Journal Home > Volume 1 , Issue 4

Apoptosis in postmortem muscle is a potential factor affecting meat quality. This study aimed to investigate the changes in apoptotic genes and proteins, reactive oxygen species (ROS), caspase-3 activity and their underlying relationship with meat tenderization. As postmortem time extended, there was a significant increase in myofibril fragmentation index (MFI) and destruction of muscle fibers. Oxidative stress deepened alongside the onset of apoptosis. Mitochondrial membrane potential (MMP) decreased, and caspase-3 activity increased during the first 24 h postmortem. Forty apoptotic genes displayed significant differences, involving DNA damage, autophagy, the death receptor pathway, the mitochondrial pathway, the Bcl-2 family, and the caspases family. The expression of most apoptotic genes was abundant in the early postmortem stage, enhancing the potential for early apoptosis. Apoptotic proteins of apoptosis-inducing factor, mitochondrion-associated 1 (AIFM1) and endonuclease G (ENDOG) showed the damage of apoptosis to DNA. Also, the decreasing expression of Bcl2 and increasing expression of Bak1 with time demonstrated the effects of mitochondrial apoptosis on postmortem muscle. These findings suggest that postmortem muscle apoptosis is a physiological process co-regulated by multiple genes, and potentially contributes to meat tenderization and quality.


menu
Abstract
Full text
Outline
About this article

Changes of postmortem apoptotic factors, genes and proteins and their potential associations with beef tenderization

Show Author's information Bo Zou1Fei Jia2Han Wang1Miaolin Duan1Xingmin Li1Ruitong Dai1( )
College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China
Department of Biological and Agricultural Engineering, University of Arkansas, Fayetteville 72701, USA

Abstract

Apoptosis in postmortem muscle is a potential factor affecting meat quality. This study aimed to investigate the changes in apoptotic genes and proteins, reactive oxygen species (ROS), caspase-3 activity and their underlying relationship with meat tenderization. As postmortem time extended, there was a significant increase in myofibril fragmentation index (MFI) and destruction of muscle fibers. Oxidative stress deepened alongside the onset of apoptosis. Mitochondrial membrane potential (MMP) decreased, and caspase-3 activity increased during the first 24 h postmortem. Forty apoptotic genes displayed significant differences, involving DNA damage, autophagy, the death receptor pathway, the mitochondrial pathway, the Bcl-2 family, and the caspases family. The expression of most apoptotic genes was abundant in the early postmortem stage, enhancing the potential for early apoptosis. Apoptotic proteins of apoptosis-inducing factor, mitochondrion-associated 1 (AIFM1) and endonuclease G (ENDOG) showed the damage of apoptosis to DNA. Also, the decreasing expression of Bcl2 and increasing expression of Bak1 with time demonstrated the effects of mitochondrial apoptosis on postmortem muscle. These findings suggest that postmortem muscle apoptosis is a physiological process co-regulated by multiple genes, and potentially contributes to meat tenderization and quality.

Keywords: mitochondria, apoptosis, ROS, postmortem, meat tenderization

References(38)

[1]

R. D. Warner, T. L. Wheeler, M. Ha, et al., Meat tenderness: advances in biology, biochemistry, molecular mechanisms and new technologies, Meat Sci. 185 (2022) 108657. https://doi.org/10.1016/j.meatsci.2021.108657.

[2]
F. Toldrá (Ed.), Lawrie’s meat science, Woodhead Publishing, 2022, pp. 393-400.
[3]

J. Y. Zhang, W. P. Ge, Q. L. Yu, Structural evaluation of cytochrome c by Raman spectroscopy and its relationship with apoptosis and protein degradation in postmortem bovine muscle, Food Chem. 362 (2021) 130189. https://doi.org/10.1016/j.foodchem.2021.130189.

[4]

B. Zou, Q. Q. Yu, L. L. Shao, et al., Alteration of mitochondrial lipidome and its potential effect on apoptosis, mitochondrial reactive oxygen species production, and muscle oxidation in beef during early postmortem, J. Agric. Food Chem. 70 (2022) 8064–8074. https://doi.org/10.1021/acs.jafc.2c02519.

[5]

L. L. Wang, L. Han, X. L. Ma, et al., Effect of mitochondrial apoptotic activation through the mitochondrial membrane permeability transition pore on yak meat tenderness during postmortem aging, Food Chem. 234 (2017) 323–331. https://doi.org/10.1016/j.foodchem.2017.04.185.

[6]

B. Zou, L. L. Shao, Q. Q. Yu, et al., Changes of mitochondrial lipid molecules, structure, cytochrome c and ROS of beef Longissimus lumborum and Psoas major during postmortem storage and their potential associations with beef quality, Meat Sci. 195 (2023) 109013. https://doi.org/10.1016/j.meatsci.2022.109013.

