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Lifetime regular exercise affects the incident of different arrhythmias and improves organismal health in aging female Drosophila melanogaster

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Abstract

We used Drosophila melanogaster as an animal model system to study the impact of exercise training initiated early in life on cardiac function using a well-established model of inherent myogenic properties of the heart and discussed the changes on myosin, a myocardial contractile protein. We also explored the effect of early physical exercise on organismal aging by analyzing the wake–sleep pattern using a Drosophila activity monitor system. We found that a variety of arrhythmias are part of the heart spectrum in old flies after a lifetime of physical exercise as evidenced by reducing the incidence of fibrillations and increasing the occurrence of bradycardias. Maintenance of myocardial myosin levels may be an underlying contributor to these exercise-induced improvements in cardiac function at an advanced age. Moreover, we found that exercise training resulted in improved sleep quality by ameliorating age-related sleep inefficiency, fragmentation and sleep consolidation.

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References

  • Andersen LB, Riddoch C, Kriemler S, Hills AP (2011) Physical activity and cardiovascular risk factors in children. Br J Sports Med 45:871–876

    Article  PubMed  Google Scholar 

  • Andretic R, Shaw PJ (2005) Essentials of sleep recordings in Drosophila: moving beyond sleep time. Methods Enzymol 393:759–772

    Article  PubMed  Google Scholar 

  • Bhella PS, Hastings JL, Fujimoto N, Shibata S, Carrick-Ranson G, Palmer MD, Boyd KN, Adams-Huet B, Levine BD (2014) Impact of lifelong exercise “dose” on left ventricular compliance and distensibility. J Am Coll Cardiol 64:1257–1266

    Article  PubMed  PubMed Central  Google Scholar 

  • Boyett MR, D’Souza A, Zhang H, Morris GM, Dobrzynski H, Monfredi O (2013) Viewpoint: is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol 114:1351–1355

    Article  CAS  PubMed  Google Scholar 

  • Bugge A, El-Naaman B, McMurray RG, Froberg K, Andersen LB (2013) Tracking of clustered cardiovascular disease risk factors from childhood to adolescence. Pediatr Res 73:245–249

    Article  PubMed  Google Scholar 

  • Cammarato A, Dambacher CM, Knowles AF, Kronert WA, Bodmer R, Ocorr K, Bernstein SI (2008) Myosin transducer mutations differentially affect motor function, myofibril structure, and the performance of skeletal and cardiac muscles. Mol Biol Cell 19:553–562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G (2005) Reduced sleep in Drosophila Shaker mutants. Nature 434:1087–1092

    Article  CAS  PubMed  Google Scholar 

  • D’Andrea A, Riegler L, Cocchia R, Scarafile R, Salerno G, Gravino R, Golia E, Vriz O, Citro R, Limongelli G, Calabrò P, Di Salvo G, Caso P, Russo MG, Bossone E, Calabrò R (2010) Left atrial volume index in highly trained athletes. Am Heart J 159:1155–1161

    Article  PubMed  Google Scholar 

  • den Hoed M, Eijgelsheim M, Esko T et al (2013) Identification of heart rate–associated loci and their effects on cardiac conduction and rhythm disorders. Nat Genet 45:621–631

    Article  Google Scholar 

  • DiMenna FJ, Jones AM (2016) Cardiorespiratory control of exercise and adaptation to training. In: Jeffireys I, Moody J (eds) Strength and conditioning for sports performance. Routledge, New York, pp 92–117

    Google Scholar 

  • D’Souza A, Bucchi A, Johnsen AB, Logantha SJ, Monfredi O, Yanni J, Prehar S, Hart G, Cartwright E, Wisloff U, Dobryznski H, DiFrancesco D, Morris GM, Boyett MR (2014) Exercise training reduces resting heart rate via downregulation of the funny channel HCN4. Nat Commun 5:3775

