Messenger RNA sequencing and pathway analysis provide novel insights into the biological basis of chickens' feed efficiency

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Zhou, Nan ^a   Lee, William R ^b   Abasht, Behnam ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b Maple Leaf Farms   (United States)

Author keywords

Breast muscle; Chicken feed efficiency; Differential expression analysis; IGFs PI3K Akt signaling pathway; Muscle remodeling; RNA seq

Indexed keywords

GROWTH HORMONE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; SCAVENGER; SOMATOMEDIN B; SOMATOMEDIN C; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; BREAST MUSCLE; BROILER; CONTROLLED STUDY; DOWN REGULATION; FEED EFFICIENCY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE MAPPING; GENETIC TRAIT; GENOME; HIGH THROUGHPUT RNA SEQUENCING; INFLAMMATION; MALE; MUSCLE; MUSCLE GROWTH; NONHUMAN; PHENOTYPE; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANIMAL FOOD; CHEMISTRY; CHICKEN; GENETICS; METABOLISM; OXIDATIVE STRESS; SKELETAL MUSCLE;

AVES; GALLUS GALLUS;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CHICKENS; DOWN-REGULATION; FREE RADICAL SCAVENGERS; GENOME; GROWTH HORMONE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; MALE; MUSCLE, SKELETAL; OXIDATIVE STRESS; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSCRIPTOME; UP-REGULATION;

EID: 84928551535     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1364-0     Document Type: Article

References (122)

