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Modulation of senoinflammation by calorie restriction based on biochemical and Omics big data analysis

  • Bang, EunJin (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Lee, Bonggi (Korean Medicine (KM)-Application Center, Korea Institute of Oriental Medicine (KIOM)) ;
  • Noh, Sang-Gyun (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Kim, Dae Hyun (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Jung, Hee Jin (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Ha, Sugyeong (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Yu, Byung Pal (Department of Physiology, The University of Texas Health Science Center at San Antonio) ;
  • Chung, Hae Young (Department of Pharmacy, College of Pharmacy, Pusan National University)
  • Received : 2018.10.23
  • Published : 2019.01.31

Abstract

Aging is a complex and progressive process characterized by physiological and functional decline with time that increases susceptibility to diseases. Aged-related functional change is accompanied by a low-grade, unresolved chronic inflammation as a major underlying mechanism. In order to explain aging in the context of chronic inflammation, a new integrative concept on age-related chronic inflammation is necessary that encompasses much broader and wider characteristics of cells, tissues, organs, systems, and interactions between immune and non-immune cells, metabolic and non-metabolic organs. We have previously proposed a novel concept of senescent (seno)-inflammation and provided its frameworks. This review summarizes senoinflammation concept and additionally elaborates modulation of senoinflammation by calorie restriction (CR). Based on aging and CR studies and systems-biological analysis of Omics big data, we observed that senescence associated secretory phenotype (SASP) primarily composed of cytokines and chemokines was notably upregulated during aging whereas CR suppressed them. This result further strengthens the novel concept of senoinflammation in aging process. Collectively, such evidence of senoinflammation and modulatory role of CR provide insights into aging mechanism and potential interventions, thereby promoting healthy longevity.

