Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity

Poultry Science

Volumn 83, Issue 3, 2004, Pages 474-484

  Iqbal, M ^a   Pumford, N R ^a   Tang, Z X ^a,c   Lassiter, K ^a   Wing, T ^b   Cooper, M ^a   Bottje, W ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b Cobb Vantress Inc ^*  (United States)

^c SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Complex activity; Feed efficiency; Mitochondria; Protein oxidation; Proteomics

Indexed keywords

AVES;

CYTOCHROME C OXIDASE; MUSCLE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL; ANIMAL FOOD; ARTICLE; CHEMISTRY; CHICKEN; ENZYMOLOGY; GENE EXPRESSION; GENETICS; MALE; METABOLISM; MUSCLE MITOCHONDRION; OXIDATIVE STRESS; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SKELETAL MUSCLE; ULTRASTRUCTURE;

ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; CHICKENS; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION; MALE; MITOCHONDRIA, MUSCLE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS;

EID: 2042440962     PISSN: 00325791     EISSN: None     Source Type: Journal    
DOI: 10.1093/ps/83.3.474     Document Type: Article

References (85)

1. Adamo, A. M., L. A. Pasquini, M. B. Moreno, E. F. Oteiza, and J. M. Pasquini. 1999. Effect of oxidant system on the ubiquitination of proteins in the central nervous system. J. Neurosci. Res. 55:523-531.
2. Almeida, A., and J. M. Medina. 1998. A rapid method for the isolation of metabolically active mitochondria from rat neurons and astrocytes in primary culture. Brain Res. Brain Res. Protoc. 2:209-214.
3. Ames, B. N., M. K. Shigenaga, and T. M. Hagen. 1993. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. 90:7915-7922.
4. Anderson, S., A. T. Bankier, B. G. Barrell, M. H. L. Debruijn, A. R. Coulson, J. Drouin, I. C. Eperon, D. P. Nierlich, B. A. Roe, F. Sanger, P. H. Schreier, A. J. H. Smith, R. Staden, and I. G. Young. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:457-465.
5. Bernardi, P., K. M. Broekemeier, and D. R. Pfeiffer. 1994. Recent progress on regulation of the mitochondrial permeability transition pore; a cyclsporin-senisitve pore in the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26:509-517.
6. Bhattacharya, S. K., J. H. Thakar, P. L. Johnson, and D. R. Shanklin. 1991. Isolation of skeletal muscle mitochondria from hamsters using an ionic medium containing ethylenediamine tetraacetic acid and nagarase. Anal. Biochem. 192:344-349.
7. 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.
8. Boveris, A., and B. Chance. 1973. The mitochondrial generation of hydrogen peroxide. Biochem. J. 134:707-711.
9. Breitbart, H., S. Rubinstein, and M. Gruberger. 1996. Calcium efflux mechanism in sperm mitochondria. Biochem. Biopys. Acta 1312:79-84.
10. Brookes, P. S., A. Pinner, A. Ramachandran, F. Coward, S. Barnes, H. Kim, and V. M. Darley-Usmar. 2002. High throughput two-dimensional blue-native electrophoresis: A tool for functional proteomics of mitochondria and signaling complexes. Proteomics 2:969-977.
11. Brown, D. R., S. K. DeNise, and R. G. McDaniel. 1986. Hepatic mitochondrial activity in two breeds of chicken. Poult. Sci. 65:613-615.
12. Buchczyk, D. P., K. Briviba, F. U. Hartl, and H. Sies. 2000. Responses to peroxynitrite in yeast: glycerinaldehyd-3-phosphate dehydrogenase (GAPDH) as a sensitive intracellular target for nitration and enhancement of chaperone expression and ubiquitination. Biol. Chem. 381:121-126.
13. Bulteau, A. L., I. Petropoulos, and B. Friguet. 2000. Age-related alterations of proteasome structure and function in aging epidermis. Exp. Gerontol. 35:767-777.
14. Butterfield, D. A., and C. M. Lauderback. 2002. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Rad. Biol. Med. 32:1050-1060.
15. Castegna, A., M. Aksenov, M. Aksenova, V. Thongboonkerd, J. B. Klein, W. M. Pierce, R. Booze, W. R. Markesbery, and D. A. Butterfield. 2002a. Proteomics identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxyterminal hydrolase L-1. Free Rad. Biol. Med. 33:562-571.
