Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (10): 2192-2202.doi: 10.3864/j.issn.0578-1752.2021.10.014

• FOOD SCIENCE AND ENGINEERING • Previous Articles     Next Articles

Research Progress on Mechanisms of Apoptosis to Postmortem Tenderization in Muscle

HUANG Feng(),WEI QiChao,LI Xia,LIU ChunMei,ZHANG ChunHui()   

  1. Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences/Key Laboratory of Agro-Products Processing, Ministry of Agriculture, Beijing 100193
  • Received:2020-08-30 Accepted:2020-11-24 Online:2021-05-16 Published:2021-05-24
  • Contact: ChunHui ZHANG E-mail:huangfeng226@foxmail.com;dr_zch@163.com

Abstract:

Tenderness has been considered as one of the most important eating quality characteristics of meat, while inconsistent changes of tenderness in postmortem (PM) muscles can significantly reduce the purchasing intention. Therefore, investigating mechanism of postmortem muscle tenderization is becoming more and more important in the past decade. Since apoptosis definition was highlighted in the PM tenderization process, it has been widely concerned. Shortly after slaughter, the reactive oxygen species (ROS) was significantly accumulated, and ATP (adenosine triphosphate) was gradually exhausted within muscle fibers, which inevitably led to skeletal cell death. Both PM cell death and meat tenderization refer to the activation of muscle endogenous enzymes by a series of regulatory factors, followed by the degradation of muscle structural proteins. The two biochemical processes are considered to be highly related. PM muscle cells die mainly through apoptosis. Besides, in the early stage of PM, when a small amount of ROS is produced, the cells start their defense system by autophagy and ATP therefore gradually deplete muscle cells in the later stage, which may change from apoptosis to necrosis. It has been documented that mitochondrial pathway is crucial for the apoptosis activation in PM muscles. The release of apoptotic factors from mitochondria is the master node of the intracellular death cascade reaction. The opening status of mitochondrial outer membrane directly determines the way, in which the muscle fiber dies. In this paper, the release mechanism of apoptotic factors induced by PM mitochondrial damage was discussed from the perspectives of mitochondrial membrane permeability and cristae remodeling, and the regulation of mitochondrial damage on PM muscle tenderization was discussed. Moreover the underlying mechanism behind it was also analyzed to reveal the effect of mitochondria on muscle pH regulation through energy metabolism, the release of apoptotic factors and regulation of apoptosis enzyme activity. At the same time, the interaction between mitochondria and endoplasmic reticulum were discussed, focusing on Ca2+ signal transduction and cell apoptosis process. The interaction between mitochondria and lysosome was further investigated, by highlighting the stability of lysosomal membrane and the subsequently released cathepsin to activate Bax and Bid to accelerate mitochondrial membrane permeability. Caspases were activated and involved in the limited degradation of some myofibrils in the early stage of PM tenderization, followed by the inactivation resulting from the decreasing ATP or other factors with the extended PM time. Therefore, caspases maybe only involve the early stage of tenderization. This review could provide a theoretical reference for the perfection of PM muscle tenderization investigations.

Key words: postmortem tenderization, apoptosis, caspases, mitochondrial damage, apoptotic factors

Fig. 1

Biochemical changes of postmortem muscle tenderization"

Fig. 2

The main pathways of apoptosis"

[1] HOLMAN B W B, VAN DE VEN R J, MAO Y W, COOMBS C E O, HOPKINS D L. Using instrumental (CIE and reflectance) measures to predict consumers' acceptance of beef colour. Meat Science, 2017,127:57-62.
doi: 10.1016/j.meatsci.2017.01.005
[2] SHACKELFORD S D, WHEELER T L, MEADE M K, REAGAN J O, BYRNES B L, KOOHMARAIE M. Consumer impressions of Tender Select beef. Journal of Animal Science, 2001,79(10):2605-2614.