1. Hayes BJ, Lewin HA, Goddard ME. The future of livestock breeding: genomic selection for efficiency, reduced emissions intensity, and adaptation. Trends Genet. 2013;29:206-14.
2. Dekkers JCM, Hospital F. The use of molecular genetics in the improvement of agricultural populations. Nat Rev Genet. 2002;3:22-32.
3. Goddard ME, Hayes BJ. Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet. 2009;10:381-91.
4. Deeb N, Lamont SJ. Genetic architecture of growth and body composition in unique chicken populations. J Hered. 1998;93:107-18.
5. Emmerson DA. Commercial approaches to genetic selection for growth and feed conversion in domestic poultry. Poult Sci. 1997;76:1121-5.
6. Rauw W, Kanis E, Noordhuizen-Stassen E, Grommers F. Undesirable side effects of selection for high production efficiency in farm animals: a review. Livest Prod Sci. 1998;56:15-33.
7. Dransfield E, Sosnicki AA. Relationship between muscle growth and poultry meat quality. Poult Sci. 1999;78:743-6.
8. Wilson BW, Nieberg PS, Buhr RJ, Kelly BJ, Shultz FT. Turkey muscle growth and focal myopathy. Poult Sci. 1990;69:1553-62.
9. Petracci M, Cavani C. Muscle growth and poultry meat quality issues. Nutrients. 2012;4:1-12.
10. Julian RJ. Rapid growth problems: ascites and skeletal deformities in broilers. Poult Sci. 1998;77:1773-80.
11. Mills LJ, Mitchell MA, Mahon M. Incidence of skeletal muscle damage in selected and unselected strains of turkey. Br Poult Sci. 1998;1998(39 Suppl):S27-8.
12. Dunnington EA, Siegel PB. Enzyme activity and organ development in newly hatched chicks selected for high or low eight-week body weight. Poult Sci. 1995;74:761-70.
13. Willems OW, Miller SP, Wood BJ. Aspects of selection for feed efficiency in meat producing poultry. World's Poult Sci J. 2013;69:77-88.
14. Aggrey SE, Karnuah AB, Sebastian B, Anthony NB. Genetic properties of feed efficiency parameters in meat-type chickens. Genet Sel Evol. 2010;42:25.
15. Bottje W, Iqbal M, Tang ZX, Cawthon D, Okimoto R, Wing T, et al. Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poult Sci. 2002;81:546-55.
16. Kong B-W, Song JJ, Lee JY, Hargis BM, Wing T, Lassiter K, et al. Gene expression in breast muscle associated with feed efficiency in a single male broiler line using a chicken 44 K oligo microarray. I. Top differentially expressed genes. Poult Sci. 2011;90:2535-47.
17. Bottje WG, Kong B-W, Song JJ, Lee JY, Hargis BM, Lassiter K, et al. 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. Poult Sci. 2012;19:2576-87.
18. Shendure J. The beginning of the end for microarrays? Nat Methods. 2008;5:585-7.
19. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10:57-63.
20. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008;18:1509-17.
21. Wang C, Gong B, Bushel PR, Thierry-Mieg J, Thierry-Mieg D, Xu J, et al. The concordance between RNA-seq and microarray data depends on chemical treatment and transcript abundance. Nat Biotechnol. 2014;32:926-32.
22. Babraham Bioinformatics. [ http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ ]
23. TopHat. [ http://ccb.jhu.edu/software/tophat/index.shtml ]
24. SAMtools. [ http://samtools.sourceforge.net ]
25. Cufflinks. [ http://cufflinks.cbcb.umd.edu/ ]
26. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562-78.
27. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol. 2008;26:317-25.
28. Inc. SI. JMP® 11 Multivariate Methods. Cary: NC SAS Inst Inc; 2013.
29. Chargé SBP, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209-38.
30. Gal-Levi R, Leshem Y, Aoki S, Nakamura T, Halevy O. Hepatocyte growth factor plays a dual role in regulating skeletal muscle satellite cell proliferation and differentiation. Biochim Biophys Acta. 1998;1402:39-51.
31. Kaliman P, Canicio J, Testar X, Palacín M, Zorzano A. Insulin-like growth factor-II, phosphatidylinositol 3-kinase, nuclear factor-kappaB and inducible nitric-oxide synthase define a common myogenic signaling pathway. J Biol Chem. 1999;274:17437-44.
32. Zanou N, Gailly P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cell Mol Life Sci. 2013;70:4117-30.
33. Kong Y, Flick MJ, Kudla AJ, Konieczny SF. Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol Cell Biol. 1997;17:4750-60.
34. Demonbreun AR, Lapidos KA, Heretis K, Levin S, Dale R, Pytel P, et al. Myoferlin regulation by NFAT in muscle injury, regeneration and repair. J Cell Sci. 2010;123:2413-22.
