Familial longevity is characterized by high circadian rhythmicity of serum cholesterol in healthy elderly individuals

Aging Cell

Volumn 16, Issue 2, 2017, Pages 237-243

  van den Berg, Rosa ^a,b   Noordam, Raymond ^c   Kooijman, Sander ^a,b   Jansen, Steffy W M ^c   Akintola, Abimbola A ^c   Slagboom, P Eline ^a   Pijl, Hanno ^a   Rensen, Patrick C N ^a,b   Biermasz, Nienke R ^a   van Heemst, Diana ^c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Einthoven Laboratory for Experimental Vascular Medicine   (Netherlands)

^c Department of Gerontology and Geriatrics ^*  (Netherlands)

Author keywords

aging; biological clock; cholesterol; circadian rhythm; longevity

Indexed keywords

CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

AGED; AGING; ARTICLE; BIOCHEMICAL ANALYSIS; BLOOD SAMPLING; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CIRCADIAN RHYTHM; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; HUMAN; ISOCALORIC MEAL; LONGEVITY; MALE; MEAL; PRIORITY JOURNAL; PROGENY; SIBLING; TRIACYLGLYCEROL BLOOD LEVEL; VERY ELDERLY; BIOLOGICAL RHYTHM; BLOOD; CASE CONTROL STUDY; LIPID METABOLISM; MIDDLE AGED; PHYSIOLOGY;

AGED; AGED, 80 AND OVER; BIOLOGICAL CLOCKS; CASE-CONTROL STUDIES; CHOLESTEROL, HDL; CHOLESTEROL, LDL; CIRCADIAN RHYTHM; HUMANS; LIPID METABOLISM; LONGEVITY; MIDDLE AGED; SIBLINGS; TRIGLYCERIDES;

EID: 85004130229     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12547     Document Type: Article

References (42)