[7]

L. L. Wang, Q. L. Yu, L. Han, et al., Study on the effect of reactive oxygen species-mediated oxidative stress on the activation of mitochondrial apoptosis and the tenderness of yak meat, Food Chem. 244 (2018) 394–402. https://doi.org/10.1016/j.foodchem.2017.10.034.

[8]

F. Huang, M. Huang, G. H. Zhou, et al., In vitro proteolysis of myofibrillar proteins from beef skeletal muscle by caspase-3 and caspase-6, J. Agric. Food Chem. 59 (2011) 9658–9663. https://doi.org/10.1021/jf202129r.

[9]

S. Bedoui, M. J. Herold, A. Strasser, Emerging connectivity of programmed cell death pathways and its physiological implications, Nat. Rev. Mol. Cell Bio. 21 (2020) 678–695. https://doi.org/10.1038/s41580-020-0270-8.

[10]

F. J. Bock, S. W. G. Tait, Mitochondria as multifaceted regulators of cell death, Nat. Rev. Mol. Cell Bio. 21 (2020) 85–100. https://doi.org/10.1038/s41580-019-0173-8.

[11]

T. A. Bhat, A. K. Chaudhary, S. Kumar, et al., Endoplasmic reticulum-mediated unfolded protein response and mitochondrial apoptosis in cancer, BBA-Rev. Cancer. 1867 (2017) 58–66. https://doi.org/10.1016/j.bbcan.2016.12.002.

[12]

L. L. Wang, G. Y. Ma, Y. B. Zhang, et al., Effect of mitochondrial cytochrome c release and its redox state on the mitochondrial-dependent apoptotic cascade reaction and tenderization of yak meat during postmortem aging, Food Res. Int. 111 (2018) 488–497. https://doi.org/10.1016/j.foodres.2018.05.049.

[13]

B. Zou, L. L. Shao, Y. Liu, et al., Muscle fiber characteristics and apoptotic factor differences in beef Longissimus lumborum and Psoas major during early postmortem, Meat Sci. 198 (2023) 109092. https://doi.org/10.1016/j.meatsci.2022.109092.

[14]

B. Guo, W. G. Zhang, R. K. Tume, et al., Disorder of endoplasmic reticulum calcium channel components is associated with the increased apoptotic potential in pale, soft, exudative pork, Meat Sci. 115 (2016) 34–40. https://doi.org/10.1016/j.meatsci.2016.01.003.

[15]

L. Chen, Y. W. Chai, J. Luo, et al., Apoptotic changes and myofibrils degradation in post-mortem chicken muscles by ultrasonic processing, LWT-Food Sci. Technol. 142 (2021) 110985. https://doi.org/10.1016/j.lwt.2021.110985.

[16]

Y. L. Ke, R. M. Mitacek, A. Abraham, et al., Effects of muscle-specific oxidative stress on cytochrome c release and oxidation-reduction potential properties, J. Agric. Food Chem. 65 (2017) 7749–7755. https://doi.org/10.1021/acs.jafc.7b01735.

[17]

B. Zou, D. Zhao, G. J. He, et al., Acetylation and phosphorylation of proteins affect energy metabolism and pork quality, J. Agric. Food Chem. 68 (2020) 7259–7268. https://doi.org/10.1021/acs.jafc.0c01822.

[18]

Y. L. Mao, X. D. Wang, C. S. Chen, et al., Immune-awakening Saccharomyces-inspired nanocarrier for oral target delivery to lymph and tumors, Acta Pharm. Sin. B. 12 (2022) 4501–4518. https://doi.org/10.1016/j.apsb.2022.04.018.

[19]

T. T. Wang, X. C. Feng, L. Z. Li, et al., Effects of quercetin on tenderness, apoptotic and autophagy signalling in chickens during post-mortem ageing, Food Chem. 383 (2022) 132409. https://doi.org/10.1016/j.foodchem.2022.132409.

[20]

P. P. Purslow, M. Gagaoua, R. D. Warner, Insights on meat quality from combining traditional studies and proteomics, Meat Sci. 174 (2021) 108423. https://doi.org/10.1016/j.meatsci.2020.108423.

[21]

H. Sies, D. P. Jones, Reactive oxygen species (ROS) as pleiotropic physiological signalling agents, Nat. Rev. Mol. Cell Bio. 21 (2020) 363–383. https://doi.org/10.1038/s41580-020-0230-3.

[22]

A. E. D. A. Bekhit, D. L. Hopkins, F. T. Fahri, et al., Oxidative processes in muscle systems and fresh meat: sources, markers, and remedies, Compr. Rev. Food Sci. F. 12 (2013) 565–597. https://doi.org/10.1111/1541-4337.12027.

