Quantitative genomics of voluntary exercise in mice: Transcriptional analysis and mapping of expression QTL in muscle

Physiological Genomics

Volumn 46, Issue 16, 2014, Pages 593-601

  Kelly, Scott A ^a   Nehrenberg, Derrick L ^b   Hua, Kunjie ^b   Garland Jr , Theodore ^c   Pomp, Daniel ^b  

^a OHIO WESLEYAN UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Body weight; eQTL; Experimental evolution; Wheel running

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BODY WEIGHT; BRAIN TISSUE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; MOUSE; MUSCLE EXERCISE; MUSCLE TISSUE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; RUNNING; VELOCITY; ANIMAL; C57BL MOUSE; CHROMOSOME; CHROMOSOME MAP; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; HINDLIMB; MALE; METABOLISM; MOTOR ACTIVITY; PROCEDURES; QUANTITATIVE TRAIT LOCUS; SKELETAL MUSCLE;

ANIMALS; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; FEMALE; GENE EXPRESSION PROFILING; GENOMICS; HINDLIMB; MALE; MICE, INBRED C57BL; MOTOR ACTIVITY; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYSICAL CONDITIONING, ANIMAL; QUANTITATIVE TRAIT LOCI;

EID: 84906087319     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00023.2014     Document Type: Article

References (43)

