Gene expression in breast muscle associated with feed efficiency in a single male broiler line using a chicken 44K microarray. II. Differentially expressed focus genes

Poultry Science

Volumn 91, Issue 10, 2012, Pages 2576-2587

  Bottje, W G ^a   Kong, B W ^a   Song, J J ^a   Lee, J Y ^a   Hargis, B M ^a   Lassiter, K ^a   Wing, T ^b   Hardiman, J ^b  

^a UNIVERSITY OF ARKANSAS   (United States)

^b Cobb Vantress Inc ^*  (United States)

Author keywords

Broiler; Feed efficiency; Global gene expression; Microarray

Indexed keywords

EID: 84866480301     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2012-02204     Document Type: Article

References (90)

1. Alberts, B., and A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. Molecular Biology of the Cell. 4th ed. National Center for Biotechnology Information (NCBI) Bookshelf. US Library of Medicine, National Institutes of Health, Bethesda, MD.
2. Almeida, A., S. Moncada, and J. P. Bolanos. 2004. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat. Cell Biol. 6:45-51.
3. Angdisen, J., V. D. G. Moore, J. M. Cline, R. M. Payne, and J. A. Ibdah. 2005. Mitochondrial trifunctional protein defects: Molecular basis and novel therapeutic approaches. Curr. Drug Targets Immune Endocr. Metabol. Disord. 5:27-40.
4. Arber, S., G. Halder, and P. Caroni. 1994. Muscle LIM protein, a novel essential regulator of myogenesis, promotes myogenic differentiation. Cell 79:221-231.
5. Arber, S., J. J. Hunter, J. Ross Jr., M. Hongo, G. Sansig, J. Borg, J.-C. Perriard, K. R. Chien, and P. Caroni. 1997. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88:393-403.
6. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc., B 57:289-300.
7. Biondi, R. M. 2004. Phosphoinositide-dependent protein kinase 1, a sensor of protein conformation. Trends Biochem. Sci. 29:136-142.
8. Bjorbak, C., H. J. Lavery, B. H. Bates, C. Bjørbæk, H. J. Lavery, S. H. Bates, R. K. Olson, S. M. Davis, J. S. Flier, and M. G. Myers Jr. 2000. SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985. J. Biol. Chem. 275:40649-40657.
9. Bottje, W., M. D. Brand, C. Ojano-Dirain, K. Lassiter, M. Toyomizu, and T. Wing. 2009. Mitochondrial proton leak kinetics and relationship with feed efficiency within a single genetic line of male broilers. Poult. Sci. 88:1683-1693.
10. Bottje, W. G., and G. E. Carstens. 2009. Association of mitochondrial function and feed efficiency in poultry and livestock species. J. Anim. Sci. 87:E48-E63.
11. Bottje, W., Z. Tang, M. Iqbal, D. Cawthon, R. Okimoto, T. Wing, and M. Cooper. 2002. Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poult. Sci. 81:546-555.
12. Brunet, A., J. Park, H. Tran, L. S. Hu, B. A. Hemmings, and M. E. Greenberg. 2001. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21:952-965.
13. Carling, D. 2004. The AMP-activated protein kinase cascade-A unifying system for energy control. Trends Biochem. Sci. 29:18-24.
14. Chen, P., W. Hao, L. Rife, X. P. Wang, D. Shen, J. Chen, T. Ogden, G. B. Van Boemel, L. Wu, and M. Yang. 2001. A photic visual cycle of rhodopsin regeneration is dependent on Rgr. Nat. Genet. 28:256-260.
15. Chiang, H.-I., C. L. Swaggerty, M. H. Kogut, S. E. Dowd, X. Li, I. Y. Pevzner, and H. Zhou. 2008. Gene expression profiling in chicken heterophils with Salmonella Enteritidis stimulation using a chicken 44 K Agilent microarray. BMC Genomics 9:526.
16. De Souza, E. B., T. R. Insel, M. H. Perrin, J. Rivier, W. W. Vale, and M. J. Kuhar. 1985. Corticotropin-releasing factor receptors are widely distributed within the rat central nervous system: An autoradiographic study. J. Neurosci. 5:3189-3203.