doi: 10.2527/2001.79102605x
[3] KOOHMARAIE M, KENT M P, SHACKELFORD S D, VEISETH E, WHEELER T L. Meat tenderness and muscle growth: Is there any relationship? Meat Science, 2002,62(3):345-352.
doi: 10.1016/S0309-1740(02)00127-4
[4] KOOHMARAIE M, GEESINK G H. Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system. Meat Science, 2006,74(1):34-43.
doi: 10.1016/j.meatsci.2006.04.025
[5] GEESINK G H, KUCHAY S, CHISHTI A H, KOOHMARAIE M. µ-calpain is essential for postmortem proteolysis of muscle proteins. Journal of Animal Science, 2006,84(10):2834-2840.
doi: 10.2527/jas.2006-122
[6] OUALI A, HERRERA-MENDEZ C H, COULIS G, BECILA S, BOUDJELLAL A, AUBRY L, SENTANDREU M A. Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Science, 2006,74(1):44-58.
doi: 10.1016/j.meatsci.2006.05.010
[7] SENTANDREU M A, COULIS G, OUALI A. Role of muscle endopeptidases and their inhibitors in meat tenderness. Trends in Food Science & Technology, 2002,13(12):400-421.
[8] NIKOLETOPOULOU V, MARKAKI M, PALIKARAS K, TAVERNARAKIS N. Crosstalk between apoptosis, necrosis and autophagy. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 2013,1833(12):3448-3459.
doi: 10.1016/j.bbamcr.2013.06.001
[9] 黄明, 黄峰, 黄继超, 徐宝才, 周光宏, 徐幸莲. 内源性蛋白酶对宰后肌肉嫩化机制研究进展. 中国农业科学, 2011,44(15):3214-3222.
HUANG M, HUANG F, HUANG J C, XU B C, ZHOU G H, XU X L. Advances in research on postmortem tenderization mechanism of endogenous proteolytic enzymes in muscle. Scientia Agricultura Sinica, 2011,44(15):3214-3222. (in Chinese)
[10] OUALI A, HERRERA-MENDEZ C H, COULIS G, SAMIRA B, BOUDJELLAL A, HARHOURA K, AUBRY L, SENTANDREU M A. Meat tenderisation and muscle cell death, two highly related events. Tehnologija Mesa, 2007,48(1/2):1-15.
[11] HERRERA-MENDEZ C H, BECILA S, BOUDJELLAL A, OUALI A. Meat ageing: Reconsideration of the current concept. Trends in Food Science & Technology, 2006,17(8):394-405.
[12] CAO J X, SUN W Q, ZHOU G H, XU X L, PENG Z Q, HU Z L. Morphological and biochemical assessment of apoptosis in different skeletal muscles of bulls during conditioning. Journal of Animal Science, 2010,88(10):3439-3444.
doi: 10.2527/jas.2009-2412
[13] BECILA S, HERRERA-MENDEZ C H, COULIS G, LABAS R, ASTRUC T, PICARD B, BOUDJELLAL A, PELISSIER P, BREMAUD L, OUALI A. Postmortem muscle cells die through apoptosis. European Food Research and Technology, 2010,231(3):485-493.
doi: 10.1007/s00217-010-1296-5
[14] HERRERA-MENDEZ C H, BECILA S, COULIS G, SENTANDREU M A, AUBRY L, OUALI A. Purification and partial characterization of antithrombin III from bovine skeletal muscle and possible role of thrombin in postmortem apoptosis development and in efficiency of low voltage electrical stimulation. Food Research International, 2010,43(1):356-363.
doi: 10.1016/j.foodres.2009.10.012
[15] KEMP C M, PARR T, BARDSLEY R G, BUTTERY P J. Comparison of the relative expression of caspase isoforms in different porcine skeletal muscles. Meat Science, 2006,73(3):426-431.
doi: 10.1016/j.meatsci.2005.12.009
[16] CHEN L, FENG X C, LU F, XU X L, ZHOU G H, Li Q Y, GUO X Y. Effects of camptothecin, etoposide and Ca2+ on caspase-3 activity and myofibrillar disruption of chicken during postmortem ageing. Meat Science, 2011,87(3):165-174.
doi: 10.1016/j.meatsci.2010.10.002
[17] UNDERWOOD K R, MEANS W J, DU M. Caspase 3 is not likely involved in the postmortem tenderization of beef muscle. Journal of Animal Science, 2008,86(4):960-966.
doi: 10.2527/jas.2007-0549
[18] ADHIHETTY P J, HOOD D A. Mechanisms of apoptosis in skeletal muscle. Basic & Applied Myology, 2003,13(4):171-179.