    PubMed  PubMed Central  Google Scholar 

  • Duffy JF, Czeisler CA (2002) Age-related change in the relationship between circadian period, circadian phase, and diurnal preference in humans. Neurosci Lett 318:117–120

    Article  CAS  PubMed  Google Scholar 

  • Fink M, Callol-Massot C, Chu A, Ruiz-Lozano P, Izpisua Belmonte JC, Giles W, Bodmer R, Ocorr K (2009) A new method for detection and quantification of heartbeat parameters in Drosophila, zebrafish, and embryonic mouse hearts. Biotechniques 46:101–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanson MA, Gluckman PD (2014) Early developmental conditioning of later health and disease: physiology orpathophysiology? Physiol Rev 94(4):1027–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan S, Dauvilliers Y, Mongrain V, Franken P, Tafti M (2012) Age-related changes in sleep in inbred mice are genotype dependent. Neurobiol Aging 33(195):e13–e26

    Google Scholar 

  • Heidbüchel H, Hoogsteen J, Fagard R, Vanhees L, Ector H, Willems R, Van Lierde J (2003) High prevalence of right ventricular involvement in endurance athletes with ventricular arrhythmias. Role of an electrophysiologic study in risk stratification. Eur Heart J 24:1473–1480

    Article  PubMed  Google Scholar 

  • Kaushik G, Fuhrmann A, Cammarato A, Engler AJ (2011) In situ mechanical analysis of myofibrillar perturbation and aging on soft, bilayered Drosophila myocardium. Biophys J 101:2629–2637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kavey RE, Daniels SR, Lauer RM, Atkins DL, Hayman LL, Taubert K (2003) American Heart Association guidelines for primary prevention of atherosclerotic cardiovascular disease beginning in childhood. J Pediatr 142:368–372

    Article  PubMed  Google Scholar 

  • Kemi OJ, Ellingsen O, Smith GL, Wisloff U (2008) Exercise-induced changes in calcium handling in left ventricular cardiomyocytes. Front Biosci 13:356–368

    Article  CAS  PubMed  Google Scholar 

  • Koh K, Evans JM, Hendricks JC, Sehgal A (2006) A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci U S A 103:13843–13847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondratova AA, Kondratov RV (2012) The circadian clock and pathology of the ageing brain. Nat Rev Neurosci 13(5):325–335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leise TL, Harrington ME, Molyneux PC, Song I, Queenan H, Zimmerman E, Lall GS, Biello SM (2013) Voluntary exercise can strengthen the circadian system in aged mice. Age (Dordr). 35(6):2137–2152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindblom R, Ververis K, Tortorella SM, Karagiannis TC (2015) The early life origin theory in the development of cardiovascular disease and type 2 diabetes. Mol Biol Rep 42(4):791–797

    Article  CAS  PubMed  Google Scholar 

  • Linke A, Adams V, Schulze PC, Erbs S, Gielen S, Fiehn E, Möbius-Winkler S, Schubert A, Schuler G, Hambrecht R (2005) Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation 111:1763–1770

    Article  CAS  PubMed  Google Scholar 

  • Luo W, Chen WF, Yue Z, Chen D, Sowcik M, Sehgal A, Zheng X (2012) Old flies have a robust central oscillator but weaker behavioral rhythms that can be improved by genetic and environmental manipulations. Aging Cell 11(3):428–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maron BJ, Pelliccia A (2006) The heart of trained athletes: cardiac remodeling and the risks of sports, including sudden death. Circulation 114:1633–1644

    Article  PubMed  Google Scholar 

  • Matusik P, Malecka-Tendera E (2011) Overweight prevention strategies in preschool children. Int J Pediatr Obes 2:2–5

