Genetic basis of inter-individual variability in the effects of exercise on the alleviation of lifestyle-related diseases

Journal of Physiology

Volumn 587, Issue 23, 2009, Pages 5577-5584

  Mori, Masayuki ^a   Higuchi, Keiichi ^a   Sakurai, Akihiro ^b   Tabara, Yasuharu ^c   Miki, Tetsuro ^d   Nose, Hiroshi ^a,e  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Basic Medical Research and Education   (Japan)

^d EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e Jukunen Taiikudaigaku Research Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; AUTOTAXIN; BETA 2 ADRENERGIC RECEPTOR; BETA 3 ADRENERGIC RECEPTOR; CATECHOL METHYLTRANSFERASE; DIPEPTIDYL CARBOXYPEPTIDASE; GUANINE NUCLEOTIDE BINDING PROTEIN; LIPOPROTEIN LIPASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 3;

AEROBIC CAPACITY; BODY MASS; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DNA POLYMORPHISM; DYSLIPIDEMIA; ENZYME ACTIVITY; EXERCISE; EXON; GENETIC PREDISPOSITION; HEREDITY; HUMAN; HYPERTENSION; INDIVIDUALITY; LIFESTYLE; MOLECULAR GENETICS; OBESITY; PHENOTYPE; PREVENTIVE MEDICINE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTOLIC BLOOD PRESSURE; ARTICLE; GENOTYPE; INTERINDIVIDUAL VARIABILITY; SEDENTARY LIFESTYLE; TREATMENT RESPONSE; WALKING;

DYSLIPIDEMIAS; EXERCISE; GENETICS; GENOTYPE; HUMANS; HYPERTENSION; LIFE STYLE; OBESITY; OXYGEN CONSUMPTION; PHYSICAL FITNESS; POLYMORPHISM, GENETIC; WALKING;

EID: 71249105844     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.179283     Document Type: Review

References (44)