17. Dong, L. Q., and F. Liu. 2005. PDK2: The missing piece in the receptor tyrosine kinase signaling pathway puzzle. Am. J. Physiol. Endocrinol. Metab. 289:E187-E196.
18. Doupnik, C. A., N. Davidson, H. A. Lester, and P. Kofuji. 1997. RGS proteins reconstitute the rapid gating kinetics of G bg-activated inwardly rectifying K1 channels. Proc. Natl. Acad. Sci. USA 94:10461-10466.
19. Dunn, S. L., M. Bjornholm, S. H. Bates, Z. Chen, M. Seifert, and M. G. Myers. 2005. Feedback inhibition of leptin receptor/Jak2 signaling via Tyr1138 of the leptin receptor and suppressor of cytokine signaling 3. Mol. Endocrinol. 19:925-938.
20. Eichhorn, P. J. A., M. P. Creyghton, and R. Bernards. 2009. Protein phosphatase 2A regulatory subunits and cancer. Biochim. Biophys. Acta 1795:1-15.
21. Emanuelli, B., P. Peraldi, C. Filloux, D. Sawka-Verhelle, D. Hilton, and E. Van Obberghen. 2000. SOCS-3 is an insulin-induced negative regulator of insulin signaling. J. Biol. Chem. 275:15985-15991.
22. Flick, M. J., and S. F. Konieczny. 2000. The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of BIspectrin. J. Cell Sci. 113:1553-1564.
23. Fong, J. C., and H. Shulz. 1977. Purification and properties of pig heart crotonase and the presence of short chain and long chain enoyl coenzyme A hydratases in pig and guinea pig tissues. J. Biol. Chem. 252:542-547.
24. Fredriksson, R., and H. B. Schioth. 2005. The repertoire of G-protein coupled receptors in fully sequenced genomes. Mol. Pharmacol. 67:1414-1425.
25. Fujimoto, M., and T. Naka. 2003. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol. 24:659-666.
26. Georgopoulos, C., and W. J. Welch. 1993. Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9:601-634.
27. Hardie, D. G. 2005. New roles for the LKB1→AMPK pathway. Curr. Opinion Cell Biol. 17:167-173.
28. Hardie, D. G. 2007. AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 8:774-785.
29. Hardie, D. G., J. W. Scott, D. A. Pan, and E. R. Hudson. 2003. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546:113-120.
30. Hepler, J. R. 1999. Emerging roles for RGS proteins in cell signaling. Trends Pharmacol. Sci. 20:376-382.
31. Hepler, J. R., D. M. Berman, A. G. Gilman, and T. Kozasa. 1997. RGS4 and GAIP are GTPase-activating proteins for Gqα and block activation of phospholipase Cβ by γ-thio-GTP-Gqα. Proc. Natl. Acad. Sci. USA 94:428-432.
32. Hoffman, C., and C. Eichele. 1994. Retinoids in development. Pages 387-441 in The Retinoids: Biology, Chemistry, and Medicine. 2nd ed. M. B. Spom, A. B. Roberts, and D. S. Goodman, ed. Raven Press Ltd., New York, NY.
33. Hoffmann, M., R. J. Ward, A. Cavalli, I. Craig Carr, and G. Milligan. 2001. Differential capacities of the RGS1, RGS16, and RGS-GAIP regulators of G protein signaling to enhance α2Aadrenoreceptor agonist-stimulated GTPase activity of Go1α. J. Neurochem. 78:797-806.
34. Iqbal, M., N. Pumford, K. Lassiter, Z. X. Tang, T. Wing, M. Cooper, and W. G. Bottje. 2005. Compromised liver mitochondrial function and complex activity in low feed efficient broilers within a single genetic line associated with higher oxidative stress and differential protein expression. Poult. Sci. 84:933-941.
35. Iqbal, M., N. R. Pumford, Z. X. Tang, K. Lassiter, T. Wing, M. Cooper, and W. Bottje. 2004. Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poult. Sci. 83:474-484.
36. Ito, J., M. Ito, H. Nambu, T. Fujikawa, K. Tanaka, H. Iwaasa, and S. Tokita. 2009. Anatomical and histological profiling of orphan G-protein-coupled receptor expression in gastrointestinal tract of C57BL/6J mice. Cell Tissue Res. 338:257-269.