[19] 王莲, 刘永红, 魏玲. 细胞死亡方式的新理念. 医学与哲学(临床决策论坛版), 2011,32(14):61-63.
WANG L, LIU Y H, WEI L. New theories and concepts of the mode of cell death. Medicine and Philosophy (Clinical Decision Making Forum Edition), 2011,32(14):61-63. (in Chinese)
[20] LANA A, ZOLLA L. Apoptosis or autophagy, that is the question: Two ways for muscle sacrifice towards meat. Trends in Food Science & Technology, 2015,46(2):231-241.
[21] 贾旭. 羊肉成熟过程中细胞自噬对细胞凋亡的影响机制[D]. 杨凌: 西北农林科技大学, 2017.
JIA X. The research of the effect of autophagy on the apoptosis of mutton[D]. Yangling: Northwest A&F University, 2017. (in Chinese)
[22] DEGTEREV A, HUANG Z H, BOYCE M, LI Y Q, JAGTAP P, MIZUSHIMA N, CUNY G D, MITCHISON T J, MOSKOWITZ M A, YUAN J Y. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nature Chemical Biology, 2005,1(2):112-119.
doi: 10.1038/nchembio711
[23] HENCKEL P, KARLSSON A, JENSEN M T, OKSBJERG N, PETERSEN J S. Metabolic conditions in porcine longissimus muscle immediately pre-slaughter and its influence on peri- and post mortem energy metabolism. Meat Science, 2002,62(2):145-155.
doi: 10.1016/S0309-1740(01)00239-X
[24] BHOLA P D, LETAI A. Mitochondria-Judges and executioners of cell death sentences. Molecular Cell, 2016,61(5):695-704.
doi: 10.1016/j.molcel.2016.02.019
[25] BOCK F J, TAIT S W G. Mitochondria as multifaceted regulators of cell death. Nature Reviews Molecular Cell Biology, 2020,21(2):85-100.
doi: 10.1038/s41580-019-0173-8
[26] HUANG F, HUANG M, ZHANG H, GUO B, ZHANG D Q, ZHOU G H. Cleavage of the calpain inhibitor, calpastatin, during postmortem ageing of beef skeletal muscle. Food Chemistry, 2014,148:1-6.
doi: 10.1016/j.foodchem.2013.10.016
[27] SHI Y X, MELNIKOV V Y, SCHRIER R W, EDELSTEIN C L. Downregulation of the calpain inhibitor protein calpastatin by caspases during renal ischemia-reperfusion. American Journal of Physiology-Renal Physiology, 2000,279(3):F509-F517.
doi: 10.1152/ajprenal.2000.279.3.F509
[28] PÖRN-ARES M I, SAMALI A, ORRENIUS S. Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death & Differentiation, 1998,5(12):1028-1033.
[29] CHUA B T, GUO K, LI P. Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. Journal of Biological Chemistry, 2000,275(7):5131-5135.
doi: 10.1074/jbc.275.7.5131
[30] GUPTA S, GOLLAPUDI S. Susceptibility of naïve and subsets of memory T cells to apoptosis via multiple signaling pathways. Autoimmunity Reviews, 2007,6(7):476-481.
doi: 10.1016/j.autrev.2007.02.005
[31] NAKANISHI K, SUDO T, MORISHIMA N. Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. Journal of Cell Biology, 2005,169(4):555-560.
