1932

Abstract

The functional unit in skeletal muscle is the multinucleated myofiber, which is composed of parallel arrays of microfibrils. The myofiber and sarco-mere structure of skeletal muscle are established during embryogenesis, when mononuclear myoblast cells fuse to form multinucleated myotubes and develop into muscle fibers. With the myoblasts permanently unable to enter a proliferative state again after they fuse to form the multinucleated myotube, postnatal myofiber growth, muscle homeostasis, and myofiber regeneration are dependent on a myogenic stem cell, the satellite cell. Because the satellite cell is a partially differentiated stem cell controlling the state of skeletal muscle structure throughout the life of the bird, it can impact muscle development and structure, growth, and regeneration and, subsequently, meat quality. When myofibers are damaged, muscle repair is dependent on the satellite cells. Regenerated myofibers after the repair process should be similar to the original muscle fiber. Despite significant improvements in meat-type birds, degenerative myopathies have arisen. In many of these degenerative breast muscle myopathies, like Wooden Breast, satellite cell–mediated regeneration of muscle is suppressed. Thus, the biological function of avian myogenic satellite cells and their influence on cellular mechanisms affecting breast muscle development and growth, function during degenerative myopathies, and meat quality are discussed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020518-115311
2019-02-15
2024-10-16
Loading full text...

Full text loading...

/deliver/fulltext/animal/7/1/annurev-animal-020518-115311.html?itemId=/content/journals/10.1146/annurev-animal-020518-115311&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Smith JH 1963. Relation of body size to muscle cell size and number in the chicken. Poult. Sci. 42:619–23
    [Google Scholar]
  2. 2.  Mauro A 1961. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:493–95
    [Google Scholar]
  3. 3.  Moss FP, LeBlond CP 1971. Satellite cells are the source of nuclei in muscles of growing rats. Anat. Rec. 170:421–35
    [Google Scholar]
  4. 4.  Dransfield E, Sosnicki AA 1999. Relationship between muscle growth and poultry meat quality. Poult. Sci. 78:743–46
    [Google Scholar]
  5. 5.  Swatland HJ 1990. A note on the growth of connective tissues binding turkey muscle fibers together. Can. Inst. Food Sci. Technol. J. 23:239–41
    [Google Scholar]
  6. 6.  Wilson BW, Nieberg PS, Buhr RJ 1990. Turkey muscle growth and focal myopathy. Poult. Sci. 69:1553–62
    [Google Scholar]
  7. 7.  Velleman SG, Anderson JW, Coy CS, Nestor KE 2003. Effect of selection for growth rate on muscle damage during turkey breast muscle development. Poult. Sci. 82:1069–74
    [Google Scholar]
  8. 8.  Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P 2008. Molecular Biology of the Cell New York: Garland Sci
    [Google Scholar]
  9. 9.  Fowler VM, Sussmann MA, Miller PG, Flucher BE, Daniels MP 1993. Tropomodulin is associated with the free (pointed) ends of the thin filaments in rat skeletal muscle. J. Cell Biol. 120:411–20
    [Google Scholar]
  10. 10.  Weber IT, Harrison RW, Iozzo RV 1996. Model structure of decorin and implications for collagen fibrillogenesis. J. Biol. Chem. 271:31767–70
    [Google Scholar]
  11. 11.  Velleman SG, Yeager JD, Krider H, Carrino DA, Zimmerman SD, McCormick RJ 1996. The avian low score normal muscle weakness alters decorin expression and collagen crosslinking. Connect. Tissue Res. 34:33–39
    [Google Scholar]
  12. 12.  Velleman SG, McFarland DC, Li Z, Ferrin NH, Whitmoyer R, Dennis JE 1997. Alterations in sarcomere structure, collagen organization mitochondrial activity, and protein metabolism in the avian Low Score Normal muscle weakness. Dev. Growth Differ. 39:563–70
    [Google Scholar]
  13. 13.  Bangsbo J, Gollnick PD, Grahm TE, Saltin B 1991. Substrates for muscle glycogen synthesis in recovery from intense exercise in man. J. Physiol. 434:423–40