Keywords

References

  1. Chung HY, Cesari M, Anton S et al (2009) Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 8, 18-30 https://doi.org/10.1016/j.arr.2008.07.002
  2. Chung HY, Kim DH, Lee EK et al (2018) Redefining Chronic Inflammation in Aging and Age-Related Diseases: Proposal of the Senoinflammation Concept. Aging Dis [Epub ahead of print]
  3. Vasto S, Candore G, Balistreri CR et al (2007) Inflammatory networks in ageing, age-related diseases and longevity. Mech Ageing Dev 128, 83-91 https://doi.org/10.1016/j.mad.2006.11.015
  4. Yu BP and Yang R (1996) Critical evaluation of the free radical theory of aging. A proposal for the oxidative stress hypothesis. Ann N Y Acad Sci 786, 1-11 https://doi.org/10.1111/j.1749-6632.1996.tb39047.x
  5. Groslambert M and Py BF (2018) Spotlight on the NLRP3 inflammasome pathway. J Inflamm Res 11, 359-374 https://doi.org/10.2147/JIR.S141220
  6. Hanouna G, Mesnard L, Vandermeersch S et al (2017) Specific calpain inhibition protects kidney against inflammaging. Sci Rep 7, 8016 https://doi.org/10.1038/s41598-017-07922-1
  7. Baker DJ, Childs BG, Durik M et al (2016) Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 530, 184-189 https://doi.org/10.1038/nature16932
  8. Salminen A, Kauppinen A and Kaarniranta K (2012) Emerging role of NF-kappaB signaling in the induction of senescence-associated secretory phenotype (SASP). Cell Signal 24, 835-845 https://doi.org/10.1016/j.cellsig.2011.12.006
  9. Young AR and Narita M (2009) SASP reflects senescence. EMBO Rep 10, 228-230 https://doi.org/10.1038/embor.2009.22
  10. Coppe JP, Patil CK, Rodier F et al (2008) Senescenceassociated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6, 2853-2868
  11. Freund A, Orjalo AV, Desprez PY and Campisi J (2010) Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med 16, 238-246 https://doi.org/10.1016/j.molmed.2010.03.003
  12. Seo YH, Jung HJ, Shin HT et al (2008) Enhanced glycogenesis is involved in cellular senescence via GSK3/GS modulation. Aging Cell 7, 894-907 https://doi.org/10.1111/j.1474-9726.2008.00436.x
  13. Coppe JP, Desprez PY, Krtolica A and Campisi J (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5, 99-118 https://doi.org/10.1146/annurev-pathol-121808-102144
  14. Georgilis A, Klotz S, Hanley CJ et al (2018) PTBP1- Mediated Alternative Splicing Regulates the Inflammatory Secretome and the Pro-tumorigenic Effects of Senescent Cells. Cancer Cell 34, 85-102.e109 https://doi.org/10.1016/j.ccell.2018.06.007
  15. Fuhrmann-Stroissnigg H, Niedernhofer LJ and Robbins PD (2018) Hsp90 inhibitors as senolytic drugs to extend healthy aging. Cell Cycle 17, 1048-1055 https://doi.org/10.1080/15384101.2018.1475828
  16. Redman LM and Ravussin E (2011) Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxid Redox Signal 14, 275-287 https://doi.org/10.1089/ars.2010.3253
  17. Gonzalez O, Tobia C, Ebersole J and Novak MJ (2012) Caloric restriction and chronic inflammatory diseases. Oral Dis 18, 16-31 https://doi.org/10.1111/j.1601-0825.2011.01830.x
  18. Anderson RM and Weindruch R (2012) The caloric restriction paradigm: implications for healthy human aging. Am J Hum Biol 24, 101-106 https://doi.org/10.1002/ajhb.22243
  19. Nadon NL, Strong R, Miller RA et al (2008) Design of aging intervention studies: the NIA interventions testing program. Age (Dordr) 30, 187-199 https://doi.org/10.1007/s11357-008-9048-1
  20. Mattson MP, Duan W, Lee J and Guo Z (2001) Suppression of brain aging and neurodegenerative disorders by dietary restriction and environmental enrichment: molecular mechanisms. Mech Ageing Dev 122, 757-778 https://doi.org/10.1016/S0047-6374(01)00226-3
  21. Cohen DE, Supinski AM, Bonkowski MS, Donmez G and Guarente LP (2009) Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction. Genes Dev 23, 2812-2817 https://doi.org/10.1101/gad.1839209
  22. Pahlavani MA (2000) Caloric restriction and immunosenescence: a current perspective. Front Biosci 5, D580-587
  23. Kurki E, Shi J, Martonen E, Finckenberg P and Mervaala E (2012) Distinct effects of calorie restriction on adipose tissue cytokine and angiogenesis profiles in obese and lean mice. Nutr Metab (Lond) 9, 64 https://doi.org/10.1186/1743-7075-9-64
  24. Lijnen HR, Van Hul M and Hemmeryckx B (2012) Caloric restriction improves coagulation and inflammation profile in obese mice. Thromb Res 129, 74-79 https://doi.org/10.1016/j.thromres.2011.05.023
  25. Choi WH, Um MY, Ahn J, Jung CH and Ha TY (2014) Cooked rice inhibits hepatic fat accumulation by regulating lipid metabolism-related gene expression in mice fed a high-fat diet. J Med Food 17, 36-42 https://doi.org/10.1089/jmf.2013.3058
  26. Jung KJ, Lee EK, Kim JY et al (2009) Effect of short term calorie restriction on pro-inflammatory NF-kB and AP-1 in aged rat kidney. Inflamm Res 58, 143-150 https://doi.org/10.1007/s00011-008-7227-2
  27. Sadagurski M, Landeryou T, Cady G, Bartke A, Bernal-Mizrachi E and Miller RA (2015) Transient early food restriction leads to hypothalamic changes in the long-lived crowded litter female mice. Physiol Rep 3, e12379 https://doi.org/10.14814/phy2.12379