1. Andreasen CH, Stender-Petersen KL, Mogensen MS, Torekov SS, Wegner L, Andersen G, Nielsen AL, Albrechtsen A, Borch-Johnsen K, Rasmussen SS, Clausen JO, Sandbaek A, Lauritzen T, Hansen L, Jørgensen T, Pedersen O, Hansen T. Low physical activity accentuates the effect of the FTO rs9939609 polymorphism on body fat accumulation. Diabetes 2008, 57:95-101.
2. Bouchard C, Rankinen T. Individual differences in response to regular physical activity. Med Sci Sports Exerc 2001, 33:S446-S451.
3. Bray MS, Hagberg JM, Perusse L, Rankinen T, Roth SM, Wolfarth B, Bouchard C. The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med Sci Sports Exrc 2009, 41:35-73.
4. Corbalán MS, Marti A, Forga L, Martínez-González MA, Martínez JA. The 27Glu polymorphism of the β2-adrenergic receptor gene interacts with physical activity influencing obesity risk among female subjects. Clin Genet 2002, 61:305-307.
5. Danser AH, Schalekamp MA, Bax WA, Van Den Brink AM, Saxena PR, Riegger GA, Schunkert H. Angiotensin-converting enzyme in the human heart. Effect of the deletion/insertion polymorphism. Circulation 1995, 92:1387-1388.
6. Frayling TM, Timpson NJ, Weedon MN, Zeggini E, Freathy RM, Lindgren CM, Perry JR, Elliott KS, Lango H, Rayner NW, Shields B, Harries LW, Barrett JC, Ellard S, Groves CJ, Knight B, Patch AM, Ness AR, Ebrahim S, Lawlor DA, Ring SM, Ben-Shlomo Y, Jarvelin MR, Sovio U, Bennett AJ, Melzer D, Ferrucci L, Loos RJ, Barroso I, Wareham NJ, Karpe F, Owen KR, Cardon LR, Walker M, Hitman GA, Palmer CN, Doney AS, Morris AD, Smith GD, Hattersley AT, McCarthy MI. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 2007, 316:889-894.
7. Garenc C, Pérusse L, Bergeron J, Gagnon J, Chagnon YC, Borecki IB, Leon AS, Skinner JS, Wilmore JH, Rao DC, Bouchard C. Evidence of LPL gene-exercise interaction for body fat and LPL activity: the HERITAGE family study. J Appl Physiol 2001, 91:1334-1340.
8. Garenc C, Pérusse L, Chagnon YC, Rankinen T, Gagnon J, Borecki IB, Leon AS, Skinner JS, Wilmore JH, Rao DC, Bouchard C. Effects of β2-adrenergic receptor gene variants on adiposity: the HERITAGE Family Study. Obes Res 2003, 11:612-618.
9. Grove ML, Morrison A, Folsom AR, Boerwinkle E, Hoelscher DM, Bray MS. Gene-environment interaction and the GNB3 gene in the Atherosclerosis Risk in Communities study. Int J Obes 2007, 31:919-926.
10. Hagberg JM, Ferrell RE, Dengel DR, Wilund KR. Exercise training-induced blood pressure and plasma lipid improvements in hypertensives may be genotype dependent. Hypertension 1999, 34:18-23.
11. Hawley JA, Holloszy JO. Exercise: it's the real thing!. Nutr Rev 2009, 67:172-178.
12. Kogure A, Yoshida T, Sakane N, Umekawa T, Takakura Y, Kondo M. Synergic effect of polymorphisms in uncoupling protein 1 and β3-adrenergic receptor genes on weight loss in obese Japanese. Diabetologia 1998, 41:1399.
13. Kraus WE, Housmard JA, Duscha BD, Knetzger KJ, Wharton MB, McCartney JS, Bales CW, Henes S, Samsa GP, Otvos JD, Kulkarni KR, Slentz CA. Effects of the amount and intensity of exercise on plasma lipoproteins. N Eng J Med 2002, 347:1438-1492.
14. Lakka TA, Laukkanen JA, Rauramaa R, Salonen R, Lakka HM, Kaplan GA, Salonen JT. Cardiorespiratory fitness and the progression of carotid atherosclerosis in middle-aged men. Ann Intern Med 2001, 134:12-20.