    [Google Scholar]
  14. 14.  Christov C, Chrétien F, Abou-Khalil R, Bassez G, Vallet G et al. 2007. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol. Biol. Cell 18:1397–409
    [Google Scholar]
  15. 15.  Bi P, Kuang S 2012. Meat Science and Muscle Biology Symposium: stem cell niche and postnatal muscle growth. J. Anim. Sci. 90:924–35
    [Google Scholar]
  16. 16.  Rhoads RP, Johnson RM, Rathbone CR, Liu X, Temm-Grove C et al. 2009. Satellite cell-mediated angiogenesis in vitro coincides with a functional hypoxia-inducible factor pathway. Am. J. Physiol. Cell Physiol. 296:C1321–28
    [Google Scholar]
  17. 17.  Velleman SG 2015. Relationship of skeletal muscle development and growth to breast muscle myopathies: a review. Avian Dis 59:525–31
    [Google Scholar]
  18. 18.  Velleman SG, Clark DL, Tonniges JR 2018. The effect of the Wooden Breast myopathy on sarcomere structure and organization. Avian Dis 62:28–35
    [Google Scholar]
  19. 19.  Shefer G, Wielinski-Lee M, Yablonka-Reuveni Z 2004. Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. J. Cell Sci. 117:5393–404
    [Google Scholar]
  20. 20.  Hoh JFY, Hughes S 1988. Myogenic and neurogenic regulation of myosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds. J. Muscle Res. Cell Motil. 9:59–72
    [Google Scholar]
  21. 21.  Stockdale FE 1990. The myogenic lineage: evidence for multiple precursors during avian limb development. Proc. Soc. Exp. Biol. Med. 194:71–75
    [Google Scholar]
  22. 22.  Feldman JL, Stockdale FE 1991. Skeletal muscle satellite cell diversity: Satellite cells form fibers of different types in cell culture. Dev. Biol. 143:320–34
    [Google Scholar]
  23. 23.  McFarland DC, Gilkerson KK, Pesall JE, Walker JS, Yun Y 1995. Heterogeneity in growth characteristics of satellite cell populations. Cytobios 82:21–27
    [Google Scholar]
  24. 24.  Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM et al. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364:501–6
    [Google Scholar]
  25. 25.  Rudnicki MA, Schnesgelsber PN, Stead H, Braun T, Arnold HH, Jaenisch R 1993. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75:1351–59
    [Google Scholar]
  26. 26.  Yablonka-Reuveni Z, Rivera AJ 1994. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol. 164:588–603
    [Google Scholar]
  27. 27.  Yablonka-Reuveni Z, Day K, Vine A, Shefer G 2008. Defining the transcriptional signature of skeletal muscle stem cells. J. Anim. Sci. 86:E. Suppl.E207–16
    [Google Scholar]
  28. 28.  Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR 2004. Muscle satellite cells adopt divergent fates: A mechanism for self-renewal?. J. Cell Biol. 166:347–57
    [Google Scholar]
  29. 29.  Kuang S, Kuroda K, LeGrand F, Rudnicki M 2007. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010
    [Google Scholar]
  30. 30.  Asakura A, Komaki M, Rudnicki M 2001. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245–53
    [Google Scholar]
  31. 31.  Beauchamp JR, Heslop L, Yu D, Tajbakhsh S, Kelly RG et al. 2000. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151:1221–33
    [Google Scholar]
  32. 32.  Seale P, Sabourin LA, Girgis-Gabrado A, Mansouri A, Gruss P, Rudnicki M 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–86
    [Google Scholar]
  33. 33.  Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE et al. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38:228–33
    [Google Scholar]
  34. 34.  Kim HK, Lee YS, Sivaprasad U, Malhora A, Dutta A 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. J. Cell Biol. 174:677–87
    [Google Scholar]
  35. 35.  Koning M, Werker P, van Luyn M, Krenning G, Harmsen M 2012. A global downregulation of microRNAs occurs in human quiescent satellite cells during myogenesis. Differentiation 84:314–21
    [Google Scholar]
  36. 36.  Ameres SL, Zamore PD 2013. Diversifying microRNA sequences and function. Nat. Rev. 14:475–88
