Every-other-day feeding extends lifespan but fails to delay many symptoms of aging in mice

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Xie, Kan ^a   Neff, Frauke ^b   Markert, Astrid ^a   Rozman, Jan ^b,c   Aguilar Pimentel, Juan Antonio ^b,d   Amarie, Oana Veronica ^b   Becker, Lore ^b   Brommage, Robert ^b   Garrett, Lillian ^b   Henzel, Kristin S ^a   Hölter, Sabine M ^b   Janik, Dirk ^b   Lehmann, Isabelle ^a   Moreth, Kristin ^b   Pearson, Brandon L ^a   Racz, Ildiko ^b,e   Rathkolb, Birgit ^b,c,f   Ryan, Devon P ^a   Schröder, Susanne ^a   Treise, Irina ^b,d   Bekeredjian, Raffi ^g   Busch, Dirk H ^d   Graw, Jochen ^b   Ehninger, Gerhard ^h   Klingenspor, Martin ^d   Klopstock, Thomas ^a,i,j   Ollert, Markus ^k,l   Sandholzer, Michael ^b   Schmidt Weber, Carsten ^d,m   Weiergräber, Marco ⁿ   Wolf, Eckhard ^f   Wurst, Wolfgang ^a,b,d,j   Zimmer, Andreas ^e   Gailus Durner, Valerie ^b   Fuchs, Helmut ^b   Hrabě De Angelis, Martin ^b,c,d   Ehninger, Dan ^a   more..

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF BONN   (Germany)

^f UNIVERSITY OF MUNICH   (Germany)

^g UNIVERSITY OF HEIDELBERG   (Germany)

^h UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

ⁱ LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^j Technische Universität München Munich Cluster for Systems Neurology   (Germany)

^k LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^l UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^m German Center for Lung Research   (Germany)

ⁿ FEDERAL INSTITUTE FOR DRUGS AND MEDICAL DEVICES   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; IMMUNOGLOBULIN E; RNA; WATER;

AGING; CELLS AND CELL COMPONENTS; FEEDING; HISTOPATHOLOGY; LONGEVITY; MOLECULAR ANALYSIS; PHENOTYPE; PHYSIOLOGY; RODENT; SYMPTOM;

AGING; ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BRONCHI ASSOCIATED LYMPHATIC TISSUE; CALORIC INTAKE; CALORIMETRY; CATARACTOGENESIS; CLINICAL CHEMISTRY; CONTROLLED STUDY; DIET RESTRICTION; FRACTURE; GLUCOSE HOMEOSTASIS; HEARING IMPAIRMENT; HEART WEIGHT; HEMATOCRIT; IMMUNE DEFICIENCY; IMMUNOGLOBULIN BLOOD LEVEL; LEUKOCYTE COUNT; LIFE EXTENSION; LONGEVITY; LYMPHOID TISSUE; MALE; MOUSE; NEOPLASM; NONHUMAN; ORGAN WEIGHT; OSTEOPOROSIS; PHENOTYPE; RNA SEQUENCE; SKIN WATER LOSS; TESTIS ATROPHY; TURNOVER TIME; ANIMAL; C57BL MOUSE; FOOD DEPRIVATION;

ANIMALIA; MUS;

AGING; ANIMALS; FOOD DEPRIVATION; LONGEVITY; MALE; MICE; MICE, INBRED C57BL;

EID: 85026551882     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00178-3     Document Type: Article

References (70)

