Microarray gene expression profiles of fasting induced changes in liver and adipose tissues of pigs expressing the melanocortin-4 receptor D298N variant

Physiological Genomics

Volumn 38, Issue 1, 2009, Pages 98-111

  Lkhagvadorj, Sender ^a   Qu, Long ^a,b   Cai, Weiguo ^a,b   Couture, Oliver P ^a   Barb, C Richard ^c   Hausman, Gary J ^c   Nettleton, Dan ^a,b   Anderson, Lloyd L ^a   Dekkers, Jack C M ^a   Tuggle, Christopher K ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

ESR1; Feed deprivation; MC4R; Transcription

Indexed keywords

AMINO ACID; FATTY ACID; GLUCOSE; LIPID; MELANOCORTIN 4 RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEROID; TRANSCRIPTION FACTOR; UREA;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL ADHESION; CELL JUNCTION; DIET RESTRICTION; DOWN REGULATION; ENZYME METABOLISM; EXTRACELLULAR MATRIX; FATTY ACID BLOOD LEVEL; FATTY ACID OXIDATION; GENE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENOTYPE; GILT (SWINE); LIPOGENESIS; LIVER; MC4R GENE; MICROARRAY ANALYSIS; MISSENSE MUTATION; MORPHOGENESIS; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN VARIANT; STEROIDOGENESIS; UREA BLOOD LEVEL;

ADIPOSE TISSUE; ANIMALS; FASTING; GENE EXPRESSION PROFILING; LIVER; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RECEPTOR, MELANOCORTIN, TYPE 4; SWINE;

SUIDAE; SUS;

EID: 67649488084     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.90372.2008     Document Type: Article

References (82)

