Functional genomic architecture of predisposition to voluntary exercise in mice: Expression QTL in the brain

Genetics

Volumn 191, Issue 2, 2012, Pages 643-654

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

^a OHIO WESLEYAN UNIVERSITY   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE RECEPTOR; HELIX LOOP HELIX PROTEIN; HORMONE; MESSENGER RNA; NEUROTRANSMITTER; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY WEIGHT; BRAIN REGION; BRAIN TISSUE; EXERCISE; FUNCTIONAL GENOMICS; GENE ACTIVITY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MAPPING; GENETIC ASSOCIATION; HAPLOTYPE; MOTIVATION; MOUSE; NEUROBIOLOGY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; REWARD; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84862524625     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.140509     Document Type: Article

References (72)

1. Aylor, D. L., W. Valdar, W. Foulds-Mathes, R. J. Buus, R. A. Verdugo et al., 2011 Genetic analysis of complex traits in the emerging Collaborative Cross. Genome Res. 21: 1213-1222.
2. Belke, T. W., 2006 Concurrent schedules of wheel-running reinforcement: choice between different durations of opportunity to run in rats. Learn. Behav. 34: 61-70.
3. Belke, T. W., and T. Garland Jr., 2007 A brief opportunity to run does not function as a reinforcer for mice selected for high daily wheel-running rates. J. Exp. Anal. Behav. 88: 199-213.
4. Booth, F. W., S. E. Gordon, C. J. Carlson, and M. T. Hamilton, 2000 Waging war on modern chronic diseases: primary prevention through exercise biology. J. Appl. Physiol. 88: 774-787.
5. Bray, M. S., J. M. Hagberg, L. Perusse, T. Rankinen, S. M. Roth et al., 2009 The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update. Med. Sci. Sports Exerc. 41: 35-73.
6. Brené, S., A. Bjørnebekk, E. Åberg, A. A. Mathé, L. Olson et al., 2007 Running is rewarding and antidepressive. Physiol. Behav. 92: 136-140.
7. Broman, K.W., H. Wu, S. Sen, and G. A. Churchill, 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
8. Bronikowski, A. M., J. S. Rhodes, T. Garland Jr., T. A. Prolla, T. Awad et al., 2004 The evolution of gene expression in the hippocampus in response to selective breeding for increased locomotor activity. Evolution 58: 2079-2086.
9. Burns, B., K. Schmidt, S. R. Williams, S. Kim, S. Giriajan et al., 2010 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.
10. Cagniard, B., P. D. Balsam, D. Brunner, and X. Zhuang, 2006 Mice with chronically elevated dopamine exhibit enhanced motivation, but not learning, for a food reward. Neuropsychopharmacology 31: 1362-1370.
11. Cai, G., S. A. Cole, N. Butte, C. Bacino, V. Diego et al., 2006 A quantitative trait locus on chromosome 18q for physical activity and dietary intake in Hispanic children. Obesity (Silver Spring) 14: 1596-1604.
12. Centers for Disease Control and Prevention (CDC), 2003 Physical activity levels among children aged 9-13 years-United States, 2002. MMWR Morb. Mortal. Wkly. Rep. 52: 785-788.
13. Cervino, A. C., G. Li, S. Edwards, J. Zhu, C. Laurie et al., 2005 Integrating QTL and high-density SNP analyses in mice to identify Insig2 as a susceptibility gene for plasma cholesterol levels. Genomics 86: 505-517.
14. Chen, J. L., D. Merl, C. W. Peterson, J. Wu, P. Y. Liu et al., 2010 Lactic acidosis triggers starvation response with paradoxical induction of TXNIP through MondoA. PLoS Genet. 6 (9): pii:e1001093.
15. Curran-Everett, D., 2000 Multiple comparisons: philosophies and illustrations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279: R1-R8.
16. Davis, C., R. D. Levitan, A. S. Kaplan, J. Carter, C. Reid et al., 2008 Reward sensitivity and the D2 dopamine receptor gene: a case-control study of binge eating disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 32: 620-628.