[32] BRUNELLE J K, CHANDEL N S. Oxygen deprivation induced cell death: An update. Apoptosis, 2002,7(6):475-482.
doi: 10.1023/A:1020668923852
[33] CAO J X, OU C R, ZOU Y F, YE K P, ZHANG Q Q, KHAN M A, PAN D D, ZHOU G. Activation of caspase-3 and its correlation with shear force in bovine skeletal muscles during postmortem conditioning. Journal of Animal Science, 2013,91(9):4547-4552.
doi: 10.2527/jas.2013-6469
[34] HUANG F, HUANG M, ZHANG H, ZHANG C J, ZHANG D Q, ZHOU G H. Changes in apoptotic factors and caspase activation pathways during the postmortem aging of beef muscle. Food Chemistry, 2016,190:110-114.
doi: 10.1016/j.foodchem.2015.05.056
[35] WANG L L, HAN L, MA X L, YU Q L, ZHAO S N. Effect of mitochondrial apoptotic activation through the mitochondrial membrane permeability transition pore on yak meat tenderness during postmortem aging. Food Chemistry, 2017,234:323-331.
doi: 10.1016/j.foodchem.2017.04.185
[36] RØNNING S B, ANDERSEN P V, PEDERSEN M E, HOLLUNG K. Primary bovine skeletal muscle cells enters apoptosis rapidly via the intrinsic pathway when available oxygen is removed. Plos ONE, 2017,12(8):e0182928.
doi: 10.1371/journal.pone.0182928
[37] 蒋显. 线粒体释放细胞凋亡因子的机理研究[D]. 北京: 北京协和医学院, 2014.
JIANG X. Mechanism of release of mitochondrial apoptotic proteins[D]. Beijing: Peking Union Medical College, 2014. (in Chinese)
[38] QUINTANA-CABRERA R, MEHROTRA A, RIGONI G, SORIANO M E. Who and how in the regulation of mitochondrial cristae shape and function. Biochemical and Biophysical Research Communications, 2018,500(1):94-101.
doi: 10.1016/j.bbrc.2017.04.088
[39] GOGVADZE V, ORRENIUS S, ZHIVOTOVSKY B. Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 2006,1757(5):639-647.
doi: 10.1016/j.bbabio.2006.03.016
[40] 黄国敏, 王玉佩, 孙超, 张雪甜, 张红. 线粒体超微结构及其调控机制的研究进展. 生物化学与生物物理进展, 2019,46(12):1141-1149.
HUANG G M, WANG Y P, SUN C, ZHANG X T, ZHANG H. Advances in the study of mitochondrial ultrastructure and its regulatory mechanism. Progress in Biochemistry and Biophysics, 2019,46(12):1141-1149. (in Chinese)
[41] 陈丽, 董君, 闫朝君, 宋质银. 线粒体嵴重构及其调控. 生理科学进展, 2018,49(1):3-13.
CHEN L, DONG J, YAN C J, SONG Z Y. The role and regulation of mitochondrial cristae remodeling. Progress in Physiological Sciences, 2018,49(1):3-13. (in Chinese)
[42] 郑凯, 杨梅桂, 闫朝君, 汤明亮, 宋质银. 线粒体动力学与细胞凋亡. 中国细胞生物学学报, 2019,41(8):1467-1476.
ZHENG K, YANG M G, YAN C J, TANG M L, SONG Z Y. Mitochondrial dynamics and apoptosis. Chinese Journal of Cell Biology, 2019,41(8):1467-1476. (in Chinese)
[43] MALHEIROS J M, BRAGA C P, GROVE R A, RIBEIRO F A, CALKINS C R, ADAMEC J, CHARDULO L A L. Influence of oxidative damage to proteins on meat tenderness using a proteomics approach. Meat Science, 2019,148:64-71.
doi: 10.1016/j.meatsci.2018.08.016
[44] CHRIKI S, GARDNER G E, JURIE C, PICARD B, MICOL D, BRUN J P, JOURNAUX L, HOCQUETTE J F. Cluster analysis application identifies muscle characteristics of importance for beef tenderness. BMC Biochemistry, 2012,13:29.
