Identification of genetic loci associated with different responses to high-fat diet-induced obesity in C57BL/6N and C57BL/6J substrains

Physiological Genomics

Volumn 46, Issue 11, 2014, Pages 377-384

  Heiker, John T ^a   Kunath, Anne ^a   Kosacka, Joanna ^a   Flehmig, Gesine ^a   Knigge, Anja ^a   Kern, Matthias ^a   Stumvoll, Michael ^a   Kovacs, Peter ^a   Blüher, Matthias ^a   Klöting, Nora ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

C57BL 6; DIO; Genetic background; High fat diet; Obesity; SNAP29; Visceral fat mass

Indexed keywords

LEPTIN; MESSENGER RNA; GLUCOSE; VESICULAR TRANSPORT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; C57BL 6 MOUSE; C57BL/6N MOUSE; CONTROLLED STUDY; FAT MASS; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; GENETIC DIFFERENCE; GENETIC VARIABILITY; GENOTYPE; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN TISSUE; HYBRID MOUSE STRAIN; INSULIN SENSITIVITY; LIPID DIET; LIPID STORAGE; MALE; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SUBCUTANEOUS FAT; SYNAPSE VESICLE; WEIGHT GAIN; ADIPOSE TISSUE; ALLELE; ANIMAL; BLOOD; C57BL MOUSE; GENETICS; METABOLISM; MIDDLE AGED;

ADIPOSE TISSUE; ALLELES; ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; FEMALE; GENETIC LOCI; GENOTYPE; GLUCOSE; HUMANS; LEPTIN; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; OBESITY; POLYMORPHISM, SINGLE NUCLEOTIDE; VESICULAR TRANSPORT PROTEINS; WEIGHT GAIN;

EID: 84901707054     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00014.2014     Document Type: Article

References (51)

