Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T08:03:45.991Z Has data issue: false hasContentIssue false
  • English
  • Français

Activation of caspase-9 and its influencing factors in beef during conditioning

Published online by Cambridge University Press:  05 December 2013

J. Cao ,
G. Zhou ,
Y. Liu ,
G. Liao ,
Q. Zhang ,
K. Ye ,
D. Pan  and
C. Ou
J. Cao
Affiliation:
Department of Food Science and Engineering, Ningbo University, Ningbo 315211, P. R. China National Center of Meat Quality and Safety Control, MOST, Nanjing Agricultural University, Nanjing 210095, P. R. China
G. Zhou
Affiliation:
National Center of Meat Quality and Safety Control, MOST, Nanjing Agricultural University, Nanjing 210095, P. R. China
Y. Liu
Affiliation:
College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, P. R. China
G. Liao
Affiliation:
College of Food Science and Technology, Yunnan Agricultural University, Kunming 650201, P. R. China
Q. Zhang
Affiliation:
National Center of Meat Quality and Safety Control, MOST, Nanjing Agricultural University, Nanjing 210095, P. R. China
K. Ye
Affiliation:
National Center of Meat Quality and Safety Control, MOST, Nanjing Agricultural University, Nanjing 210095, P. R. China
D. Pan
Affiliation:
Department of Food Science and Engineering, Ningbo University, Ningbo 315211, P. R. China
C. Ou*
Affiliation:
Department of Food Science and Engineering, Ningbo University, Ningbo 315211, P. R. China
*
E-mail: Ouchangrong@nbu.edu.cn
Get access

Abstract

To study the activation of caspase-9 and its potential influence in conditioning, longissimus thoracis (LT), semitendinosus (STN) and psoas minor (PMi) muscles were used to analyze the ratio of pro-apoptotic bax to anti-apoptotic bcl-2 in fresh tissues and observe the changes in ATP, cytosolic cytochrome c and caspase-9 activity levels during storage at 4°C. Caspase-9 activity at 5 h is higher than the activity at 0 and 24 h in the muscles (P<0.001). The ATP content decreased between 0 and 3 h, between 8 and 14 h in the PMi and LT muscles (P<0.0001), whereas between 0 and 5 h, between 8 and 14 h in the STN muscle (P<0.0001). There is 60.2%, 55.3% and 43.1% available ATP in the STN, LT and PMi muscles at 5 h, respectively. The cytosolic cytochrome c level increased during 5 and 24 h storage in the LT and PMi muscles (P<0.0001), during 5 and 96 h in the STN muscle (P<0.0001). The cytosolic cytochrome c at 24 h (P<0.001) and ratio of bax to bcl-2 (P<0.05) was higher in the PMi than in other muscles. We concluded that the increase in cytosolic cytochrome c and available intracellular ATP should be responsible for the increase in caspase-9 activity; the activation of caspase-9 could be limited by the subsequent depletion of ATP; the postmortem release level of cytochrome c could be determined by the ratio of bax to bcl-2 in fresh tissues.

Keywords

conditioningcaspase-9bovine skeletal musclescytochrome c releasebcl-2 family proteins
Type
Full Paper
Information
animal , Volume 8 , Issue 3 , March 2014 , pp. 504 - 509
Copyright
© The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

The first two authors contribute equally to this study/work.