37. Janssens, V., and J. Goris. 2001. Protein phosphatase 2A: A highly regulated family of serine threonine phosphatases implicated in cell growth and signaling. Biochem. J. 353:417-439.
38. Janssens, V., J. Goris, and C. V. Hoof. 2005. PP2A: The expected tumor suppressor. Curr. Opin. Genet. Dev. 15:34-41.
39. Jolly, R. A., K. M. Goldstein, T. Wei, H. Gao, P. Chen, S. Huang, J.-M. Colet, T. P. Ryan, C. E. Thomas, and S. T. Estrem. 2005. Pooling samples within microarray studies: A comparative analysis of rat liver transcription response to prototypical toxicants. Physiol. Genomics 22:346-355.
40. Kemp, B. E., D. Stapleton, D. J. Campbell, Z. P. Chen, S. Murthy, M. Walter, A. Gupta, J. J. Adams, F. Katsis, B. Van Denderen, I. G. Jennings, T. Iseli, B. J. Michell, and L. A. Witters. 2003. AMP-activated protein kinase, super metabolic regulator. Biochem. Soc. Trans. 31:162-168.
41. Kendziorski, C., R. A. Irizarry, K.-S. Chen, J. D. Haag, and M. N. Gould. 2005. On the utility of pooling biological samples in microarray experiments. Proc. Natl. Acad. Sci. USA 102:4252-4257.
42. Kendziorski, C. M., Y. Zhang, H. Lan, and A. D. Attie. 2003. The efficiency of pooling mRNA in microarray experiments. Biostatistics 4:465-477.
43. Kishimoto, T., R. V. Pearse, C. R. Lin, and M. G. Rosenfeld. 1995. A saugavine/corticotropin-releasing factor receptor expressed in heart and skeletal muscle. Proc. Natl. Acad. Sci. USA 92:1108-1112.
44. Kong, B.-W., J. J. Song, J. Y. Lee, B. M. Hargis, T. Wing, K. Lassiter, and W. Bottje. 2011. Gene expression in breast muscle associated with feed efficiency in a single male broiler line using a chicken 44k microarray I. Top differentially expressed genes. Poult. Sci. 90:2535-2547.
45. Kong, Y., M. Flick, A. J. Kudla, and S. F. Konieczny. 1997. Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol. Cell. Biol. 17:4750-4760.
46. Lang, F., C. Bohmer, M. Palmada, G. Seebohm, N. Strutz-Seebohm, and V. Vallon. 2006. (Patho)physiological significance of the serum-and glucocorticoid inducible kinase isoforms. Physiol. Rev. 86:1151-1178.
47. Lebrun, P., E. Cognard, R. Bellon-Paul, P. Gontard, C. Filloux, C. Jehl-Pietri, P. Grimaldi, M. Samson, L. Pénicaud, J. Ruberte, T. Ferre, A. Pujol, F. Bosch, and E. Van Obberghen. 2009. Constitutive expression of suppressor of cytokine signalling-3 in skeletal muscle leads to reduced mobility and overweight in mice. Diabetologia 52:2201-2212.
48. Leevers, S. J., D. Weinkove, L. K. MacDougall, E. Hafen, and M. D. Waterfield. 1996. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15:6584-6594.
49. Lehnert, S. A., K. Byrne, A. Reverter, G. Nattrass, P. Greenwood, Y. Wang, N. Hudson, and G. Harper. 2006. Gene expression profiling of bovine skeletal muscle in response to and during recovery from chronic and severe under nutrition. J. Anim. Sci. 84:3239-3250.
50. Lehninger, A. L., D. L. Nelson, and M. M. Cox. 1993. Principles of Biochemistry. 2nd ed. Worth Publishers, New York, NY.
51. Leong, M. L., A. C. Maiyar, B. Kim, B. A. O'Keeffe, and G. L. Firestone. 2003. Expression of the serum-and glucocorticoid-inducible protein kinase, Sgk, is a cell survival response to multiple types of environmental stress stimuli in mammary epithelial cells. J. Biol. Chem. 278:5871-5882.
52. Lindberg, K., S. G. Rønn, D. Tornehave, H. Richter, J. A. Hansen, J. Rømer, M. Jackerott, and N. Billestrup. 2005. Regulation of pancreatic beta-cell mass and proliferation by SOCS-3. J. Mol. Endocrinol. 35:231-243.
53. Louis, H. A., D. Pino, K. L. Schmeichel, P. Pomiés, and M. C. Beckerle. 1997. Comparison of three members of the cystine-rich protein family reveals functional conservation and divergent patterns of gene expression. J. Biol. Chem. 272:27484-27491.
