Chrono-exercise: Time-of-day-dependent physiological responses to exercise

Hyeon-Ki Kim, Zsolt Radak, Masaki Takahashi, Takayuki Inami, Shigenobu Shibata

Sports Medicine and Health Science ›› 2023, Vol. 5 ›› Issue (1) : 50-58.

Sports Medicine and Health Science ›› 2023, Vol. 5 ›› Issue (1) : 50-58. DOI: 10.1016/j.smhs.2022.11.003
Review

Chrono-exercise: Time-of-day-dependent physiological responses to exercise

Author information +
History +

Abstract

Exercise is an effective strategy to prevent and improve obesity and related metabolic diseases. Exercise increases the metabolic demand in the body. Although many of the metabolic health benefits of exercise depend on skeletal muscle adaptations, exercise exerts many of its metabolic effects through the liver, adipose tissue, and pancreas. Therefore, exercise is the physiological state in which inter-organ signaling is most important. By contrast, circadian rhythms in mammals are associated with the regulation of several physiological and biological functions, including body temperature, sleep-wake cycle, physical activity, hormone secretion, and metabolism, which are controlled by clock genes. Glucose and lipid tolerance reportedly exhibit diurnal variations, being lower in the evening than in the morning. Therefore, the effects of exercise on substrate metabolism at different times of the day may differ. In this review, the importance of exercise timing considerations will be outlined, incorporating a chrono-exercise perspective.

Keywords

Chrono-exercise / Exercise timing / Inter-organ communication / Circadian rhythm / Energy metabolism

Cite this article

Download citation ▾
Hyeon-Ki Kim, Zsolt Radak, Masaki Takahashi, Takayuki Inami, Shigenobu Shibata. Chrono-exercise: Time-of-day-dependent physiological responses to exercise. Sports Medicine and Health Science, 2023, 5(1): 50‒58 https://doi.org/10.1016/j.smhs.2022.11.003