15. Levy D, Ehret GB, Rice K, Verwoert GC, Launer LJ, Dehghan A, Glazer NL, Morrison AC, Johnson AD, Aspelund T, Aulchenko Y, Lumley T, Köttgen A, Vasan RS, Rivadeneira F, Eiriksdottir G, Guo X, Arking DE, Mitchell GF, Mattace-Raso FU, Smith AV, Taylor K, Scharpf RB, Hwang SJ, Sijbrands EJ, Bis J, Harris TB, Ganesh SK, O'Donnell CJ, Hofman A, Rotter JI, Coresh J, Benjamin EJ, Uitterlinden AG, Heiss G, Fox CS, Witteman JC, Boerwinkle E, Wang TJ, Gudnason V, Larson MG, Chakravarti A, Psaty BM, van Duijn CM. Genome-wide association study of blood pressure and hypertension. Nat Genet 2009, 41:677-687.
16. Lindi VI, Uusitupa MI, Lindström J, Louheranta A, Eriksson JG, Valle TT, Hämäläinen H, Ilanne-Parikka P, Keinänen-Kiukaanniemi S, Laakso M, Tuomilehto J. Association of the Pro12Ala polymorphism in the PPAR-γ2 gene with 3-year incidence of type 2 diabetes and body weight change in the Finnish Diabetes Prevention Study. Diabetes 2002, 51:2581-2586.
17. Meirhaeghe A, Helbecque N, Cottel D, Amouyel P. Beta2-adrenoceptor gene polymorphism, body weight, and physical activity. Lancet 1999, 353:896.
18. Montgomery H, Clarkson P, Barnard M, Bell J, Brynes A, Dollery C, Hajnal J, Hemingway H, Mercer D, Jarman P, Marshall R, Prasad K, Rayson M, Saeed N, Talmud P, Thomas L, Jubb M, World M, Humphries S. Angiotensin-converting-enzyme gene insertion/deletion polymorphism and response to physical training. Lancet 1999, 353:541-545.
19. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, Kang H, Shaw RJ, Evans RM. AMPK and PPARδ agonists are exercise mimetics. Cell 2008, 134:405-415.
20. Nemoto K, Gen-no H, Masuki S, Okazaki K, Nose H. Effects of high-intensity interval walking training on physical fitness and blood pressure in middle-aged and older people. Mayo Clin Proc 2007, 82:803-811.
21. Newton-Cheh C, Johnson T, Gateva V, Tobin MD, Bochud M, Coin L, Najjar SS, Zhao JH, Heath SC, Eyheramendy S, Papadakis K, Voight BF, Scott LJ, Zhang F, Farrall M, Tanaka T, Wallace C, Chambers JC, Khaw KT, Nilsson P, Van Der Harst P, Polidoro S, Grobbee DE, Onland-Moret NC, Bots ML, Wain LV, Elliott KS, Teumer A, Luan J, Lucas G, Kuusisto J, Burton PR, Hadley D, McArdle WL, Brown M, Dominiczak A, Newhouse SJ, Samani NJ, Webster J, Zeggini E, Beckmann JS, Bergmann S, Lim N, Song K, Vollenweider P, Waeber G, Waterworth DM, Yuan X, Groop L, Orho-Melander M, Allione A, Di Gregorio A, Guarrera S, Panico S, Ricceri F, Romanazzi V, Sacerdote C, Vineis P, Barroso I, Sandhu MS, Luben RN, Crawford GJ, Jousilahti P, Perola M, Boehnke M, Bonnycastle LL, Collins FS, Jackson AU, Mohlke KL, Stringham HM, Valle TT, Willer CJ, Bergman RN, Morken MA, Döring A, Gieger C, Illig T, Meitinger T, Org E, Pfeufer A, Wichmann HE, Kathiresan S, Marrugat J, O'Donnell CJ, Schwartz SM, Siscovick DS, Subirana I, Freimer NB, Hartikainen AL, McCarthy MI, O'Reilly PF, Peltonen L, Pouta A, de Jong PE, Snieder H, van Gilst WH, Clarke R, Goel A, Hamsten A, Peden JF, Seedorf U, Syvänen AC, Tognoni G, Lakatta EG, Sanna S, Scheet P, Schlessinger D, Scuteri A, Dörr M, Ernst F, Felix SB, Homuth G, Lorbeer R, Reffelmann T, Rettig R, Völker U, Galan P, Gut IG, Hercberg S, Lathrop GM, Zelenika D, Deloukas P, Soranzo N, Williams FM, Zhai G, Salomaa V, Laakso M, Elosua R, Forouhi NG, Völzke H, Uiterwaal CS, Van Der Schouw YT, Numans ME, Matullo G, Navis G, Berglund G, Bingham SA, Kooner JS, Connell JM, Bandinelli S, Ferrucci L, Watkins H, Spector TD, Tuomilehto J, Altshuler D, Strachan DP, Laan M, Meneton P, Wareham NJ, Uda M, Jarvelin MR, Mooser V, Melander O, Loos RJ, Elliott P, Abecasis GR, Caulfield M, Munroe PB. Genome-wide association study identifies eight loci associated with blood pressure. Nat Genet 2009, 41:666-676.