54. Maden, M. 1994. Role of retinoids in embryonic development. Pages 289-322 in Vitamin A in Health and Disease. R. Blomhoff, ed. Marcel Dekker, New York, NY.
55. Marone, R., V. Cmiljanovic, B. Giese, and M. P. Wymann. 2008. Targeting phosphoinositide 3-kinase-Moving towards therapy. Biochim. Biophys. Acta 1784:159-185.
56. Martin, B., R. Schneider, S. Janetzky, Z. Waibler, P. Pandur, M. Kuhl, J. Behrens, K. von der Mark, A. Starzinski-Powitz, and V. Wixler. 2002. The LIM-only protein FHL2 interacts with betacatenin and promotes differentiation of mouse myoblasts. J. Cell Biol. 159:113-122.
57. Mehta, P. K., and K. K. Griendling. 2007. Angiotensin II cell signaling: Physiological and pathological effects in the cardiovascular system. Am. J. Physiol. 292:C82-C97.
58. Minokoshi, Y., T. Alquier, N. Furukawa, Y. B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferre, and M. J. Birnbaum. 2004. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428:569-574.
59. Momken, I., P. Lechene, N. Koulmann, D. Fortin, P. Mateo, B. T. Doan, J. Hoerter, X. Bigard, V. Veksler, and R. Ventura-Clapier. 2005. Impaired voluntary running capacity of creatine kinasedeficient mice. J. Physiol. 565:951-964.
60. Niemann, H., B. Kuhla, and G. Glachowshy. 2011. Perspectives for feed-efficient animal production. J. Anim. Sci. 89:4344-4363.
61. Nolan, C., W. B. Novoa, E. G. Krebs, and E. H. Fischer. 1964. Further studies on the site phosphorylated in the phosphorylase B to a reaction. Biochemistry 3:542-551.
62. Noy, N. 2000. Retinoid-binding proteins: Mediators of retinoid action. Biochem. J. 348:481-495.
63. Ojano-Dirain, C. P., M. Iqbal, D. Cawthon, S. Swonger, T. Wing, M. Cooper, and W. Bottje. 2004. Site-specific defects in electron transport in duodenal mitochondria are associated with low feed efficiency in broiler breeder males. Poult. Sci. 83:1394-1403.
64. Palmieri, F. 2004. The mitochondrial transporter family (SLC25): Physiological and pathological implications. Pflugers Arch. 447:689-709.
65. Pitcher, J. A., N. J. Freedman, and R. J. Lefkowitz. 1998. G proteincoupled receptors. Annu. Rev. Biochem. 67:653-692.
66. Rønn, S. G., A. Börjesson, C. Bruun, P. E. Heding, H. Frobøse, T. Mandrup-Poulsen, A. E. Karlsen, J. Rasschaert, S. Sandler, and N. Billestrup. 2008. Suppressor of cytokine signalling-3 expression inhibits cytokine-mediated destruction of primary mouse and rat pancreatic islets and delays allograft rejection. Diabetologia 51:1873-1882.
67. Roush, W. 1996. Cell biology: Regulating G protein signaling. Science 271:1056-1058.
68. Sakoda, H., Y. Gotoh, H. Katagiri, M. Kurokawa, H. Ono, Y. Onishi, M. Anai, T. Ogihara, M. Fujishiro, Y. Fukushima, M. Abe, N. Shojima, M. Kikuchi, Y. Oka, H. Hirai, and T. Asano. 2003. Differing roles of Akt and serum-and glucocorticoid-regulated kinase in glucose metabolism, DNA synthesis, and oncogenic activity. J. Biol. Chem. 278:25802-25807.
69. Sankarganesh, J., C. Boehmer, F. Lang, and M. Palmada. 2007. Role of SGK1 kinase in regulating glucose transport via glucose transporter GLUT4. Biochim. Biophy. Res. Comm. 236:629-635.
70. Schraufstatter, I. U., T. Khanh, L. Sikora, P. Sriramarao, and R. DiScipio. 2002. Complement C3a and C5a induce different signal transduction cascades in endothelial cells. J. Immunol. 169:2102-2110.
71. Sharifabadi, H. R., M. J. Zamir, E. Rowghani, and W. G. Bottje. 2012. Relationship between the activity of mitochondrial respiratory chain complexes and feed efficiency in fat-tailed ghezel lambs. J. Anim. Sci. In press.