References

[[1]]
R Guthold, GA Stevens, LM Riley, FC Bull. Worldwide trends in insufficient physical activity from 2001 to 2016: a pooled analysis of 358 population-based surveys with 1·9 million participants. Lancet Global Health, 6 (10) ( 2018), pp. e1077-e1086, DOI: 10.1016/s2214-109x(18)30357-7
[[2]]
JM Jakicic, AD Otto. Treatment and prevention of obesity: what is the role of exercise?. Nutr Rev, 64 (2 Pt 2) ( 2006), pp. S57-S61, DOI: 10.1111/j.1753-4887.2006.tb00235.x
[[3]]
WL Haskell, IM Lee, RR Pate, et al.. Physical activity and public health: updated recommendation for adults from the american college of sports medicine and the american heart association. Med Sci Sports Exerc, 39 (8) ( 2007), pp. 1423-1434, DOI: 10.1249/mss.0b013e3180616b27
[[4]]
KM Diaz, D Shimbo. Physical activity and the prevention of hypertension. Curr Hypertens Rep, 15 (6) ( 2013), pp. 659-668, DOI: 10.1007/s11906-013-0386-8
[[5]]
JA Hawley, M Hargreaves, MJ Joyner, JR Zierath. Integrative biology of exercise. Cell, 159 (4) ( 2014), pp. 738-749, DOI: 10.1016/j.cell.2014.10.029
[[6]]
B Egan, JR Zierath. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metabol, 17 (2) ( 2013), pp. 162-184, DOI: 10.1016/j.cmet.2012.12.012
[[7]]
JP Thyfault, A Bergouignan. Exercise and metabolic health: beyond skeletal muscle. Diabetologia, 63 (8) ( 2020), pp. 1464-1474, DOI: 10.1007/s00125-020-05177-6
[[8]]
LS Chow, RE Gerszten, JM Taylor, et al.. Exerkines in health, resilience and disease. Nat Rev Endocrinol, 18 (5) ( 2022), pp. 273-289, DOI: 10.1038/s41574-022-00641-2
[[9]]
MS Bray, ME Young. Circadian rhythms in the development of obesity: potential role for the circadian clock within the adipocyte. Obes Rev, 8 (2) ( 2007), pp. 169-181, DOI: 10.1111/j.1467-789X.2006.00277.x
[[10]]
T Akerstedt, L Levi. Circadian rhythms in the secretion of cortisol, adrenaline and noradrenaline. Eur J Clin Invest, 8 (2) ( 1978), pp. 57-58, DOI: 10.1111/j.1365-2362.1978.tb00811.x
[[11]]
FA Scheer, K Hu, H Evoniuk, et al.. Impact of the human circadian system, exercise, and their interaction on cardiovascular function. Proc Natl Acad Sci U S A, 107 (47) ( 2010), pp. 20541-20546, DOI: 10.1073/pnas.1006749107
[[12]]
SA Rahman, O Castanon-Cervantes, FA Scheer, et al.. Endogenous circadian regulation of pro-inflammatory cytokines and chemokines in the presence of bacterial lipopolysaccharide in humans. Brain Behav Immun, 47 ( 2015), pp. 4-13, DOI: 10.1016/j.bbi.2014.11.003
[[13]]
S Shibata, H Sasaki, Y Ikeda. [chrono-nutrition and chrono-exercise]. Nihon Rinsho, 71 (12) ( 2013), pp. 2194-2199
[[14]]
M Doi. Circadian clock-deficient mice as a tool for exploring disease etiology. Biol Pharm Bull, 35 (9) ( 2012), pp. 1385-1391, DOI: 10.1248/bpb.b12-00364
[[15]]
JA Mohawk, CB Green, JS Takahashi. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci, 35 ( 2012), pp. 445-462, DOI: 10.1146/annurev-neuro-060909-153128
[[16]]
U Schibler, J Ripperger, SA Brown. Peripheral circadian oscillators in mammals: time and food. J Biol Rhythm, 18 (3) ( 2003), pp. 250-260, DOI: 10.1177/0748730403018003007
[[17]]
S Shibata. Neural regulation of the hepatic circadian rhythm. Anat Rec A Discov Mol Cell Evol Biol, 280 (1) ( 2004), pp. 901-909, DOI: 10.1002/ar.a.20095
[[18]]
Y Tahara, S Aoyama, S Shibata. The mammalian circadian clock and its entrainment by stress and exercise. J Physiol Sci, 67 (1) ( 2017), pp. 1-10, DOI: 10.1007/s12576-016-0450-7