16. Castegna, A., M. Aksenov, V. Thongboonkerd, J. B. Klein, W. M. Pierce, R. Booze, W. R. Markesbery, and D. A. Butterfield. 2002b. Proteomics identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 82:1524-1532.
17. Cawthon, D., K. Beers, and W. G. Bottje. 2002. Electron transport chain defect and inefficient respiration may both underlie pulmonary hypertension syndrome (PHS)-associated mitochondrial dysfunction in broilers. Poult. Sci. 80:474-484.
18. Chance, B., H. Sies, and A. Boveris. 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:527-605.
19. Chapman, H. D., Z. B. Johnson, and J. L. McFarland. 2003. Improvements in the performance of commercial broilers in the USA: analysis for the years 1997 to 2001. Poult. Sci. 82:50-53.
20. Coates, P. J., R. Nenutil, A. McGregor, S. M. Picksley, D. H. Crouch, P. A. Hall. 2001. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp. Cell Res. 265:262-273.
21. Das, N., R. L. Levine, W. C. Orr, and R. S. Sohal. 2001. Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 360:209-216.
22. Davey, G. P., and J. B. Clark. 1996. Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria. J. Neurochem. 66:1617-1624.
23. De Schrijver, R., and O. S. Privett. 1984. Energetic efficiency and mitochondrial function in rats fed trans fatty acids. J. Nutr. 114:1183-1191.
24. Desjardins, P., and R. Morais. 1990. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J. Mol. Biol. 212:599-634.
25. DeWit, R., M. Making, J. Bootstrap, A. J. Berkley, and J. A. Post. 2001. Hydrogen peroxide reversible inhibits epidermal growth factor (EGF) receptor internalization and coincident ubiquitination of EGF receptor and Eps15. FASEB J. 15:306-308.
26. Drogue, W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82:47-95.
27. Drape, V., and R. Wassmuth. 1983. Growth stimulating effect of salinomycin in breeding and fattening of pigs. Dtsch. Tierarztl. Wochenschr. 88:14-18.
28. Dzapo, V. V., and R. Wassmuth. 1983. MItochondrialer Stoffwechsel und Heterotische Effekte Beim Schwein: Ergebnisse eines Reziproken Kreuzungsversuches. II. Atmungsaktita "te und Osidative Phosphorylierung in Herz-, Leber- und Hodenmitochondrien. Z. Tierzuecht. Zuechtungsbiol. 100:280-295.
29. Dziewiecki, C., and A. Kolataj. 1976. Rate of oxygen uptake by liver mitochondria in purebred chickens and in their hybrids. Genet. Pol. 17:219-224.
30. Emmerson, D. A. 1997. Commercial approaches to genetic selection for growth and feed conversion in domestic poultry. Poult. Sci. 76:1121-1125.
31. Galante, Y. M. and Y. Hatefi. 1978. Resolution of Complex I and isolation of NADH Dehydrogenase and an Iron-Sulfur Protein. Methods Enzymol. 53:15-47.
32. 2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source. J. Bioenerg. Biomembr. 33:279-287.
33. Gredilla, R., A. Sanz, M. Lopez-Torres, and G. Barja. 2001b. Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J. 15:1589-1591.
34. Hatefi, Y. 1978. Reconstitution of the electron-transport system of bovine heart mitochondria. Pages 35-38 in Methods in Enzymaology. S. Fleischer and L. Packer, ed. Academic Press, New York.
35. Hatefi, Y. 1985. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54:1015-1069.
36. Hatefi, Y., and D. L. Stiggall. 1978. Preparation and properties of succinate: ubiquinone reductase (Complex II). Methods Enzymol. 53:21-27.
37. Havenstein, G. B., P. R. Ferket, S. E. Scheidler, and B. T. Larson. 1994. Growth, livability, and feed conversion if 1957 and 1991 broilers when fed 'typical' 1957 and 1991 broiler diets. Poult. Sci. 73:1785-1794.
38. Havenstein, G. B., P.R. Ferket, and M. A. Qureshi. 2003. Growth, livability, and feed conversion of 1957 versus 2001 broilers fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500-1508.
39. Hershko, A., and A. Ciechanover. 1986. The ubiquitin pathway for the degradation of intracellular proteins. Prog. Nucleic Acid Res. Mol. Biol. 33:19-56.
40. Iqbal, M., L. L. Probert, N. H. Al-Humadi, and H. Klandorf. 1999. Protein glycosylation and advanced glycoslation endproducts (AGEs) accumulation: An avian solution? J. Gerontol. Biol. Sci. 54A:B171-B176.