  28. Tsutsumi A, Motoshima H, Kondo T et al (2011) Caloric restriction decreases ER stress in liver and adipose tissue in ob/ob mice. Biochem Biophys Res Commun 404, 339-344 https://doi.org/10.1016/j.bbrc.2010.11.120
  29. Escriva F, Gavete ML, Fermin Y et al (2007) Effect of age and moderate food restriction on insulin sensitivity in Wistar rats: role of adiposity. J Endocrinol 194, 131-141 https://doi.org/10.1677/joe.1.07043
  30. Zheng Y, Zhang W, Pendleton E et al (2009) Improved insulin sensitivity by calorie restriction is associated with reduction of ERK and p70S6K activities in the liver of obese Zucker rats. J Endocrinol 203, 337-347 https://doi.org/10.1677/JOE-09-0181
  31. Park MH, Park JY, Lee HJ et al (2013) Potent anti-diabetic effects of MHY908, a newly synthesized PPAR alpha/gamma dual agonist in db/db mice. PLoS One 8, e78815 https://doi.org/10.1371/journal.pone.0078815
  32. Youm YH, Nguyen KY, Grant RW et al (2015) The ketone metabolite beta-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat Med 21, 263-269 https://doi.org/10.1038/nm.3804
  33. Fann DY, Santro T, Manzanero S et al (2014) Intermittent fasting attenuates inflammasome activity in ischemic stroke. Exp Neurol 257, 114-119 https://doi.org/10.1016/j.expneurol.2014.04.017
  34. Traba J, Kwarteng-Siaw M, Okoli TC et al (2015) Fasting and refeeding differentially regulate NLRP3 inflammasome activation in human subjects. J Clin Invest 125, 4592-4600 https://doi.org/10.1172/JCI83260
  35. Chung KW, Kim DH, Park MH et al (2013) Recent advances in calorie restriction research on aging. Exp Gerontol 48, 1049-1053 https://doi.org/10.1016/j.exger.2012.11.007
  36. Kim HJ, Jung KJ, Yu BP, Cho CG, Choi JS and Chung HY (2002) Modulation of redox-sensitive transcription factors by calorie restriction during aging. Mech Ageing Dev 123, 1589-1595 https://doi.org/10.1016/S0047-6374(02)00094-5
  37. Sung B, Park S, Yu BP and Chung HY (2004) Modulation of PPAR in aging, inflammation, and calorie restriction. J Gerontol A Biol Sci Med Sci 59, 997-1006 https://doi.org/10.1093/gerona/59.10.B997
  38. Delerive P, Gervois P, Fruchart JC and Staels B (2000) Induction of IkappaBalpha expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-alpha activators. J Biol Chem 275, 36703-36707 https://doi.org/10.1074/jbc.M004045200
  39. Chung SW, Kang BY, Kim SH et al (2000) Oxidized low density lipoprotein inhibits interleukin-12 production in lipopolysaccharide-activated mouse macrophages via direct interactions between peroxisome proliferator-activated receptor-gamma and nuclear factor-kappa B. J Biol Chem 275, 32681-32687 https://doi.org/10.1074/jbc.M002577200
  40. Chung JH, Seo AY, Chung SW et al (2008) Molecular mechanism of PPAR in the regulation of age-related inflammation. Ageing Res Rev 7, 126-136 https://doi.org/10.1016/j.arr.2008.01.001
  41. Satoh A, Brace CS, Rensing N et al (2013) Sirt1 extends life span and delays aging in mice through the regulation of Nk2 homeobox 1 in the DMH and LH. Cell Metab 18, 416-430 https://doi.org/10.1016/j.cmet.2013.07.013
  42. Nisoli E, Tonello C, Cardile A et al (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314-317 https://doi.org/10.1126/science.1117728
  43. Frescas D, Valenti L and Accili D (2005) Nuclear trapping of the forkhead transcription factor FoxO1 via Sirtdependent deacetylation promotes expression of glucogenetic genes. J Biol Chem 280, 20589-20595 https://doi.org/10.1074/jbc.M412357200
  44. Hong SE, Heo HS, Kim DH et al (2010) Revealing system-level correlations between aging and calorie restriction using a mouse transcriptome. Age (Dordr) 32, 15-30 https://doi.org/10.1007/s11357-009-9106-3
  45. Park D, Lee EK, Jang EJ et al (2013) Identification of the dichotomous role of age-related LCK in calorie restriction revealed by integrative analysis of cDNA microarray and interactome. Age (Dordr) 35, 1045-1060 https://doi.org/10.1007/s11357-012-9426-6
  46. Park D, Kim BC, Kim CH et al (2016) RNA-Seq analysis reveals new evidence for inflammation-related changes in aged kidney. Oncotarget 7, 30037-30048 https://doi.org/10.18632/oncotarget.9152
  47. He S and Sharpless NE (2017) Senescence in Health and Disease. Cell 169, 1000-1011 https://doi.org/10.1016/j.cell.2017.05.015
  48. Kim CH, Lee EK, Choi YJ et al (2016) Short-term calorie restriction ameliorates genomewide, age-related alterations in DNA methylation. Aging Cell 15, 1074-1081 https://doi.org/10.1111/acel.12513
  49. Park MH, Kim DH, Lee EK et al (2014) Age-related inflammation and insulin resistance: a review of their intricate interdependency. Arch Pharm Res 37, 1507-1514 https://doi.org/10.1007/s12272-014-0474-6
  50. Kim DH, Kim JY, Yu BP and Chung HY (2008) The activation of NF-kappaB through Akt-induced FOXO1 phosphorylation during aging and its modulation by calorie restriction. Biogerontology 9, 33-47 https://doi.org/10.1007/s10522-007-9114-6