References

Adams, JM 2003. Ways of dying: multiple pathways to apoptosis. Genes & Development 17, 2481–2495.Google Scholar
Cao, J, Sun, W, Zhou, G, Xu, X, Peng, Z and Hu, Z 2010. Morphological and biochemical assessment of apoptosis in different skeletal muscles of bulls during conditioning. Journal of Animal Science 88, 3439–3444.Google Scholar
Cao, J, Yu, X, Khan, MA, Shao, J, Xiang, Y and Zhou, G 2012. The effect of calcium chloride injection on shear force and caspase activities in bovine longissimus muscles during postmortem conditioning. Animal 6, 1018–1022.Google Scholar
Cao, J, Ou, C, Zou, Y, Ye, K, Zhang, Q, Khan, M, Pan, D and Zhou, G 2013. Activation of caspase-3 and its correlation with shear force in bovine skeletal muscles during postmortem conditioning. Journal of Animal Science 91, 4547–4552.Google Scholar
Chen, L, Feng, X, Lu, F, Xu, X, Zhou, G, Li, Q and Guo, X 2011. Effects of camptothecin, etoposide and Ca2+ on caspase-3 activity and myofibrillar disruption of chicken during postmortem ageing. Meat Science 87, 165–174.Google Scholar
Delivoria-Papadopoulos, M, Gorn, M, Ashraf, QM and Mishra, OP 2007. ATP and cytochrome c-dependent activation of caspase-9 during hypoxia in the cerebral cortex of newborn piglets. Neuroscience Letters 429, 115–119.Google Scholar
Du, M, Shen, QW and Zhu, MJ 2005. Role of beta-adrenoceptor signaling and AMP-activated protein kinase in glycolysis of postmortem skeletal muscle. Journal of Agricultural and Food Chemistry 53, 3235–3239.Google Scholar
Fritz, JD and Greaser, ML 1991. Changes in titin and nebulin in postmortem bovine muscle revealed by gel electrophoresis, western blotting and immunofluorescence microscopy. Journal of Food Science 56, 607–610.CrossRefGoogle Scholar
Fujimura, M, Morita-Fujimura, Y, Murakami, K, Kawase, M and Chan, PH 1998. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. Journal of Cerebral Blood Flow & Metabolism 18, 1239–1247.CrossRefGoogle ScholarPubMed
Gross, A, McDonnell, JM and Korsmeyer, SJ 1999. BCL-2 family members and the mitochondria in apoptosis. Genes & Development 13, 1899–1911.Google Scholar
Gross, A, Jockel, J, Wei, MC and Korsmeyer, SJ 1998. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO Journal 17, 3878–3885.Google Scholar
Havaki, S, Kouloukoussa, M, Amawi, K, Drosos, Y, Arvanitis, LD, Goutas, N, Vlachodimitropoulos, D, Vassilaros, SD, Katsantoni, EZ, Voloudakis-Baltatzis, I, Aleporou-Marinou, V, Kittas, C and Marinos, E 2007. Altered expression pattern of integrin alphavbeta3 correlates with actin cytoskeleton in primary cultures of human breast cancer. Cancer Cell International 7, 16–28.CrossRefGoogle ScholarPubMed
Hocquette, JF, Botreau, R, Picard, B, Jacquet, A, Pethick, DW and Scollan, ND 2012. Opportunities for predicting and manipulating beef quality. Meat Science 92, 197–209.Google Scholar
Hopkins, D and Thompson, J 2002. The degradation of myofibrillar proteins in beef and lamb using denaturing electrophoresis: an overview. Journal of Muscle Foods 13, 81–102.Google Scholar
Huang, F, Huang, M, Zhou, G, Xu, X and Xue, M 2011. In vitro proteolysis of myofibrillar proteins from beef skeletal muscle by caspase-3 and caspase-6. Journal of Agricultural and Food Chemistry 59, 9658–9663.Google Scholar
Huang, M, Huang, F, Xue, M, Xu, X and Zhou, G 2011. The effect of active caspase-3 on degradation of chicken myofibrillar proteins and structure of myofibrils. Food Chemistry 128, 22–27.Google Scholar
Kemp, CM, Bardsley, RG and Parr, T 2006a. Changes in caspase activity during the postmortem conditioning period and its relationship to shear force in porcine longissimus muscle. Journal of Animal Science 84, 2841–2846.Google Scholar
Kemp, CM, Parr, T, Bardsley, RG and Buttery, PJ 2006b. Comparison of the relative expression of caspase isoforms in different porcine skeletal muscles. Meat Science 73, 426–431.Google Scholar