22. Oberbach A, Lehmann S, Kirsch K, Krist J, Sonnabend M, Linke A, Tonjes A, Stumvoll M, Bluher M, Kovacs P. Long-term exercise training decreases interleukin-6 (IL-6) serum levels in subjects with impaired glucose tolerance: effect of the -174G/C variant in IL-6 gene. Eur J Endocrinol 2008, 159:129-136.
23. O'Gorman DJ, Krook A. Exercise and the treatment of diabetes and obesity. Endocrinol Metab Clin North Am 2008, 37:887-903.
24. Orkunoglu-Suer FE, Gordish-Dressman H, Clarkson PM, Thompson PD, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Harmon B, Seip RL, Hoffman EP, Devaney JM. INSIG2 gene polymorphism is associated with increased subcutaneous fat in women and poor response to resistance training in men. BMC Med Genet 2008, 9:117-124.
25. Ostergard T, Ek J, Hamid Y, Saltin B, Pedersen OB, Hansen T, Schmitz O. Influence of the PPAR-γ2 Pro12Ala and ACE I/D polymorphisms on insulin sensitivity and training effects in healthy offspring of type 2 diabetic subjects. Horm Metab Res 2005, 37:99-105.
26. Otabe S, Clement K, Dina C, Pelloux V, Guy-Grand B, Froguel P, Vasseur F. A genetic variation in the 5′ flanking region of the UCP3 gene is associated with body mass index in humans in interaction with physical activity. Diabetologia 2000, 43:245-249.
27. Park S, Han T, Son T, Kang HS. PC-1 genotype and IRS response to exercise training. Int J Sports Med 2008, 29:294-249.
28. Pescatello LS, Franklin BA, Fagard R, Farquhar WB, Kelley GA, Ray CA. American College of Sports Medicine position stand. Exercise and hypertension. Med Sci Sports Exerc 2004, 36:533-553.
29. Phares DA, Halverstadt AA, Shuldiner AR, Ferrell RE, Douglass LW, Ryan AS, Goldberg AP, Hagberg JM. Association between body fat response to exercise training and multilocus ADR genotypes. Obes Res 2004, 12:807-815.
30. Prior SJ, Hagberg JM, Paton CM, Douglass LW, Brown MD, McLenithan JC, Roth SM. DNA sequence variation in the promoter region of the VEGF gene impacts VEGF gene expression and maximal oxygen consumption. Am J Physiol Heart Circ Physiol 2006, 290:H1848-H1855.
31. Rankinen T, Rice T, Leon AS, Skinner JS, Wilmore JH, Rao DC. G protein beta 3 polymorphism and hemodynamic and body composition phenotypes in the HERITAGE Family Study. Physiol Genomics 2002, 8:151-157.
32. Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, Pérusse L, Bouchard C. The human obesity gene map: the 2005 update. Obesity 2006, 14:529-644.
33. Rush JW, Aultman CD. Vascular biology of angiotensin and the impact of physical activity. Appl Physiol Nutr Metab 2008, 33:162-172.
34. Sakane N, Yoshida T, Umekawa T, Kogure A, Kondo M. β2-adrenoreceptor gene polymorphism and obesity. Lancet 1999, 353:1976.
35. Sawada S, Tanaka H, Funakoshi M, Shindo M, Kono S, Ishiko T. Five year prospective study on blood pressure and maximal oxygen uptake. Clin Exp Pharmacol Physiol 1993, 20:483-487.
36. Sawada SS, Lee IM, Muto T, Matuszaki K, Blair SN. Cardiorespiratory fitness and the incidence of type 2 diabetes: prospective study of Japanese men. Diabetes Care 2003, 26:2918-2922.
37. Stefan N, Thamer C, Staiger H, Machicao F, Machann J, Schick F, Venter C, Niess A, Laakso M, Fritsche A, Häring HU. Genetic variations in PPARD and PPARGCIA determine mitochondrial function and change in aerobic physical fitness and insulin sensitivity during lifestyle intervention. J Clin Endocrinol Metab 2007, 92:1827-1833.