1. Aoi W, Naito Y, Takagi T, Tanimura Y, Takanami Y, Kawai Y, Sakuma K, Hang LP, Mizushima K, Hirai Y, Koyama R, Wada S, Higashi A, Kokura S, Ichikawa H, Yoshikawa T. A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise. Gut 62: 882-889, 2013.
2. Asselbergs FW, Guo Y, van Iperen EP, Sivapalaratnam S, Tragante V, Lanktree MB, Lange LA, Almoguera B, Appelman YE, Barnard J, Baumert J, Beitelshees AL, Bhangale TR, Chen YD, Gaunt TR, Gong Y, Hopewell JC, Johnson T, Kleber ME, Langaee TY, Li M, Li YR, Liu K, McDonough CW, Meijs MF, Middelberg RP, Musunuru K, Nelson CP, O'Connell JR, Padmanabhan S, Pankow JS, Pankratz N, Rafelt S, Rajagopalan R, Romaine SP, Schork NJ, Shaffer J, Shen H, Smith EN, Tischfield SE, van der Most PJ, van Vliet-Ostaptchouk JV, Verweij N, Volcik KA, Zhang L, Bailey KR, Bailey KM, Bauer F, Boer JM, Braund PS, Burt A, Burton PR, Buxbaum SG, Chen W, Cooper-Dehoff RM, Cupples LA, deJong JS, Delles C, Duggan D, Fornage M, Furlong CE, Glazer N, Gums JG, Hastie C, Holmes MV, Illig T, Kirkland SA, Kivimaki M, Klein R, Klein BE, Kooperberg C, Kottke-Marchant K, Kumari M, LaCroix AZ, Mallela L, Murugesan G, Ordovas J, Ouwehand WH, Post WS, Saxena R, Scharnagl H, Schreiner PJ, Shah T, Shields DC, Shimbo D, Srinivasan SR, Stolk RP, Swerdlow DI, Taylor HA Jr, Topol EJ, Toskala E, van Pelt JL, van Setten J, Yusuf S, Whittaker JC, Zwinderman AH; LifeLines Cohort Study, Anand SS, Balmforth AJ, Berenson GS, Bezzina CR, Boehm BO, Boerwinkle E, Casas JP, Caulfield MJ, Clarke R, Connell JM, Cruickshanks KJ, Davidson KW, Day IN, de Bakker PI, Doevendans PA, Dominiczak AF, Hall AS, Hartman CA, Hengstenberg C, Hillege HL, Hofker MH, Humphries SE, Jarvik GP, Johnson JA, Kaess BM, Kathiresan S, Koenig W, Lawlor DA, März W, Melander O, Mitchell BD, Montgomery GW, Munroe PB, Murray SS, Newhouse SJ, Onland-Moret NC, Poulter N, Psaty B, Redline S, Rich SS, Rotter JI, Schunkert H, Sever P, Shuldiner AR, Silverstein RL, Stanton A, Thorand B, Trip MD, Tsai MY, van der Harst P, van der Schoot E, van der Schouw YT, Verschuren WM, Watkins H, Wilde AA, Wolffenbuttel BH, Whitfield JB, Hovingh GK, Ballantyne CM, Wijmenga C, Reilly MP, Martin NG, Wilson JG, Rader DJ, Samani NJ, Reiner AP, Hegele RA, Kastelein JJ, Hingorani AD, Talmud PJ, Hakonarson H, Elbers CC, Keating BJ, Drenos F. Large-scale genecentric meta-analyses across 32 studies identifies multiple lipid loci. Am J Hum Genet 91: 823-838, 2012.
3. Audet GN, Meek TH, Garland T Jr, Olfert IM. Expression of angiogenic regulators and skeletal muscle capillarity in selectively bred high aerobic capacity mice. Exp Physiol 96: 1138-1150, 2011.
4. Aylor DL, Valdar W, Foulds-Mathes W, Buus RJ, Verdugo RA, Baric RS, Ferris MT, Frelinger JA, Heise M, Frieman MB, Gralinski LE, Bell TA, Didion JD, Hua K, Nehrenberg DL, Powell CL, Steigerwalt J, Xie Y, Kelada SN, Collins FS, Yang IV, Schwartz DA, Branstetter LA, Chesler EJ, Miller DR, Spence J, Liu EY, McMillan L, Sarkar A, Wang J, Wang W, Zhang Q, Broman KW, Korstanje R, Durrant C, Mott R, Iraqi FA, Pomp D, Threadgill D, de Villena FP, Churchill GA. Genetic analysis of complex traits in the emerging Collaborative Cross. Genome Res 21: 1213-1222, 2011.
5. Baldwin KM, Haddad F. Research in the exercise sciences: where are we and where do we go from here-part II. Sport Sci Rev 38: 42-50, 2010.
6. Bray MS, Hagberg JM, Pérusse 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 Exerc 41: 35-73, 2009.
7. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890, 2003.
8. Burns B, Schmidt K, Williams SR, Kim S, Giriajan S, Elsea SH. Rai1 haploinsufficiency causes reduced Bdnf expression resulting in hyperphagia, obesity and altered fat distribution in mice and humans with no evidence of metabolic syndrome. Hum Mol Genet 19: 4026-4042, 2010.
9. Cervino AC, Li G, Edwards S, Zhu J, Laurie C, Tokiwa G, Lum PY, Wang S, Castellani LW, Lusis AJ, Carlson S, Sachs AB, Schadt EE. Integrating QTL and high-density SNP analyses in mice to identify Insig2 as a susceptibility gene for plasma cholesterol levels. Genomics 86: 505-517, 2005.
10. Curran-Everett D. Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol 279: R1-R8, 2000.
11. Dina C, Meyre D, Samson C, Tichet J, Marre M, Jouret B, Charles MA, Balkau B, Froguel P. Comment on "A common genetic variant is associated with adult and childhood obesity". Science 315: 187, 2007.
12. Doss S, Schadt EE, Drake TA, Lusis AJ. Cis-acting expression quantitative trait loci in mice. Genome Res 15: 681-691, 2005.
13. Farber CR, Kelly SA, Baruch E, Yu D, Hua K, Nehrenberg DL, de Villena FP, Buus RJ, Garland T Jr, Pomp D. Identification of quantitative trait loci influencing skeletal architecture in mice: emergence of Cdh11 as a primary candidate gene regulating femoral morphology. J Bone Miner Res 26: 2174-2183, 2011.
14. Garland T Jr, Kelly SA. Phenotypic plasticity and experimental evolution. J Exp Biol 209: 2344-2361, 2006.
15. Garland T Jr, Schutz H, Chappell MA, Keeney BK, Meek TH, Copes LE, Acosta W, Drenowatz C, Maciel RC, van Dijk G, Kotz CM, Eisenmann JC. The biological control of voluntary exercise, spontaneous physical activity, and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol 214: 206-229, 2011.
16. Garland T Jr, Kelly SA, Malisch JL, Kolb EM, Hannon RM, Keeney BK, Van Cleave SL, Middleton KM. How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc Biol Soc 278: 574-581, 2011.
17. O2max response to exercise training. J Appl Physiol 115: 1343-1359, 2013.
