Metabolomic profiles indicate distinct physiological pathways affected by two loci with major divergent effect on Bos taurus growth and lipid deposition

Physiological Genomics

Volumn 42 A, Issue 2, 2010, Pages 79-88

  Weikard, Rosemarie ^a   Altmaier, Elisabeth ^b   Suhre, Karsten ^b   Weinberger, Klaus M ^c   Hammon, Harald M ^a   Albrecht, Elke ^a   Setoguchi, Kouji ^d   Takasuga, Akiko ^e   Kühn, Christa ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c BIOCRATES LIFE SCIENCES AG   (Austria)

^d Cattle Breeding Development Institute of Kagoshima Prefecture   (Japan)

^e Japan Livestock Technology Association   (Japan)

Author keywords

Arginine; Carnitine; Disproportional growth; Genetic association; Non SMC condensin I complex, subunit G gene

Indexed keywords

CARNITINE; CELL CYCLE PROTEIN; MYOSTATIN; PHOSPHATIDYLCHOLINE; PROTEIN NCAPG; SPHINGOMYELIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BODY MASS; CONTROLLED STUDY; COW; GENE LOCUS; GENE MUTATION; GENETIC ASSOCIATION; LIPID STORAGE; MALE; METABOLOMICS; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PUBERTY;

ALLELES; AMINO ACID SUBSTITUTION; ANIMALS; ANIMALS, NEWBORN; ARGININE; BODY COMPOSITION; CARNITINE; CATTLE; CELL CYCLE PROTEINS; GENETIC LOCI; LIPID METABOLISM; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MUTATION; MYOSTATIN; PHOSPHATIDYLCHOLINES; REPRODUCIBILITY OF RESULTS; SEXUAL MATURATION; SPHINGOMYELINS;

ANIMALIA; BOS; BOS TAURUS; BOVINAE; MAMMALIA;

EID: 77958032880     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00120.2010     Document Type: Article

References (61)

