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PMID: 17875344 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Chronic caloric restriction induces forestomach hypertrophy with enhanced ghrelin levels during aging.

Peptides ·Vol. 28 ·No. 10 ·2007-10-00 ·Pages 1931-6

Yang H, Youm YH, Nakata C, Dixit VD

Abstract

Caloric restriction (CR) is the only preventive intervention that has robust pro-longevity effects in experimental models. Various circulating hormones that regulate the state of negative energy balance may drive the multi-system beneficial effects of the CR phenomenon. Ghrelin, one such stomach-derived circulating peptide hormone stimulates food intake, promotes GH release and inhibits pro-inflammatory cytokines. We have recently demonstrated that ghrelin also reverses age-related thymic involution. Here, we report that chronic CR in aging mice results in reduction in body weight, and spleen size but remarkably, leads to a significant increase in the size and weight of stomach. The increased size of stomach was largely due to increased size of fundus (forestomach) and also smaller but statistically significant enlargement of antrum. The analysis of serial stomach sections revealed that chronic CR leads to a striking hypertrophy of lamina propria, stratum basale, stratum corneum and the stratified squamous epithelium of forestomach of the aged animals. We also report for the first time that chronic CR during aging significantly increases circulating ghrelin levels as well as total ghrelin production in the stomach and reverses age-related loss of ghrelin receptor expression in pituitary. Our data suggests that long-term CR-induced increased ghrelin production from hypertrophic stomach in mice may be an adaptive survival strategy in response to sustained negative energy balance that triggers heightened state of food seeking. Taken together, these data provide new insights into the underlying mechanism behind the salutary effects of chronic caloric restriction during aging process.