    [Google Scholar]
  37. 37.  Finnegan E, Pasquinelli A 2013. MicroRNA biogenesis: regulating the regulators. Crit. Rev. Biochem. Mol. Biol. 48:51–68
    [Google Scholar]
  38. 38.  Harding RL, Velleman SG 2016. MicroRNA regulation of myogenic satellite cell proliferation and differentiation. Mol. Cell. Biochem. 412:181–95
    [Google Scholar]
  39. 39.  Chen JF, Tao Y, Li J, Deng Z, Yan Z et al. 2010. microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J. Cell Biol. 190:867–69
    [Google Scholar]
  40. 40.  Dey B, Gagan J, Dutta A 2011. miR-206 and -489 induce myoblast differentiation by downregulating Pax7. Mol. Cell. Biol. 31:203–14
    [Google Scholar]
  41. 41.  Cheung TH, Quach NL, Charville GW, Liu L, Park L et al. 2012. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524–28
    [Google Scholar]
  42. 42.  Velleman SG, Coy CS, McFarland DC 2007. Effect of syndecan-1, syndecan-4, and glypican-1 on turkey muscle satellite cell proliferation, differentiation, and responsiveness to fibroblast growth factor 2. Poult. Sci. 86:1406–13
    [Google Scholar]
  43. 43.  Shin J, McFarland DC, Velleman SG 2013. Migration of turkey muscle satellite cells is enhanced by the syndecan-4 cytoplasmic domain through the activation of RhoA. Mol. Cell. Biochem. 375:115–30
    [Google Scholar]
  44. 44.  Velleman SG, Harding RL 2017. Regulation of turkey myogenic satellite cell migration by microRNAs miR-128 and miR-24. Poult. Sci. 96:1910–17
    [Google Scholar]
  45. 45.  Krek A, Grün D, Poy MN, Wolf R, Rosenberg L et al. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37:495–500
    [Google Scholar]
  46. 46.  Sanchez N, Gallagher M, Lao N, Gallagher C, Clarke C et al. 2013. miR-7 triggers cell cycle arrest at the G1/S transition by targeting multiple genes including Skp2 and Psme3. PLOS ONE 8:e65671
    [Google Scholar]
  47. 47.  Sun Q, Zhang Y, Yang G, Chen X, Zhang Y et al. 2008. Transforming growth factor-β-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res 36:2690–99
    [Google Scholar]
  48. 48.  Yahav S 2009. Alleviating heat stress in domestic fowl: different strategies. Worlds Poult. Sci. J. 65:719–32
    [Google Scholar]
  49. 49.  Azada MAK, Kikusatoa M, Maekawaa T, Shirakawab H, Toyomizua M 2010. Metabolic characteristics and oxidative damage to skeletal muscle in broiler chickens exposed to chronic heat stress. Comp. Biochem. Physiol. A 155:401–6
    [Google Scholar]
  50. 50.  Yahav S, Straschnow A, Plavnik I, Hurwitz S 1996. Effect of diurnal cyclic versus constant temperatures on chicken growth and food intake. Br. Poult. Sci. 37:43–54
    [Google Scholar]
  51. 51.  Baziz HA, Geraert PA, Padilha JCF, Guillaumin S 1996. Chronic heat exposure enhances fat deposition and modifies muscle and fat partition in broiler carcasses. Poult. Sci. 75:505–13
    [Google Scholar]
  52. 52.  Halevy O, Geyra A, Barak M, Uni Z, Sklan D 2000. Early posthatch starvation decreases satellite cell proliferation and skeletal muscle growth in chicks. J. Nutr. 130:858–64
    [Google Scholar]
  53. 53.  Mozdziak PR, Evans JJ, McCoy DW 2002. Early posthatch starvation induces myonuclear apoptosis in chickens. J. Nutr. 132:901–3
    [Google Scholar]
  54. 54.  Halevy O, Krispin A, Leshem Y, McMurtry JF, Yahav S 2001. Early age heat stress accelerates skeletal muscle satellite cell proliferation and differentiation in chicks. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R302–17
    [Google Scholar]
  55. 55.  Pietsun Y, Halevy O, Yahav S 2009. Thermal manipulations of broiler embryos: the effect on thermoregulation and development during embryogenesis. Poult. Sci. 88:2677–88
    [Google Scholar]
  56. 56.  Piestun Y, Halevy O, Shinder D, Ruzal M, Druyan S, Yahav S 2011. Thermal manipulations during embryogenesis improves post hatch performance under hot conditions. J. Thermal Biol. 36:469–74
    [Google Scholar]