    Article  Google Scholar 

  • Melkani GC, Bodmer R, Ocorr K, Bernstein SI (2011) The UNC-45 chaperone is critical for establishing myosin-based myofibrillar organization and cardiac contractility in the Drosophila heart model. PLoS ONE 6:e22579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitnitski AB, Graham JE, Mogilner AJ, Rockwood K (2002) Frailty, fitness and late-life mortality in relation to chronological and biological age. BMC Geriatr 2:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Morita H, Nagai R, Seidman JG, Seidman CE (2010) Sarcomere gene mutations in hypertrophy and heart failure. J Cardiovasc Transl Res 3:297–303

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy MO, Cohn DM, Loria AS (2016) Developmental origins of cardiovascular disease: impact of early life stress in humans and rodents. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2016.07.018

    Google Scholar 

  • Nishimura M, Ocorr K, Bodmer R, Cartry J (2011) Drosophila as a model to study cardiac aging. Exp Gerontol 46:326–330

    Article  CAS  PubMed  Google Scholar 

  • O’Dwyer MV, Fairclough SJ, Knowles Z, Stratton G (2012) Effect of a family focused active play intervention on sedentary time and physical activity in preschool children. Int J Behav Nutr Phys Act 9:117

    Article  PubMed  PubMed Central  Google Scholar 

  • Ocorr K, Reeves NL, Wessells RJ, Fink M, Chen HS, Akasaka T, Yasuda S, Metzger JM, Giles W, Posakony JW, Bodmer R (2007) KCNQ potassium channel mutations cause cardiac arrhythmias in Drosophila that mimic the effects of aging. Proc Natl Acad Sci U S A 104:3943–3948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ocorr K, Fink M, Cammarato A, Bernstein S, Bodmer R (2009) Semi-automated optical heartbeat analysis of small hearts. J Vis Exp. doi:10.3791/1435

    Google Scholar 

  • Pandi-Perumal SR, Seils LK, Kayumov L, Ralph MR, Lowe A, Moller H, Swaab DF (2002) Senescence, sleep, and circadian rhythms. Ageing Res Rev 1:559–604

    Article  CAS  PubMed  Google Scholar 

  • Pelliccia A, Culasso F, Di Paolo FM, Maron BJ (1999) Physiologic left ventricular cavity dilatation in elite athletes. Ann Intern Med 130:23–31

    Article  CAS  PubMed  Google Scholar 

  • Piazza N, Gosangi B, Devilla S, Arking R, Wessells R (2009) Exercise-training in young Drosophila melanogaster reduces age-related decline in mobility and cardiac performance. PLoS ONE 4:e5886

    Article  PubMed  PubMed Central  Google Scholar 

  • Piccini JP, Hammill BG, Sinner MF, Jensen PN, Hernandez AF, Heckbert SR, Benjamin EJ, Curtis LH (2012) Incidence and prevalence of atrial fibrillation and associated mortality among Medicare beneficiaries, 1993–2007. Circ Cardiovasc Qual Outcomes 5:85–93

    Article  PubMed  PubMed Central  Google Scholar 

  • Rakshit K, Krishnan N, Guzik EM, Pyza E, Giebultowicz JM (2012) Effects of aging on the molecular circadian oscillations in Drosophila. Chronobiol Int 29(1):5–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakshit K, Wambua R, Giebultowicz TM, Giebultowicz JM (2013) Effects of exercise on circadian rhythms and mobility in aging Drosophila melanogaster. Exp Gerontol 48(11):1260–1265

    Article  PubMed  PubMed Central  Google Scholar 

  • Santoro A, Alvino F, Antonelli G, Caputo M, Padeletti M, Lisi M, Mondillo S (2014) Endurance and strength athlete’s heart: analysis of myocardial deformation by speckle tracking echocardiography. J Cardiovasc Ultrasound 22:196–204

    Article  PubMed  PubMed Central  Google Scholar 

  • Seugnet L, Suzuki Y, Thimgan M, Donlea J, Gimbel SI, Gottschalk L, Duntley SP, Shaw PJ (2009) Identifying sleep regulatory genes using a Drosophila model of insomnia. J Neurosci 29:7148–7157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837