[[19]]
S Aoyama, S Shibata.The role of circadian rhythms in muscular and osseous physiology and their regulation by nutrition and exercise. Front Neurosci, 11 ( 2017), p. 63, DOI: 10.3389/fnins.2017.00063
[[20]]
A Balsalobre, SA Brown, L Marcacci, et al.. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science, 289 (5488) ( 2000), pp. 2344-2347, DOI: 10.1126/science.289.5488.2344
[[21]]
SD Jordan, KA Lamia. Ampk at the crossroads of circadian clocks and metabolism. Mol Cell Endocrinol, 366 (2) ( 2013), pp. 163-169, DOI: 10.1016/j.mce.2012.06.017
[[22]]
S Sitaula, J Zhang, F Ruiz, TP Burris. Rev-erb regulation of cholesterologenesis. Biochem Pharmacol, 131 ( 2017), pp. 68-77, DOI: 10.1016/j.bcp.2017.02.006
[[23]]
D Feng, T Liu, Z Sun, et al.. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science, 331 (6022) ( 2011), pp. 1315-1319, DOI: 10.1126/science.1198125
[[24]]
EE Zhang, Y Liu, R Dentin, et al.. Cryptochrome mediates circadian regulation of camp signaling and hepatic gluconeogenesis. Nat Med, 16 (10) ( 2010), pp. 1152-1156, DOI: 10.1038/nm.2214
[[25]]
MD Li, CM Li, Z Wang. The role of circadian clocks in metabolic disease. Yale J Biol Med, 85 (3) ( 2012), pp. 387-401
[[26]]
B Marcheva, KM Ramsey, CB Peek, A Affinati, E Maury, J Bass. Circadian clocks and metabolism. A Kramer, M Merrow ( Handb Exp Pharmacol, Springer (Eds.), Circadian Clocks. 2013), pp. 127-155
[[27]]
RJ Jarrett, H Keen. Diurnal variation of oral glucose tolerance: a possible pointer to the evolution of diabetes mellitus. Br Med J, 2 (5653) ( 1969), pp. 341-344, DOI: 10.1136/bmj.2.5653.341
[[28]]
RJ Jarrett, IA Baker, H Keen, NW Oakley. Diurnal variation in oral glucose tolerance: blood sugar and plasma insulin levels morning, afternoon, and evening. Br Med J, 1 (5794) ( 1972), pp. 199-201, DOI: 10.1136/bmj.1.5794.199
[[29]]
J Wojtczak-Jaroszowa. Physiological and clinical aspects of circadian variations in glucose tolerance. Chronobiologia, 4 (4) ( 1977), pp. 363-384
[[30]]
A Hulmán, K Færch, D Vistisen, et al.. Effect of time of day and fasting duration on measures of glycaemia: analysis from the whitehall ii study. Diabetologia, 56 (2) ( 2013), pp. 294-297, DOI: 10.1007/s00125-012-2770-3
[[31]]
KF Carroll, PJ Nestel. Diurnal variation in glucose tolerance and in insulin secretion in man. Diabetes, 22 (5) ( 1973), pp. 333-348, DOI: 10.2337/diab.22.5.333
[[32]]
T Sonnier, J Rood, JM Gimble, CM Peterson. Glycemic control is impaired in the evening in prediabetes through multiple diurnal rhythms. J Diabet Complicat, 28 (6) ( 2014), pp. 836-843, DOI: 10.1016/j.jdiacomp.2014.04.001
[[33]]
E Van Cauter, KS Polonsky, AJ Scheen. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr Rev, 18 (5) ( 1997), pp. 716-738, DOI: 10.1210/edrv.18.5.0317
[[34]]
GKW Leung, CE Huggins, MP Bonham. Effect of meal timing on postprandial glucose responses to a low glycemic index meal: a crossover trial in healthy volunteers. Clin Nutr, 38 (1) ( 2019), pp. 465-471, DOI: 10.1016/j.clnu.2017.11.010
[[35]]
M Takahashi, M Ozaki, MI Kang, et al.. Effects of meal timing on postprandial glucose metabolism and blood metabolites in healthy adults. Nutrients, 10 (11) ( 2018), p. 1763, DOI: 10.3390/nu10111763
[[36]]
JH O’Keefe, DS Bell. Postprandial hyperglycemia/hyperlipidemia (postprandial dysmetabolism) is a cardiovascular risk factor. Am J Cardiol, 100 (5) ( 2007), pp. 899-904, DOI: 10.1016/j.amjcard.2007.03.107
