Potential clinical translation of juvenile rodent inactivity models to study the onset of childhood obesity

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 3, 2012, Pages 247-258

  Roberts, Michael D ^a   Company, Joseph M ^a   Brown, Jacob D ^a   Toedebusch, Ryan G ^a   Padilla, Jaume ^a   Jenkins, Nathan T ^a   Harold Laughlin, M ^a,b,c   Booth, Frank W ^a,b,c,d  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d University of Missouri   (United States)

Author keywords

Juvenile obesity; Primordial prevention; Rodent model

Indexed keywords

ANIMAL MODEL; CAUSE OF DEATH; CHILDHOOD DISEASE; CHILDHOOD OBESITY; DIET; HUMAN; IMMOBILIZATION; INSULIN RESISTANCE; MORTALITY; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHYSICAL ACTIVITY; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; RISK FACTOR; RODENT; SEDENTARY LIFESTYLE; VASCULAR DISEASE;

ANIMALS; CHILD; DISEASE MODELS, ANIMAL; HOMEOSTASIS; HUMANS; OBESITY; PHYSICAL CONDITIONING, ANIMAL; RATS; REPRODUCIBILITY OF RESULTS; RISK FACTORS; SEDENTARY LIFESTYLE;

EID: 84865639531     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00167.2012     Document Type: Review

References (81)