1. 2 uptake, and β-oxidation. Am J Physiol Regul Integr Comp Physiol 272: R1641-R1646, 1997.
2. Adan RA, Tiesjema B, Hillebrand JJ, la Fleur SE, Kas MJ, de Krom M. The MC4 receptor and control of appetite. Br J Pharmacol 149: 815-827, 2006. (Pubitemid 44851706)
3. Affymetrix Inc. Statistical algorithms description document. http://www.affymetrixcom/support/technical/whitepapers/sadd-whitepaperpdf 2002.
4. Barb CR, Robertson AS, Barrett JB, Kraeling RR, Houseknecht KL. The role of melanocortin-3 and -4 receptor in regulating appetite, energy homeostasis and neuroendocrine function in the pig. J Endocrinol 181: 39-52, 2004. (Pubitemid 38584662)
5. Barboni B, Martelli A, Berardinelli P, Russo V, Turriani M, Bernabo N, Lucidi P, Mattioli M. Ovarian follicle vascularization in fasted pig. Theriogenology 62: 943-957, 2004. (Pubitemid 38893949)
6. Barendse W, Reverter A, Bunch RJ, Harrison BE, Barris W, Thomas MB. A validated whole-genome association study of efficient food conversion in cattle. Genetics 176: 1893-1905, 2007.
7. Bauer M, Hamm AC, Bonaus M, Jacob A, Jaekel J, Schorle H, Pankratz MJ, Katzenberger JD. Starvation response in mouse liver shows strong correlation with life-span-prolonging processes. Physiol Genomics 17: 230-244, 2004. (Pubitemid 38924168)
8. Bustin SA. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29: 23-39, 2002. (Pubitemid 34965744)
9. Cai W, Casey DS, Dekkers JC. Selection response and genetic parameters for residual feed intake in Yorkshire swine. J Anim Sci 86: 287-298, 2008. (Pubitemid 351229750)
10. Cao Y. Angiogenesis modulates adipogenesis and obesity. J Clin Invest 117: 2362-2368, 2007. (Pubitemid 47494333)
11. Cazes A, Galaup A, Chomel C, Bignon M, Brechot N, Le Jan S, Weber H, Corvol P, Muller L, Germain S, Monnot C. Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ Res 99: 1207-1215, 2006. (Pubitemid 44808657)
12. Cederberg A, Gronning LM, Ahren B, Tasken K, Carlsson P, Enerback S. FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106: 563-573, 2001. (Pubitemid 32879318)
13. Cheng PT, Mukherjee R. PPARs as targets for metabolic and cardiovascular diseases. Mini Rev Med Chem 5: 741-753, 2005. (Pubitemid 41051897)
14. Cheon Y, Nara TY, Band MR, Beever JE, Wallig MA, Nakamura MT. Induction of overlapping genes by fasting and a peroxisome proliferator in pigs: evidence of functional PPARalpha in nonproliferating species. Am J Physiol Regul Integr Comp Physiol 288: R1525-R1535, 2005. (Pubitemid 40720702)
15. Cherel Y, Le Maho Y. Refeeding after the late increase in nitrogen excretion during prolonged fasting in the rat. Physiol Behav 50: 345-349, 1991.
16. Dawson HD, Beshah E, Nishi S, Solano-Aguilar G, Morimoto M, Zhao A, Madden KB, Ledbetter TK, Dubey JP, Shea-Donohue T, Lunney JK, Urban JF Jr. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect Immun 73: 1116-1128, 2005. (Pubitemid 40165772)
17. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3, 2003.
18. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev 86: 465-514, 2006.
19. Dietschy JM, Siperstein MD. Effect of cholesterol feeding and fasting on sterol synthesis in seventeen tissues of rat. J Lipid Res 8: 97-104, 1967.
20. Eberle D, Hegarty B, Bossard P, Ferre P, Foufelle F. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86: 839-848, 2004. (Pubitemid 39602764)
21. Fan ZC, Sartin JL, Tao YX. Pharmacological analyses of two naturally occurring porcine melanocortin-4 receptor mutations in domestic pigs. Domest Anim Endocrinol 34: 383-390, 2008.
22. Fausch HD, Richmond R, Thomas A. Influence of fasting on body composition and tissue cholesterol levels in swine. J Anim Sci 27: 1273-1276, 1968.
23. Ferraz AL, Ojeda A, Lopez-Bejar M, Fernandes LT, Castello A, Folch JM, Perez-Enciso M. Transcriptome architecture across tissues in the pig. BMC Genomics 9: 173, 2008. (Pubitemid 351587116)