41. Iqbal, M., D. Cawthon, R. F. Wideman, Jr., and W. Bottje. 2001a. Lung mitochondrial dysfunction in pulmonary hypertension syndrome. I. Site specific defects in electron transport chain. Poult. Sci. 80:485-495.
42. Iqbal, M., D. Cawthon, R. F. Wideman, Jr., and W. Bottje. 2001b. Lung mitochondrial dysfunction in pulmonary hypertension syndrome. II. Inability to improve function with repeated addition of ADP. Poult. Sci. 80:656-665.
43. Iqbal, M., J. D. Freiburger, E. F. Erf, and W. Bottje. 2002a. Immunohistochemical evidence of cytochrome c oxidase subunit II involvement in pulmonary hypertension syndrome (PHS) in broilers. Poult. Sci. 81:1231-1235.
44. Iqbal, M., N. R. Pumford, K. Lassiter, Z. X. Tang, D. Cawthon, and W. Bottje. 2002b. Modulation by feed efficiency of bc1 Complex in male broilers within single genetic line. Free Rad. Biol. Med. 33:S338 (Abstr.)
45. Iqbal, M., N. R. Pumford, K. Lassiter, Z. X. Tang, T. Wing, M. Cooper, W. Bottje. 2003. Association of mitochondrial dysfunction with feed efficiency in male broilers within single genetic line: A proteomics approach. Poult. Sci. 82(Suppl. 1):101. (Abstr.)
46. Keller, R. J., N. C. Halmes, J. A. Hinson, and N. R. Pumford. 1993. Immunochemical detection of oxidized proteins. Chem. Res. Toxicol. 6:430-433.
47. Kristal, B., S. Koopmans, C. T. Jackson, Y. Ikeno, B. Par, and B. P. Yu, 1997. Oxidant-mediated repression of mitochondrial transcription in diabetic rats. Free Rad. Biol. Med. 22:813-822.
48. Kristal, B., B. Park, and B. P. Yu. 1994. Antioxidants reduce peroxyl-mediated inhibition of mitochondrial transcription. Free Rad. Biol. Med. 16:653-660.
49. Kroemer, G., N. Zamzami, and S. A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today 18:44-51.
50. Kuan, J., and M. H. Saier, Jr. 1993. The mitochondrial carrier family of transport proteins: Structural, functional, and evolutionary relationships. Crit. Rev. Biochem. Mol. Biol. 28:209-233.
51. Laemmli, U. K. 1970. Cleavage of structure proteins during assembly of the head of bacteriophage T4. Nature 227:680-685.
52. Lopez-Torres, M., R. Gredilla, A. Sanz, and G. Barja. 2002. Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Rad. Biol. Med. 32:882-889.
53. Lutz, R. T., and T. S. Stahly. 2003. Quantitative relationship between mitochondrial bioenergetics and efficiency of animal growth. J. Anim. Sci. 8(Suppl 1.):141. (Abstr.)
54. Malgat, M., T. Letellier, and R. Rossignol. 2000. Metabolic control analysis and threshold effect in oxidative phosphorylation: Study in an intermediate state of respiration. Pages125-134 in Conference Program of the 9th International BioTheroKinetics Meeting, Stellenbosch, South Africa. BioThermoKinetics Study Group, University of Stellenbosch, Matieland, South Africa.
55. Mehlhase, J., and T. Grune. 2002. Proteolytic response to oxidative stress in mammalian cells. Biol. Chem. 383:559-567.
56. Mukherjee T. K., R. W. Stevens, M. P. Hoogendoorn. 1970. Oxygen uptake of mitochondrial isolates from two breeds of chickens and their F cross. Poult. Sci. 49:1130-1131.
57. Nijtmans, L. G. J., A. M. Sanz, L. A. Grivell, and P. J. Coates. 2002. The mitochondrial PHB complex: Roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol. Life Sci. 59:43-155.
58. Ojano-Dirain, C., M. Iqbal, D. Cawthon, S. Swonger, T. Wing, M. Cooper, and W. Bottje. 2003. Site-specific defects in electron transport chain in duodenal mitochondria are associated with low feed efficiency in broiler breeder males. Poult. Sci. (Suppl. 1)82:99-100. (Abstr.)
59. Okada, K., C. Wangpoengtrakul, T. Osawa, S. Toyokuni, K. Tanaka, and K. Uchida, 1999. 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. J. Biol. Chem. 274:23787-23793.
60. Opalka, J. R., M. Wicke, F. N. Gellerich, S. Zierz, and G. von Lengerken. 2000. Influence of mitochondrial function on growth and meat quality in turkey. Eur. J. Med. Res. 5 (Suppl. 1):57. (Abstr.)