MeSH Terms
Aging/metabolism,pathology Animals Caloric Restriction Enzyme-Linked Immunosorbent Assay Female Ghrelin/biosynthesis,metabolism Hypertrophy Immunohistochemistry Mice Polymerase Chain Reaction Stomach/pathology
Chemicals
Ghrelin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yang Hyunwon
Laboratory of Neuroendocrine-Immunology, Pennington Biomedical Research Center, Louisiana State University System, 6400 Perkins Road, Baton Rouge, LA 70808, USA.
Youm Yun-Hee
Nakata Chiaki
Dixit Vishwa Deep
References (31)
31 references, click to expand
  1. Effects of mild calorie restriction on reproduction, plasma parameters and hepatic gene expression in mice with altered GH/IGF-I axis.
    Mech Ageing Dev. 2007 Apr;128(4):317-31 PMID: 17376513
  2. Ghrelin and growth hormone secretagogue receptor expression in mice during aging.
    Endocrinology. 2007 Mar;148(3):1323-9 PMID: 17158206
  3. Calorie restriction mimetics: an emerging research field.
    Aging Cell. 2006 Apr;5(2):97-108 PMID: 16626389
  4. Toward a unified theory of caloric restriction and longevity regulation.
    Mech Ageing Dev. 2005 Sep;126(9):987-1002 PMID: 15893363
  5. Ghrelin is a growth-hormone-releasing acylated peptide from stomach.
    Nature. 1999 Dec 9;402(6762):656-60 PMID: 10604470
  6. Food restriction enhances endogenous and corticotropin-induced plasma elevations of free but not total corticosterone throughout life in rats.
    J Gerontol A Biol Sci Med Sci. 2001 Sep;56(9):B391-7 PMID: 11524440
  7. Ghrelin increases neuropeptide Y and agouti-related peptide gene expression in the arcuate nucleus in rat hypothalamic organotypic cultures.
    Endocrinology. 2006 Nov;147(11):5102-9 PMID: 16887908
  8. Targeted disruption of growth hormone receptor interferes with the beneficial actions of calorie restriction.
    Proc Natl Acad Sci U S A. 2006 May 16;103(20):7901-5 PMID: 16682650
  9. Gut peptides in the regulation of food intake and energy homeostasis.
    Endocr Rev. 2006 Dec;27(7):719-27 PMID: 17077190
  10. Dietary restriction in mice beginning at 1 year of age: effect on life-span and spontaneous cancer incidence.
    Science. 1982 Mar 12;215(4538):1415-8 PMID: 7063854
  11. Gonadotropin-releasing hormone attenuates pregnancy-associated thymic involution and modulates the expression of antiproliferative gene product prohibitin.
    Endocrinology. 2003 Apr;144(4):1496-505 PMID: 12639934
  12. Ghrelin and immunity: a young player in an old field.
    Exp Gerontol. 2005 Nov;40(11):900-10 PMID: 16233968
  13. Twenty-four-hour ghrelin is elevated after calorie restriction and exercise training in non-obese women.
    Obesity (Silver Spring). 2007 Feb;15(2):446-55 PMID: 17299118
  14. Calorie restriction increases life span: a molecular mechanism.
    Nutr Rev. 2006 Feb;64(2 Pt 1):89-92 PMID: 16536186
  15. The molecular inflammatory process in aging.
    Antioxid Redox Signal. 2006 Mar-Apr;8(3-4):572-81 PMID: 16677101
  16. Ghrelin inhibits proinflammatory responses and nuclear factor-kappaB activation in human endothelial cells.
    Circulation. 2004 May 11;109(18):2221-6 PMID: 15117840
  17. Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6659-63 PMID: 15096581
  18. Ghrelin promotes thymopoiesis during aging.
    J Clin Invest. 2007 Oct;117(10):2778-90 PMID: 17823656
  19. Starving for life: what animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan.
    J Nutr. 2007 Apr;137(4):1078-86 PMID: 17374682
  20. Hyperleptinemia prevents increased plasma ghrelin concentration during short-term moderate caloric restriction in rats.
    Gastroenterology. 2003 May;124(5):1188-92 PMID: 12730858
  21. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery.
    N Engl J Med. 2002 May 23;346(21):1623-30 PMID: 12023994
  22. Differences in the appetite-stimulating effect of orexin, neuropeptide Y and ghrelin among young, adult and old rats.
    Neuroendocrinology. 2005;82(5-6):256-63 PMID: 16721031
  23. Calorie restriction and iopanoic acid effects on thyroid hormone metabolism.
    Am J Clin Nutr. 1990 Aug;52(2):263-6 PMID: 2375292
  24. Effect of aging on the response of ghrelin to acute weight loss.
    J Am Geriatr Soc. 2006 Apr;54(4):648-53 PMID: 16686877
  25. Aging influences the level and functions of fasting plasma ghrelin levels: the POWIRS-Study.
    Regul Pept. 2007 Mar 1;139(1-3):65-71 PMID: 17113660
  26. Physiological, pathological and potential therapeutic roles of ghrelin.
    Drug Discov Today. 2007 Apr;12(7-8):276-88 PMID: 17395087
  27. Ghrelin inhibits leptin- and activation-induced proinflammatory cytokine expression by human monocytes and T cells.
    J Clin Invest. 2004 Jul;114(1):57-66 PMID: 15232612
  28. Ghrelin controls hippocampal spine synapse density and memory performance.
    Nat Neurosci. 2006 Mar;9(3):381-8 PMID: 16491079
  29. SIR2: a potential target for calorie restriction mimetics.
    Trends Mol Med. 2007 Feb;13(2):64-71 PMID: 17207661
  30. Minireview: ghrelin and the regulation of energy balance--a hypothalamic perspective.
    Endocrinology. 2001 Oct;142(10):4163-9 PMID: 11564668
  31. Therapeutic action of ghrelin in a mouse model of colitis.
    Gastroenterology. 2006 May;130(6):1707-20 PMID: 16697735
Article Info
Journal
Peptides
Abbr.
Peptides
ISSN
0196-9781
Published
2007-10-00
Epub
2007-00-19
Pages
1931-6
Language
English
Region
United States
NLM ID
8008690
PMCID
PMC5682623
Subset
IM
Grants
NCRR NIH HHS · P20 RR021945 · United States
NIDDK NIH HHS · P30 DK072476 · United States
NCRR NIH HHS · 1 P20 RR02/1945 · United States
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