24. Fortier M, Wang SP, Mauriege P, Semache M, Mfuma L, Li H, Levy E, Richard D, Mitchell GA. Hormone-sensitive lipase-independent adipocyte lipolysis during beta-adrenergic stimulation, fasting, and dietary fat loading. Am J Physiol Endocrinol Metab 287: E282-E288, 2004. (Pubitemid 38943894)
25. Gabler NK, Spencer JD, Webel DM, Spurlock ME. In utero and postnatal exposure to long chain (n-3) PUFA enhances intestinal glucose absorption and energy stores in weanling pigs. J Nutr 137: 2351-2358, 2007. (Pubitemid 350058700)
26. Gallagher CJ, Langefeld CD, Gordon CJ, Campbell JK, Mychaleckyj JC, Bryer-Ash M, Rich SS, Bowden DW, Sale MM. Association of the estrogen receptor-alpha gene with the metabolic syndrome and its component traits in African-American families: the Insulin Resistance Atherosclerosis Family Study. Diabetes 56: 2135-2141, 2007. (Pubitemid 47195830)
27. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80, 2004.
28. Govoni N, De Iasio R, Cocco C, Parmeggiani A, Galeati G, Pagotto U, Brancia C, Spinaci M, Tamanini C, Pasquali R, Ferri GL, Seren E. Gastric immunolocalization and plasma profiles of acyl-ghrelin in fasted and fasted-refed prepuberal gilts. J Endocrinol 186: 505-513, 2005. (Pubitemid 41404069)
29. Graeme T, Roese G. Pork-cost of production. New South Wales Department of Primary Industries 66: 1-3, 2006.
30. Hato T, Tabata M, Oike Y. The role of angiopoietin-like proteins in angiogenesis and metabolism. Trends Cardiovasc Med 18: 6-14, 2008.
31. Hausman GJ, Barb CR, Dean RG. Patterns of gene expression in pig adipose tissue: Insulin-like growth factor system proteins, neuropeptide Y (NPY), NPY receptors, neurotrophic factors and other secreted factors. Domest Anim Endocrinol 35: 24-34, 2008.
32. Hausman GJ, Richardson RL. Adipose tissue angiogenesis. J Anim Sci 82: 925-934, 2004. (Pubitemid 38572359)
33. Hayashi H, Sano H, Seo S, Kume T. The Foxc2 transcription factor regulates angiogenesis via induction of integrin-3 expression. J Biol Chem 283: 23791-23800, 2008.
34. Huang Q, Wang TH, Lu WS, Mu PW, Yang YF, Liang WW, Li CX, Lin GP. Estrogen receptor alpha gene polymorphism associated with type 2 diabetes mellitus and the serum lipid concentration in Chinese women in Guangzhou. Chin Med J (Engl) 119: 1794 - 1801, 2006. (Pubitemid 44768609)
35. Huang S, Mills L, Mian B, Tellez C, McCarty M, Yang XD, Gudas JM, Bar-Eli M. Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol 161: 125-134, 2002. (Pubitemid 34760778)
36. Irizarry RA, Gautier L, Bolstad BM, Miller C, From WC, Astrand M, Cope LM, Gentleman R, Gentry J, Halling C, Huber W, MacDonald J, Rubinstein BIP, Workman C, Zhang J. Affy: methods for Afffymetrix oligonucleotide arrays. R package version 1142, 2007.
37. Ishizuka T, Lazar MA. The nuclear receptor corepressor deacetylase activating domain is essential for repression by thyroid hormone receptor. Mol Endocrinol 19: 1443-1451, 2005. (Pubitemid 41002976)
38. Kenward MG, Roger JH. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983-997, 1997. (Pubitemid 27391027)
39. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103: 1489-1498, 1999.
40. Kim JB, Sarraf P, Wright M, Yao KM, Mueller E, Solanes G, Lowell BB, Spiegelman BM. Nutritional and insulin regulation of fatty acid synthetase and leptin gene expression through ADD1/SREBP1. J Clin Invest 101: 1-9, 1998. (Pubitemid 28058896)
41. Kim KS, Larsen N, Short T, Plastow G, Rothschild MF. A missense variant of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth, and feed intake traits. Mamm Genome 11: 131-135, 2000. (Pubitemid 30054415)
42. Kim KS, Reecy JM, Hsu WH, Anderson LL, Rothschild MF. Functional and phylogenetic analyses of a melanocortin-4 receptor mutation in domestic pigs. Domest Anim Endocrinol 26: 75-86, 2004. (Pubitemid 38106235)