  57. 57.  Hartley RS, Bandman E, Yablonka-Reuveni Z 1992. Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol. 153:206–12
    [Google Scholar]
  58. 58.  Stockdale FE 1992. Myogenic cell lineages. Dev. Biol. 154:284–98
    [Google Scholar]
  59. 59.  Yahav S, Collin A, Shinder D, Picard M 2004. Thermal manipulations during broiler chick embryo-genesis: effects of timing and temperature. Poult. Sci. 83:1959–63
    [Google Scholar]
  60. 60.  Piestun Y, Shinder D, Ruzal M, Halevy O, Yahav S 2008. The effect of thermal manipulations during the development of the thyroid and adrenal axes on in-hatch and post-hatch thermoregulation. J. Therm. Biol. 33:413–18
    [Google Scholar]
  61. 61.  Piestun Y, Shinder D, Ruzal M, Halevy O, Brake J, Yahav S 2008. Thermal manipulations during broiler embryogenesis: effect on the acquisition of thermotolerance. Poult. Sci. 87:1516–25
    [Google Scholar]
  62. 62.  Piestun Y, Harel M, Barak M, Yahav S, Halevy O 2009. Thermal manipulations in late-term chick embryos affect skeletal muscle development and promote myoblast proliferation and muscle hypertrophy. J. Appl. Physiol. 106:233–40
    [Google Scholar]
  63. 63.  Piestun Y, Druyan S, Brake J, Yahav S 2013. Thermal manipulations during broiler incubation alter performance of broilers to 70 days of age. Poult. Sci. 92:1155–63
    [Google Scholar]
  64. 64.  Clark DL, Coy CS, Strasburg GM, Reed KM, Velleman SG 2016. Temperature effect on proliferation and differentiation of satellite cells from turkeys with different growth rates. Poult. Sci. 95:934–47
    [Google Scholar]
  65. 65.  Piestun Y, Patael T, Yahav S, Velleman SG, Halevy O 2017. Early posthatch thermal stress affects breast muscle development and satellite cell growth and characteristics in broilers. Poult. Sci. 96:2877–88
    [Google Scholar]
  66. 66.  Arce L, Berger M, Coello CL 1992. Control of ascites syndrome by feed restriction techniques. J. Appl. Poult. Res. 1:1–5
    [Google Scholar]
  67. 67.  Acar N, Sizemore FG, Leach GR, Wideman RF Jr, Owen RL, Barbato GG 1995. Growth of broiler chickens in response to fed restriction regimes to reduce ascites. Poult. Sci 74:833–43
    [Google Scholar]
  68. 68.  Katanbaf MN, Dunnington EA, Siegel PB 1988. Allomorphic relationships from hatching to 56 days in parental lines and F1 crosses of chickens selected 27 generations for high or low body weight. Growth Dev. Aging 52:11–22
    [Google Scholar]
  69. 69.  Auckland JN 1972. Compensatory growth in turkeys: practical implications and limitations. World's Poult. Sci. J. 28:291–300
    [Google Scholar]
  70. 70.  Cherry JA, Siegel PB, Beane WL 1978. Genetic-nutritional relationships in growth and carcass characteristics of broiler chickens. Poult. Sci. 57:1482–87
    [Google Scholar]
  71. 71.  Malone GW, Chaloupka GW, Walpole EW, Littlefield LL 1980. The effect of dietary energy and light treatment on broiler performance. Poult. Sci. 59:567–81
    [Google Scholar]
  72. 72.  Ferket PR, Sell JL 1989. Effect of severity of early protein restriction on large turkey toms. 1. Performance characteristics and leg weakness. Poult. Sci. 68:676–86
    [Google Scholar]
  73. 73.  Washburn KW 1990. Effect of restricted feeding on fatness, efficiency, and the relationship between fatness and efficiency in broilers. Poult. Sci. 69:502–8
    [Google Scholar]
  74. 74.  Mozdziak PE, Walsh TJ, McCoy DW 2002. The effect of early posthatch nutrition on satellite cell mitotic activity. Poult. Sci. 81:1703–8
    [Google Scholar]
  75. 75.  Plavnik I, Hurwitz S 1988. Early feed restriction in chicks: effect of age, duration, and sex. Poult. Sci. 67:1407–13
    [Google Scholar]
  76. 76.  Plavnik I, Hurwitz S 1990. Performance of broiler chickens and turkey poults subjected to feed restriction or to feeding low-protein or low-sodium diets at an early age. Poult. Sci. 69:945–52
    [Google Scholar]