1. Berndt J, Kovacs P, Ruschke K, Kloting N, Fasshauer M, Schon MR, Korner A, Stumvoll M, Bluher M. Fatty acid synthase gene expression in human adipose tissue: association with obesity and type 2 diabetes. Diabetologia 50: 1472-1480, 2007.
2. Bielawska-Pohl A, Blesson S, Benlalam H, Trenado A, Opolon P, Bawa O, Rouffiac V, Dus D, Kieda C, Chouaib S. The anti-angiogenic activity of IL-12 is increased in iNOS-/-mice and involves NK cells. J Mol Med (Berl) 88: 775-784, 2010.
3. Blottner D, Serradj N, Salanova M, Touma C, Palme R, Silva M, Aerts JM, Berckmans D, Vico L, Liu Y, Giuliani A, Rustichelli F, Cancedda R, Jamon M. Morphological, physiological and behavioural evaluation of a 'Mice in Space' housing system. J Comp Physiol B 179: 519-533, 2009.
4. Bothe GW, Bolivar VJ, Vedder MJ, Geistfeld JG. Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Genes Brain Behav 3: 149-157, 2004.
5. Bourdi M, Davies JS, Pohl LR. Mispairing C57BL/6 substrains of genetically engineered mice and wild-type controls can lead to confounding results as it did in studies of JNK2 in acetaminophen and concanavalin A liver injury. Chem Res Toxicol 24: 794-796, 2011.
6. Brancaz MV, Iratni R, Morrison A, Mancini SJ, Marche P, Sundberg J, Nonchev S. A new allele of the mouse hairless gene interferes with Hox/LacZ transgene regulation in hair follicle primordia. Exp Mol Pathol 76: 173-181, 2004.
7. Brose N. For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic 9: 1403-1413, 2008.
8. Bryant CD, Zhang NN, Sokoloff G, Fanselow MS, Ennes HS, Palmer AA, McRoberts JA. Behavioral differences among C57BL/6 substrains: implications for transgenic and knockout studies. J Neurogenet 22: 315-331, 2008.
9. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329: 1663-1667, 2010.
10. Collins S, Martin TL, Surwit RS, Robidoux J. Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol Behav 81: 243-248, 2004.
11. Derby MC, Gleeson PA. New insights into membrane trafficking and protein sorting. Int Rev Cytol 261: 47-116, 2007.
12. Diwan BA, Blackman KE. Differential susceptibility of 3 sublines of C57BL/6 mice to the induction of colorectal tumors by 1,2-dimethylhydrazine. Cancer Lett 9: 111-115, 1980.
13. Freeman H, Shimomura K, Horner E, Cox RD, Ashcroft FM. Nicotinamide nucleotide transhydrogenase: a key role in insulin secretion. Cell Metab 3: 35-45, 2006.
14. Freeman HC, Hugill A, Dear NT, Ashcroft FM, Cox RD. Deletion of nicotinamide nucleotide transhydrogenase-A new quantitive trait locus accounting for glucose intolerance in C57BL/6J mice. Diabetes 55: 2153-2156, 2006.
15. Fuchs-Telem D, Stewart H, Rapaport D, Nousbeck J, Gat A, Gini M, Lugassy Y, Emmert S, Eckl K, Hennies HC, Sarig O, Goldsher D, Meilik B, Ishida-Yamamoto A, Horowitz M, Sprecher E. CEDNIK syndrome results from loss-of-function mutations in SNAP29. Br J Dermatol 164: 610-616, 2011.
16. Geng X, Lou H, Wang J, Li L, Swanson AL, Sun M, Beers-Stolz D, Watkins S, Perez RG, Drain P. alpha-Synuclein binds the K(ATP) channel at insulin-secretory granules and inhibits insulin secretion. Am J Physiol Endocrinol Metab 300: E276-E286, 2011.
17. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120: 885-890, 1984.
18. Green ML, Singh AV, Zhang Y, Nemeth KA, Sulik KK, Knudsen TB. Reprogramming of genetic networks during initiation of the Fetal Alcohol Syndrome. Dev Dyn 236: 613-631, 2007.
19. Grottick AJ, Bagnol D, Phillips S, McDonald J, Behan DP, Chalmers DT, Hakak Y. Neurotransmission-and cellular stress-related gene expression associated with prepulse inhibition in mice. Brain Res Mol Brain Res 139: 153-162, 2005.
20. Heber S, Herms J, Gajic V, Hainfellner J, Aguzzi A, Rulicke T, von Kretzschmar H, von Koch C, Sisodia S, Tremml P, Lipp HP, Wolfer DP, Muller U. Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci 20: 7951-7963, 2000.
21. Herms J, Anliker B, Heber S, Ring S, Fuhrmann M, Kretzschmar H, Sisodia S, Muller U. Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J 23: 4106-4115, 2004.
22. Hida K, Wada J, Eguchi J, Zhang H, Baba M, Seida A, Hashimoto I, Okada T, Yasuhara A, Nakatsuka A, Shikata K, Hourai S, Futami J, Watanabe E, Matsuki Y, Hiramatsu R, Akagi S, Makino H, Kanwar YS. Visceral adipose tissue-derived serine protease inhibitor: a unique insulin-sensitizing adipocytokine in obesity. Proc Natl Acad Sci USA 102: 10610-10615, 2005.
23. Jourdan T, Demizieux L, Gresti J, Djaouti L, Gaba L, Vergès B, Degrace P. Antagonism of peripheral hepatic cannabinoid receptor-1 improves liver lipid metabolism in mice: evidence from cultured explants. Hepatology 55: 790-799, 2012.
24. Kern M, Knigge A, Heiker JT, Kosacka J, Stumvoll M, Kovacs P, Blüher M, Kloeting N. C57BL/6JRj mice are protected against diet induced obesity (DIO). Biochem Biophys Res Commun 417: 717-720, 2012.
25. Kloeting N, Graham TE, Berndt J, Kralisch S, Kovacs P, Wason CJ, Fasshauer M, Schon MR, Stumvoll M, Bluher M, Kahn BB. Serum retinol-binding protein is more highly expressed in visceral than in subcutaneous adipose tissue and is a marker of intra-abdominal fat mass. Cell Metab 6: 79-87, 2007.