35. Velleman SG, Song Y, Shin J, McFarland DC. Modulation of turkey myogenic satellite cell differentiation through the shedding of glypican-1. Comp Biochem Physiol - A Mol Integr Physiol. 2013;164:36-43.
36. Lu H, Shah P, Ennis D, Shinder G, Sap J, Le-Tien H, et al. The differentiation of skeletal muscle cells involves a protein-tyrosine phosphatase-alpha-mediated C-Src signaling pathway. J Biol Chem. 2002;277:46687-95.
37. Araya R, Eckardt D, Maxeiner S, Krüger O, Theis M, Willecke K, et al. Expression of connexins during differentiation and regeneration of skeletal muscle: functional relevance of connexin43. J Cell Sci. 2005;118:27-37.
38. Wang L, Wang Y. Molecular characterization, expression patterns and subcellular localization of Myotrophin (MTPN) gene in porcine skeletal muscle. Mol Biol Rep. 2012;39:2733-8.
39. Cao DJ, Jiang N, Blagg A, Johnstone JL, Gondalia R, Oh M, et al. Mechanical unloading activates FoxO3 to trigger Bnip3-dependent cardiomyocyte atrophy. J Am Heart Assoc. 2013;2:e000016.
40. Kipreos ET, Pagano M. Protein family review The F-box protein family. Genome Biol. 2000;1:R3002.
41. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004;117:399-412.
42. Skurk C, Izumiya Y, Maatz H, Razeghi P, Shiojima I, Sandri M, et al. The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling. J Biol Chem. 2005;280:20814-23.
43. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A. 2001;98:14440-5.
44. Ye J, Zhang Y, Xu J, Zhang Q, Zhu D. FBXO40, a gene encoding a novel muscle-specific F-box protein, is upregulated in denervation-related muscle atrophy. Gene. 2007;404:53-60.
45. Serrano AL, Muñoz-Cánoves P. Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res. 2010;316:3050-8.
46. Chen X, Li Y. Role of matrix metalloproteinases in skeletal muscle. cell Adhes Migr. 2009;3:337-41.
47. Carmeli E, Moas M, Reznick AZ, Coleman R. Matrix metalloproteinases and skeletal muscle: a brief review. Muscle Nerve. 2004;29:191-7.
48. Cornelison DDW. Context matters: in vivo and in vitro influences on muscle satellite cell activity. J Cell Biochem. 2008;105:663-9.
49. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 2002;3:207-14.
50. Wang W, Pan H, Murray K, Jefferson BS, Li Y. Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol. 2009;174:541-9.
51. Wu N, Jansen ED, Davidson JM. Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J Invest Dermatol. 2003;121:926-32.
52. Kherif S, Lafuma C, Dehaupas M, Lachkar S, Fournier JG, Verdière-Sahuqué M, et al. Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev Biol. 1999;205:158-70.
53. Rullman E, Rundqvist H, Wågsäter D, Fischer H, Eriksson P, Sundberg CJ, et al. A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol. 2007;102:2346-51.
54. Baum O, Ganster M, Baumgartner I, Nieselt K, Djonov V. Basement membrane remodeling in skeletal muscles of patients with limb ischemia involves regulation of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases. J Vasc Res. 2007;44:202-13.
55. Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet. 2009;18:2584-98.
56. Raffaello A, Milan G, Masiero E, Carnio S, Lee D, Lanfranchi G, et al. JunB transcription factor maintains skeletal muscle mass and promotes hypertrophy. J Cell Biol. 2010;191:101-13.
57. Braun T, Gautel M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol. 2011;12:349-61.
58. Potthoff MJ, Arnold MA, McAnally J, Richardson JA, Bassel-Duby R, Olson EN. Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol Cell Biol. 2007;27:8143-51.
59. Hinits Y, Hughes SM. Mef2s are required for thick filament formation in nascent muscle fibres. Development. 2007;134:2511-9.
60. Molkentin JD, Black BL, Martin JF, Olson EN. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 1995;83:1125-36.
61. Frey N, Barrientos T, Shelton JM, Frank D, Rütten H, Gehring D, et al. Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat Med. 2004;10:1336-43.
62. Wan L, Ma J, Wang N, Wang D, Xu G. Molecular cloning and characterization of different expression of MYOZ2 and MYOZ3 in Tianfu goat. PLoS One. 2013;8:e82550.
63. Jørgensen JOL, Jessen N, Pedersen SB, Vestergaard E, Gormsen L, Lund SA, et al. GH Receptor Signaling in Skeletal Muscle and Adipose Tissue in Human Subjects Following Exposure to an Intravenous GH Bolus. Am J Physiol Endocrinol Metab. 2006;291:E899-905.