1. Aksglaede L, Olsen LW, Sorensen TIA, Juul A. Forty years trends in timing of pubertal growth spurt in 157,000 Danish school children. Plos One 3: e2728, 2008.
2. Allais S, Leveziel H, Payet-Duprat N, Hocquette JF, Lepetit J, Rousset S, Denoyelle C, Bernard-Capel C, Journaux L, Bonnot A, Renand G. The two mutations, Q204X and nt821, of the myostatin gene affect carcass and meat quality in young heterozygous bulls of French beef breeds. J Anim Sci 88: 446-454, 2010.
3. Altmaier E, Ramsay SL, Graber A, Mewes HW, Weinberger KM, Suhre K. Bioinformatics analysis of targeted metabolomics - Uncovering old and new tales of diabetic mice under medication. Endocrinology 149: 3478-3489, 2008. (Pubitemid 351919596)
4. Andersson L, Georges M. Domestic-animal genomics: deciphering the genetics of complex traits. Nat Rev Genet 5: 202-212, 2004.
5. Ansay M, Hanset R. Anatomical, physiological and biochemical differences between conventional and double-muscled cattle in the Belgian blue and white breed. Livestock Prod Sci 6: 5-13, 1979.
6. Barber KA, Almquist JO. Growth and feed efficiency and their relationship to puberal traits of Charolais bulls. J Anim Sci 40: 288-301, 1975.
7. Bedford MT, Richard S. Arginine methylation: an emerging regulator of protein function. Mol Cell 18: 263-272, 2005.
8. Bellmann O, Wegner J, Teuscher F, Schneider F, Ender K. Muscle characteristics and corresponding hormone concentrations in different types of cattle. Livestock Prod Sci 85: 45-57, 2004. (Pubitemid 38086364)
9. Brody S. Bioenergetics and Growth. New York: Reinhold, 1945.
10. Bulau P, Zakrzewicz D, Kitowska K, Leiper J, Gunther A, Grimminger F, Eickelberg O. Analysis of methylarginine metabolism in the cardiovascular system identifies the lung as a major source of ADMA. Am J Physiol Lung Cell Mol Physiol 292: L18-L24, 2007.
11. Casas E, Lunstra DD, Cundiff LV, Ford JJ. Growth and pubertal development of F-1 bulls from Hereford, Angus, Norwegian Red, Swedish Red and White, Friesian, and Wagyu sires. J Anim Sci 85: 475, 2007.
12. Chelh I, Meunier B, Picard B, Reecy MJ, Chevalier C, Hocquette JF, Cassar-Malek I. Molecular profiles of quadriceps muscle in myostatinnull mice reveal PI3K and apoptotic pathways as myostatin targets. BMC Genomics 10: 196, 2009.
13. Cui Z, Houweling M. Phosphatidylcholine and cell death. Biochim Biophys Acta 1585: 87-96, 2002.
14. De Smet S, Raes K, Demeyer D. Meat fatty acid composition as affected by fatness and genetic factors: a review. Anim Res 53: 81-98, 2004.
15. Dej KJ, Ahn C, Orr-Weaver TL. Mutations in the Drosophila condensin subunit dCAP-G: Defining the role of condensin for chromosome condensation in mitosis and gene expression in interphase. Genetics 168: 895-906, 2004. (Pubitemid 39491466)
16. Dumas ME, Wilder SP, Bihoreau MT, Barton RH, Fearnside JF, Argoud K, D'Amato L, Wallis RH, Blancher C, Keun HC, Baunsgaard D, Scott J, Sidelmann UG, Nicholson JK, Gauguier D. Direct quantitative trait locus mapping of mammalian metabolic phenotypes in diabetic and normoglycemic rat models. Nat Genet 39: 666-672, 2007.
17. Dunner S, Miranda ME, Amigues Y, Canon J, Georges M, Hanset R, Williams J, Menissier F. Haplotype diversity of the myostatin gene among beef cattle breeds. Genet Sel Evol 35: 103-118, 2003.
18. Eberlein A, Takasuga A, Setoguchi K, Pfuhl R, Flisikowski K, Fries R, Klopp N, Furbass R, Weikard R, Kuhn C. Dissection of genetic factors modulating fetal growth in cattle indicates a substantial role of the non-SMC condensin I complex, subunit G (NCAPG) gene. Genetics 183: 951-964, 2009.
19. Everts RE, Chavatte-Palmer P, Razzak A, Hue I, Green CA, Oliveira R, Vignon X, Rodriguez-Zas SL, Tian XC, Yang XZ, Renard JP, Lewin HA. Aberrant gene expression patterns in placentomes are associated with phenotypically normal and abnormal cattle cloned by somatic cell nuclear transfer. Physiol Genomics 33: 65-77, 2008.
20. Geiman TM, Sankpal UT, Robertson AK, Chen Y, Mazumdar M, Heale JT, Schmiesing JA, Kim W, Yokomori K, Zhao YM, Robertson KD. Isolation and characterization of a novel DNA methyltransferase complex linking DNMT3B with components of the mitotic chromosome condensation machinery. Nucl Acids Res 32: 2716-2729, 2004.
21. Gieger C, Geistlinger L, Altmaier E, de Angelis MH, Kronenberg F, Meitinger T, Mewes HW, Wichmann HE, Weinberger KM, Adamski J, Illig T, Suhre K. Genetics meets metabolomics: a genome-wide association study of metabolite profiles in human serum. Plos Genet 4: e1000282, 2008.