1. Adams N, Boice R. A longitudinal study of dominance in an outdoor colony of domestic rats. J Comp Psychol 97: 24-33, 1983.
2. Angevaren M, Aufdemkampe G, Verhaar HJ, Aleman A, Vanhees L. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 3: CD005381, 2008.
3. Arciero PJ, Smith DL, Calles-Escandon J. Effects of short-term inactivity on glucose tolerance, energy expenditure, and blood flow in trained subjects. J Appl Physiol 84: 1365-1373, 1998.
4. Balagopal PB, de Ferranti SD, Cook S, Daniels SR, Gidding SS, Hayman LL, McCrindle BW, Mietus-Snyder ML, Steinberger J. Nontraditional risk factors and biomarkers for cardiovascular disease: mechanistic, research, and clinical considerations for youth: a scientific statement from the American Heart Association. Circulation 123: 2749-2769, 2011.
5. Barash IA, Bang ML, Mathew L, Greaser ML, Chen J, Lieber RL. Structural and regulatory roles of muscle ankyrin repeat protein family in skeletal muscle. Am J Physiol Cell Physiol 293: C218-C227, 2007.
6. Barash IA, Mathew L, Lahey M, Greaser ML, Lieber RL. Muscle LIM protein plays both structural and functional roles in skeletal muscle. Am J Physiol Cell Physiol 289: C1312-C1320, 2005.
7. Belgrano A, Rakicevic L, Mittempergher L, Campanaro S, Martinelli VC, Mouly V, Valle G, Kojic S, Faulkner G. Multi-tasking role of the mechanosensing protein Ankrd2 in the signaling network of striated muscle. PLos One 6: e25519, 2011.
8. Benton MJ, Whyte MD, Dyal BW. Sarcopenic obesity: strategies for management. Am J Nurs 111: 38-44; quiz 45-36, 2011.
9. Booth FW, Gordon SE, Carlson CJ, Hamilton MT. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol 88: 774-787, 2000.
10. Burstein R, Polychronakos C, Toews CJ, MacDougall JD, Guyda HJ, Posner BI. Acute reversal of the enhanced insulin action in trained athletes. Association with insulin receptor changes. Diabetes 34: 756-760, 1985.
11. Centers for Disease Control, and Prevention. Data and Statistics: Obesity Rates Among All Children in the United States. http:// www.cdc.gov/obesity/childhood/data.html.
12. Chironi GN, Boulanger CM, Simon A, Dignat-George F, Freyssinet JM, Tedgui A. Endothelial microparticles in diseases. Cell Tissue Res 335: 143-151, 2009.
13. Church TS, Thomas DM, Tudor-Locke C, Katzmarzyk PT, Earnest CP, Rodarte RQ, Martin CK, Blair SN, Bouchard C. Trends over 5 decades in US. Occupation-related physical activity and their associations with obesity. PLos One 6: e19657, 2011.
14. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61: 1166-1170, 2006.
15. Dulloo AG. Adipose tissue plasticity in catch-up-growth trajectories to metabolic syndrome: hyperplastic versus hypertrophic catch-up fat. Diabetes 58: 1037-1039, 2009.
16. Eaton SB, Konner M. Paleolithic nutrition. A consideration of its nature and current implications. N Engl J Med 312: 283-289, 1985.
17. 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 316: 889-894, 2007.
18. Freedman DS, Khan LK, Dietz WH, Srinivasan SR, Berenson GS. Relationship of childhood obesity to coronary heart disease risk factors in adulthood: the Bogalusa Heart Study. Pediatrics 108: 712-718, 2001.
19. Haram PM, Adams V, Kemi OJ, Brubakk AO, Hambrecht R, Elling-sen O, Wisloff U. Time-course of endothelial adaptation following acute and regular exercise. Eur J Cardiovasc Prev Rehabil 13: 585-591, 2006.
20. Harms SJ, Hickson RC. Skeletal muscle mitochondria and myoglobin, endurance, and intensity of training. J Appl Physiol 54: 798-802, 1983.
21. Heath GW, Gavin JR, 3rd, Hinderliter JM, Hagberg JM, Bloomfield SA, Holloszy JO. Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity. J Appl Physiol 55: 512-517, 1983.
22. Hickson RC. Skeletal muscle cytochrome c and myoglobin, endurance, and frequency of training. J Appl Physiol 51: 746-749, 1981.
23. Hinney A, Nguyen TT, Scherag A, Friedel S, Bronner G, Muller TD, Grallert H, Illig T, Wichmann HE, Rief W, Schafer H, Hebebrand J. Genome wide association (GWA) study for early onset extreme obesity supports the role of fat mass and obesity associated gene (FTO) variants. PLos One 2: e1361, 2007.