doi: 10.1186/1471-2091-13-29
[45] MATARNEH S K, ENGLAND E M, SCHEFFLER T L, YEN C N, WICKS J C, SHI H, GERRARD D E. A mitochondrial protein increases glycolytic flux. Meat Science, 2017,133:119-125.
doi: 10.1016/j.meatsci.2017.06.007
[46] MATARNEH S K, BELINE M, DE LUZ E SILVA S, SHI H, GERRARD D E. Mitochondrial F1-ATPase extends glycolysis and pH decline in an in vitro model. Meat Science, 2018,137:85-91.
doi: 10.1016/j.meatsci.2017.11.009
[47] SCHEFFLER T L, MATARNEH S K, ENGLAND E M, GERRARD D E. Mitochondria influence postmortem metabolism and pH in an in vitro model. Meat Science, 2015,110:118-125.
doi: 10.1016/j.meatsci.2015.07.007
[48] LIU Z Y, DU X N, DENG J, GU M Y, HU H L, GUI M, YIN C C, CHANG Z Z. The interactions between mitochondria and sarcoplasmic reticulum and the proteome characterization of mitochondrion- associated membrane from rabbit skeletal muscle. Proteomics, 2015,15(15):2701-2704.
doi: 10.1002/pmic.v15.15
[49] HUANG F, DING Z J, ZHANG C J, HU H H, ZHANG L, ZHANG H. Effects of calcium and zinc ions injection on caspase-3 activation and tenderness in post-mortem beef skeletal muscles. International Journal of Food Science & Technology, 2018,53(3):582-589.
[50] 薛亮, 尹长城. 线粒体-内质网结构偶联的研究进展. 中国细胞生物学学报, 2013,35(12):1791-1796.
XUE L, YIN C C. Progress in the study of mitochondria-endoplasmic reticulum physical coupling. Chinese Journal of Cell Biology, 2013,35(12):1791-1796. (in Chinese)
[51] CHERUBINI M, LOPEZ-MOLINA L, GINES S. Mitochondrial fission in Huntington's disease mouse striatum disrupts ER-mitochondria contacts leading to disturbances in Ca2+ efflux and Reactive Oxygen Species (ROS) homeostasis. Neurobiology of Disease, 2020,136:104741.
doi: 10.1016/j.nbd.2020.104741
[52] O'HALLORAN G R, TROY D J, BUCKLEY D J, REVILLE W J. The role of endogenous proteases in the tenderisation of fast glycolysing muscle. Meat Science, 1997,47(3/4):187-210.
doi: 10.1016/S0309-1740(97)00046-6
[53] ZHANG J Y, LI M Q, YU Q L, HAN L, MA Z L. Effects of lysosomal-mitochondrial apoptotic pathway on tenderness in post-mortem bovine longissimus muscle. Journal of Agricultural and Food Chemistry, 2019,67(16):4578-4587.
doi: 10.1021/acs.jafc.9b00894
[54] KEMP C M, BARDSLEY R G, PARR T. Changes in caspase activity during the postmortem conditioning period and its relationship to shear force in porcine longissimus muscle. Journal of Animal Science, 2006,84(10):2841-2846.
doi: 10.2527/jas.2006-163
[55] ZHANG M H, WANG D Y, HUANG W, LIU F, ZHU Y Z, XU W M, CAO J X. Apoptosis during postmortem conditioning and its relationship to duck meat quality. Food Chemistry, 2013,138(1):96-100.
doi: 10.1016/j.foodchem.2012.10.142
[56] BERNARD C, CASSAR-MALEK I, LE CUNFF M, DUBROEUCQ H, RENAND G, HOCQUETTE J F. New indicators of beef sensory quality revealed by expression of specific genes. Journal of Agricultural and Food Chemistry, 2007,55(13):5229-5237.