1. Miller, R. A. in Hazzard's Geriatric Medicine and Gerontology (eds Halter, J. B., Ouslander, J. G., Tinetti, M. E., Studenski, S., High, K. P. & Asthana S.) (The McGraw-Hill Companies, Inc., 2009).
2. Olshansky, S. J., Perry, D., Miller, R. A. & Butler, R. N. Pursuing the longevity dividend: scientific goals for an aging world. Ann. N. Y. Acad. Sci. 1114, 11-13 (2007).
3. Speakman, J. R. & Mitchell, S. E. Caloric restriction. Mol. Aspects Med. 32, 159-221 (2011).
4. Weindruch, R. & Walford, R. L. Dietary restriction in mice beginning at 1 year of age: effect on life-span and spontaneous cancer incidence. Science 215, 1415-1418 (1982).
5. Weindruch, R. Effect of caloric restriction on age-associated cancers. Exp. Gerontol. 27, 575-581 (1992).
6. Blackwell, B. N., Bucci, T. J., Hart, R. W. & Turturro, A. Longevity, body weight, and neoplasia in ad libitum-fed and diet-restricted C57BL6 mice fed NIH-31 open formula diet. Toxicol. Pathol. 23, 570-582 (1995).
7. Weindruch, R. & Sohal, R. S. Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N. Engl. J. Med. 337, 986-994 (1997).
8. Talan, M. I. & Ingram, D. K. Effect of intermittent feeding on thermoregulatory abilities of young and aged C57BL/6J mice. Arch. Gerontol. Geriatr. 4, 251-259 (1985).
9. Goodrick, C. L., Ingram, D. K., Reynolds, M. A., Freeman, J. R. & Cider, N. Effects of intermittent feeding upon body weight and lifespan in inbred mice: interaction of genotype and age. Mech. Ageing Dev. 55, 69-87 (1990).
10. Anson, R. M. et al. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc. Natl Acad. Sci. USA 100, 6216-6220 (2003).
11. Selman, C. Dietary restriction and the pursuit of effective mimetics. Proc. Nutr. Soc. 73, 260-270 (2014).
12. Neff, F. et al. Rapamycin extends murine lifespan but has limited effects on aging. J. Clin. Invest. 123, 3272-3291 (2013).
13. Swindell, W. R. Dietary restriction in rats and mice: a meta-analysis and review of the evidence for genotype-dependent effects on lifespan. Ageing Res. Rev. 11, 254-270 (2012).
14. Pettan-Brewer, C., Treuting, P. M. Practical pathology of aging mice. Pathobiol. Aging Age Relat. Dis. 1, 7202 (2011).
15. Fahlstrom, A., Yu, Q. & Ulfhake, B. Behavioral changes in aging female C57BL/6 mice. Neurobiol. Aging 32, 1868-1880 (2011).
16. Harding, J. J. in Aging of Organs and Systems (ed Aspinall, R.). (Kluwer Academic Publishers, 2003).
17. Lehmann, K., Schmidt, K. F. & Lowel, S. Vision and visual plasticity in ageing mice. Restor. Neurol. Neurosci. 30, 161-178 (2012).
18. Someya, S. et al. Age-related hearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis. Proc. Natl Acad. Sci. USA 106, 19432-19437 (2009).
19. Young, J. W., Wallace, C. K., Geyer, M. A. & Risbrough, V. B. Age-associated improvements in cross-modal prepulse inhibition in mice. Behav. Neurosci. 124, 133-140 (2010).
20. Dai, D. F. & Rabinovitch, P. S. Cardiac aging in mice and humans: the role of mitochondrial oxidative stress. Trends Cardiovasc. Med. 19, 213-220 (2009).
21. Alcendor, R. R. et al. Sirt1 regulates aging and resistance to oxidative stress in the heart. Circ. Res. 100, 1512-1521 (2007).
22. Sikka, G. et al. Interleukin 10 knockout frail mice develop cardiac and vascular dysfunction with increased age. Exp. Gerontol. 48, 128-135 (2013).
23. Kassem M., Brixen K., Mosekilde L. in Aging of Organs and Systems (ed. Aspinall, R.) (Kluwer Academic Publishers, 2003).