  77. 77.  Boettiger D, Enomoto-Iwamot M, Yoon HY, Hofer U, Menklo AS, Chiquet-Ehrismann R 1995. Regulation of integrin α5β1 affinity during myogenic differentiation. Dev. Biol. 169:261–72
    [Google Scholar]
  78. 78.  Zhang Z, Vuori K, Reed JC, Ruoslahti E 1995. The alpha5 beta1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. PNAS 92:6161–65
    [Google Scholar]
  79. 79.  McCormick RJ 1999. The flexibility of the collagen compartment of muscle. Poult. Sci. 78:778–84
    [Google Scholar]
  80. 80.  Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV 1997. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136:729–43
    [Google Scholar]
  81. 81.  Hildebrand A, Romaris M, Rasmussen LM, Heinegård D, Twadzik DR et al. 1994. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor β. Biochem. J 302:527–34
    [Google Scholar]
  82. 82.  Miura T, Kishioka Y, Wakamatsu J, Hattori A, Hennebry A et al. 2006. Decorin binds myostatin and modulates its activity to muscle cells. Biochem. Biophys. Res. Commun. 340:675–80
    [Google Scholar]
  83. 83.  Drougett R, Cabello-Verrugio C, Riquelme C, Brandan E 2006. Extracellular matrix proteoglycans modify TGF-β bio-availability attenuating its signaling during skeletal muscle differentiation. Matrix Biol 25:332–41
    [Google Scholar]
  84. 84.  Mehra A, Wrana JL 2002. TGF-β and Smad signal transduction pathway. Biochem. Cell Biol. 80:605–22
    [Google Scholar]
  85. 85.  Brandan E, Retamal C, Cabello-Verrugiom C, Marzolo MP 2006. The low density lipoprotein receptor-related protein, LRP, functions as an endocytic receptor for decorin. J. Biol. Chem. 281:31562–71
    [Google Scholar]
  86. 86.  Li X, McFarland DC, Velleman SG 2006. Effect of transforming growth factor-β on decorin and β1 integrin expression during muscle development in chickens. Poult. Sci. 85:326–32
    [Google Scholar]
  87. 87.  Li X, Velleman SG 2009. Effect of transforming growth factor-β1 on decorin expression and muscle morphology during chicken embryonic and posthatch growth and development. Poult. Sci. 88:387–97
    [Google Scholar]
  88. 88.  Kishioka Y, Thomas T, Wakamatsu J, Hattori A, Sharma M et al. 2008. Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J. Cell. Physiol. 215:856–67
    [Google Scholar]
  89. 89.  Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B et al. 1997. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat. Genet. 17:71–74
    [Google Scholar]
  90. 90.  Kambadur R, Sharma M, Smith TPL, Bass JJ 1997. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7:910–16
    [Google Scholar]
  91. 91.  McPherron AC, Lee S-J 1997. Double muscling in cattle due to mutations in the myostatin gene. PNAS 94:12457–61
    [Google Scholar]
  92. 92.  Yang W, Wang K, Chen Y, Zhang Y, Huang B, Zhu D 2003. Functional characterization of recombinant myostatin and its inhibitory role to chicken muscle development. Acta Biochem. Biophys. 35:1016–22
    [Google Scholar]
  93. 93.  McFarland DC, Velleman SG, Pesall JE, Liu C 2006. Effect of myostatin on turkey myogenic satellite cells and embryonic myoblasts. Comp. Biochem. Physiol. 144A:501–8
    [Google Scholar]
  94. 94.  Xu Z, Ichikawa N, Kosaki K, Yamada Y, Sasaki T et al. 2010. Perlecan deficiency causes muscle hypertrophy, a decrease in myostatin expression, and changes in muscle fiber composition. Matrix Biol 29:461–70
    [Google Scholar]
  95. 95.  Vial C, Zúñiga LM, Cabello-Verrugio C, Cañón P, Fadic R, Brandan E 2008. Skeletal muscle cells express the profibrotic cytokine connective tissue growth factor (CTGF/CCN2), which induces their dedifferentiation. J. Cell. Physiol. 215:410–21
    [Google Scholar]
  96. 96.  Vial C, Gutiérrez J, Santander C, Cabrera D, Brandan E 2011. Decorin interacts with connective tissue growth factor (CTGF)/CCN2 by LRR12 inhibiting its biological activity. J. Biol. Chem. 286:24242–52
    [Google Scholar]
  97. 97.  Moscatello DK, Santra M, Mann DM, McQuillan DJ, Wong AJ, Iozzo RJ 1998. Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J. Clin. Investig. 101:406–12