22. Grobet L, Martin LJR, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M. A deletion in the bovine myostatin gene causes the double- muscled phenotype in cattle. Nat Genet 17: 71-74, 1997.
23. Gudbjartsson DF, Walters GB, Thorleifsson G, Stefansson H, Halldorsson BV, Zusmanovich P, Sulem P, Thorlacius S, Gylfason A, Steinberg S, Helgadottir A, Ingason A, Steinthorsdottir V, Olafsdottir EJ, Olafsdottir GH, Jonsson T, Borch-Johnsen K, Hansen T, Andersen G, Jorgensen T, Pedersen O, Aben KK, Witjes JA, Swinkels DW, den Heijer M, Franke B, Verbeek ALM, Becker DM, Yanek LR, Becker LC, Tryggvadottir L, Rafnar T, Gulcher J, Kiemeney LA, Kong A, Thorsteinsdottir U, Stefansson K. Many sequence variants affecting diversity of adult human height. Nat Genet 40: 609-615, 2008.
24. Illig T, Gieger C, Zhai G, Römisch-Margl W, Wang-Sattler R, Prehn C, Altmaier E, Kastenmuller G, Kato BS, Mewes HW, Meitinger T, Hrabe de Angelis M, Kronenberg F, Soranzo N, Wichmann HE, Spector TD, Adamski J, Suhre K. A genome-wide perspective of genetic variation in human metabolism. Nat Genet 42: 137-141, 2010.
25. Kashyap SR, Lara A, Zhang R, Park YM, DeFronzo RA. Insulin reduces plasma arginase activity in type 2 diabetic patients. Diabetes Care 31: 134-139, 2008.
26. Kielstein JT, Salpeter SR, Bode-Boeger SM, Cooke JP, Fliser D. Symmetric dimethylarginine (SDMA) as endogenous marker of renal function - a meta-analysis. Nephrol Dial Transpl 21: 2446-2451, 2006. (Pubitemid 44644516)
27. Kluge R, Giesen K, Bahrenberg G, Plum L, Ortlepp JR, Joost HG. Quantitative trait loci for obesity and insulin resistance (Nob1, Nob2) and their interaction with the leptin receptor allele (Lper(A720T/T1044I)) in New Zealand obese mice. Diabetologia 43: 1565-1572, 2000.
28. Kühn C, Bellmann O, Voigt J, Wegner J, Guiard V, Ender K. An experimental approach for studying the genetic and physiological background of nutrient transformation in cattle with respect to nutrient secretion and accretion type. Arch Anim Breed 45: 317-330, 2002.
29. Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277: 49831-49840, 2002.
30. Lee J, Ryu H, Ferrante RJ, Morris SM, Ratan RR. Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proc Natl Acad Sci USA 100: 4843-4848, 2003.
31. Lira VA, Soltow QA, Long JHD, Betters JL, Sellman JE, Criswell DS. Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am J Physiol Endocrinol Metab 293: E1062-E1068, 2007.
32. Losel D, Kalbe C, Rehfeldt C. L-Carnitine supplementation during suckling intensifies the early postnatal skeletal myofiber formation in piglets of low birth weight. J Anim Sci 87: 2216-2226, 2009.
33. Mangoni AA. The emerging role of symmetric dimethylarginine in vascular disease. Adv Clin Chem 48: 73-94, 2009.
34. McKay S, Schnabel R, Murdoch B, Matukumalli L, Aerts J, Coppieters W, Crews D, Dias Neto E, Gill C, Gao C, Mannen H, Wang Z, Tassell C, Williams J, Taylor J, Moore S. An assessment of population structure in eight breeds of cattle using a whole genome SNP panel. BMC Genetics 9: 37, 2008.
35. Morris CA, Pitchford WS, Cullen NG, Esmailizadeh AK, Hickey SM, Hyndman D, Dodds KG, Afolayan RA, Crawford AM, Bottema CDK. Quantitative trait loci for live animal and carcass composition traits in Jersey and Limousin back-cross cattle finished on pasture or feedlot. Anim Genet 40: 648-654, 2009.
36. Oikawa T, Sanehira T, Sato K, Mizoguchi Y, Yamamoto H, Baba M. Genetic parameters for growth and carcass traits of Japanese Black (Wagyu) cattle. Anim Sci 71: 59-64, 2000.
37. Perez-Enciso M, Misztal I. Qxpak: a versatile mixed model application for genetical genomics and QTL analyses. Bioinformatics 20: 2792-2798, 2004.
38. Pfuhl R, Bellmann O, Kuhn C, Teuscher F, Ender K, Wegner J. Beef versus dairy cattle: a comparison of feed conversion, carcass composition, and meat quality. Arch Anim Breed 50: 59-70, 2007.
39. Pope AJ, Karrupiah K, Kearns PN, Xia Y, Cardounel AJ. Role of dimethylarginine dimethylaminohydrolases in the regulation of endothelial nitric oxide production. J Biol Chem 284: 35338-35347, 2009.
40. Ringseis R, Wege N, Wen GP, Rauer C, Hirche F, Kluge H, Eder K. Carnitine synthesis and uptake into cells are stimulated by fasting in pigs as a model of nonproliferating species. J Nutr Biochem 20: 840-847, 2009.
41. Rios R, Carneiro I, Arce VM, Devesa J. Myostatin is an inhibitor of myogenic differentiation. Am J Physiol Cell Physiol 282: C993-C999, 2002.