43. Kouda K, Nakamura H, Kohno H, Ha-Kawa SK, Tokunaga R, Sawada S. Dietary restriction: effects of short-term fasting on protein uptake and cell death/proliferation in the rat liver. Mech Ageing Dev 125: 375-380, 2004. (Pubitemid 38595189)
44. Larson B, Kliebenstein J. Cost of organic pork production. Iowa State University Animal Industry Report Iowa State University AS Leaflet Management/Economics: R1784B, 2003.
45. Le Jan S, Amy C, Cazes A, Monnot C, Lamande N, Favier J, Philippe J, Sibony M, Gasc JM, Corvol P, Germain S. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol 162: 1521-1528, 2003. (Pubitemid 36512834)
46. Lee CH, Olson P, Evans RM. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144: 2201-2207, 2003. (Pubitemid 36629867)
47. Lee OH, Bae SK, Bae MH, Lee YM, Moon EJ, Cha HJ, Kwon YG, Kim KW. Identification of angiogenic properties of insulin-like growth factor II in in vitro angiogenesis models. Br J Cancer 82: 385-391, 2000. (Pubitemid 30045386)
48. Li JY, Lescure PA, Misek DE, Lai YM, Chai BX, Kuick R, Thompson RC, Demo RM, Kurnit DM, Michailidis G, Hanash SM, Gantz I. Food deprivation-induced expression of minoxidil sulfotransferase in the hypothalamus uncovered by microarray analysis. J Biol Chem 277: 9069-9076, 2002. (Pubitemid 34952982)
49. Li RY, Zhang QH, Liu Z, Qiao J, Zhao SX, Shao L, Xiao HS, Chen JL, Chen MD, Song HD. Effect of short-term and long-term fasting on transcriptional regulation of metabolic genes in rat tissues. Biochem Biophys Res Commun 344: 562-570, 2006.
50. Liu WM, Mei R, Di X, Ryder TB, Hubbell E, Dee S, Webster TA, Harrington CA, Ho MH, Baid J, Smeekens SP. Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics 18: 1593-1599, 2002. (Pubitemid 36097724)
51. Mandard S, Zandbergen F, van Straten E, Wahli W, Kuipers F, Muller M, Kersten S. The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem 281: 934-944, 2006.
52. Martin-Requero A, Ayuso MS, Parrilla R. Rate-limiting steps for hepatic gluconeogenesis. Mechanism of oxamate inhibition of mitochondrial pyruvate metabolism. J Biol Chem 261: 13973-13978, 1986. (Pubitemid 17196296)
53. McNeel RL, Mersmann HJ. Nutritional deprivation reduces the transcripts for transcription factors and adipocyte-characteristic proteins in porcine adipocytes. J Nutr Biochem 11: 139-146, 2000. (Pubitemid 30163086)
54. Miller ER, Ullrey DE. The pig as a model for human nutrition. Annu Rev Nutr 7: 361-382, 1978.
55. Nakai Y, Hashida H, Kadota K, Minami M, Shimizu K, Matsumoto I, Kato H, Abe K. Up-regulation of genes related to the ubiquitin-proteasome system in the brown adipose tissue of 24-h-fasted rats. Biosci Biotechnol Biochem 72: 139-148, 2008. (Pubitemid 351158967)
56. Neubert E, Scholze C, Kratzsch J, Gurtler H. Plasma levels of catecholamines and lipolysis during starvation in growing pigs. Zentralbl Veterinarmed A 46: 247-253, 1999. (Pubitemid 129572336)
57. Nikitin A, Egorov S, Daraselia N, Mazo I. Pathway studio-the analysis and navigation of molecular networks. Bioinformatics 19: 2155-2157, 2003. (Pubitemid 37408171)
58. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90, 2003. (Pubitemid 36223280)
59. Quilter CR, Gilbert CL, Oliver GL, Jafer O, Furlong RA, Blott SC, Wilson AE, Sargent CA, Mileham A, Affara NA. Gene expression profiling in porcine maternal infanticide: a model for puerperal psychosis. Am J Med Genet B Neuropsychiatr Genet 47B: 1126-1137, 2008.
60. R Development Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2007.
61. Schadendorf D, Moller A, Algermissen B, Worm M, Sticherling M, Czarnetzki BM. IL-8 produced by human malignant melanoma cells in vitro is an essential autocrine growth factor. J Immunol 151: 2667-2675, 1993. (Pubitemid 23264518)
62. Schinner S, Scherbaum WA, Bornstein SR, Barthel A. Molecular mechanisms of insulin resistance. Diabet Med 22: 674-682, 2005. (Pubitemid 40805885)
