Cited by 229Genetics, Aging, and Longevity in Model OrganismsGrowth Hormone and Insulin-like Growth FactorsDietary Effects on Health

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Pleiotropic Effects of Growth Hormone and Insulin-like Growth Factor (IGF)-1 on Biological Aging: Inferences From Moderate Caloric-Restricted Animals

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Sonntag, W. E., Lynch, C. D., Cefalu, W. T., Ingram, R. L., Bennett, S. A., Thornton, P. L., Khan, A. S.·1999·The Journals of Gerontology Series A: Biological Sciences and Medical Sciences

DOI 10.1093/gerona/54.12.b521

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Abstract

Moderate caloric restriction (60% of ad libitum intake) is an important model to investigate potential mechanisms of biological aging. This regimen has been reported to decrease the number of pathologies and increase life span in all species tested to date. Although moderate caloric restriction induces a wide range of physiological changes within the organism, adaptive changes within the endocrine system are evident and serve to maintain blood levels of glucose. These alterations include an increase in growth hormone secretory dynamics and a decline in plasma levels of IGF-1. These endocrine compensatory mechanisms can be induced at any age, and we have proposed that these alterations mediate some of the beneficial aspects of moderate caloric restriction. Numerous studies indicate that growth hormone and IGF-1 decrease with age and that administration of these hormones ameliorates the deterioration of tissue function evident in aged ad libitum-fed animals, suggesting that the absence of these hormones contributes to the phenotype of aging. Nevertheless, IGF-1 is an important risk factor in age-related pathologies including lung, breast, and prostate cancer. From these studies, we propose that endocrine compensatory mechanisms induced by moderate caloric restriction (including increased growth hormone and decreased IGF-1) decrease the stimulus for cellular replication, resulting in a decline in pathologies and increased life span observed in these animals. These findings have important implications for potential mechanisms of moderate caloric restriction and suggest that neuroendocrine compensatory mechanisms exert a key role on the actions of moderate caloric restriction on life span.

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Hypothalamic Polypeptide That Inhibits the Secretion of Immunoreactive Pituitary Growth Hormone
Brazeau, P., Vale, W., Burgus, R. C., LING, N. C., Butcher, M., Rivier, J., & Guillemin, R. (1973) · Science · doi:10.1126/science.179.4068.77 · Cited by 3,536
Tissue concentrations of somatomedin C: further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of action.
D’Ercole, A. J., Stiles, A. D., & Underwood, L. E. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.3.935 · Cited by 1,179
Characterization of a growth hormone-releasing factor from a human pancreatic islet tumour
Rivier, J., Spiess, J., Thorner, M. O., & Vale, W. (1982) · Nature · doi:10.1038/300276a0 · Cited by 1,102
The Retardation of Aging in Mice by Dietary Restriction: Longevity, Cancer, Immunity and Lifetime Energy Intake
Weindruch, R. H., Walford, R. L., Fligiel, S., & Guthrie, D. (1986) · Journal of Nutrition · doi:10.1093/jn/116.4.641 · Cited by 992
Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase
Argetsinger, L. S., Campbell, G. S., Yang, X.-J., Witthuhn, B. A., Silvennoinen, O., Ihle, J. N., & Carter‐Su, C. (1993) · Cell · doi:10.1016/0092-8674(93)90415-m · Cited by 974
Somatomedin-C Mediates Growth Hormone Negative Feedback by Effects on Both the Hypothalamus and the Pituitary
Berelowitz, M., Szabó, M., Frohman, L. A., Firestone, S. L., Chu, L., & Hintz, R. L. (1981) · Science · doi:10.1126/science.6262917 · Cited by 829
Reduced tyrosine kinase activity of the insulin receptor in obesity-diabetes. Central role of tumor necrosis factor-alpha.
Hotamisligil, G. S., Budavari, A., Murray, D., & Spiegelman, B. M. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117495 · Cited by 819
Dietary Restriction in Mice Beginning at 1 Year of Age: Effect on Life-Span and Spontaneous Cancer Incidence
Weindruch, R. H., & Walford, R. L. (1982) · Science · doi:10.1126/science.7063854 · Cited by 766
Evidence for an Endogenous Ultradian Rhythm Governing Growth Hormone Secretion in the Rat
Tannenbaum, G. S., & Martin, J. B. (1976) · Endocrinology · doi:10.1210/endo-98-3-562 · Cited by 744
Impaired growth hormone secretion in the adult population: relation to age and adiposity.
Rudman, D. R., Kutner, M., Rogers, C. M., Lubin, M., Fleming, G. A., & Bain, R. P. (1981) · Journal of Clinical Investigation · doi:10.1172/jci110164 · Cited by 641