1. Akintola AA, Jansen SW, Wilde RB, Hultzer G, Rodenburg R, van Heemst D (2015) A simple and versatile method for frequent 24 h blood sample collection in healthy older adults. MethodsX 2, 33–38.
2. Bailey M, Silver R (2014) Sex differences in circadian timing systems: implications for disease. Front. Neuroendocrinol. 35, 111–139.
3. Barzilai N, Gabriely I, Gabriely M, Iankowitz N, Sorkin JD (2001) Offspring of centenarians have a favorable lipid profile. J. Am. Geriatr. Soc. 49, 76–79.
4. Barzilai N, Atzmon G, Schechter C, Schaefer EJ, Cupples AL, Lipton R, Cheng S, Shuldiner AR (2003) Unique lipoprotein phenotype and genotype associated with exceptional longevity. JAMA 290, 2030–2040.
5. Buysse DJ, Reynolds CF III, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 28, 193–213.
6. Carpenter JS, Andrykowski MA (1998) Psychometric evaluation of the Pittsburgh Sleep Quality Index. J. Psychosom. Res. 45, 5–13.
7. Chua EC, Shui G, Lee IT, Lau P, Tan LC, Yeo SC, Lam BD, Bulchand S, Summers SA, Puvanendran K, Rozen SG, Wenk MR, Gooley JJ (2013) Extensive diversity in circadian regulation of plasma lipids and evidence for different circadian metabolic phenotypes in humans. Proc. Natl Acad. Sci. USA 110, 14468–14473.
8. Coomans CP, van den Berg SA, Houben T, van Klinken JB, van den Berg R, Pronk AC, Havekes LM, Romijn JA, van Dijk KW, Biermasz NR, Meijer JH (2013) Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. FASEB J. 27, 1721–1732.
9. De Benedictis G, Falcone E, Rose G, Ruffolo R, Spadafora P, Baggio G, Bertolini S, Mari D, Mattace R, Monti D, Morellini M, Sansoni P, Franceschi C (1997) DNA multiallelic systems reveal gene/longevity associations not detected by diallelic systems. The APOB locus. Hum. Genet. 99, 312–318.
10. Froy O (2011) Circadian rhythms, aging, and life span in mammals. Physiology 26, 225–235.
11. Garasto S, Rose G, Derango F, Berardelli M, Corsonello A, Feraco E, Mari V, Maletta R, Bruni A, Franceschi C, Carotenuto L, De Benedictis G (2003) The study of APOA1, APOC3 and APOA4 variability in healthy ageing people reveals another paradox in the oldest old subjects. Ann. Hum. Genet. 67, 54–62.
12. Graham I, Cooney MT, Bradley D, Dudina A, Reiner Z (2012) Dyslipidemias in the prevention of cardiovascular disease: risks and causality. Curr. Cardiol. Rep. 14, 709–720.
13. Hermida RC, Ayala DE, Mojon A, Fernandez JR (2013) Blunted sleep-time relative blood pressure decline increases cardiovascular risk independent of blood pressure level–the “normotensive non-dipper” paradox. Chronobiol. Int. 30, 87–98.
14. Hofman MA, Swaab DF (2006) Living by the clock: the circadian pacemaker in older people. Ageing Res. Rev. 5, 33–51.
15. Hofman MA, Zhou JN, Swaab DF (1996) Suprachiasmatic nucleus of the human brain: an immunocytochemical and morphometric analysis. Anat. Rec. 244, 552–562.
16. Hurd MW, Ralph MR (1998) The significance of circadian organization for longevity in the golden hamster. J. Biol. Rhythms 13, 430–436.
17. Jansen SW, Akintola AA, Roelfsema F, van der Spoel E, Cobbaert CM, Ballieux BE, Egri P, Kvarta-Papp Z, Gereben B, Fekete C, Slagboom PE, van der Grond J, Demeneix BA, Pijl H, Westendorp RG, van Heemst D (2015a) Human longevity is characterised by high thyroid stimulating hormone secretion without altered energy metabolism. Sci. Rep. 5, 11525.
18. Jansen SW, Roelfsema F, van der Spoel E, Akintola AA, Postmus I, Ballieux BE, Slagboom PE, Cobbaert CM, van der Grond J, Westendorp RG, Pijl H, van Heemst D (2015b) Familial longevity is associated with higher TSH secretion and strong TSH-fT3 relationship. J. Clin. Endocrinol. Metab. 100, 3806–3813.
19. Jones PJ, Schoeller DA (1990) Evidence for diurnal periodicity in human cholesterol synthesis. J. Lipid Res. 31, 667–673.
20. Kooijman S, van den Berg R, Ramkisoensing A, Boon MR, Kuipers EN, Loef M, Zonneveld TC, Lucassen EA, Sips HC, Chatzispyrou IA, Houtkooper RH, Meijer JH, Coomans CP, Biermasz NR, Rensen PC (2015) Prolonged daily light exposure increases body fat mass through attenuation of brown adipose tissue activity. Proc. Natl Acad. Sci. USA 112, 6748–6753.
21. Miettinen TA (1982) Diurnal variation of cholesterol precursors squalene and methyl sterols in human plasma lipoproteins. J. Lipid Res. 23, 466–473.
22. Mirani-Oostdijk CP, Havekes L, Terpstra J, Frolich M, Van Gent CM, Jansen H (1983) Diurnal changes in serum triglycerides as related to changes in lipolytic enzymes, (apo) lipoproteins and hormones in normal subjects on a carbohydrate-rich diet. Eur. J. Clin. Invest. 13, 301–309.
23. Oeppen J, Vaupel JW (2002) Demography. Broken limits to life expectancy. Science 296, 1029–1031.