42. Roy D, Perreault M, Marette A. Insulin stimulation of glucose uptake in skeletal muscles and adipose tissues in vivo is NO dependent. Am J Physiol Endocrinol Metab 274: E692-E699, 1998.
43. Schulze F, Carter AM, Schwedhelm E, Ajjan R, Maas R, von Holten RA, Atzler D, Grant PJ, Boger RH. Symmetric dimethylarginine predicts all-cause mortality following ischemic stroke. Atherosclerosis 208: 518-523, 2010.
44. Seipold S, Priller FC, Goldsmith P, Harris WA, Baier H, Abdelilah-Seyfried S. Non-SMC condensin I complex proteins control chromosome segregation and survival of proliferating cells in the zebrafish neural retina BMC. Dev Biol 9: 40, 2009.
45. Setoguchi K, Furuta M, Hirano T, Nagao T, Watanabe T, Sugimoto Y, Takasuga A. Cross-breed comparisons identified a critical 591 kb region for bovine carcass weight QTL (CW-2) on chromosome 6 and the Ile-442-Met substitution in NCAPG as a positional candidate. BMC Genetics 10: 43, 2009.
46. Snelling WM, Allan MF, Keele JW, Kuehn LA, McDaneld T, Smith TPL, Sonstegard TS, Thallman RM, Bennett GL. Genome-wide association study of growth in crossbred beef cattle. J Anim Sci 88: 837-848, 2010.
47. Soranzo N, Rivadeneira F, Chinappen-Horsley U, Malkina I, Richards JB, Hammond N, Stolk L, Nica A, Inouye M, Hofman A, Stephens J, Wheeler E, Arp P, Gwilliam R, Jhamai PM, Potter S, Chaney A, Ghori MJR, Ravindrarajah R, Ermakov S, Estrada K, Pols HAP, Williams FM, McArdle WL, van Meurs JB, Loos RJF, Dermitzakis ET, Ahmadi KR, Hart DJ, Ouwehand WH, Wareham NJ, Barroso I, Sandhu MS, Strachan DP, Livshits G, Spector TD, Uitterlinden AG, Deloukas P. Meta-analysis of genome-wide scans for human adult stature identifies novel loci and associations with measures of skeletal frame size. Plos Genet 5: e1000445, 2009.
48. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445, 2003.
49. Symonds ME, Sebert SP, Hyatt MA, Budge H. Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 5: 604-610, 2009.
50. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275: 40235-40243, 2000.
51. Tomassini V, Pozzilli C, Onesti E, Pasqualetti P, Marinelli F, Pisani A, Fieschi C. Comparison of the effects of acetyl L-carnitine and amantadine for the treatment of fatigue in multiple sclerosis: results of a pilot, randomised, double-blind, crossover trial. J Neurol Sci 218: 103-108, 2004.
52. Tu P, Bhasin S, Hruz P, Herbst K, Castellani L, Hua N, Hamilton J, Guo W. Genetic disruption of myostatin reduces the development of proatherogenic dyslipidemia and atherogenic lesions in Ldlr null mice. Diabetes 58: 1739-1748, 2009.
53. Wang ZN, Tang WHW, Cho L, Brennan DM, Hazen SL. Targeted metabolomic evaluation of arginine methylation and cardiovascular risks potential mechanisms beyond nitric oxide synthase inhibition. Arterioscler Thromb Vasc Biol 29: 1383-1391, 2009.
54. Weedon MN, Lango H, Lindgren CM, Wallace C, Evans DM, Mangino M, Freathy RM, Perry JRB, Stevens S, Hall AS, Samani NJ, Shields B, Prokopenko I, Farrall M, Dominiczak A; Diabetes Genetics Initiative; Wellcome Trust Case Control Consortium, Johnson T, Bergmann S, Beckmann JS, Vollenweider P, Waterworth DM, Mooser V, Palmer CNA, Morris AD, Ouwehand WH; Cambridge GEM Consortium, Zhao JH, Li S, Loos RJ, Barroso I, Deloukas P, Sandhu MS, Wheeler E, Soranzo N, Inouye M, Wareham NJ, Caulfield M, Munroe PB, Hattersley AT, McCarthy MI, Frayling TM. Genome-wide association analysis identifies 20 loci that influence adult height. Nat Genet 40: 575-583, 2008.
55. Weinberger KM. Metabolomics in diagnosing metabolic diseases. Ther Umsch 65: 487-491, 2005.
56. Weinberger KM, Graber A. Using comprehensive metabolomics to identify novel biomarkers. Screen Trends Drug Discov 6: 42-45, 2008.
57. Wenk MR. The emerging field of lipidomics. Nat Rev Drug Discov 4: 594-610, 2005.
58. Wu G, Bazer F, Davis T, Kim S, Li P, Rhoads J, Satterfield M, Smith S, Spencer T, Yin Y. Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37: 153-168, 2009.
59. Wu GY, Knabe DA, Flynn NE, Yan WE, Flynn SP. Arginine degradation in developing porcine enterocytes. Am J Physiol Gastrointest Liver Physiol 271: G913-G919, 1996. (Pubitemid 126757999)
60. Wu GY, Meininger CJ. Regulation of nitric oxide synthesis by dietary factors. Ann Rev Nutr 22: 61-86, 2002.
61. Yao K, Yin YL, Chu WY, Li ZQ, Deng D, Li TJ, Huang RL, Zhang JS, Tan B, Wang W, Wu G. Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138: 867-872, 2008.