24. Ferguson, V. L., Ayers, R. A., Bateman, T. A. & Simske, S. J. Bone development and age-related bone loss in male C57BL/6J mice. Bone 33, 387-398 (2003).
25. Hamrick, M. W. et al. Age-related loss of muscle mass and bone strength in mice is associated with a decline in physical activity and serum leptin. Bone 39, 845-853 (2006).
26. Houtkooper, R. H. et al. The metabolic footprint of aging in mice. Sci. Rep. 1, 134 (2011).
27. Leuenberger, H. G. & Kunstyr, I. Gerontological data of C57BL/6J mice. II. Changes in blood cell counts in the course of natural aging. J. Gerontol. 31, 648-653 (1976).
28. Frith, C. H., Suber, R. L. & Umholtz, R. Hematologic and clinical chemistry findings in control BALB/c and C57BL/6 mice. Lab. Anim. Sci. 30, 835-840 (1980).
29. Dorshkind, K., Montecino-Rodriguez, E. & Signer, R. A. The ageing immune system: is it ever too old to become young again? Nat. Rev. Immunol. 9, 57-62 (2009).
30. Henson S. M., Aspinall R. in Aging of Organs and Systems (ed. Richard, A.). (Kluwer Academic Publishers, 2003).
31. Chen, J., Flurkey, K. & Harrison, D. E. A reduced peripheral blood CD4(+) lymphocyte proportion is a consistent ageing phenotype. Mech. Ageing Dev. 123, 145-153 (2002).
32. Fang, M., Roscoe, F. & Sigal, L. J. Age-dependent susceptibility to a viral disease due to decreased natural killer cell numbers and trafficking. J. Exp. Med. 207, 2369-2381 (2010).
33. Alter-Wolf, S., Blomberg, B. B. & Riley, R. L. Old mice retain bone marrow B1 progenitors, but lose B2 precursors, and exhibit altered immature B cell phenotype and light chain usage. Mech. Ageing Dev. 130, 401-408 (2009).
34. Miller, J. P. & Allman, D. The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J. Immunol. 171, 2326-2330 (2003).
35. Walunas, T. L., Bruce, D. S., Dustin, L., Loh, D. Y. & Bluestone, J. A. Ly-6C is a marker of memory CD8+ T cells. J. Immunol. 155, 1873-1883 (1995).
36. Ding, J. & Kopchick, J. J. Plasma biomarkers of mouse aging. Age 33, 291-307 (2011).
37. Yanai, T. et al. Eosinophilic neuronal inclusions in the thalamus of ageing B6C3F1 mice. J. Comp. Pathol. 113, 287-290 (1995).
38. Culebras, A., Segarra, J. M. & Feldman, R. G. Eosinophilic bodies within neurons in the human thalamus. An age-related histological feature. J. Neurol. Sci. 16, 177-182 (1972).
39. Kmiec, Z., Kotlarz, G., Smiechowska, B. & Mysliwski, A. The effect of fasting and refeeding on thyroid follicule structure and thyroid hormone levels in young and old rats. Arch. Gerontol. Geriatr. 26, 161-175 (1998).
40. Haines, D. C., Chattopadhyay, S. & Ward, J. M. Pathology of aging B6;129 mice. Toxicol. Pathol. 29, 653-661 (2001).
41. Zhang, Y. M. et al. Expression of tissue inhibitor of matrix metalloproteinase-1 in aging of transgenic mouse liver. Chin. Med. J. 119, 504-509 (2006).
42. Weinstein, J. R. & Anderson, S. The aging kidney: physiological changes. Adv. Chronic Kidney Dis. 17, 302-307 (2010).
43. Schmitt, R. et al. Ageing mouse kidney - not always the SAME old story. Nephrol. Dial. Transplant. 24, 3002-3005 (2009).
44. Zhou, X. J. et al. The aging kidney. Kidney Int. 74, 710-720 (2008).
45. Schmidt, J. A., Oatley, J. M. & Brinster, R. L. Female mice delay reproductive aging in males. Biol. Reprod. 80, 1009-1014 (2009).
46. Ehninger, D., Neff, F. & Xie, K. Longevity, aging and rapamycin. Cell Mol. Life Sci. 71, 4325-4346 (2014).
47. Longo, V. D. & Fontana, L. Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends Pharmacol. Sci. 31, 89-98 (2010).