18. Girard I, Rezende EL, Garland T Jr. Leptin levels and body composition of mice selectively bred for high voluntary activity. Physiol Biochem Zool 80: 568-579, 2007.
19. Gordon RR, La Merrill M, Hunter KW, Sørensen P, Threadgill DW, Pomp D. Dietary fat-dependent transcriptional architecture and copy number alterations associated with modifiers of mammary cancer metastasis. Clin Exp Metastasis 27: 279-293, 2010.
20. Herbert A, Gerry NP, McQueen MB, Heid IM, Pfeufer A, Illig T, Wichmann HE, Meitinger T, Hunter D, Hu FB, Colditz G, Hinney A, Hebebrand J, Koberwitz K, Zhu X, Cooper R, Ardlie K, Lyon H, Hirschhorn JN, Laird NM, Lenburg ME, Lange C, Christman MF. A common genetic variant is associated with adult and childhood obesity. Science 312: 279-283, 2006.
21. Howlett RA, Kirkton SD, Gonzalez NC, Wagner HE, Britton SL, Koch LG, Wagner PD. Peripheral oxygen transport and utilization in rats following continued selective breeding for endurance running capacity. J Appl Physiol 106: 1819-1825, 2009.
22. Jeong JK, Szabo G, Raso GM, Meli R, Diano S. Deletion of prolyl carboxypeptidase attenuates the metabolic effects of diet-induced obesity. Am J Physiol Endocrinol Metab 302: E1502-E1510, 2012.
23. Kelly SA, Nehrenberg DL, Hua K, Gordon RR, Garland T Jr, Pomp D. Parent-of-origin effects on voluntary exercise levels and body composition in mice. Physiol Genomics 40: 111-120, 2010.
24. Kelly SA, Nehrenberg DL, Peirce JL, Hua K, Steffy BM, Wiltshire T, Pardo-Manuel de Villena F, Garland T Jr, Pomp D. Genetic architecture of voluntary exercise in an advanced intercross line of mice. Physiol Genomics 42: 190-200, 2010.
25. Kelly SA, Nehrenberg DL, Hua K, Garland T Jr, Pomp D. Exercise, weight loss, and changes in body composition in mice: phenotypic relationships and genetic architecture Physiol Genomics 43: 199-212, 2011.
26. Kelly SA, Nehrenberg DL, Hua K, Garland T Jr, Pomp D. Functional genomic architecture of predisposition to voluntary exercise in mice: expression QTL in the brain. Genetics 191: 266-284, 2012.
27. Kelly SA, Pomp D. Genetic determinants of voluntary exercise. Trends Genet 29: 348-357, 2013.
28. Kelly SA, Bell TA, Selitsky SR, Buus RJ, Hua K, Weinstock GM, Garland T Jr, Pardo-Manuel de Villena F, Pomp D. A novel intronic SNP in the Myosin heavy polypeptide 4 gene is responsible for the Mini-Muscle phenotype characterized by major reduction in hindlimb muscle mass in mice. Genetics 195: 1385-1395, 2013.
29. Lightfoot JT. Current understanding of the genetic basis for physical activity. J Nutr 141: 526-530, 2011.
30. Lyon HN, Emilsson V, Hinney A, Heid IM, Lasky-Su J, Zhu X, Thorleifsson G, Gunnarsdottir S, Walters GB, Thorsteinsdottir U, Kong A, Gulcher J, Nguyen TT, Scherag A, Pfeufer A, Meitinger T, Brönner G, Rief W, Soto-Quiros ME, Avila L, Klanderman B, Raby BA, Silverman EK, Weiss ST, Laird N, Ding X, Groop L, Tuomi T, Isomaa B, Bengtsson K, Butler JL, Cooper RS, Fox CS, O'Donnell CJ, Vollmert C, Celedón JC, Wichmann HE, Hebebrand J, Stefansson K, Lange C, Hirschhorn JN. The association of a SNP upstream of INSIG2 with body mass index is reproduced in several but not all cohorts. PLoS Genet 3: e61, 2007.
31. Okano AH, Fontes EB, Montenegro RA, Farinatti PD, Cyrino ES, Li LM, Bikson M, Noakes TD. Brain stimulation modulates the autonomic nervous system, rating of perceived exertion and performance during maximal exercise. Br J Sports Med [Epub ahead of print].
32. O'Leary J, Osborne LR. Global analysis of gene expression in the developing brain of Gtf2ird1 knockout mice. PLoS One 6: e23868, 2011.
33. Pomp D, Nehrenberg D, Estrada-Smith D. Complex genetics of obesity in mouse models. Annu Rev Nutr 28: 331-345, 2008.
34. Roth SM, Rankinen T, Hagberg JM, Loos RJ, Pérusse L, Sarzynski MA, Wolfarth B, Bouchard C. Advances in exercise, fitness, and performance genomics in 2011. Med Sci Sports Exerc 44: 809-817, 2012.
35. Sen S, Churchill GA. A statistical framework for quantitative trait mapping. Genetics 159: 371-387, 2001.
36. Swallow JG, Carter PA, Garland T Jr. Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28: 227-237, 1998.
37. Swallow JG, Koteja P, Carter PA, Garland T Jr. Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity. J Exp Biol 202: 2513-2520, 1999.
38. Swallow JG, Koteja P, Carter PA, Garland T Jr. Food consumption and body composition in mice selected for high wheel-running activity. J Comp Physiol B 171: 651-659, 2001.
39. Swallow JG, Hayes JP, Koteja P, Garland T Jr. Selection experiments and experimental evolution of performance and physiology, in: Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, edited by Garland Jr T, Rose MR. Berkeley, CA: Univ. of California Press, 2009.
40. Vaanholt LM, Meerlo P, Garland T Jr, Visser GH, van Dijk G. Plasma adiponectin is increased in mice selectively bred for high wheel-running activity, but not by wheel running per se. Horm Metab Res 39: 377-383, 2007.
41. Vaanholt LM, Jonas I, Doornbos M, Schubert KA, Nyakas C, Garland T Jr, Visser GH, van Dijk G. Responses in energy balance to high-fat feeding in mice selectively bred for high wheel-running activity. Int J Obes 32: 1566-1575, 2008.
42. van Nas A, Ingram-Drake L, Sinsheimer JS, Wang SS, Schadt EE, Drake T, Lusis AJ. Expression quantitative trait loci: replication, tissueand sex-specificity in mice. Genetics 185: 1059-1068, 2010.
43. Wallingford N, Perroud B, Gao Q, Coppola A, Gyengesi E, Liu ZW, Gao XB, Diament A, Haus KA, Shariat-Madar Z, Mahdi F, Wardlaw SL, Schmaier AH, Warden CH, Diano S. Prolycarboxpeptidase regulates food intake by inactivating alpha-MSH in rodents. J Clin Invest 119: 2291-2303, 2009.