17. Dina, C., D. Meyre, C. Samson, J. Tichet, M. Marre et al., 2007 Comment on "A common genetic variant is associated with adult and childhood obesity". Science 315: 187.
18. Dishman, R. K., 2008 Gene-physical activity interactions in the etiology of obesity: behavioral considerations. Obesity (Silver Spring) 16: S60-S65.
19. Doss, S., E. E. Schadt, T. A. Drake, and A. J. Lusis, 2005 Cis-acting expression quantitative trait loci in mice. Genome Res. 15: 681-691.
20. Druka, A., E. Potokina, Z. Luo, N. Jiang, X. Chen et al., 2010 Expression quantitative trait loci analysis in plants. Plant Biotechnol. J. 8: 10-27.
21. Farber, C. R., S. A. Kelly, E. Baruch, D. Yu, K. Hua et al., 2011 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.
22. Foley, T. E., B. N. Greenwood, H. E. Day, L. G. Koch, S. L. Britton et al., 2006 Elevated central monoamine receptor mRNA in rats bred for high endurance capacity: implications for central fatigue. Behav. Brain Res. 174: 132-142.
23. Friedenreich, C. M., and M. R. Orenstein, 2002 Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J. Nutr. 132: 3456S-3464S.
24. Garland, T. Jr., S. A. Kelly, J. L. Malisch, E. M. Kolb, R. M. Hannon et al., 2011a How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc. Biol. Sci. 278: 574-581.
25. Garland, T. Jr., H. Schutz, M. A. Chappell, B. K. Keeney, T. H. Meek et al., 2011b 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.
26. Ghazalpour, A., S. Doss, H. Kang, C. Farber, P. Z. Wen et al., 2008 High-resolution mapping of gene expression using association in an outbred mouse stock. PLoS Genet. 4: e1000149.
27. Gomes, F. R., E. L. Rezende, J. L. Malisch, S. K. Lee, D. A. Rivas et al., 2009 Glycogen storage and muscle glucose transporters (GLUT-4) of mice selectively bred for high voluntary wheel running. J. Exp. Biol. 212: 238-248.
28. Gordon, R. R., M. la Merrill, K. W. Hunter, P. Sørensen, D. W. Threadgill et al., 2010 Dietary fat-dependent transcriptional architecture and copy number alterations associated with modifiers of mammary cancer metastasis. Clin. Exp. Metastasis 27: 279-293.
29. He, Y., X. Wu, R. S. Khan, A. J. Kastin, G. G. Cornelissen-Guillaume et al., 2010 IL-15 receptor deletion results in circadian changes of locomotor and metabolic activity. J. Mol. Neurosci. 41: 315-321.
30. Herbert, A., N. P. Gerry, M. B. McQueen, I. M. Heid, A. Pfeufer et al., 2006 A common genetic variant is associated with adult and childhood obesity. Science 312: 279-283.
31. Jansen, R. C., and J. P. Nap, 2001 Genetical genomics: the added value from segregation. Trends Genet. 17: 388-391.
32. Keeney, B. K., D. A. Raichlen, T. H. Meek, R. S. Wijeratne, K. M. Middleton et al., 2008 Differential response to a selective cannabinoid receptor antagonist (SR141716: rimonabant) in female mice from lines selectively bred for high voluntary wheel-running behaviour. Behav. Pharmacol. 19: 812-820.
33. Kelly, S. A., P. P. Czech, J. T. Wight, K. M. Blank, and T. Garland Jr. 2006 Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice. J. Morphol. 267: 360-374.
34. Kelly, S. A., D. L. Nehrenberg, K. Hua, R. R. Gordon, T. Garland Jr. et al. 2010a Parent-of-origin effects on voluntary exercise levels and body composition in mice. Physiol. Genomics 40: 111-120.