64. Goodyer CG, Figueiredo RM, Krackovitch S, De Souza LL, Manalo JA, Zogopoulos G. Characterization of the growth hormone receptor in human dermal fibroblasts and liver during development. Am J Physiol Endocrinol Metab. 2001;281:E1213-20.
65. Carter-Su C, Schwartz J, Smit LS. Molecular mechanism of growth hormone action. Annu Rev Physiol. 1996;58:187-207.
66. Hull KL, Harvey S. Autoregulation of central and peripheral growth hormone receptor mRNA in domestic fowl. J Endocrinol. 1998;156:323-9.
67. Mao JNC, Cogburn LA, Burnside J. Growth hormone down-regulates growth hormone receptor mRNA in chickens but developmental increases in growth hormone receptor mRNA occur independently of growth hormone action. Mol Cell Endocrinol. 1997;129:135-43.
68. Yamada PM, Lee K-W. Perspectives in mammalian IGFBP-3 biology: local vs. systemic action. Am J Physiol Cell Physiol. 2009;296:C954-76.
69. Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle. 2011;1:4.
70. Duclos MJ. Insulin-like growth factor-I (IGF-1) mRNA levels and chicken muscle growth. J Physiol Pharmacol. 2005;56 Suppl 3:25-35.
71. Fuentes EN, Björnsson BT, Valdés JA, Einarsdottir IE, Lorca B, Alvarez M, et al. IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. Am J Physiol Regul Integr Comp Physiol. 2011;300:R1532-42.
72. Ogawa W, Matozaki T, Kasuga M. Role of binding proteins to IRS-1 in insulin signalling. Mol Cell Biochem. 1998;182:13-22.
73. Saltiel A, Kahn C. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001;414:799-806.
74. Bottje WG, Kong BW, Lee JY, Washington T, Baum J. Potential Roles of mTOR and Protein Degradation Pathways in the Phenotypic Expression of Feed Efficiency in Broilers. Biochem Physiol Open Access. 2014;03:1-8.
75. Pedersen BK, Akerström TCA, Nielsen AR, Fischer CP. Role of myokines in exercise and metabolism. J Appl Physiol. 2007;103:1093-8.
76. Pedersen BK. Muscles and their myokines. J Exp Biol. 2011;214:337-46.
77. Nara N, Nakayama Y, Okamoto S, Tamura H, Kiyono M, Muraoka M, et al. Disruption of CXC motif chemokine ligand-14 in mice ameliorates obesity-induced insulin resistance. J Biol Chem. 2007;282:30794-803.
78. Webster EL, Torpy DJ, Elenkov IJ, Chrousos GP. Corticotropin-releasing hormone and inflammation. Ann N Y Acad Sci. 1998;840:21-32.
79. Solinas G, Summermatter S, Mainieri D, Gubler M, Montani JP, Seydoux J, et al. Corticotropin-releasing hormone directly stimulates thermogenesis in skeletal muscle possibly through substrate cycling between de novo lipogenesis and lipid oxidation. Endocrinology. 2006;147:31-8.
80. Lu H, Huang D, Ransohoff RM, Zhou L. Acute skeletal muscle injury: CCL2 expression by both monocytes and injured muscle is required for repair. FASEB J. 2011;25:3344-55.
81. Lu H, Huang D, Saederup N, Charo IF, Ransohoff RM, Zhou L. Macrophages recruited via CCR2 produce insulin-like growth factor-1 to repair acute skeletal muscle injury. FASEB J. 2011;25:358-69.
82. Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol. 2005;288:R345-53.
83. Pillon NJ, Bilan PJ, Fink LN, Klip A. Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications. Am J Physiol Endocrinol Metab. 2013;304:E453-65.
84. Philippou A, Maridaki M, Theos A, Koutsilieris M. Cytokines in Muscle Damage. Adv Clin Chem. 2012;58:49-87.
85. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol. 2005;37:1974-84.
86. Andreucci JJ, Grant D, Cox DM, Tomc LK, Prywes R, Goldhamer DJ, et al. Composition and function of AP-1 transcription complexes during muscle cell differentiation. J Biol Chem. 2002;277:16426-32.
87. Xia R, Webb JA, Gnall LLM, Cutler K, Abramson JJ. Skeletal muscle sarcoplasmic reticulum contains a NADH-dependent oxidase that generates superoxide. Am J Physiol Cell Physiol. 2003;285:C215-21.
88. Mofarrahi M, Brandes RP, Gorlach A, Hanze J, Terada LS, Quinn MT, et al. Regulation of proliferation of skeletal muscle precursor cells by NADPH oxidase. Antioxid Redox Signal. 2008;10:559-74.
89. Bottje WG, Carstens GE. Association of mitochondrial function and feed efficiency in poultry and livestock species. J Anim Sci. 2009;87:E48-63.
90. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, et al. Mitochondrial superoxide: Production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med. 2004;37:755-67.
