Apoptosis

, Volume 22, Issue 6, pp 777–785 | Cite as

Study on the apoptosis mediated by cytochrome c and factors that affect the activation of bovine longissimus muscle during postmortem aging

  • Jiaying Zhang
  • Qunli Yu
  • Ling Han
  • Cheng Chen
  • Hang Li
  • Guangxing Han
Article
  • 212 Downloads

Abstract

This study investigates whether bovine longissimus muscle cell apoptosis occurs during postmortem aging and whether apoptosis is dependent on the mitochondria pathway. This study also determines the apoptosis process mediated by cytochrome c after its release from mitochondria and the factors that affect the activation processes. Results indicate that apoptotic nuclei were detected at 12 h postmortem. Cytochrome c release from the mitochondria to the cytoplasm activated the caspase-9 and caspase-3 at early postmortem aging and the activation of caspase-9 occurs before the activation of caspase-3. The pH level decreased during the first 48 h postmortem, whereas the mitochondria membrane permeability increased from 6 to 12 h. Results demonstrate that an apoptosis process of bovine muscle occurred during postmortem aging. Apoptosis was dependent on the mitochondria pathway and occurred at early postmortem aging. Increased mitochondria membrane permeability and low pH are necessary conditions for the release of cytochrome c during postmortem aging.

Keywords

Apoptosis Cytochrome c-mediated Mitochondria Bovine longissimus muscle Postmortem aging 

Notes

Acknowledgements

We thank colleagues in the laboratory and our collaborators for their useful suggestions. This work was supported by the China Agriculture Research System (CARS-38), National Natural Science Foundation of China (Grant No.: 31560463).