doi: 10.1021/jf063372l
[57] LAVILLE E, SAYD T, MORZEL M, BLIENT S, CHAMBON C, LEPETIT J, RENAND G, HOCQUETTE J F. Proteome changes during meat aging in tough and tender beef suggest the importance of apoptosis and protein solubility for beef aging and tenderization. Journal of Agricultural and Food Chemistry, 2009,57(22):10755-10764.
doi: 10.1021/jf901949r
[58] CHEN L, FENG X C, ZHANG Y Y, LIU X B, ZHANG W G, LI C B, ULLAH N, Xu X L, ZHOU G H. Effects of ultrasonic processing on caspase-3, calpain expression and myofibrillar structure of chicken during post-mortem ageing. Food Chemistry, 2015,177:280-287.
doi: 10.1016/j.foodchem.2014.11.064
[59] HUANG M, HUANG F, XU X L, ZHOU G H. Influence of caspase3 selective inhibitor on proteolysis of chicken skeletal muscle proteins during post mortem aging. Food Chemistry, 2009,115(1):181-186.
doi: 10.1016/j.foodchem.2008.11.095
[60] HUANG M, HUANG F, MA H J, XU X L, ZHOU G H. Preliminary study on the effect of caspase-6 and calpain inhibitors on postmortem proteolysis of myofibrillar proteins in chicken breast muscle. Meat Science, 2012,90(3):536-542.
doi: 10.1016/j.meatsci.2011.09.004
[61] KEMP C M, PARR T. The effect of recombinant caspase 3 on myofibrillar proteins in porcine skeletal muscle. Animal, 2008,2(8):1254-1264.
doi: 10.1017/S1751731108002310
[62] HUANG M, HUANG F, XUE M, XU X L, ZHOU G H. The effect of active caspase-3 on degradation of chicken myofibrillar proteins and structure of myofibrils. Food Chemistry, 2011,128(1):22-27.
doi: 10.1016/j.foodchem.2011.02.062
[63] MOHRHAUSER D A, UNDERWOOD K R, WEAVER A D. In vitro degradation of bovine myofibrils is caused by μ-calpain, not caspase-3. Journal of Animal Science, 2011,89(3):798-808.
doi: 10.2527/jas.2010-3149
[64] HUANG F, HUANG M, ZHOU G H, XU X L, XUE M. In vitro proteolysis of myofibrillar proteins from beef skeletal muscle by caspase-3 and caspase-6. Journal of Agricultural and Food Chemistry, 2011,59(17):9658-9663.
doi: 10.1021/jf202129r
[1] LIU YuFang,CHEN YuLin,ZHOU ZuYang,CHU MingXing. miR-221-3p Regulates Ovarian Granulosa Cells Apoptosis by Targeting BCL2L11 in Small-Tail Han Sheep [J]. Scientia Agricultura Sinica, 2022, 55(9): 1868-1876.
[2] WANG JiaMin,SHI JiaChen,MA FangFang,CAI Yong,QIAO ZiLin. Effects of Soy Isoflavones on the Proliferation and Apoptosis of Yak Ovarian Granulosa Cells [J]. Scientia Agricultura Sinica, 2022, 55(8): 1667-1675.
[3] LI WenHui,HE YiJing,JIANG Yao,ZHAO HongYu,PENG Lei,LI Jia,RUI Rong,JU ShiQiang. Effects of FB1 on Apoptosis and Autophagy of Porcine Oocytes in vitro Maturation [J]. Scientia Agricultura Sinica, 2022, 55(6): 1241-1252.
[4] MingJie XING,XianHong GU,XiaoHong WANG,Yue HAO. Effects of IL-15 Overexpression on Myoblast Differentiation of Porcine Skeletal Muscle Cells [J]. Scientia Agricultura Sinica, 2022, 55(18): 3652-3663.
[5] YANG ChangPei,WANG NaiXiu,WANG Kai,HUANG ZiQing,LIN HaiLan,ZHANG Li,ZHANG Chen,FENG LuQiu,GAN Ling. Effects and Mechanisms of Exogenous GABA Against Oxidative Stress in Piglets [J]. Scientia Agricultura Sinica, 2022, 55(17): 3437-3449.