[[37]]
WF Bremner, RB Sothern, EL Kanabrocki, et al.. Relation between circadian patterns in levels of circulating lipoprotein(a), fibrinogen, platelets, and related lipid variables in men. Am Heart J, 139 (1 Pt 1) ( 2000), pp. 164-173, DOI: 10.1016/s0002-8703(00)90324-7
[[38]]
A Rivera-Coll, X Fuentes-Arderiu, A Díez-Noguera. Circadian rhythmic variations in serum concentrations of clinically important lipids. Clin Chem, 40 (8) ( 1994), pp. 1549-1553
[[39]]
HP Sennels, HL Jørgensen, J Fahrenkrug. Diurnal changes of biochemical metabolic markers in healthy young males - the bispebjerg study of diurnal variations. Scand J Clin Lab Invest, 75 (8) ( 2015), pp. 686-692, DOI: 10.3109/00365513.2015.1080385
[[40]]
LW van Kerkhof, KC Van Dycke, EH Jansen, et al.. Diurnal variation of hormonal and lipid biomarkers in a molecular epidemiology-like setting. PLoS One, 10 (5) ( 2015), p. e0135652, DOI: 10.1371/journal.pone.0135652
[[41]]
D van Moorsel, J Hansen, B Havekes, et al.. Demonstration of a day-night rhythm in human skeletal muscle oxidative capacity. Mol Metabol, 5 (8) ( 2016), pp. 635-645, DOI: 10.1016/j.molmet.2016.06.012
[[42]]
BE Statland, P Winkel, H Bokelund. Factors contributing to intra-individual variation of serum constituents. 2. Effects of exercise and diet on variation of serum constituents in healthy subjects. Clin Chem, 19 (12) ( 1973), pp. 1380-1383
[[43]]
PN Demacker, RW Schade, RT Jansen, A Van ’t Laar. Intra-individual variation of serum cholesterol, triglycerides and high density lipoprotein cholesterol in normal humans. Atherosclerosis, 45 (3) ( 1982), pp. 259-266, DOI: 10.1016/0021-9150(82)90227-1
[[44]]
LK Cella, E Van Cauter, DA Schoeller. Diurnal rhythmicity of human cholesterol synthesis: normal pattern and adaptation to simulated ”jet lag”. Am J Physiol, 269 (3 Pt 1) ( 1995), pp. E489-E498, DOI: 10.1152/ajpendo.1995.269.3.E489
[[45]]
Y Yang, A Creer, B Jemiolo, S Trappe. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol ( 1985), 98 (5) ( 2005), pp. 1745-1752, DOI: 10.1152/japplphysiol.01185.2004
[[46]]
NJ Hoffman, BL Parker, R Chaudhuri, et al.. Global phosphoproteomic analysis of human skeletal muscle reveals a network of exercise-regulated kinases and ampk substrates. Cell Metabol, 22 (5) ( 2015), pp. 922-935, DOI: 10.1016/j.cmet.2015.09.001
[[47]]
D Thompson, F Karpe, M Lafontan, K Frayn. Physical activity and exercise in the regulation of human adipose tissue physiology. Physiol Rev, 92 (1) ( 2012), pp. 157-191, DOI: 10.1152/physrev.00012.2011
[[48]]
VA Cornelissen, B Verheyden, AE Aubert, RH Fagard. Effects of aerobic training intensity on resting, exercise and post-exercise blood pressure, heart rate and heart-rate variability. J Hum Hypertens, 24 (3) ( 2010), pp. 175-182, DOI: 10.1038/jhh.2009.51
[[49]]
SE Kahn, RL Prigeon, DK McCulloch, et al.. Quantification of the relationship between insulin sensitivity and beta-cell function in human subjects. Evidence for a hyperbolic function. Diabetes, 42 (11) ( 1993), pp. 1663-1672, DOI: 10.2337/diab.42.11.1663
[[50]]
L Sylow, M Kleinert, EA Richter, TE Jensen. Exercise-stimulated glucose uptake - regulation and implications for glycaemic control. Nat Rev Endocrinol, 13 (3) ( 2017), pp. 133-148, DOI: 10.1038/nrendo.2016.162
[[51]]
G Fisher, TC Hyatt, GR Hunter, RA Oster, RA Desmond, BA Gower. Effect of diet with and without exercise training on markers of inflammation and fat distribution in overweight women. Obesity, 19 (6) ( 2011), pp. 1131-1136, DOI: 10.1038/oby.2010.310