Khurana, P, Ashraf, QM, Mishra, OP and Delivoria-Papadopoulos, M 2002. Effect of hypoxia on caspase-3, -8, and -9 activity and expression in the cerebral cortex of newborn piglets. Neurochemical Research 27, 931–938.CrossRefGoogle ScholarPubMed
Kluck, RM, Bossy-Wetzel, E, Green, DR and Newmeyer, DD 1997. The release of cytochrome c from mitochondria: a primary site for bcl-2 regulation of apoptosis. Science 275, 1132–1136.Google Scholar
Kolczak, T, Pospiech, E, Palka, K and Lacki, J 2003. Changes in structure of psoas major and minor and semitendinosus muscles of calves, heifers and cows during post-mortem ageing. Meat Science 64, 77–83.Google Scholar
Liu, X, Kim, CN, Yang, J, Jemmerson, R and Wang, X 1996. Induction of apoptotic program in cell-free extracts, requirement for dATP and cytochrome c. Cell 86, 147–157.Google Scholar
Marzetti, E, Lees, HA, Manini, TM, Buford, TW Jr, Aranda, JM, Calvani, R, Capuani, G, Marsiske, M, Lott, DJ, Vandenborne, K, Bernabei, R, Pahor, M, Leeuwenburgh, C and Wohlgemuth, SE 2012. Skeletal muscle apoptotic signaling predicts thigh muscle volume and gait speed in community-dwelling older persons: an exploratory study. PLoS One 7, e32829.Google Scholar
Nagasaka, R, Okamoto, N and Ushio, H 2006. Elevated levels of oxidative DNA damage activate p53 and caspases in brain of ayu with aging. Journal of Applied Ichthyology 22, 357–362.Google Scholar
Ouali, A, Herrera-Mendez, CH, Coulis, G, Becila, S, Boudjellal, A, Aubry, L and Sentandreu, MA 2006. Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Science 74, 44–58.Google Scholar
Pastorino, JG, Chen, ST, Tafani, M, Snyder, JW and Farber, JL 1998. The overexpression of bax produces cell death upon induction of the mitochondrial permeability transition. Journal of Biological Chemistry 273, 7770–7775.Google Scholar
Phaneuf, S and Leeuwenburgh, C 2002. Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 282, R423–R430.Google Scholar
Rice, KM and Blough, ER 2006. Sarcopenia-related apoptosis is regulated differently in fast- and slow-twitch muscles of the aging F344/N×BN rat model. Mechanisms of Ageing and Development 127, 670–679.Google Scholar
Soeda, J, Miyagawa, S, Sano, K, Masumoto, J, Taniguchi, SI and Kawasaki, S 2001. Cytochrome c release into cytosol with subsequent caspase activation during warm ischemia in rat liver. American Journal of Physiology – Gastrointestinal and Liver Physiology 281, G1115–G1123.Google Scholar
Stoetzer, OJ, Nussler, V, Darsow, M, Gullis, E, Pelka-Fleischer, R, Scheel, U and Wilmanns, W 1996. Association of bcl-2, bax, bcl-xL and interleukin-1 beta-converting enzyme expression with initial response to chemotherapy in acute myeloid leukemia. Leukemia 10, S18–S22.Google Scholar
Thornberry, NA and Lazebnik, Y 1998. Caspases: enemies within. Science 281, 1312–1316.Google Scholar
Veciana-Nogués, MT, Izquierdo-Pulido, M and Vidal-Carou, MC 1997. Determination of ATP related compounds in fresh and canned tuna fish by HPLC. Food Chemistry 59, 467–472.CrossRefGoogle Scholar
Vendelin, J, Pulkkinen, V, Rehn, M, Pirskanen, A, Räisänen-Sokolowski, A, Laitinen, A, Haahtela, T, Saarialho-Kere, U, Laitinen, A and Kere, J 2006. Downstream target genes of the neuropeptide S-NPSR1 pathway. Human Molecular Genetics 15, 2923–2935.Google Scholar
Viemann, D, Barczyk, K, Vogl, T, Fischer, U, Sunderkötter, C, Schulze-Osthoff, K and Roth, J 2007. MRP8/MRP14 impairs endothelial integrity and induces a caspase-dependent and -independent cell death program. Blood 9, 2453–2460.Google Scholar
Zou, H, Henzel, WJ, Liu, X, Lutschg, A and Wang, X 1997. Apaf-1, a human protein homologous to C elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405–413.CrossRefGoogle Scholar