    Article  CAS  PubMed  Google Scholar 

  • Skouteris H, McCabe M, Swinburn B, Hill B (2010) Healthy eating and obesity prevention for preschoolers: a randomised controlled trial. BMC Public Health 10:220

    Article  PubMed  PubMed Central  Google Scholar 

  • Sujkowski A, Saunders S, Tinkerhess M, Piazza N, Jennens J, Healy L, Zheng L, Wessells R (2012) dFatp regulates nutrient distribution and long-term physiology in Drosophila. Aging Cell 11:921–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swank DM, Wells L, Kronert WA, Morrill GE, Bernstein SI (2000) Determining structure/function relationships for sarcomeric myosin heavy chain by genetic and transgenic manipulation of Drosophila. Microsc Res Tech 50:430–442

    Article  CAS  PubMed  Google Scholar 

  • Tinkerhess MJ, Healy Lindsey, Morgan Matthew, Sujkowski Alyson, Matthys Erin, Zheng Li, Wessells Robert J (2012) The Drosophila PGC-1a homolog spargel modulates the physiological effects of endurance exercise. PLoS ONE 7(2):e31633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsoutsman T, Bagnall RD, Semsarian C (2008) Impact of multiple gene mutations in determining the severity of cardiomyopathy and heart failure. Clin Exp Pharmacol Physiol 35:1349–1357

    Article  CAS  PubMed  Google Scholar 

  • Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave R, Atkinson G, George K (2013) Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete’s heart. Heart 99:1727–1733

    Article  PubMed  Google Scholar 

  • Wessells RJ, Bodmer R (2007) Age-related cardiac deterioration: insights from Drosophila. Front Biosci 12:39–48

    Article  CAS  PubMed  Google Scholar 

  • Wolf MJ, Rockman HA (2008) Drosophila melanogaster as a model system for genetics of postnatal cardiac function. Drug Discov Today Dis Models 5:117–123

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolf MJ, Amrein H, Izatt JA, Choma MA, Reedy MC, Rockman HA (2006) Drosophila as a model for the identification of genes causing adult human heart disease. Proc Natl Acad Sci U.S.A 103:1394–1399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanaka Y, Hashimoto S, Tanahashi Y, Nishide SY, Honma S, Honma K (2010) Physical exercise accelerates reentrainment of human sleep–wake cycle but not of plasma melatonin rhythm to 8-h phase-advanced sleep schedule. Am J Physiol Regul Integr Comp Physiol 298(3):R681–R691

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Feng Y, Wen DT, Wang H, Wu XS (2015) Fatiguing exercise initiated later in life reduces incidence of fibrillation and improves sleep quality in Drosophila. Age (Dordr) 37(4):9816

    Article  Google Scholar 

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Acknowledgements

We thank Karen Ocorr and Rolf Bodmer for generously providing semiautomated optical heartbeat analysis program.

Funding

This research was supported by grants from National Natural Science Foundation of China (Grant No. 31671243) and Research Fund for the Doctoral Program of Higher Education of China (Grant No. 20134306110009).

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Authors and Affiliations

  1. Key Laboratory of Physical Fitness and Exercise Rehabilitation of Hunan Province, Hunan Normal University, Changsha, Hunan Province, China

    Lan Zheng, Qiu Fang Li, Liu Ni, Hui Wang & Xiang Cheng Ruan

  2. Heart Development Center, Hunan Normal University, Changsha, Hunan Province, China

    Xiu Shan Wu

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  1. Lan Zheng
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  2. Qiu Fang Li
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  3. Liu Ni
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Correspondence to Lan Zheng.

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Zheng, L., Li, Q.F., Ni, L. et al. Lifetime regular exercise affects the incident of different arrhythmias and improves organismal health in aging female Drosophila melanogaster . Biogerontology 18, 97–108 (2017). https://doi.org/10.1007/s10522-016-9665-5

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