Show all 131 references

Research works printed but not linked: 30

Timiras PS. Neuroendocrinology of aging: retrospective, current, and prospective views. In: Meites J, ed. Neuroendocrinology ofAging. New York: Plenum Press; 1983:5-30.
Reichlin S. Neuroendocrinology. In: Williams RH, ed. Textbook of Endocrinology. 5th ed. Philadelphia:WB Saunders; 1974;774-831.
Weaver DR. The suprachiasmatic nucleus: a 25-year retrospective [Review; 248 refs]. J Biolog Rhythms. 1998;13:100-112.
Meites J. Neuroendocrinology ofAging. New York: Plenum Press; 1983.
McCay CM, Sperling G, Barnes LL. Growth, aging, chronic diseases and lifespan in rats. Arch Biochem Biophys. 1943;2:469-479.
Lipman 1M, Turturro A, Hart RW. The influence of dietary restriction on DNA repair in rodents: a preliminary study [Review; 31 refs). Mech Ageing Dev. 1989;48:135-143.
Turturro AT, Hart RW. DNA repair mechanisms in aging. In: Schiapelli D, Migaki G, eds. ComparativeBiology ofMajor Age-Related Diseases. New York:Alan Liss; 1984:351-361.
Hart RW, Leakey IE, Chou M, Duffy PH, Allaben WT, Feuers RI. Modulation of chemical toxicity by modification of caloric intake [Review; 36 refs}.Adv Exp Med Biol. 1992;322:73-81.
Sonntag WE, Lenham JE, Ingram RL. Effects of aging and dietary re- striction on tissue protein synthesis: relationship to plasma insulin-like growth factor-I. J GerontolBiol Sci. 1992;47:B159-B 163.
Verdery RB, Ingram DK, Roth GS, Lane MA. Caloric restriction in- creases HDL2 levels in rhesus monkeys (Macaca mulatta). Am J Physiol. I997;273:E714-E719.
McCarter RI. Role of caloric restriction in the prolongation of life [Review; 53 refs}.Clin GeriatrMed. 1995;11:553-565.
Weindruch R. The retardation of aging by caloric restriction: studies in ro- dents and primates [Review; 26 refs}.ToxicolPathol. 1996;24:742-745.
Richardson A, Cheung HT. Current concepts: I. The relationship between age-related changes in gene expression, protein turnover, and the respon- siveness of an organism to stimuli [Review; 42 refs]. Life Sci. 1982;31: 605--613.
Walter CA, Grabowski DT, Street KA, Conrad CC, Richardson A. Analysis and modulation of DNA repair in aging [Review; 84 refs]. MechAgeing Dev. 1997;98:203-222.
Rudman D, Feller AG, Cohn L, Shetty KR, Rudman IW, Draper MW. Effects of human growth hormone on body composition in elderly men [Review]. Honn Res. 1991;36(Suppll ):73-81.
Haley-Zitlin V, Richardson A. Effect of dietary restriction on DNA repair and DNA damage [Review; 32 refs]. Mutat Res. 1993;295:237-245.
Li CH, Evans HM, Simpson ME. Isolation and properties of the anterior pituitary hypophyseal growth hormone. J Bioi Chern. 1945;159:353-356.
Corpas E, Harman SM, Blackman MR. Human growth hormone and human aging [Review]. Endocr Rev. 1993;14:20-39.
Cohick WS, Clemmons DR. The insulin-like growth factors [Review; 137 refs]. Annu Rev Physiol. 1993;55: 131-153.
Yamamoto H, Murphy U. Enzymatic conversion of IGF-I to des(l- 3)IGF-I in rat serum and tissues: a further potential site of growth hor- mone regulation ofIGF-I action. J Endocrinol. 1995;146:141-148.
Isaksson OG, Lindahl A, Nilsson A, Isgaard 1. Action of growth hor- mone: current views [Review; 45 refs]. Acta Paediatr Scand [Supplj. 1988;343: 12-18.
Tannenbaum GS, Ling N. The interrelationship of growth hormone (GH)-releasing factor and somatostatin in generation of the ultradian rhythm ofGH secretion. Endocrinology. 1984;115:1952-1957.
Sonntag WE, Steger RW, Forman U, Meites 1. Decreased pulsatile re- lease of growth hormone in old male rats. Endocrinology. 1980; 107: 1875-1879.
Florini JR, Harned JA, Richman RA, Weiss JP. Effect of rat age on serum levels of growth hormone and somatomedins. Mech Ageing Dev. 1981; 15:165-176.
Sonntag WE, Hylka VW, Meites J. Growth hormone restores protein syn- thesis in skeletal muscle of old male rats. J Gerontol. 1985;40:689--694.
Sonntag WE, Boyd RL. Chronic ethanol feeding inhibits plasma levels of insulin-like growth factor-I. Life Sci. 1988;43:1325-1330.
Sonntag WE, Hylka VW, Meites 1. Impaired ability of old male rats to secrete growth hormone in vivo but not in vitro in response to hpGRF( 1- 44). Endocrinology. 1983;113:2305-2307.
Sotiropoulos A, Perrot-Applanat M, Dinerstein H, et al. Distinct cyto- plasmic regions of the growth hormone receptor are required for activa- tion of JAK2, mitogen-activated protein kinase, and transcription [see comments]. Endocrinology. 1994;135:1292-1298.
Carvalho CR, Brenelli SL, Silva AC, Nunes AL, Velloso LA, Saad MJ. Effect of aging on insulin receptor, insulin receptor substrate-I, and phos- phatidylinositol 3-kinase in liver and muscle of rats. Endocrinology. 1996;137:151-159.
Werther GA, Abate M, Hogg A, et al. Localization of insulin-like growth factor-I mRNA in rat brain by in situ hybridization-relationship to IGF- I receptors. Mol Endocrinol. 1990;4:773-778.