[23]

A. A. Bekhit, D. L. Hopkins, G. Geesink, et al., Exogenous proteases for meat tenderization, Crit. Rev. Food Sci. 54 (2014) 1012–1031. https://doi.org/10.1080/10408398.2011.623247.

[24]

H. U. Simon, A. Haj-Yehia, F. Levi-Schaffer, Role of reactive oxygen species (ROS) in apoptosis induction, Apoptosis 5 (2000) 415–418. https://doi.org/10.1023/A:1009616228304.

[25]

M. Falabella, H. J. Vernon, M. G. Hanna, et al., Cardiolipin, mitochondria, and neurological disease, Trends Endocrin. Met. 32 (2021) 224–237. https://doi.org/10.1016/j.tem.2021.01.006.

[26]

J. Y. Zhang, Q. L. Yu, L. Han, et al., Effects of lysosomal iron involvement in the mechanism of mitochondrial apoptosis on postmortem muscle protein degradation, Food Chem. 328 (2020) 127174. https://doi.org/10.1016/j.foodchem.2020.127174.

[27]

J. Y. Zhang, D. Y. Ma, Y. H. B. Kim, Mitochondrial apoptosis and proteolytic changes of myofibrillar proteins in two different pork muscles during aging, Food Chem. 319 (2020) 126571. https://doi.org/10.1016/j.foodchem.2020.126571.

[28]

D. S. C. Han, Y. M. D. Lo, The nexus of cfDNA and nuclease biology, Trends Genet. 37 (2021) 758–770. https://doi.org/10.1016/j.tig.2021.04.005.

[29]

D. Bano, J. H. M. Prehn, Apoptosis-inducing factor (AIF) in physiology and disease: the tale of a repented natural born killer, EBioMedicine. 30 (2018) 29–37. https://doi.org/10.1016/j.ebiom.2018.03.016.

[30]

D. D. Zhdanov, T. Fahmi, X. Y. Wang, et al., Regulation of apoptotic endonucleases by EndoG, DNA Cell Biol. 34 (2015) 316–326. https://doi.org/10.1089/dna.2014.2772.

[31]

Q. Chen, J. Kang, C. Y. Fu, The independence of and associations among apoptosis, autophagy, and necrosis, Signal Transduct. Tar. 3 (2018) 18. https://doi.org/10.1038/s41392-018-0018-5.

[32]

M. Noguchi, N. Hirata, T. Tanaka, et al., Autophagy as a modulator of cell death machinery, Cell Death Dis. 11 (2020) 517. https://doi.org/10.1038/s41419-020-2724-5.

[33]

M. Saleem, M. I. Qadir, N. Perveen, et al., Inhibitors of apoptotic proteins: new targets for anticancer therapy, Chem. Biol. Drug Des. 82 (2013) 243–251. https://doi.org/10.1111/cbdd.12176.

[34]

J. Karch, M. J. Bround, H. Khalil, et al., Inhibition of mitochondrial permeability transition by deletion of the ANT family and CypD, Sci. Adv. 5 (2019) eaaw4597. https://doi.org/10.1126/sciadv.aaw4597.

[35]

Y. X. Li, H. J. Wu, R. Khardori, et al., Insulin-like growth factor-1 receptor activation prevents high glucose-induced mitochondrial dysfunction, cytochrome-c release and apoptosis, Biochem. Bioph. Res. Co. 384 (2009) 259–264. https://doi.org/10.1016/j.bbrc.2009.04.113.

[36]

R. Singh, A. Letai, K. Sarosiek, Regulation of apoptosis in health and disease: the balancing act of Bcl-2 family proteins, Nat. Rev. Mol. Cell Bio. 20 (2019) 175–193. https://doi.org/10.1038/s41580-018-0089-8.

[37]

J. Li, J. Yuan, Caspases in apoptosis and beyond, Oncogene. 27 (2008) 6194–6206. https://doi.org/10.1038/onc.2008.297.

[38]

B. Zou, F. Jia, L. Ji, et al., Effects of mitochondria on postmortem meat quality: characteristic, isolation, energy metabolism, apoptosis and oxygen consumption, Crit. Rev. Food Sci. (2023) 1–24. https://doi.org/10.1080/10408398.2023.2235435.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 07 November 2023
Revised: 05 December 2023
Accepted: 15 December 2023
Published: 20 February 2024
Issue date: December 2023

Copyright

© Beijing Academy of Food Sciences 2023.

Acknowledgements

This work was funded by the National Natural Science Foundation of China (No. 32072286).

Rights and permissions

Food Science of Animal Products published by Tsinghua University Press. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return