35. Kelly, S. A., D. L. Nehrenberg, J. L. Peirce, K. Hua, B. M. Steffy et al., 2010b Genetic architecture of voluntary exercise in an advanced intercross line of mice. Physiol. Genomics 42: 190-200.
36. Kelly, S. A., D. L. Nehrenberg, K. Hua, and T. Garland Jr., and D. Pomp, 2011 Exercise, weight loss, and changes in body composition in mice: phenotypic relationships and genetic architecture. Physiol. Genomics 43: 199-212.
37. Knab, A. M., and J. T. Lightfoot, 2010 Does the difference between physically active and couch potato lie in the dopamine system? Int. J. Biol. Sci. 6: 133-150.
38. Kotz, C. M., J. A. Teske, and C. J. Billington, 2008 Neuroregulation of nonexercise activity thermogenesis and obesity resistance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294: R699-R710.
39. Kumar, K. G., L. M. DiCarlo, J. Volaufova, A. R. Zuberi, and B. K. Richards, 2010 Increased physical activity cosegregates with higher intake of carbohydrate and total calories in a subcongenic mouse strain. Mamm. Genome 12: 52-63.
40. Lein, E. S., M. J. Hawrylycz, N. Ao, M. Ayres, A. Bensinger et al., 2006 Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
41. Lenard, N. R., and H. R. Berthoud, 2008 Central and peripheral regulation of food intake and physical activity: pathways and genes. Obesity (Silver Spring) 16(Suppl 3): S11-S22.
42. Lightfoot, J. T., 2011 Current understanding of the genetic basis for physical activity. J. Nutr. 141: 526-530.
43. Lightfoot, J. T., M. J. Turner, M. Daves, A. Vordermark, and S. R. Kleeberger, 2004 Genetic influence on daily wheel running activity level. Physiol. Genomics 19: 270-276.
44. Liu, C., 2011 Brain expression quantitative locus mapping informs genetic studies of psychiatric diseases. Neurosci. Bull. 27: 123-133.
45. Lyon, H. N., V. Emilsson, A. Hinney, I. M. Heid, J. Lasky-Su et al., 2007 The association of a SNP upstream of INSIG2 with body mass index is reproduced in several but not all cohorts. PLoS Genet. 3: e61.
46. MacLaren, V. V., and L. A. Best, 2010 Multiple addictive behaviors in young adults: student norms for the Shorter PROMIS Questionnaire. Addict. Behav. 35: 252-255.
47. Mathes, W. F., D. L. Nehrenberg, R. Gordon, K. Hua, T. Garland Jr. et al. 2010 Dopaminergic dysregulation in mice selectively bred for excessive exercise or obesity. Behav. Brain Res. 210: 155-163.
48. Meek, T. H., B. P. Lonquich, R. M. Hannon, and T. Garland Jr. 2009 Endurance capacity of mice selectively bred for high voluntary wheel running. J. Exp. Biol. 212: 2908-2917.
49. O'Leary, J., and L. R. Osborne, 2011 Global analysis of gene expression in the developing brain of Gtf2ird1 knockout mice. PLoS ONE 6: e23868.
50. Parts, L., O. Stegle, J. Winn, and R. Durbin, 2011 Joint genetic analysis of gene expression data with inferred cellular phenotypes. PLoS Genet. 7: e1001276.
51. Patwari, P., W. A. Chutkow, K. Cummings, V. L. Verstraeten, J. Lammerding et al., 2009 Thioredoxin-independent regulation of metabolism by the alpha-arrestin proteins. J. Biol. Chem. 284: 24996-25003.
52. Pomp, D., 2005 Genomic dissection of complex trait predisposition, pp. 237-262 in The Mouse in Animal Genetics and Breeding Research, edited by E. J. Eisen. Imperial College Press, London.
53. R Development Core Team, 2008 R: A Language and Environmentfor Statistical Computing. R Foundation for Statistical Computing, Vienna (http://www.R-project.org).