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Authors: Sonntag, W. E., Lynch, C. D., Cefalu, W. T., Ingram, R. L., Bennett, S. A., Thornton, P. L., & Khan, A. S.
Affiliations: Wake Forest University Health Sciences (US)
ORCID: Sonntag, W. E.
Cefalu, W. T.
Venue: The Journals of Gerontology Series A: Biological Sciences and Medical Sciences
Publisher: Oxford University Press (OUP)
Published: 1999-12-01
Volume: 54
Issue: 12
Pages: B521-B538
ISSN: 1079-5006 (ISSN-L)
1758-535X
DOI: 10.1093/gerona/54.12.b521
OpenAlex: W2166656167
Cited by: 229
References: 131
Citations by year: 2026: 2 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 12 · 2020: 10 · 2019: 14 · 2018: 3 · 2017: 7 · 2016: 12 · 2015: 4 · 2014: 3 · 2013: 6 · 2012: 9
FWCI: 1.41
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: The Journals of Gerontology Series A (publishedVersion)
PubMed (publishedVersion)
DigitalCommons-Cedarville (Cedarville University) (submittedVersion)
Funders: Wake Forest University
National Institutes of Health (5r01ag007752-07)
National Institute on Aging (AG-11370, P01AG011370, AG 07752)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
Health Sciences › Medicine › Physiology (medical) › Dietary Effects on Health
Keywords: biological aging, growth hormone, insulin-like growth factor I, lifespan extension, age-related diseases, cancer risk, neuroendocrine adaptation, glucose homeostasis
MeSH terms: Aging, Animals, Blood Glucose, Energy Intake, Cell Division, Disease Models, Animal, Female, Insulin-Like Growth Factor I, Longevity, Lung Neoplasms, Male, Mammary Neoplasms, Experimental, Neurosecretory Systems, Phenotype, Prostatic Neoplasms, Risk Factors, Growth Hormone

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Pleiotropic Effects of Growth Hormone and Insulin-like Growth Factor (IGF)-1 on Biological Aging: Inferences From Moderate Caloric-Restricted Animals

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