[[52]]
VJ Vieira, RJ Valentine, KR Wilund, N Antao, T Baynard, JA Woods. Effects of exercise and low-fat diet on adipose tissue inflammation and metabolic complications in obese mice. Am J Physiol Endocrinol Metab, 296 (5) ( 2009), pp. E1164-E1171, DOI: 10.1152/ajpendo.00054.2009
[[53]]
GI Shulman, DL Rothman, T Jue, P Stein, RA DeFronzo, RG Shulman. Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13c nuclear magnetic resonance spectroscopy. N Engl J Med, 322 (4) ( 1990), pp. 223-228, DOI: 10.1056/nejm199001253220403
[[54]]
BK Pedersen, MA Febbraio. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol, 8 (8) ( 2012), pp. 457-465, DOI: 10.1038/nrendo.2012.49
[[55]]
H Ellingsgaard, JA Ehses, EB Hammar, et al.. Interleukin-6 regulates pancreatic alpha-cell mass expansion. Proc Natl Acad Sci U S A, 105 (35) ( 2008), pp. 13163-13168, DOI: 10.1073/pnas.0801059105
[[56]]
H Ellingsgaard, I Hauselmann, B Schuler, et al.. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from l cells and alpha cells. Nat Med, 17 (11) ( 2011), pp. 1481-1489, DOI: 10.1038/nm.2513
[[57]]
HK Kim, M Konishi, M Takahashi, et al.. Effects of acute endurance exercise performed in the morning and evening on inflammatory cytokine and metabolic hormone responses. PLoS One, 10 (9) ( 2015), p. e0137567, DOI: 10.1371/journal.pone.0137567
[[58]]
M Savikj, BM Gabriel, PS Alm, et al.. Afternoon exercise is more efficacious than morning exercise at improving blood glucose levels in individuals with type 2 diabetes: a randomised crossover trial. Diabetologia, 62 (2) ( 2019), pp. 233-237, DOI: 10.1007/s00125-018-4767-z
[[59]]
R Mancilla, B Brouwers, VB Schrauwen-Hinderling, MKC Hesselink, J Hoeks, P Schrauwen.Exercise training elicits superior metabolic effects when performed in the afternoon compared to morning in metabolically compromised humans. Phys Rep, 8 (24) ( 2021), p. e14669, DOI: 10.14814/phy2.14669
[[60]]
T Moholdt, EB Parr, BL Devlin, J Debik, G Giskeødegård, JA Hawley. The effect of morning vs evening exercise training on glycaemic control and serum metabolites in overweight/obese men: a randomised trial. Diabetologia, 64 (9) ( 2021), pp. 2061-2076, DOI: 10.1007/s00125-021-05477-5
[[61]]
HK Kim, S Furuhashi, M Takahashi, et al.. Late-afternoon endurance exercise is more effective than morning endurance exercise at improving 24-h glucose and blood lipid levels. Front Endocrinol, 13 ( 2022), p. 957239, DOI: 10.3389/fendo.2022.957239
[[62]]
AM Gomez, C Gomez, P Aschner, et al.. Effects of performing morning versus afternoon exercise on glycemic control and hypoglycemia frequency in type 1 diabetes patients on sensor-augmented insulin pump therapy. J Diabetes Sci Technol, 9 (3) ( 2015), pp. 619-624, DOI: 10.1177/1932296814566233
[[63]]
H Chtourou, N Souissi. The effect of training at a specific time of day: a review. J Strength Condit Res, 26 (7) ( 2012), pp. 1984-2005, DOI: 10.1519/JSC.0b013e31825770a7
[[64]]
M Küüsmaa, M Schumann, M Sedliak, et al.. Effects of morning versus evening combined strength and endurance training on physical performance, muscle hypertrophy, and serum hormone concentrations. Appl Physiol Nutr Metabol, 41 (12) ( 2016), pp. 1285-1294, DOI: 10.1139/apnm-2016-0271
[[65]]
A Ammar, H Chtourou, N Souissi. Effect of time-of-day on biochemical markers in response to physical exercise. J Strength Condit Res, 31 (1) ( 2017), pp. 272-282, DOI: 10.1519/jsc.0000000000001481