38. Thorleifsson G, Walters GB, Gudbjartsson DF, Steinthorsdottir V, Sulem P, Helgadottir A, Styrkarsdottir U, Gretarsdottir S, Thorlacius S, Jonsdottir I, Jonsdottir T, Olafsdottir EJ, Olafsdottir GH, Jonsson T, Jonsson F, Borch-Johnsen K, Hansen T, Andersen G, Jorgensen T, Lauritzen T, Aben KK, Verbeek AL, Roeleveld N, Kampman E, Yanek LR, Becker LC, Tryggvadottir L, Rafnar T, Becker DM, Gulcher J, Kiemeney LA, Pedersen O, Kong A, Thorsteinsdottir U, Stefansson K. Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nat Genet 2008, 41:18-24.
39. Tworoger SS, Chubak J, Aiello EJ, Yasui Y, Ulrich CM, Farin FM, Stapleton PL, Irwin ML, Potter JD, Schwartz RS, McTiernan A. The effect of CYP19 and COMT polymorphisms on exercise-induced fat loss in postmenopausal women. Obes Res 2004, 12:972-981.
40. Uthurralt J, Gordish-Dressman H, Bradbury M, Tesi-Rocha C, Devaney J, Harmon B, Reeves EK, Brandoli C, Hansen BC, Seip RL, Thompson PD, Price TB, Angelopoulos TJ, Clarkson PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Gordon PM, Hoffman EP. PPARα L162V underlies variation in serum triglycerides and subcutaneous fat volume in young males. BMC Med Genet 2007, 8:55.
41. Wei M, Gibbons LW, Mitchell TL, Kampert JB, Lee CD, Blair SN. The association between cardiorespiratory fitness and impaired fasting glucose and type 2 diabetes mellitus in men. Ann Intern Med 1999, 130:89-96.
42. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007, 447:661-678. The Wellcome Trust Case Control Consortium
43. Willer CJ, Speliotes EK, Loos RJ, Li S, Lindgren CM, Heid IM, Berndt SI, Elliott AL, Jackson AU, Lamina C, Lettre G, Lim N, Lyon HN, McCarroll SA, Papadakis K, Qi L, Randall JC, Roccasecca RM, Sanna S, Scheet P, Weedon MN, Wheeler E, Zhao JH, Jacobs LC, Prokopenko I, Soranzo N, Tanaka T, Timpson NJ, Almgren P, Bennett A, Bergman RN, Bingham SA, Bonnycastle LL, Brown M, Burtt NP, Chines P, Coin L, Collins FS, Connell JM, Cooper C, Smith GD, Dennison EM, Deodhar P, Elliott P, Erdos MR, Estrada K, Evans DM, Gianniny L, Gieger C, Gillson CJ, Guiducci C, Hackett R, Hadley D, Hall AS, Havulinna AS, Hebebrand J, Hofman A, Isomaa B, Jacobs KB, Johnson T, Jousilahti P, Jovanovic Z, Khaw KT, Kraft P, Kuokkanen M, Kuusisto J, Laitinen J, Lakatta EG, Luan J, Luben RN, Mangino M, McArdle WL, Meitinger T, Mulas A, Munroe PB, Narisu N, Ness AR, Northstone K, O'Rahilly S, Purmann C, Rees MG, Ridderstråle M, Ring SM, Rivadeneira F, Ruokonen A, Sandhu MS, Saramies J, Scott LJ, Scuteri A, Silander K, Sims MA, Song K, Stephens J, Stevens S, Stringham HM, Tung YC, Valle TT, Van Duijn CM, Vimaleswaran KS, Vollenweider P, Waeber G, Wallace C, Watanabe RM, Waterworth DM, Watkins N, Witteman JC, Zeggini E, Zhai G, Zillikens MC, Altshuler D, Caulfield MJ, Chanock SJ, Farooqi IS, Ferrucci L, Guralnik JM, Hattersley AT, Hu FB, Jarvelin MR, Laakso M, Mooser V, Ong KK, Ouwehand WH, Salomaa V, Samani NJ, Spector TD, Tuomi T, Tuomilehto J, Uda M, Uitterlinden AG, Wareham NJ, Deloukas P, Frayling TM, Groop LC, Hayes RB, Hunter DJ, Mohlke KL, Peltonen L, Schlessinger D, Strachan DP, Wichmann HE, McCarthy MI, Boehnke M, Barroso I, Abecasis GR, Hirschhorn JN. Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nat Genet 2009, 41:25-34.
44. Yoshida T, Sakane N, Umekawa T, Sakai M, Takahashi T, Kondo M. Mutation of β3-adrenergic-receptor gene and resonse to treatment of obesity. Lancet 1995, 346:1433-1434.