26. Larsen KE, Schmitz Y, Troyer MD, Mosharov E, Dietrich P, Quazi AZ, Savalle M, Nemani V, Chaudhry FA, Edwards RH, Stefanis L, Sulzer D. Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis. J Neurosci 26: 11915-11922, 2006.
27. Lee SB, Park SM, Ahn KJ, Chung KC, Paik SR, Kim J. Identification of the amino acid sequence motif of alpha-synuclein responsible for macrophage activation. Biochem Biophys Res Commun 381: 39-43, 2009.
28. Lelu K, Laffont S, Delpy L, Paulet PE, Perinat T, Tschanz SA, Pelletier L, Engelhardt B, Guery JC. Estrogen receptor alpha signaling in T lymphocytes is required for estradiol-mediated inhibition of Th1 and Th17 cell differentiation and protection against experimental autoimmune encephalomyelitis. J Immunol 187: 2386-2393, 2011.
29. Lynch JJ 3rd, Shek EW, Castagne V, Mittelstadt SW. The proconvulsant effects of leptin on glutamate receptor-mediated seizures in mice. Brain Res Bull 82: 99-103, 2010.
30. Mehta R, Birerdinc A, Hossain N, Afendy A, Chandhoke V, Younossi Z, Baranova A. Validation of endogenous reference genes for qRT-PCR analysis of human visceral adipose samples. BMC Mol Biol 11: 39, 2010.
31. Mekada K, Abe K, Murakami A, Nakamura S, Nakata H, Moriwaki K, Obata Y, Yoshiki A. Genetic Differences among C57BL/6 Substrains. Exp Anim 58: 141-149, 2009.
32. Mulligan MK, Ponomarev I, Boehm SL 2nd, Owen JA, Levin PS, Berman AE, Blednov YA, Crabbe JC, Williams RW, Miles MF, Bergeson SE. Alcohol trait and transcriptional genomic analysis of C57BL/6 substrains. Genes Brain Behav 7: 677-689, 2008.
33. Mural RJ, Pfannkoch CM, Barnstead M, Stephenson LD. Erratum to "A comparison of whole-genome shotgun-derived mouse chromosome 16 and the human genome". Science 297: 1278, 2002.
34. Murphy DD, Rueter SM, Trojanowski JQ, Lee VM. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20: 3214-3220, 2000.
35. Needham BE, Wlodek ME, Ciccotosto GD, Fam BC, Masters CL, Proietto J, Andrikopoulos S, Cappai R. Identification of the Alzheimer's disease amyloid precursor protein (APP) and its homologue APLP2 as essential modulators of glucose and insulin homeostasis and growth. J Pathol 215: 155-163, 2008.
36. Nicholson A, Reifsnyder PC, Malcolm RD, Lucas CA, MacGregor GR, Zhang WD, Leiter EH. Diet-induced obesity in two C57BL/6 substrains with intact or mutant nicotinamide nucleotide transhydrogenase (Nnt) gene. Obesity (Silver Spring) 18: 1902-1905, 2010.
37. Rapaport D, Lugassy Y, Sprecher E, Horowitz M. Loss of SNAP29 impairs endocytic recycling and cell motility. PLoS One 5: e9759, 2010.
38. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology 1: 43-46, 1990.
39. Saito T, Guan F, Papolos DF, Rajouria N, Fann CS, Lachman HM. Polymorphism in SNAP29 gene promoter region associated with schizophrenia. Mol Psychiatry 6: 193-201, 2001.
40. Sluyter F, Marican CC, Crusio WE. Further phenotypical characterisation of two substrains of C57BL/6J inbred mice differing by a spontaneous single-gene mutation. Behav Brain Res 98: 39-43, 1999.
41. Spillantini MG, Goedert M. The alpha-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann NY Acad Sci 920: 16-27, 2000.
42. Sprecher E, Ishida-Yamamoto A, Mizrahi-Koren M, Rapaport D, Goldsher D, Indelman M, Topaz O, Chefetz I, Keren H, O'Brien TJ, Bercovich D, Shalev S, Geiger D, Bergman R, Horowitz M, Mandel H. A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am J Hum Genet 77: 242-251, 2005.
43. Stoehr JP, Nadler ST, Schueler KL, Rabaglia ME, Yandell BS, Metz SA, Attie AD. Genetic obesity unmasks nonlinear interactions between murine type 2 diabetes susceptibility loci. Diabetes 49: 1946-1954, 2000.
44. Su Q, Mochida S, Tian JH, Mehta R, Sheng ZH. SNAP-29: a general SNARE protein that inhibits SNARE disassembly and is implicated in synaptic transmission. Proc Natl Acad Sci USA 98: 14038-14043, 2001.
45. Tanji K, Mori F, Imaizumi T, Yoshida H, Matsumiya T, Tamo W, Yoshimoto M, Odagiri H, Sasaki M, Takahashi H, Satoh K, Wakabayashi K. Upregulation of alpha-synuclein by lipopolysaccharide and interleukin-1 in human macrophages. Pathol Int 52: 572-577, 2002.
46. Toye AA, Lippiat JD, Proks P, Shimomura K, Bentley L, Hugill A, Mijat V, Goldsworthy M, Moir L, Haynes A, Quarterman J, Freeman HC, Ashcroft FM, Cox RD. A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 48: 675-686, 2005.
47. von Koch CS, Zheng H, Chen H, Trumbauer M, Thinakaran G, van der Ploeg LH, Price DL, Sisodia SS. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol Aging 18: 661-669, 1997.
48. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigo R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O'Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562, 2002.
49. Wickner W, Schekman R. Membrane fusion. Nat Struct Mol Biol 15: 658-664, 2008.
50. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, Smith DW, Heavens RP, Dawson GR, Boyce S, Conner MW, Stevens KA, Slunt HH, Sisoda SS, Chen HY, Van der Ploeg LH. beta-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81: 525-531, 1995.
51. Zurita E, Chagoyen M, Cantero M, Alonso R, Gonzalez-Neira A, Lopez-Jimenez A, Lopez-Moreno JA, Landel CP, Benitez J, Pazos F, Montoliu L. Genetic polymorphisms among C57BL/6 mouse inbred strains. Transgenic Res 20: 481-489, 2011.