[[66]]
A Basti, M Yalçin, D Herms, et al.. Diurnal variations in the expression of core-clock genes correlate with resting muscle properties and predict fluctuations in exercise performance across the day. BMJ Open Sport Exerc Med, 7 (1) ( 2021), p. e000876, DOI: 10.1136/bmjsem-2020-000876
[[67]]
S Ezagouri, Z Zwighaft, J Sobel, et al.. Physiological and molecular dissection of daily variance in exercise capacity. Cell Metabol, 30 (1) ( 2019), pp. 78-91.e4, DOI: 10.1016/j.cmet.2019.03.012
[[68]]
S Sato, AL Basse, M Schönke, et al.. Time of exercise specifies the impact on muscle metabolic pathways and systemic energy homeostasis. Cell Metabol, 30 (1) ( 2019), pp. 92-110.e4, DOI: 10.1016/j.cmet.2019.03.013
[[69]]
K Burkewitz, Y Zhang, WB Mair. Ampk at the nexus of energetics and aging. Cell Metabol, 20 (1) ( 2014), pp. 10-25, DOI: 10.1016/j.cmet.2014.03.002
[[70]]
DJ Asby, F Cuda, M Beyaert, FD Houghton, FR Cagampang, A Tavassoli. Ampk activation via modulation of de novo purine biosynthesis with an inhibitor of atic homodimerization. Chem Biol, 22 (7) ( 2015), pp. 838-848, DOI: 10.1016/j.chembiol.2015.06.008
[[71]]
JM Corton, JG Gillespie, SA Hawley, DG Hardie. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating amp-activated protein kinase in intact cells?. Eur J Biochem, 229 (2) ( 1995), pp. 558-565, DOI: 10.1111/j.1432-1033.1995.tb20498.x
[[72]]
W Fan, RM Evans. Exercise mimetics: impact on health and performance. Cell Metabol, 25 (2) ( 2017), pp. 242-247, DOI: 10.1016/j.cmet.2016.10.022
[[73]]
VA Narkar, M Downes, RT Yu, et al.. Ampk and ppardelta agonists are exercise mimetics. Cell, 134 (3) ( 2008), pp. 405-415, DOI: 10.1016/j.cell.2008.06.051
[[74]]
MM Mihaylova, RJ Shaw. The ampk signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol, 13 (9) ( 2011), pp. 1016-1023, DOI: 10.1038/ncb2329
[[75]]
H Zouhal, C Jacob, P Delamarche, A Gratas-Delamarche. Catecholamines and the effects of exercise, training and gender. Sports Med, 38 (5) ( 2008), pp. 401-423, DOI: 10.2165/00007256-200838050-00004
[[76]]
HK Kim, M Takahashi, M Konishi, et al.. The effects of acute endurance exercise performed either in the morning or evening on metabolic and hormone responses. Jpn J Clin Sports Med, 22 ( 2014), pp. 497-505
[[77]]
GA Thomas, WJ Kraemer, BA Comstock, C Dunn-Lewis, CM Maresh, JS Volek. Obesity, growth hormone and exercise. Sports Med, 43 (9) ( 2013), pp. 839-849, DOI: 10.1007/s40279-013-0064-7
[[78]]
E Poggiogalle, H Jamshed, CM Peterson. Circadian regulation of glucose, lipid, and energy metabolism in humans. Metabolism, 84 ( 2018), pp. 11-27, DOI: 10.1016/j.metabol.2017.11.017
[[79]]
Y Saito, S Yoshida, N Nakaya, Y Hata, Y Goto. Comparison between morning and evening doses of simvastatin in hyperlipidemic subjects. A double-blind comparative study. Arterioscler Thromb, 11 (4) ( 1991), pp. 816-826, DOI: 10.1161/01.atv.11.4.816
[[80]]
R Plakogiannis, H Cohen. Optimal low-density lipoprotein cholesterol lowering--morning versus evening statin administration. Ann Pharmacother, 41 (1) ( 2007), pp. 106-110, DOI: 10.1345/aph.1G659
[[81]]
XQ Lian, D Zhao, M Zhu, et al.. The influence of regular walking at different times of day on blood lipids and inflammatory markers in sedentary patients with coronary artery disease. Prev Med, 58 ( 2014), pp. 64-69, DOI: 10.1016/j.ypmed.2013.10.020