72. Shi, H., B. Cave, K. Inouye, C. Bjørbæk, and J. S. Flier. 2006. Overexpression of suppressor of cytokine signaling 3 in adipose tissue causes local but not systemic insulin resistance. Diabetes 55:699-707.
73. Schulz, H. 1974. Long chain enoyl coenzyme A hydratase from pig heart. J. Biol. Chem. 249:2704-2709.
74. Slominski, A., J. Wortsman, A. Pisarchik, T. Zbyteck, E. A. Linto, J. E. Maurkiewicz, and E. T. Wei. 2001. Cutaneous expression of cortiotropin-releasing hormone (CRH), urocortin, and CRH receptors. FASEB J. 15:1678-1693.
75. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:e3-24.
76. Solinas, G., S. Summermatter, D. Mainieri, M. Gubler, J. P. Montani, J. Seydoux, S. R. Smith, and A. G. Dulloo. 2006. Corticotropin-releasing hormone directly stimulates thermogenesis in skeletal muscle possibly through substrate cycling between de novo lipogenesis and lipid oxidation. Endocrinology 147:31-38.
77. Steinfeld, H., P. Gerber, T. Wassenaar, V. Castel, M. Rosales, and C. De Hann. 2006. Livestock's Long Shadow: Environmental Issues and Options. Food and Agriculture Organization, Rome, Italy.
78. Tinsley, N., M. Iqbal, N. R. Pumford, K. Lassiter, C. Ojano-Dirain, T. Wing, and W. Bottje. 2010. Investigation of mitochondrial protein expression and oxidation in heart muscle in low and high feed efficient male broilers in a single genetic line. Poult. Sci. 89:349-352.
79. Ueki, K., T. Kondo, and C. R. Kahn. 2004. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin recep-tor substrate proteins by discrete mechanisms. Mol. Cell. Biol. 24:5434-5446
80. van den Bosch, B. J., C. M. M. van den Burg, K. Schoonderwoerd, P. J. Lindsey, H. R. Scholte, R. F. M. de Cood, E. van Rooij, H. A. Rockman, P. A. Doevendans, and H. J. M. Smeets. 2005. Regional absence of mitochondria causing energy depletion in the myocardium of muscle LIM protein knockout mice. Cardiovasc. Res. 65:411-418.
81. Webster, M. K., L. Goya, and G. L. Firestone. 1993a. Immediateearly transcriptional regulation and rapid mRNA turnover of a putative serine/threonine protein kinase. J. Biol. Chem. 268:11482-11485.
82. Webster, M. K., L. Goya, Y. Ge, A. C. Maiyar, and G. L. Firestone. 1993b. Characterization of sgk, a novel member of the serine/ threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol. Cell. Biol. 13:2031-2040.
83. Welch, W. J. 1992. Mammalian stress response: Cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72:1063-1081.
84. Wu, M., A. Nielsen, A. L. Swift, R. Moran, J. Tamagnine, D. Parslow, S. Armistead, K. Lemire, J. Orrell, J. Teich, S. Chomicz, and D. A. Ferrick. 2007. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292:C125-C136.
85. Yang, Y. H., and T. Speed. 2002. Design issues for cDNA microarray experiments. Nat. Rev. Genet. 3:579-588.
86. Yu, B. P. 1994. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 74:139-162.
87. Zahurak, M., G. Parmigiani, W. Yu, R. B. Scharpf, D. Berman, E. Schaeffer, S. Shabbeer, and L. Cope. 2007. Pre-processing Agilent microarray data. BMC Bioinformatics 8:142-154.
88. Zheng, Q., Y. Zhang, Y. Chen, N. Yang, X.-J. Wang, and D. Zhu. 2009. Systematic identification of genes involved in divergent skeletal muscle growth rates of broiler and layer chickens. BMC Genomics 10:87. http://www.biomedcentral.com/1471-2164/10/87.
89. Zhou, G., R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M. F. Hirshman, L. J. Goodyear, and D. E. Moller. 2001. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108:1167-1174.
90. Zhou, H., and S. J. Lamont. 2007. Global gene expression profile after Salmonella enterica serovar enteritidis challenge in two F8 advanced intercross chicken lines. Cytogenet. Genome Res. 117:131-138.