Compliance with ethical standards

Conflict of interest

Jiaying Zhang, Qunli Yu, Ling Han, Cheng Chen, Hang Li and Guangxing Han declares that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the author.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Sentandreu MA, Coulis G, Ouali A (2002) Role of muscle endopeptidases and their inhibitors in meat tenderness. Trend Food Sci Technol 13:400–421CrossRefGoogle Scholar
  2. 2.
    Ouali A, Herrera-Mendez HC, Coulis G, Becila S, Boudjellal A, Aubry L et al (2006) Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Sci 74:44–58CrossRefPubMedGoogle Scholar
  3. 3.
    Bernard C, Cassar-Malek I, Le Cunff M, Durbroeucq H, Renard G, Hocquette JF (2007) New indicators of beef sensory quality revealed by expression of specific genes. J Agric Food Chem 55:5229–5237CrossRefPubMedGoogle Scholar
  4. 4.
    Denault JB, Salvesen GS (2008) Apoptotic caspase activation and activity. Methods Mol Biol 414:191–220PubMedGoogle Scholar
  5. 5.
    Zou H, Li Y, Liu X, Wang X (1999) An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274:11549–11556sCrossRefPubMedGoogle Scholar
  6. 6.
    Renault TT, Floros KV, Chipuk JE (2013) BAK/BAX activation and cytochrome c release assays using isolated mitochondria. Methods 61:146–155CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: Requirements for dATP and cytochrome c. Cell 86:147–157CrossRefPubMedGoogle Scholar
  8. 8.
    Robertson JD, Orrenius S, Zhivotovsky B (2000) Review: nuclear events in apoptosis. J Struct Biol 129:346–358CrossRefPubMedGoogle Scholar
  9. 9.
    Becila S, Herrera-Mendez C, Coulis G, Labas R, Astruc T, Picard B et al (2010) Postmortem muscle cells die through apoptosis. Eur Food Res Technol 231(3):485–493CrossRefGoogle Scholar
  10. 10.
    Cai JY, Yang J, Jones DP (1998) Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1366(1–2):139–149CrossRefPubMedGoogle Scholar
  11. 11.
    Gogvadze V, Orrenius S, Zhivotovsky B (2006) Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim Biophys Acta (BBA)-Bioenerg 1757(5–6):639–647CrossRefGoogle Scholar
  12. 12.
    Li Y, Johnson N, Capano M, Edwards M, Crompton M (2004) Cyclophilin-D promotes the mitochondrial permeability transition but has opposite effects on apoptosis and necrosis. Biochem J 383:101–109CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H et al (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434:652–658CrossRefPubMedGoogle Scholar
  14. 14.
    Tassy C, Herrera-Mendez CH, Sentandreu MA, Aubry L, Bremaud L, Pelissier P et al (2005) Muscle endopin 1, amuscle intracellular serpin which strongly inhibits elastase: purification, characterization, cellular localization and tissue distribution. Biochem J 388:273–280CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Lokanath NK, Ohshima N, Takio K, Shiromizu I, Kuroishi C, Okazaki N et al (2005) Crystal structure of novel NADP-dependent 3-hydroxyisobutyrate dehydrogenase from Thermus thermophilus HB8. J Mol Biol 352:905–917CrossRefPubMedGoogle Scholar
  16. 16.
    Lomiwes D, Farouk MM, Wu G, Young OA (2014) The development of meat tenderness is likely to be compartmentalized by ultimate pH. Meat Sci 96:646–651CrossRefPubMedGoogle Scholar
  17. 17.
    Qian T, Nieminen AL, Herman B (1997) Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes. Am J Physiol 273:1783–1792Google Scholar
  18. 18.
    Boudjellal A, Becila S, Coulis G, Herrera-Mendez CH, Aubry L, Lepetit J et al (2008) Is the pH drop profile curvilinear and either monophasic or polyphasic? Consequences on the ultimate bovine meat texture. Afr J Agric Res 3:195–204Google Scholar
  19. 19.
    Zhang MH, Wang DY, Huang F, Liu F, Zhu YZ, Xu WM et al (2013) Apoptosis during postmortem conditioning and its relationship to duck meat quality. Food Chem 138:96–100CrossRefPubMedGoogle Scholar
  20. 20.
    Quadrilatero J, Rush JW (2006) Increased DNA fragmentation and altered apoptotic protein levels in skeletal muscle of spontaneously hypertensive rats. J Appl Physiol 101(4):1149–1161CrossRefPubMedGoogle Scholar
  21. 21.
    Cao JX, Ou CR, Zou YF, Ye KP, Zhang QQ, Khan MA et al (2013) Activation of caspase-3 and its correlation with shear force in bovine skeletal muscles during postmortem conditioning. J Anim Sci 91:4547–4552CrossRefPubMedGoogle Scholar
  22. 22.
    Sun LJ, Luo C, Long JG, Wei DZ, Liu JK (2006) Acrolein is a mitochondrial toxin: effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Mitochondrion 6(3):136–142CrossRefPubMedGoogle Scholar
  23. 23.
    Krumschnabel G, Manzl C, Berger C, Hofer B (2005) Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol Appl Pharmacol 209:62–73CrossRefPubMedGoogle Scholar
  24. 24.
    Brunelle JK, Chandel NS (2002) Oxygen deprivation induced cell death: an update. Apoptosis 7:475–482CrossRefPubMedGoogle Scholar
  25. 25.
    Deng XL, Wang Y, Chou J, Cadet JL (2001) Methamphetamine causes widespread apoptosis in the mouse brain: exidence from using as improved TUNEL histochemical method. Mol Brain Res 93:64–69Google Scholar
  26. 26.
    Alamab MS, Kurohmarub M (2016) Butybenzyl phthalate induces spermatogenic cell apoptosis in prepubertal rats. Tissue Cell 1:35–42CrossRefGoogle Scholar
  27. 27.
    Cao JX, Sun WQ, Zhou GH, Xu XL, Peng ZQ, Hu ZL (2010) Morphological and biochemical assessment of apoptosis in different skeletal muscles of bulls during conditioning. J Anim Sci 88(10):3439–3444CrossRefPubMedGoogle Scholar
  28. 28.
    Kemp CM, Parr T, Bardsley RG, Buttery PJ (2006) Comparison of the relative expression of caspase isoforms in different porcine skeletal muscles. Meat Sci 73:426–431CrossRefPubMedGoogle Scholar
  29. 29.
    Kemp CM, Bardsley RG, Parr T (2006) Changes in caspase activity during the postmortem conditioning period and its relationship to shear force in porcine longissimus muscle. J Anim Sci 84:2841–2846CrossRefPubMedGoogle Scholar
  30. 30.
    Yang JC, Cortopassi GA (1998) dATP causes specific release of cytochrome c from mitochondria. Biochem Biophys Res Commun 250:454–457CrossRefPubMedGoogle Scholar
  31. 31.
    Li T, Brustovetsky T, Antonsson B, Brustovetsky N (2008) Oligomeric BAX induces mitochondrial permeability transition and complete cytochrome c release without oxidative stress. Biochim Biophys Acta 1777(11):1409–1421CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Huang F, Huang M, Zhang H, Zhang CJ, Zhang DQ, Zhou GH (2016) Changes in apoptotic factors and caspase activation pathways during the postmortem aging of beef muscle. Food Chem 190:110–114CrossRefPubMedGoogle Scholar
  33. 33.
    Dan Y (2008) Biological functions of antioxidants in plant transformation. In vitro Cell Dev Biol Plant 44:149–161CrossRefGoogle Scholar
  34. 34.
    Philchenkov A (2004) Caspases: potential targets for regulating cell death. J Cell Mol Med 8:432–444CrossRefPubMedGoogle Scholar
  35. 35.
    Krammer PH (2000) CD95’s deadly mission in the immune system. Nature 407:789–795CrossRefPubMedGoogle Scholar
  36. 36.
    Underwood KR, Means WJ, Du M (2008) Caspase 3 is not likely involved in the postmortem tenderization of beef muscle. J Anim Sci 86:960–966CrossRefPubMedGoogle Scholar
  37. 37.
    Orrenius S (2004) Mitochondrial regulation of apoptotic cell death. Toxicol Lett 149:19–23CrossRefPubMedGoogle Scholar
  38. 38.
    Petrosillo G, Ruggiero FM, Pistolese M, Paradies G (2001) Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation. Possible role in the apoptosis. FEBS Lett 509:435–438CrossRefPubMedGoogle Scholar
  39. 39.
    Hofer T, Servais S, Seo AY, Marzetti E, Hiona A, Upadhyay SJ et al (2009) Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech Ageing Dev 130:297–307CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Matsuyama S, Llopis J, Deveraux QL, Tsien RY, Reed JC (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat Cell Biol 6:318–325Google Scholar
  41. 41.
    Sharma V, Kaur R, Bhatnagar A, Kaur J (2015) Low-pH-induced apoptosis: role of endoplasmic reticulum stress-induced calcium permeability and mitochondria-dependent signaling. Cell Stress Chaperones 20:431–440CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Jolly AJ, Wild CP, Hardie LJ (2004) Acid and bile salts induce DNA damage in human oesophageal cell lines. Mutagenesis 19:319–324CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Jiaying Zhang
    • 1
  • Qunli Yu
    • 1
  • Ling Han
    • 1
  • Cheng Chen
    • 1
  • Hang Li
    • 2
  • Guangxing Han
    • 3
  1. 1.College of Food Science and EngineeringGansu Agricultural UniversityLanzhouChina
  2. 2.Chongqing Heng Du Agricultural Development Co., Ltd.FengduChina
  3. 3.Shandong Lorain Corporation Co., Ltd.LinyiChina

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