    [Google Scholar]
  98. 98.  Sosnicki AA, Wilson BW 1991. Pathology of turkey skeletal muscle: implications for the poultry industry. Food Struct 10:317–26
    [Google Scholar]
  99. 99.  Owens CM, Alvarado CZ, Sams AR 2009. Research developments in pale, soft, and exudative turkey meat in North America. Poult. Sci. 88:1513–17
    [Google Scholar]
  100. 100.  Pietrzak M, Greaser ML, Sosnicki AA 1997. Effect of rapid rigor mortis processes on protein functionality in pectoralis major muscle of domestic turkeys. J. Anim. Sci. 75:2106–16
    [Google Scholar]
  101. 101.  Barbut S, Sosnicki AA, Lonegran SM, Knapp T, Ciobanu DC et al. 2008. Progress in reducing the pale, soft and exudative (PSE) problem in pork and poultry meat. Meat Sci 79:46–63
    [Google Scholar]
  102. 102.  Maliala Y, Carr KM, Ernst CW, Velleman SG, Reed KM, Strasburg GM 2014. Deep transcriptome sequencing reveals differences in global gene expression between normal and pale, soft, and exudative (PSE) turkey meat. J. Anim. Sci. 92:1250–60
    [Google Scholar]
  103. 103.  Kuttappan VA, Hargis BM, Owens CM 2016. White Striping and Woody Breast myopathies in the modern poultry industry: a review. Poult. Sci. 95:2724–33
    [Google Scholar]
  104. 104.  Kuttappan VA, Brewer VB, Waldroup PW, Owens CM 2012. Influence of growth rate on the occurrence of WS in broiler breast fillets. Poult. Sci. 91:2677–85
    [Google Scholar]
  105. 105.  Kuttappan VA, Shivaprasad HL, Shaw DP, Valentine BA, Hargis BM et al. 2013. Pathological changes associated with White Striping in broiler breast muscles. Poult. Sci. 92:331–38
    [Google Scholar]
  106. 106.  Sihvo H-K, Immonen K, Puolanne E 2014. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet. Pathol. 51:619–23
    [Google Scholar]
  107. 107.  Bailey RA, Watson KA, Bilgili SF, Avendano S 2015. The genetic basis of pectoralis major myopathies in modern broiler chicken lines. Poult. Sci. 94:2870–79
    [Google Scholar]
  108. 108.  Tasoniero G, Cullere M, Cecchinato M, Puolanne E, Dalle Zotte A 2016. Technological quality, mineral profile, and sensory attributes of broiler chicken breasts affected by White Striping and Wooden Breast myopathies. Poult. Sci. 95:2707–14
    [Google Scholar]
  109. 109.  Sihvo H-K, Linden J, Airas N, Immonen K, Valaja J, Puolanne E 2017. Wooden breast myodegeneration of pectoralis major muscle over the growth period in broilers. Vet. Pathol. 54:119–28
    [Google Scholar]
  110. 110.  Velleman SG, Clark DL 2015. Histopathologic and myogenic gene expression changes associated with wooden breast in broiler breast muscles. Avian Dis 59:410–18
    [Google Scholar]
  111. 111.  Abasht B, Mutryn MF, Michalek RD, Lee WR 2016. Oxidative stress and metabolic perturbations in Wooden Breast disorder in chickens. PLOS ONE 11:e0153750
    [Google Scholar]
  112. 112.  Reverter A, Okimoto R, Sapp R, Bottje W, Hawken R, Hudson NJ 2017. Chicken muscle mitochondrial content appears co-ordinately regulated and is associated with performance phenotypes. Biol. Open 6:50–58
    [Google Scholar]
  113. 113.  Mazzoni M, Petracci M, Meluzzi A, Cavani C, Clavenzani P, Sirri F 2015. Relationship between pectoralis major muscle histology and quality traits of chicken meat. Poult. Sci. 94:123–30
    [Google Scholar]
  114. 114.  Bischoff R 1989. Analysis of muscle regeneration using single myofibers in culture. Med. Sci. Sports Exerc. 21:5 SupplS164–72
    [Google Scholar]
  115. 115.  Clark DL, Velleman SG 2017. Spatial influence on breast muscle morphological structure, myofiber size, and gene expression associated with the wooden breast myopathy in broilers. Poult. Sci. 95:2930–45
    [Google Scholar]
  116. 116.  Roenigk WP 1999. World poultry consumption. Poult. Sci. 78:722–28
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020518-115311
Loading
/content/journals/10.1146/annurev-animal-020518-115311
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error