61. Ozawa, T. 1997. Genetic and functional changes in mitochondria associated with aging. Physiol. Rev. 77:425-464.
62. Petit, P. X., S. A. Susin, N. Zamzami, B. Mignotte, and G. Kroemer. 1996. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396:7-13.
63. Pumford, N. R., J. A. Hinson, R. W. Benson, and D. W. Roberts. 1990. Immunoblot analysis of protein containing 3-(cystein-S-yl)acetaminophen adducts in serum and subcellular liver fractions from acetaminophen-treated mice. Toxicol. Appl. Pharmacol. 104:521-532.
64. Renner, R., S. M. Innis, and M. T. Clandinin. 1979. Effects of high and low erucic acid rapeseed oils on energy metabolism and mitochondrial function of the chick. J. Nutr. 109:378-387.
65. 2+ homeostasis, cell death, proliferation, and differentiation. Chem. Biol. Interact. 77:1-23.
66. Robin, E., and R. Wang. 1988. Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. J. Cell Physiol. 136:507-513.
67. Roemer, I., W. Reik, W. Dean, and J. Klose. 1997. Epigenetic inheritance in the mouse. Curr. Biol. 7:277-280.
68. Shang, F., T. R. Nowell, Jr., and A. Taylor. 2001. Removal of oxidatively damaged proteins from lens cells by the ubiquitin-proteasome pathway. Exp. Eye Res. 73:229-238.
69. Sohal, R. S., and R. Weindruch. 1996. Oxidative stress, caloric restriction, and aging. Science 273:59-63.
70. Sohal, R. S. 2002. Role of oxidative stress and protein oxidation in the aging process. Free Rad. Biol. Med. 33:37-44.
71. Stadtman, E. R., and R. L. Levine. 2000. Protein oxidation. Ann. NY Acad. Sci. 899:191-208.
72. Stewart, V. C., and S. J. R. Heales. 2003. Nitric oxide-induced mitochondrial dysfunction: Implications for neurodegeneration Free Rad. Biol. Med. 34:287-303.
73. Sue, C. M., and E. A. Schon. 2000. Mitochondrial chain diseases and mutations in nuclear DNA: A promising start. Brain Pathol. 10:442-450.
74. Tang, Z., M. Iqbal, D. Cawthon, and W. Bottje, 2002. Heart and breast muscle mitochondrial dysfunction in pulmonary hypertension syndrome in broilers (Gallus domesticus). Comp. Biochem. Physiol. A132:527-540.
75. Toyomizu, M., D. Kirihara, M. Tanaka, K. Hayashi, and Y. Tomita. 1992c. Dietary protein level alters oxidative phosphorulation in heart and liver mitochondria of chicks. Br. J. Nutr. 68:89-99.
76. Toyomizu, M., K. Mehara, T. Kamada, Y. Tomita. 1992b. Effects of various fat sources on growth and hepatic mitochondrialfunction in mice. Comp. Biochem. Physiol. 101A:613-618.
77. Toyomizu, M., K. Okamoto, M. Tanaka, and T. Ishibashi. 1992a. Effect of 2,4-dinitrophenol on growth and body composition of broilers. Poult. Sci. 71:1096-1100.
78. Wallace, D. 1999. Mitochondrial diseases in man and mouse. Science 283:1482-1488.
79. Wei., Y. 1998. Oxidative stress and mitochondrial DNA mutations in human aging. Exp. Biol. Med. 217:53-63.
80. Weindruch, R., K. P. Keenan, J. M. Carney, G. Fernandes, R. J. Feuers, R. A. Floyd, J. B. Halter, J. J. Ramsey, A. Richardson, G. S. Roth, and S. R. Spindler. 2001. Caloric restriction mimetics: metabolic interventions. J. Gerontol. Biol. Sci. Med. Sci. 56(Spec. 1):20-33.
81. Wolanis, M., V. Dzapo, and R. Wassmuth. 1980. The determination of biochemical parameters of energy metabolism and their relationship vitality, fattening performance and carcass quality in sheep. 2. Respiration activity and oxidative phosphorylation of isolated mitochondria. Z. Tierzuecht. Zuechtungsbiol. 97:28-36.
82. Yan, L. J., R. L. Levine, and R. S. Sohal. 1997. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. USA 94:11168-11172.
83. Yan, L. J., and R. S. Sohal. 1998. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl. Acad. Sci. USA 95:2896-12901.
84. Zainal, T. A., T. D. Oberley, D. B. Allison, L. I. Szweda, and R. Weindruch. 2000. Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J. 14:1825-1836.
85. Zhang, J., E. Block, R., and M. J. Patel. 2002. Down-regulation of mitochondrial cytochrome c oxidase in senescent porcine pulmonary artery endothelial cells. Mech. Age. Dev. 123:1363-1374.