24. Hopkins SA, Cutfield WS. Exercise in pregnancy: weighing up the long-term impact on the next generation. Exerc Sport Sci Rev 39: 120-127, 2011.
25. Houmard JA, Shinebarger MH, Dolan PL, Leggett-Frazier N, Bruner RK, McCammon MR, Israel RG, Dohm GL. Exercise training increases GLUT-4 protein concentration in previously sedentary middle-aged men. Am J Physiol Endocrinol Metab 264: E896-E901, 1993.
26. Houmard JA, Tanner CJ, Slentz CA, Duscha BD, McCartney JS, Kraus WE. Effect of the volume and intensity of exercise training on insulin sensitivity. J Appl Physiol 96: 101-106, 2004.
27. Jenkins NT, Landers RQ, Thakkar SR, Fan X, Brown MD, Prior SJ, Spangenburg EE, Hagberg JM. Prior endurance exercise prevents postprandial lipaemia-induced increases in reactive oxygen species in circulating CD31+ cells. J Physiol 589: 5539-5553, 2011.
28. Kilpelainen TO, Qi L, Brage S, Sharp SJ, Sonestedt E, Demerath E, Ahmad T, Mora S, Kaakinen M, Sandholt CH, Holzapfel C, Auten-rieth CS, Hypponen E, Cauchi S, He M, Kutalik Z, Kumari M, Stancakova A, Meidtner K, Balkau B, Tan JT, Mangino M, Timpson NJ, Song Y, Zillikens MC, Jablonski KA, Garcia ME, Johansson S, Bragg-Gresham JL, Wu Y, van Vliet-Ostaptchouk JV, Onland-Moret NC, Zimmermann E, Rivera NV, Tanaka T, Stringham HM, Silber-nagel G, Kanoni S, Feitosa MF, Snitker S, Ruiz JR, Metter J, Larrad MT, Atalay M, Hakanen M, Amin N, Cavalcanti-Proenca C, Gront-ved A, Hallmans G, Jansson JO, Kuusisto J, Kahonen M, Lutsey PL, Nolan JJ, Palla L, Pedersen O, Perusse L, Renstrom F, Scott RA, Shungin D, Sovio U, Tammelin TH, Ronnemaa T, Lakka TA, Uus-itupa M, Rios MS, Ferrucci L, Bouchard C, Meirhaeghe A, Fu M, Walker M, Borecki IB, Dedoussis GV, Fritsche A, Ohlsson C, Boehnke M, Bandinelli S, van Duijn CM, Ebrahim S, Lawlor DA, Gudnason V, Harris TB, Sorensen TI, Mohlke KL, Hofman A, Uit-terlinden AG, Tuomilehto J, Lehtimaki T, Raitakari O, Isomaa B, Njolstad PR, Florez JC, Liu S, Ness A, Spector TD, Tai ES, Froguel P, Boeing H, Laakso M, Marmot M, Bergmann S, Power C, Khaw KT, Chasman D, Ridker P, Hansen T, Monda KL, Illig T, Jarvelin MR, Wareham NJ, Hu FB, Groop LC, Orho-Melander M, Ekelund U, Franks PW, Loos RJ. Physical activity attenuates the influence of FTO variants on obesity risk: a meta-analysis of 218,166 adults and 19,268 children. PLoS Med 8: e1001116, 2011.
29. Krogh-Madsen R, Thyfault JP, Broholm C, Mortensen OH, Olsen RH, Mounier R, Plomgaard P, van Hall G, Booth FW, Pedersen BK. A 2-wk reduction of ambulatory activity attenuates peripheral insulin sensitivity. J Appl Physiol 108: 1034-1040, 2010.
30. Kump DS, Booth FW. Alterations in insulin receptor signalling in the rat epitrochlearis muscle upon cessation of voluntary exercise. J Physiol 562: 829-838, 2005.
31. Kump DS, Booth FW. Sustained rise in triacylglycerol synthesis and increased epididymal fat mass when rats cease voluntary wheel running. J Physiol 565: 911-925, 2005.
32. Kump DS, Laye MJ, Booth FW. Increased mitochondrial glycerol-3-phosphate acyltransferase protein and enzyme activity in rat epididymal fat upon cessation of wheel running. Am J Physiol Endocrinol Metab 290: E480-E489, 2006.
33. Laitakari J, Vuori I, Oja P. Is long-term maintenance of health-related physical activity possible? An analysis of concepts and evidence. Health Educ Res 11: 463-477, 1996.
34. Laye MJ, Rector RS, Borengasser SJ, Naples SP, Uptergrove GM, Ibdah JA, Booth FW, Thyfault JP. Cessation of daily wheel running differentially alters fat oxidation capacity in liver, muscle, and adipose tissue. J Appl Physiol 106: 161-168, 2009.
35. Laye MJ, Thyfault JP, Stump CS, Booth FW. Inactivity induces increases in abdominal fat. J Appl Physiol 102: 1341-1347, 2007.
36. Lee CD, Blair SN, Jackson AS. Cardiorespiratory fitness, body composition, and all-cause and cardiovascular disease mortality in men. Am J Clin Nutr 69: 373-380, 1999.
37. Lee DC, Artero EG, Sui X, Blair SN. Mortality trends in the general population: the importance of cardiorespiratory fitness. J Psychopharma-col (Oxf) 24: 27-35, 2010.
38. Maclean PS, Bergouignan A, Cornier MA, Jackman MR. Biology's response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 301: R581-R600, 2011.