[[82]]
RL Seip, TJ Angelopoulos, CF Semenkovich. Exercise induces human lipoprotein lipase gene expression in skeletal muscle but not adipose tissue. Am J Physiol, 268 (2 Pt 1) ( 1995), pp. E229-E236, DOI: 10.1152/ajpendo.1995.268.2.E229
[[83]]
MP Arasaradnam, L Morgan, J Wright, R Gama. Diurnal variation in lipoprotein lipase activity. Ann Clin Biochem, 39 (Pt 2) ( 2002), pp. 136-139, DOI: 10.1258/0004563021901883
[[84]]
PJ Arciero, SJ Ives, AE Mohr, et al.. Morning exercise reduces abdominal fat and blood pressure in women; evening exercise increases muscular performance in women and lowers blood pressure in men. Front Physiol, 13 ( 2022), p. 893783, DOI: 10.3389/fphys.2022.893783
[[85]]
K Shimada, Y Yamamoto, K Iwayama, et al.. Effects of post-absorptive and postprandial exercise on 24 h fat oxidation. Metabolism, 62 (6) ( 2013), pp. 793-800, DOI: 10.1016/j.metabol.2012.12.008
[[86]]
Y Izumida, N Yahagi, Y Takeuchi, et al.. Glycogen shortage during fasting triggers liver-brain-adipose neurocircuitry to facilitate fat utilization. Nat Commun, 4 ( 2013), p. 2316, DOI: 10.1038/ncomms3316
[[87]]
JC Hoak, WE Connor, ED Warner. Toxic effects of glucagon-induced acute lipid mobilization in geese. J Clin Invest, 47 (12) ( 1968), pp. 2701-2710, DOI: 10.1172/jci105953
[[88]]
EE Marsh 3rd, J Biller, HP Adams Jr., et al.. Circadian variation in onset of acute ischemic stroke. Arch Neurol, 47 (11) ( 1990), pp. 1178-1180, DOI: 10.1001/archneur.1990.00530110032012
[[89]]
JR Marchesi, DH Adams, F Fava, et al.. The gut microbiota and host health: a new clinical frontier. Gut, 65 (2) ( 2016), pp. 330-339, DOI: 10.1136/gutjnl-2015-309990
[[90]]
RE Ley, PJ Turnbaugh, S Klein, JI Gordon. Microbial ecology: human gut microbes associated with obesity. Nature, 444 (7122) ( 2006), pp. 1022-1023, DOI: 10.1038/4441022a
[[91]]
DR Donohoe, N Garge, X Zhang, et al.. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metabol, 13 (5) ( 2011), pp. 517-526, DOI: 10.1016/j.cmet.2011.02.018
[[92]]
T Okada, S Fukuda, K Hase, et al.. Microbiota-derived lactate accelerates colon epithelial cell turnover in starvation-refed mice. Nat Commun, 4 ( 2013), p. 1654, DOI: 10.1038/ncomms2668
[[93]]
J Qin, Y Li, Z Cai, et al.. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature, 490 (7418) ( 2012), pp. 55-60, DOI: 10.1038/nature11450
[[94]]
LJ Mailing, JM Allen, TW Buford, CJ Fields, JA Woods. Exercise and the gut microbiome: a review of the evidence, potential mechanisms, and implications for human health. Exerc Sport Sci Rev, 47 (2) ( 2019), pp. 75-85, DOI: 10.1249/jes.0000000000000183
[[95]]
JM Allen, LJ Mailing, GM Niemiro, et al.. Exercise alters gut microbiota composition and function in lean and obese humans. Med Sci Sports Exerc, 50 (2) ( 2018), pp. 747-757, DOI: 10.1249/mss.0000000000001495
[[96]]
H Sasaki, H Miyakawa, A Watanabe, et al.. Evening rather than morning increased physical activity alters the microbiota in mice and is associated with increased body temperature and sympathetic nervous system activation. Biochim Biophys Acta, Mol Basis Dis, 1868 (6) ( 2022), p. 166373, DOI: 10.1016/j.bbadis.2022.166373
[[97]]
G Tolhurst, H Heffron, YS Lam, et al.. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein-coupled receptor ffar2. Diabetes, 61 (2) ( 2012), pp. 364-371, DOI: 10.2337/db11-1019
[[98]]