91. Kobayashi A, Kang M-I, Watai Y, Tong KI, Shibata T, Uchida K, et al. Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol Cell Biol. 2006;26:221-9.
92. D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol. 2007;8:813-24.
93. He X, Kan H, Cai L, Ma Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol. 2009;46:47-58.
94. Laurila JP, Castellone MD, Curcio A, Laatikainen LE, Haaparanta-Solin M, Gronroos TJ, et al. Extracellular superoxide dismutase is a growth regulatory mediator of tissue injury recovery. Mol Ther. 2009;17:448-54.
95. Kim S-J, Lee S-M. NLRP3 inflammasome activation in D-galactosamine and lipopolysaccharide-induced acute liver failure: role of heme oxygenase-1. Free Radic Biol Med. 2013;65:997-1004.
96. Wang X, Ling S, Zhao D, Sun Q, Li Q, Wu F, et al. Redox regulation of actin by thioredoxin-1 is mediated by the interaction of the proteins via cysteine 62. Antioxid Redox Signal. 2010;13:565-73.
97. Salinas AE, Wong MG. Glutathione S-transferases-a review. Curr Med Chem. 1999;6:279-309.
98. Bottje W, Pumford NR, Ojano-Dirain C, Iqbal M, Lassiter K. Feed efficiency and mitochondrial function. Poult Sci. 2006;85:8-14.
99. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol. 2000;279:L1005-28.
100. Barbieri E, Sestili P. Reactive Oxygen Species in Skeletal Muscle Signaling. J Signal Transduct. 2012.
101. Victor VM, Rocha M, De La Fuente M. Immune cells: Free radicals and antioxidants in sepsis. Int Immunopharmacol. 2004;4:327-47.
102. Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and Negative Regulation of Insulin Signaling by Reactive Oxygen and Nitrogen Species. Physiol Rev. 2009;89:27-71.
103. Kumasaka S, Shoji H, Okabe E. Novel mechanisms involved in superoxide anion radical-triggered Ca2+ release from cardiac sarcoplasmic reticulum linked to cyclic ADP-ribose stimulation. Antioxid Redox Signal. 1999;1:55-69.
104. Okabe E, Kato Y, Sasaki H, Saito G, Hess ML, Ito H. Calmodulin participation in oxygen radical-induced cardiac sarcoplasmic reticulum calcium uptake reduction. Arch Biochem Biophys. 1987;255:464-8.
105. Roveri A, Coassin M, Maiorino M, Zamburlini A, van Amsterdam FT, Ratti E, et al. Effect of hydrogen peroxide on calcium homeostasis in smooth muscle cells. Arch Biochem Biophys. 1992;297:265-70.
106. Periasamy M, Kalyanasundaram A. SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve. 2007;35:430-42.
107. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol. 2006;70:1469-80.
108. Stiehl DP. Ã WJ, Wenger RH, Hellwig-bu T, Allee R, Lu D-: Normoxic induction of the hypoxia-inducible factor 1 K by insulin and interleukin-1 L involves the phosphatidylinositol 3-kinase pathway. FEBS Lett. 2002;512:157-62.
109. Feldser D, Agani F, Iyer NV. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2 growth factor 2 1. Cancer Res. 1999;59:3915-8.
110. Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med. 2011;364:656-65.
111. Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. 2009;9:609-17.
112. Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645-57.
113. Bartels K, Grenz A, Eltzschig HK. Hypoxia and inflammation are two sides of the same coin. Proc Natl Acad Sci U S A. 2013;110:18351-2.
114. Frede S, Berchner-Pfannschmidt U, Fandrey J. Regulation of Hypoxia-Inducible Factors During Inflammation. Methods Enzymol. 2007;435:403-19.
115. Scheerer N, Dehne N, Stockmann C, Swoboda S, Baba HA, Neugebauer A, et al. Myeloid hypoxia-inducible factor-1α is essential for skeletal muscle regeneration in mice. J Immunol. 2013;191:407-14.
116. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998;95:11715-20.
117. Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol. 1999;15:551-78.
118. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47-95.
119. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130-8.
120. Petracci M, Mudalal S, Bonfiglio A, Cavani C. Occurrence of white striping under commercial conditions and its impact on breast meat quality in broiler chickens. Poult Sci. 2013;92:1670-5.
121. Kuttappan VA, Shivaprasad H, Shaw DP, Valentine BA, Hargis BM, Clark FD, et al. Pathological changes associated with white striping in broiler breast muscles. Poult Sci. 2013;92:331-8.
122. Sihvo H-K, Immonen K, Puolanne E. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol. 2014;51:619-23.