39. Maffeis C, Zaffanello M, Pinelli L, Schutz Y. Total energy expenditure and patterns of activity in 8-10-year-old obese and nonobese children. J Pediatr Gastroenterol Nutr 23: 256-261, 1996.
40. Maffeis C, Zaffanello M, Schutz Y. Relationship between physical inactivity and adiposity in prepubertal boys. J Pediatr 131: 288-292, 1997.
41. Manco M, Bottazzo G, DeVito R, Marcellini M, Mingrone G, Nobili V. Nonalcoholic fatty liver disease in children. J Am Coll Nutr 27: 667-676, 2008.
42. Manco M, Marcellini M, Devito R, Comparcola D, Sartorelli MR, Nobili V. Metabolic syndrome and liver histology in paediatric nonalcoholic steatohepatitis. Int J Obes (Lond) 32: 381-387, 2008.
43. Martin B, Ji S, Maudsley S, Mattson MP. "Control" laboratory rodents are metabolically morbid: why it matters. Proc Natl Acad Sci USA 107: 6127-6133, 2010.
44. Mathes WF, Nehrenberg DL, Gordon R, Hua K, Garland T Jr, Pomp D. Dopaminergic dysregulation in mice selectively bred for excessive exercise or obesity. Behav Brain Res 210: 155-163, 2010.
45. Matsuzawa Y, Funahashi T, Kihara S, Shimomura I. Adiponectin and metabolic syndrome. Arterioscler Thromb Vasc Biol 24: 29-33, 2004.
46. McGinnis JM, Foege WH. Actual causes of death in the United States. JAMA 270: 2207-2212, 1993.
47. Mikus CR, Oberlin DJ, Libla JL, Taylor AM, Booth FW, Thyfault JP. Lowering physical activity impairs glycemic control in healthy volunteers. Med Sci Sports Exerc 44: 225-231, 2012.
48. Mokdad AH, Marks JS, Stroup DF, Gerberding JL. Actual causes of death in the United States, 2000. JAMA 291: 1238-1245, 2004.
49. Moran TH, Bi S. Hyperphagia and obesity in OLETF rats lacking CCK-1 receptors. Philos Trans R Soc Lond B Biol Sci 361: 1211-1218, 2006.
50. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM. The epidemiology of obesity. Gastroenterology 132: 2087-2102, 2007.
51. Ohkawara K, Tanaka S, Miyachi M, Ishikawa-Takata K, Tabata I. A dose-response relation between aerobic exercise and visceral fat reduction: systematic review of clinical trials. Int J Obes (Lond) 31: 1786-1797, 2007.
52. Olsen RH, Krogh-Madsen R, Thomsen C, Booth FW, Pedersen BK. Metabolic responses to reduced daily steps in healthy nonexercising men. JAMA 299: 1261-1263, 2008.
53. Olshansky SJ, Passaro DJ, Hershow RC, Layden J, Carnes BA, Brody J, Hayflick L, Butler RN, Allison DB, Ludwig DS. A potential decline in life expectancy in the United States in the 21st century. N Engl J Med 352: 1138-1145, 2005.
54. Oshida Y, Yamanouchi K, Hayamizu S, Nagasawa J, Ohsawa I, Sato Y. Effects of training and training cessation on insulin action. Int J Sports Med 12: 484-486, 1991.
55. Padilla J, Jenkins NT, Roberts MD, Arce-Esquivel AA, Martin JS, Laughlin MH, Booth FW. Differential changes in vascular mRNA levels between rat iliac and renal arteries produced by cessation of voluntary running. Exp Physiol. June 18, 2012, doi:10.1113/expphysiol.2012.066076.
56. Patterson CM, Bouret SG, Dunn-Meynell AA, Levin BE. Three weeks of postweaning exercise in DIO rats produces prolonged increases in central leptin sensitivity and signaling. Am J Physiol Regul Integr Comp Physiol 296: R537-R548, 2009.
57. Patterson CM, Dunn-Meynell AA, Levin BE. Three weeks of early-onset exercise prolongs obesity resistance in DIO rats after exercise cessation. Am J Physiol Regul Integr Comp Physiol 294: R290-R301, 2008.
58. Querido JS, Sheel AW. Regulation of cerebral blood flow during exercise. Sports Med 37: 765-782, 2007.
59. Rajia S, Chen H, Morris MJ. Voluntary post weaning exercise restores metabolic homeostasis in offspring of obese rats. Nutr Metab Cardiovasc Dis 2012.
60. Rampersaud E, Mitchell BD, Pollin TI, Fu M, Shen H, O'Connell JR, Ducharme JL, Hines S, Sack P, Naglieri R, Shuldiner AR, Snitker S. Physical activity and the association of common FTO gene variants with body mass index and obesity. Arch Intern Med 168: 1791-1797, 2008.
61. Rector RS, Thyfault JP, Laye MJ, Morris RT, Borengasser SJ, Uptergrove GM, Chakravarthy MV, Booth FW, Ibdah JA. Cessation of daily exercise dramatically alters precursors of hepatic steatosis in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. J Physiol 586: 4241-4249, 2008.