SK Malin, ME Francois, NZM Eichner, et al.. Impact of short-term exercise training intensity on β-cell function in older obese adults with prediabetes. J Appl Physiol ( 1985), 125 (6) ( 2018), pp. 1979-1986, DOI: 10.1152/japplphysiol.00680.2018
[[99]]
E Trefts, AS Williams, DH Wasserman. Exercise and the regulation of hepatic metabolism. Prog Mol Biol Transl Sci, 135 ( 2015), pp. 203-225, DOI: 10.1016/bs.pmbts.2015.07.010
[[100]]
C Hu, M Hoene, P Plomgaard, et al.. Muscle-liver substrate fluxes in exercising humans and potential effects on hepatic metabolism. J Clin Endocrinol Metab, 105 (4) ( 2020), pp. 1196-1209, DOI: 10.1210/clinem/dgz266
[[101]]
K Karstoft, BK Pedersen. Skeletal muscle as a gene regulatory endocrine organ. Curr Opin Clin Nutr Metab Care, 19 (4) ( 2016), pp. 270-275, DOI: 10.1097/mco.0000000000000283
[[102]]
B Ingerslev, JS Hansen, C Hoffmann, et al.. Angiopoietin-like protein 4 is an exercise-induced hepatokine in humans, regulated by glucagon and camp. Mol Metabol, 6 (10) ( 2017), pp. 1286-1295, DOI: 10.1016/j.molmet.2017.06.018
[[103]]
H Misu, H Takayama, Y Saito, et al.. Deficiency of the hepatokine selenoprotein p increases responsiveness to exercise in mice through upregulation of reactive oxygen species and amp-activated protein kinase in muscle. Nat Med, 23 (4) ( 2017), pp. 508-516, DOI: 10.1038/nm.4295
[[104]]
MG Browning, J Khoraki, JH DeAntonio, et al.. Protective effect of black relative to white race against non-alcoholic fatty liver disease in patients with severe obesity, independent of type 2 diabetes. Int J Obes, 42 (4) ( 2018), pp. 926-929, DOI: 10.1038/ijo.2017.309
[[105]]
E Fabbrini, F Magkos, BS Mohammed, et al.. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci U S A, 106 (36) ( 2009), pp. 15430-15435, DOI: 10.1073/pnas.0904944106
[[106]]
H Ando, T Takamura, N Matsuzawa-Nagata, et al.. Clock gene expression in peripheral leucocytes of patients with type 2 diabetes. Diabetologia, 52 (2) ( 2009), pp. 329-335, DOI: 10.1007/s00125-008-1194-6
[[107]]
P Gómez-Abellán, JJ Hernández-Morante, JA Luján, JA Madrid, M Garaulet. Clock genes are implicated in the human metabolic syndrome. Int J Obes, 32 (1) ( 2008), pp. 121-128, DOI: 10.1038/sj.ijo.0803689
[[108]]
G Wolff, KA Esser. Scheduled exercise phase shifts the circadian clock in skeletal muscle. Med Sci Sports Exerc, 44 (9) ( 2012), pp. 1663-1670, DOI: 10.1249/MSS.0b013e318255cf4c
[[109]]
H Sasaki, Y Hattori, Y Ikeda, et al.. Forced rather than voluntary exercise entrains peripheral clocks via a corticosterone/noradrenaline increase in per2::Luc mice. Sci Rep, 6 ( 2016), p. 27607, DOI: 10.1038/srep27607
[[110]]
Y Tanaka, H Ogata, M Kayaba, et al.. Effect of a single bout of exercise on clock gene expression in human leukocyte. J Appl Physiol ( 1985), 128 (4) ( 2020), pp. 847-854, DOI: 10.1152/japplphysiol.00891.2019
[[111]]
AC Zambon, EL McDearmon, N Salomonis, et al.. Time- and exercise-dependent gene regulation in human skeletal muscle. Genome Biol, 4 (10) ( 2003), p. R61, DOI: 10.1186/gb-2003-4-10-r61
[[112]]
M Takahashi, A Haraguchi, Y Tahara, et al.. Positive association between physical activity and per 3 expression in older adults. Sci Rep, 7 ( 2017), p. 39771, DOI: 10.1038/srep39771

This work was supported by the Japan Society for the Promotion of Science (KAKENHI grant numbers 20K19689 and 18K17940 to H.-K. K. and 19H01089 to S.S.) and the JST-Mirai Program (grant number JMPJM120D5) to S.S.

Accesses

Citations

Detail

Sections
Recommended

/