48. Pape-Ansorge, K. A., Grande, J. P., Christensen, T. A., Maihle, N. J. & Cleary, M. P. Effect of moderate caloric restriction and/or weight cycling on mammary tumor incidence and latency in MMTV-Neu female mice. Nutr. Cancer 44, 162-168 (2002).
49. Rocha, N. S., Barbisan, L. F., de Oliveira, M. L. & de Camargo, J. L. Effects of fasting and intermittent fasting on rat hepatocarcinogenesis induced by diethylnitrosamine. Teratog. Carcinog. Mutagen. 22, 129-138 (2002).
50. Goodrick, C. L., Ingram, D. K., Reynolds, M. A., Freeman, J. R. & Cider, N. L. Differential effects of intermittent feeding and voluntary exercise on body weight and lifespan in adult rats. J. Gerontol. 38, 36-45 (1983).
51. Ahmet, I., Wan, R., Mattson, M. P., Lakatta, E. G. & Talan, M. Cardioprotection by intermittent fasting in rats. Circulation 112, 3115-3121 (2005).
52. Wan, R. et al. Cardioprotective effect of intermittent fasting is associated with an elevation of adiponectin levels in rats. J. Nutr. Biochem. 21, 413-417 (2010).
53. Challet, E. Interactions between light, mealtime and calorie restriction to control daily timing in mammals. J. Comp. Physiol. B 180, 631-644 (2010).
54. Blank, J. L. & Desjardins, C. Differential effects of food restriction on pituitary-testicular function in mice. Am. J. Physiol. 248, R181-R189 (1985).
55. Nelson, W. Food restriction, circadian disorder and longevity of rats and mice. J. Nutr. 118, 286-289 (1988).
56. Masoro, E. J., Shimokawa, I., Higami, Y., McMahan, C. A. & Yu, B. P. Temporal pattern of food intake not a factor in the retardation of aging processes by dietary restriction. J. Gerontol. A Biol. Sci. Med. Sci. 50A, B48-B53 (1995).
57. Nelson, W. & Halberg, F. Schedule-shifts, circadian rhythms and lifespan of freely-feeding and meal-fed mice. Physiol. Behav. 38, 781-788 (1986).
58. Nelson, W. & Halberg, F. Meal-timing, circadian rhythms and life span of mice. J. Nutr. 116, 2244-2253 (1986).
59. Colman, R. J. et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201-204 (2009).
60. Mattison, J. A. et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489, 318-321 (2012).
61. Colman, R. J. et al. Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat. Commun. 5, 3557 (2014).
62. Tinsley, G. M. & La Bounty, P. M. Effects of intermittent fasting on body composition and clinical health markers in humans. Nutr. Rev. 73, 661-674 (2015).
63. Fuchs, H. et al. Mouse phenotyping. Methods 53, 120-135 (2011).
64. Rogers, D. C. et al. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome 8, 711-713 (1997).
65. Sahn, D. J., DeMaria, A., Kisslo, J. & Weyman, A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58, 1072-1083 (1978).
66. Puk, O., de Angelis, M. H. & Graw, J. Longitudinal fundus and retinal studies with SD-OCT: a comparison of five mouse inbred strains. Mamm. Genome 24, 198-205 (2013).
67. Puk, O., de Angelis, M. H. & Graw, J. Lens density tracking in mice by Scheimpflug imaging. Mamm. Genome 24, 295-302 (2013).
68. Prusky, G. T., Alam, N. M., Beekman, S. & Douglas, R. M. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest. Ophthalmol. Vis. Sci. 45, 4611-4616 (2004).
69. Baumgarth, N. & Roederer, M. A practical approach to multicolor flow cytometry for immunophenotyping. J. Immunol. Methods 243, 77-97 (2000).
70. Lamprecht, M. R., Sabatini, D. M. & Carpenter, A. E. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques 42, 71-75 (2007).