454.

    Article  PubMed  CAS  Google Scholar 

  • Walton, A., Branham, A., Gash, D. M. and Grondin, R., 2006. Automated video analysis of age-related motor deficits in monkeys using EthoVision. Neurobiol Aging 27(10), 1477–1483.

    Article  PubMed  Google Scholar 

  • Wanagat, J., Cao, Z., Pathare, P. and Aiken, J. M., 2001. Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J 15(2), 322–332.

    Article  PubMed  CAS  Google Scholar 

  • Weed, J. L., Lane, M. A., Roth, G. S., Speer, D. L. and Ingram, D. K., 1997. Activity measures in rhesus monkeys on long-term calorie restriction. Physiol Behav 62(1), 97–103.

    Article  PubMed  CAS  Google Scholar 

  • Weindruch, R., Lane, M. A., Ingram, D. K., Ershler, W. B. and Roth, G. S., 1997. Dietary restriction in rhesus monkeys, lymphopenia and reduced mitogen-induced proliferation in peripheral blood mononuclear cells. Aging (Milano) 9(4), 304–308.

    CAS  Google Scholar 

  • Weindruch, R. and Walford, R. L., 1982. Dietary restriction in mice beginning at 1 year of age, effect on life-span and spontaneous cancer incidence. Science 215(4538), 1415–1418.

    Article  PubMed  CAS  Google Scholar 

  • Wikby, A., Maxson, P., Olsson, J., Johansson, B. and Ferguson, F. G., 1998. Changes in CD8 and CD4 lymphocyte subsets, T cell proliferation responses and non-survival in the very old, the Swedish longitudinal OCTO-immune study. Mech Ageing Dev 102(2–3), 187–198.

    Article  PubMed  CAS  Google Scholar 

  • Wikby, A., Nilsson, B. O., Forsey, R., Thompson, J., Strindhall, J., Lofgren, S., Ernerudh, J., Pawelec, G., Ferguson, F. and Johansson, B., 2006. The immune risk phenotype is associated with IL-6 in the terminal decline stage, findings from the Swedish NONA immune longitudinal study of very late life functioning. Mech Ageing Dev 127(8), 695–704.

    Article  PubMed  CAS  Google Scholar 

  • Zanni, F., Vescovini, R., Biasini, C., Fagnoni, F., Zanlari, L., Telera, A., Di Pede, P., Passeri, G., Pedrazzoni, M., Passeri, M., Franceschi, C. and Sansoni, P., 2003. Marked increase with age of type 1 cytokines within memory and effector/cytotoxic CD8+ T cells in humans, a contribution to understand the relationship between inflammation and immunosenescence. Exp Gerontol 38(9), 981–987.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Z., Andersen, A., Smith, C., Grondin, R., Gerhardt, G. and Gash, D., 2000. Motor slowing and parkinsonian signs in aging rhesus monkeys mirror human aging. J Gerontol A Biol Sci Med Sci 55(10), B473–B480.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank their many collaborators, past and present, who have contributed to these projects. As well, these studies would not be possible without the excellent animal care and veterinary support at both sites. The NIA study was supported in part by the Intramural Research Program of the NIH, National Institute on Aging. The WNPRC study was supported by NIH grants P01 AG-11915 and P51 RR000167 and was conducted in part at the WNPRC which received support from Research Facilities Improvement Program grant numbers RR15459-01 and RR020141-01. IM is supported by a fellowship from the Brookdale Foundation.

Author information

Authors and Affiliations

  1. Division of Pathobiology and Immunology, Vaccine and Gene Therapy Institute, Oregon National Primate Research Center, Beaverton, OR, 97006, USA

    Ilhem Messaoudi

  2. Intramural Research Program, Laboratory of Experimental Gerontology, National Institute on Aging, National Institutes of Health, Poolesville, MD, 20837, USA

    Jennifer E. Young, April M. Handy & Julie A. Mattison

  3. Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, 53715, USA

    Ricki J. Colman

  4. SoBran Inc., Fairfax, VA, 22031, USA

    April M. Handy

  5. GeroScience, Pylesville, MD, 21132, USA

    George S. Roth

  6. Nutritional Neuroscience and Aging Laboratory, Pennington Biomedical Research Center, Louisiana State University, Baton Rouge, LA, 70808, USA

    Donald K. Ingram

Authors
  1. Ilhem Messaoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer E. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricki J. Colman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. April M. Handy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George S. Roth
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Donald K. Ingram
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julie A. Mattison
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Sydney, 2006, Australia

    Arthur V. Everitt

  2. University of Aarhus, University of Aarhus, Aarhus, 8000, Denmark

    Suresh I. S. Rattan

  3. Sydney, 2006, Australia

    David G. le Couteur

  4. National Institute on Aging, Gerontology Research Center, National Institute of Health, Nathan Shock Drive 5600, Baltimore, 21224, USA

    Rafael de Cabo

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Messaoudi, I. et al. (2010). Aging and the Effect of Calorie Restriction in Rhesus Monkeys. In: Everitt, A., Rattan, S., le Couteur, D., de Cabo, R. (eds) Calorie Restriction, Aging and Longevity. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-8556-6_4

Download citation

Publish with us

Policies and ethics

Search

Navigation