63. Schook L, Beattie C, Beever J, Donovan S, Jamison R, Zuchermann F, Niemi S, Rothschild M, Rutherford M, Smith D. Swine biomedical research: Creating the building blocks of animal models. Anim Biotechnol 16: 183-190, 2005.
64. Serini G, Valdembri D, Bussolino F. Integrins and angiogenesis: a sticky business. Exp Cell Res 312: 651-658, 2006. (Pubitemid 43290341)
65. Shimano H. Sterol regulatory element-binding protein family as global regulators of lipid synthetic genes in energy metabolism. Vitam Horm 65: 167-194, 2002. (Pubitemid 135763175)
66. Spath H, Gurtler H. Impact of feed withdrawal on effects of adrenergic agonists on parameters of carbohydrate and fat metabolism in plasma of growing pigs. Proc IXth Int Conf Production Diseases in Farm Animals. Berlin: Free University of Berlin, 1995, p. 400.
67. Spurlock ME, Frank GR, Cornelius SG, Ji S, Willis GM, Bidwell CA. Obese gene expression in porcine adipose tissue is reduced by food deprivation but not by maintenance or submaintenance intake. J Nutr 128: 677-682, 1998. (Pubitemid 28158479)
68. Storey JD, Tibshirani R. Statistical significance for genome-wide experiments. Proc Natl Acad Sci USA 100: 9440-9445, 2003.
69. Sukonina V, Lookene A, Olivecrona T, Olivecrona G. Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc Natl Acad Sci USA 103: 17450-17455, 2006. (Pubitemid 44788989)
70. Suzuki J, Shen WJ, Nelson BD, Selwood SP, Murphy GM Jr, Kanehara H, Takahashi S, Oida K, Miyamori I, Kraemer FB. Cardiac gene expression profile and lipid accumulation in response to starvation. Am J Physiol Endocrinol Metab 283: E94-E102, 2002. (Pubitemid 34686673)
71. Sztalryd C, Kraemer FB. Regulation of hormone-sensitive lipase during fasting. Am J Physiol Endocrinol Metab 266: E179-E185, 1994. (Pubitemid 24099269)
72. Takeda N, Maemura K, Imai Y, Harada T, Kawanami D, Nojiri T, Manabe I, Nagai R. Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ Res 95: 146-153, 2004. (Pubitemid 38988680)
73. Te Pas MF, Hulsegge I, Coster A, Pool MH, Heuven HH, Janss LL. Biochemical pathways analysis of microarray results: regulation of myogenesis in pigs. BMC Dev Biol 7: 66, 2007. (Pubitemid 47062936)
74. Tuggle CK, Wang Y, Couture O. Advances in swine transcriptomics. Int J Biol Sci 3: 132-152, 2007. (Pubitemid 46272774)
75. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034, 2002.
76. Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS, Moller DE. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J Clin Invest 97: 2553-2561, 1996. (Pubitemid 26187343)
77. Wang YX, Lee CH, Tiep S, Yu RT, Ham J, Kang H, Evans RM. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 113: 159-170, 2003. (Pubitemid 36514968)
78. Williams DL, Schwartz MW. The melanocortin system as a central integrator of direct and indirect controls of food intake. Am J Physiol Regul Integr Comp Physiol 289: R2-R3, 2005. (Pubitemid 40874951)
79. Xia G, Kageyama Y, Hayashi T, Kawakami S, Yoshida M, Kihara K. Regulation of vascular endothelial growth factor transcription by endothelial PAS domain protein 1 (EPAS1) and possible involvement of EPAS1 in the angiogenesis of renal cell carcinoma. Cancer 91: 1429-1436, 2001. (Pubitemid 32319252)
80. Xue Y, Cao R, Nilsson D, Chen S, Westergren R, Hedlund EM, Martijn C, Rondahl L, Krauli P, Walum E, Enerback S, Cao Y. FOXC2 controls Ang-2 expression and modulates angiogenesis, vascular patterning, remodeling, and functions in adipose tissue. Proc Natl Acad Sci USA 105: 10167-10172, 2008.
81. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP.Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15, 2002.
82. Zhao SH, Kuhar D, Lunney JK, Dawson H, Guidry C, Uthe JJ, Bearson SM, Recknor J, Nettleton D, Tuggle CK. Gene expression profiling in Salmonella Choleraesuis-infected porcine lung using a long oligonucleotide microarray. Mamm Genome 17: 777-789, 2006. (Pubitemid 44079949)