54. Rhodes, J. S., G. R. Hosack, I. Girard, A. E. Kelley, G. S. Mitchell et al., 2001 Differential sensitivity to acute administration of cocaine, GBR 12909, and fluoxetine in mice selectively bred for hyperactive wheel-running behavior. Psychopharmacology (Berl.) 158: 120-131.
55. Schadt, E. E., S. A. Monks, T. A. Drake, A. J. Lusis, N. Che et al., 2003 Genetics of gene expression surveyed in maize, mouse and man. Nature 422: 297-302.
56. Sen, S., and G. A. Churchill, 2001 A statistical framework for quantitative trait mapping. Genetics 159: 371-387.
57. Sherwin, C. M., 1998 Voluntary wheel running: a review and novel interpretation. Anim. Behav. 56: 11-27.
58. Sherwin, C. M., and C. J. Nicol, 1996 Reorganization of behaviour in laboratory mice, Mus musculus, with varying cost of access to resources. Anim. Behav. 51: 1087-1093.
59. Swallow, J. G., P. A. Carter, and T. Garland Jr., 1998 Artificial selection for increased wheel-running behavior in house mice. Behav. Genet. 28: 227-237.
60. Swallow, J. G., P. Koteja, P. A. Carter, and T. Garland Jr. 1999 Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity. J. Exp. Biol. 202: 2513-2520.
61. Swallow, J. G., J. P. Hayes, P. Koteja, and T. Garland Jr., 2009 Selection experiments and experimental evolution of performance and physiology, pp. 301-333 in Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, edited by T. Garland, Jr., and M. R. Rose. University of California Press, Berkeley.
62. Vaanholt, L. M., I. Jonas, M. Doornbos, K. A. Schubert, C. Nyakas et al., 2008 Responses in energy balance to high-fat feeding in mice selectively bred for high wheel-running activity. Int. J. Obes. 32: 1566-1575.
63. Valdar, W., C. C. Holmes, R. Mott, and J. Flint, 2009 Mapping in structured populations by resample model averaging. Genetics 1182: 1263-1277.
64. van Nas, A., L. Ingram-Drake, J. S. Sinsheimer, S. S. Wang, E. E. Schadt et al., 2010 Expression quantitative trait loci: replication tissue- and sex-specificity in mice. Genetics 185: 1059-1068.
65. Verdugo, R. A., C. R. Farber, C. H. Warden, and J. F. Medrano, 2010 Serious limitations of the QTL/Microarray approach for QTL gene discovery. BMC Biol. 8: 96.
66. Wallingford, N., B. Perroud, Q. Gao, A. Coppola, E. Gyengesi et al., 2009 Prolycarboxpeptidase regulates food intake by inactivating alpha-MSH in rodents. J. Clin. Invest. 119: 2291-2303.
67. Waters, R. P., K. J. Renner, R. B. Pringle, C. H. Summers, S. L. Britton et al., 2008 Selection for aerobic capacity affects corticosterone, monoamines and wheel-running activity. Physiol. Behav. 93: 1044-1054.
68. Yang, H., Y. Ding, L. N. Hutchins, J. Szatkiewicz, T. A. Bell et al., 2009 A customized and versatile high-density genotyping array for the mouse. Nat. Methods 6: 663-666.
69. Yao, C., Z. Wang, Y. Zhou, W. Xu, Q. Li et al., 2010a A study of Y chromosome gene mRNA in human ejaculated spermatozoa. Mol. Reprod. Dev. 77: 158-166.
70. Yao, C. J., W. J. Xu, X. L. Gong, Y. Zhou, Z. Q. Yan et al., 2010b The role of Dby mRNA in early development of male mouse zygotes. Asian J. Androl. 12: 567-577.
71. Zhang, X., A. J. Cal, and J. O. Borevitz, 2011 Genetic architecture of regulatory variation in Arabidopsis thaliana. Genome Res. 21: 725-733.
72. Zhang, X., S. Huang, W. Sun, and W. Wang, 2012 Rapid and robust resampling-based multiple testing correction with application in genome-wide eQTL study. Genetics 191 (in press).