62. Reed DR, Lawler MP, Tordoff MG. Reduced body weight is a common effect of gene knockout in mice. BMC Genet 9: 4, 2008.
63. Reither EN, Olshansky SJ, Yang Y. New forecasting methodology indicates more disease and earlier mortality ahead for today's younger Americans. Health Aff (Millwood) 30: 1562-1568, 2011.
64. Rhodes JS, Garland T Jr, Gammie SC. Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behav Neurosci 117: 1243-1256, 2003.
65. Roberts CK. Inactivity and fat cell hyperplasia: fat chance? J Appl Physiol 102: 1308-1309, 2007.
66. Roberts MD, Childs TE, Brown JD, Davis JW, Booth FW. Early depression of Ankrd2 and Csrp3 mRNAs in the polyribosomal and whole-tissue fractions in skeletal muscle with decreased voluntary running. J Appl Physiol 112: 1291-1299, 2012.
67. Roberts MD, Gilpin L, Parker KE, Childs TE, Will MJ, Booth FW. Dopamine D1 receptor modulation in nucleus accumbens lowers voluntary wheel running in rats bred to run high distances. Physiol Behav 105: 661-668, 2012.
68. Schroeder M, Shbiro L, Gelber V, Weller A. Post-weaning voluntary exercise exerts long-term moderation of adiposity in males but not in females in an animal model of early-onset obesity. Horm Behav 57: 496-505, 2010.
69. Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C. Prevalence of fatty liver in children and adolescents. Pediatrics 118: 1388-1393, 2006.
70. Slentz CA, Aiken LB, Houmard JA, Bales CW, Johnson JL, Tanner CJ, Duscha BD, Kraus WE. Inactivity, exercise, and visceral fat. STRRIDE: a randomized, controlled study of exercise intensity and amount. J Appl Physiol 99: 1613-1618, 2005.
71. Slentz CA, Duscha BD, Johnson JL, Ketchum K, Aiken LB, Samsa GP, Houmard JA, Bales CW, Kraus WE. Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE-a randomized controlled study. Arch Intern Med 164: 31-39, 2004.
72. Slentz CA, Houmard JA, Johnson JL, Bateman LA, Tanner CJ, McCartney JS, Duscha BD, Kraus WE. Inactivity, exercise training and detraining, and plasma lipoproteins. STRRIDE: a randomized, controlled study of exercise intensity and amount. J Appl Physiol 103: 432-442, 2007.
73. Suvorava T, Lauer N, Kojda G. Physical inactivity causes endothelial dysfunction in healthy young mice. J Am Coll Cardiol 44: 1320-1327, 2004.
74. Takei M, Ando Y, Saitoh W, Tanimoto T, Kiyosawa N, Manabe S, Sanbuissho A, Okazaki O, Iwabuchi H, Yamoto T, Adam KP, Weiel JE, Ryals JA, Milburn MV, Guo L. Ethylene glycol monomethyl ether-induced toxicity is mediated through the inhibition of flavoprotein dehydrogenase enzyme family. Toxicol Sci 118: 643-652, 2010.
75. Telama R, Yang X, Viikari J, Valimaki I, Wanne O, Raitakari O. Physical activity from childhood to adulthood: a 21-year tracking study. Am J Prev Med 28: 267-273, 2005.
76. Teske JA, Billington CJ, Kuskowski MA, Kotz CM. Spontaneous physical activity protects against fat mass gain. Int J Obes (Lond) 36: 603-613, 2012.
77. Thijssen DH, Ellenkamp R, Kooijman M, Pickkers P, Rongen GA, Hopman MT, Smits P. A causal role for endothelin-1 in the vascular adaptation to skeletal muscle deconditioning in spinal cord injury. Arte-rioscler Thromb Vasc Biol 27: 325-331, 2007.
78. Troiano RP, Berrigan D, Dodd KW, Masse LC, Tilert T, McDowell M. Physical activity in the United States measured by accelerometer. Med Sci Sports Exerc 40: 181-188, 2008.
79. Weintraub WS, Daniels SR, Burke LE, Franklin BA, Goff DC Jr, Hayman LL, Lloyd-Jones D, Pandey DK, Sanchez EJ, Schram AP, and Whitsel LP. Value of primordial and primary prevention for cardiovascular disease: a policy statement from the American Heart Association. Circulation 124: 967-990, 2011.
80. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, Brene S. Delta FosB regulates wheel running. J Neurosci 22: 8133-8138, 2002.
81. Yang X, Telama R, Leskinen E, Mansikkaniemi K, Viikari J, Raita-kari OT. Testing a model of physical activity and obesity tracking from youth to adulthood: the cardiovascular risk in young Finns study. Int J Obes (Lond) 31: 521-527, 2007.