24. Persson L, Cao G, Stahle L, Sjoberg BG, Troutt JS, Konrad RJ, Galman C, Wallen H, Eriksson M, Hafstrom I, Lind S, Dahlin M, Amark P, Angelin B, Rudling M (2010) Circulating proprotein convertase subtilisin kexin type 9 has a diurnal rhythm synchronous with cholesterol synthesis and is reduced by fasting in humans. Arterioscler. Thromb. Vasc. Biol. 30, 2666–2672.
25. Pletcher MJ, Bibbins-Domingo K, Liu K, Sidney S, Lin F, Vittinghoff E, Hulley SB (2010) Nonoptimal lipids commonly present in young adults and coronary calcium later in life: the CARDIA (Coronary Artery Risk Development in Young Adults) study. Ann. Intern. Med. 153, 137–146.
26. Postmus I, Deelen J, Sedaghat S, Trompet S, de Craen AJ, Heijmans BT, Franco OH, Hofman A, Dehghan A, Slagboom PE, Westendorp RG, Jukema JW (2015) LDL cholesterol still a problem in old age? A Mendelian randomization study. Int. J. Epidemiol. 44, 604–612.
27. Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418, 935–941.
28. Rivera-Coll A, Fuentes-Arderiu X, Diez-Noguera A (1994) Circadian rhythmic variations in serum concentrations of clinically important lipids. Clin. Chem. 40, 1549–1553.
29. Roenneberg T, Wirz-Justice A, Merrow M (2003) Life between clocks: daily temporal patterns of human chronotypes. J. Biol. Rhythms 18, 80–90.
30. Rose G, Crocco P, D'Aquila P, Montesanto A, Bellizzi D, Passarino G (2011) Two variants located in the upstream enhancer region of human UCP1 gene affect gene expression and are correlated with human longevity. Exp. Gerontol. 46, 897–904.
31. Roszkowska-Gancarz M, Bartoszewicz Z, Polosak J, Kurylowicz A, Jonas M, Mossakowska M, Franek E, Puzianowska-Kuznicka M (2012) Total and high molecular weight adiponectin and level-modifying polymorphisms of ADIPOQ in centenarians. Endokrynol. Pol. 63, 439–446.
32. Rozing MP, Westendorp RG, de Craen AJ, Frolich M, de Goeij MC, Heijmans BT, Beekman M, Wijsman CA, Mooijaart SP, Blauw GJ, Slagboom PE, van Heemst D (2010) Favorable glucose tolerance and lower prevalence of metabolic syndrome in offspring without diabetes mellitus of nonagenarian siblings: the Leiden longevity study. J. Am. Geriatr. Soc. 58, 564–569.
33. Schoenmaker M, de Craen AJ, de Meijer PH, Beekman M, Blauw GJ, Slagboom PE, Westendorp RG (2006) Evidence of genetic enrichment for exceptional survival using a family approach: the Leiden Longevity Study. Eur. J. Hum. Genet. 14, 79–84.
34. Soerensen M, Dato S, Tan Q, Thinggaard M, Kleindorp R, Beekman M, Suchiman HE, Jacobsen R, McGue M, Stevnsner T, Bohr VA, de Craen AJ, Westendorp RG, Schreiber S, Slagboom PE, Nebel A, Vaupel JW, Christensen K, Christiansen L (2013) Evidence from case-control and longitudinal studies supports associations of genetic variation in APOE, CETP, and IL6 with human longevity. Age 35, 487–500.
35. Steinhagen-Thiessen E, Bramlage P, Losch C, Hauner H, Schunkert H, Vogt A, Wasem J, Jockel KH, Moebus S (2008) Dyslipidemia in primary care–prevalence, recognition, treatment and control: data from the German Metabolic and Cardiovascular Risk Project (GEMCAS). Cardiovasc. Diabetol. 7, 31.
36. Stowie AC, Glass JD (2015) Longitudinal study of changes in daily activity rhythms over the lifespan in individual male and female C57BL/6J mice. J. Biol. Rhythms 30, 563–568.
37. Vaarhorst AA, Beekman M, Suchiman EH, van Heemst D, Houwing-Duistermaat JJ, Westendorp RG, Slagboom PE, Heijmans BT (2011) Lipid metabolism in long-lived families: the Leiden Longevity Study. Age 33, 219–227.
38. Wang JL, Lim AS, Chiang WY, Hsieh WH, Lo MT, Schneider JA, Buchman AS, Bennett DA, Hu K, Saper CB (2015) Suprachiasmatic neuron numbers and rest-activity circadian rhythms in older humans. Ann. Neurol. 78, 317–322.
39. Westendorp RG, van Heemst D, Rozing MP, Frolich M, Mooijaart SP, Blauw GJ, Beekman M, Heijmans BT, de Craen AJ, Slagboom PE (2009) Nonagenarian siblings and their offspring display lower risk of mortality and morbidity than sporadic nonagenarians: the Leiden Longevity Study. J. Am. Geriatr. Soc. 57, 1634–1637.
40. White WB (2000) Ambulatory blood pressure monitoring: dippers compared with non-dippers. Blood Press Monit. 5(Suppl. 1), S17–S23.
41. Yoshino J, Almeda-Valdes P, Patterson BW, Okunade AL, Imai S, Mittendorfer B, Klein S (2014) Diurnal variation in insulin sensitivity of glucose metabolism is associated with diurnal variations in whole-body and cellular fatty acid metabolism in metabolically normal women. J. Clin. Endocrinol. Metab. 99, E1666–E1670.
42. Zavada A, Gordijn MC, Beersma DG, Daan S, Roenneberg T (2005) Comparison of the Munich chronotype questionnaire with the Horne-Ostberg's morningness-eveningness score. Chronobiol. Int. 22, 267–278.