[6] FENG YunKui,WANG Jian,MA JinLiang,ZHANG LiuMing,LI YongJun. Effects of miR-31-5p on the Proliferation and Apoptosis of Hair Follicle Stem Cells in Goat [J]. Scientia Agricultura Sinica, 2021, 54(23): 5132-5143.
[7] MA MengNan,WANG HuiMing,WANG MiaoMiao,YAO Wang,ZHANG JinBi,PAN ZengXiang. Identification of circINHBB During Follicular Atresia and Its Effect on Granulosa Cell Apoptosis [J]. Scientia Agricultura Sinica, 2021, 54(18): 3998-4007.
[8] LI RunTing,CHEN LongXin,ZHANG LiMeng,HE HaiYing,WANG Yong,YANG RuoChen,DUAN ChunHui,LIU YueQin,WANG YuQin,ZHANG YingJie. Transient Expression and the Effect on Proliferation and Apoptosis of Granule Cell Stimulating Factor in Ovarian Fibroblasts [J]. Scientia Agricultura Sinica, 2021, 54(11): 2434-2444.
[9] Xin ZHANG,KongLin HUO,XingXing SONG,DuoNi ZHANG,Wen HU,ChuanHuo HU,Xun LI. Effects of GnIH on Autophagy and Apoptosis of Porcine Ovarian Granulosa Cells via p38MAPK Signaling Pathway [J]. Scientia Agricultura Sinica, 2020, 53(9): 1904-1912.
[10] PAN YangYang,WANG Meng,RUI Xian,WANG LiBin,HE HongHong,WANG JingLei,MA Rui,XU GengQuan,CUI Yan,FAN JiangFeng,YU SiJiu. RNA-Binding Motif Protein 3(RBM3) Expression is Regulated by Insulin-Like Growth Factor (IGF-1) for Protecting Yak (Bos grunniens) Cumulus Cells from Apoptosis During Hypothermia Stress [J]. Scientia Agricultura Sinica, 2020, 53(11): 2285-2296.
[11] CHEN Peng,BAO XiYan,KANG TaoTao,DONG ZhanQi,ZHU Yan,PAN MinHui,LU Cheng. Screening and Identification of Proteins Interacting with Bombyx mori IAP and Their Effects on BmNPV Proliferation [J]. Scientia Agricultura Sinica, 2019, 52(3): 558-567.
[12] ShaoFeng DENG,ZuoDong YE,ShuangQi FAN,JinDing CHEN,JingYuan ZHANG,MengJiao ZHU,MingQiu ZHAO. Screen of MicroRNAs in Classical Swine Fever Virus-Infected PK-15 Cells and the Regulation of Virus Replication by miR-214 [J]. Scientia Agricultura Sinica, 2018, 51(21): 4157-4168.
[13] CHEN Lin-lin, HOU Ying, DING Sheng-li, SHI Yan, LI Hong-lian. Cloning and Expression Analysis of Apoptosis-Related Gene FpTatD in Fusarium pseudograminearum [J]. Scientia Agricultura Sinica, 2016, 49(12): 2301-2309.
[14] PAN Yang-yang, LI Qin, CUI Yan, FAN Jiang-feng, YANG Kun, HE Jun-feng, YU Si-jiu. The Expression of EGF and EGFR in Yak Oocyte and Its Function on Development Competence of Embryo [J]. Scientia Agricultura Sinica, 2015, 48(12): 2439-2448.
[15] CHENG Xing-An, QIN Xiang-Jing, JIANG Xu-Hong, Sammy ZHENG, LIU Zhan-Mei, LIU Xiang-Dong. Cytological Mechanism of Autophagosome Biogenesis During Cell Autophagic Apoptosis in Rice and Insect Cell [J]. Scientia Agricultura Sinica, 2013, 46(5): 871-880.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!