Environmental hypoxia induces apoptosis in large yellow croaker <italic style="font-style: italic">Larimichthys</italic><italic style="font-style: italic">crocea</italic> via both intrinsic and extrinsic pathways

Shengyu LUO; Cheng LIU; Xinming GAO; Jingqian WANG; Yibo ZHANG; Jie DING; Congcong HOU; Junquan ZHU; Bao LOU; Weiliang SHEN; Xiongfei WU; Chundan ZHANG

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Environmental hypoxia induces apoptosis in large yellow croaker Larimichthyscrocea via both intrinsic and extrinsic pathways

Aquaculture and Fisheries | Updated：2024-10-12

- Environmental hypoxia induces apoptosis in large yellow croaker Larimichthyscrocea via both intrinsic and extrinsic pathways
- Journal of Oceanology and Limnology Vol. 41, Issue 6, Pages: 2429-2443(2023)
- Affiliations：
  
  1. Key Laboratory of Applied Marine Biotechnology by the Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo 315211, China
  2. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
  3. State Key Laboratory of Large Yellow Croaker Breeding, Ningbo Academy of Oceanology and Fishery, Ningbo 315012, China
- Author bio：
  
  zhujunquan@nbu.edu.cn
  loubao6577@163.com
- Funds：
- DOI：
  CLC：
- Received：04 July 2022，
  
  Accepted：19 August 2022，
  
  Online First：19 October 2022，
  
  Published：01 November 2023
- Accepted：
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LUO Shengyu,LIU Cheng,GAO Xinming,et al.Environmental hypoxia induces apoptosis in large yellow croaker Larimichthys, crocea via both intrinsic and extrinsic pathways[J].Journal of Oceanology and Limnology,2023,41(06):2429-2443.
DOI：

LUO Shengyu,LIU Cheng,GAO Xinming,et al.Environmental hypoxia induces apoptosis in large yellow croaker Larimichthys, crocea via both intrinsic and extrinsic pathways[J].Journal of Oceanology and Limnology,2023,41(06):2429-2443. DOI：

摘要

Abstract

Hypoxia has become an unfavorable factor affecting the sustainable development of the large yellow croaker

Larimichthys

crocea

an economically important mariculture fish in China. Apoptosis is a consequence of hypoxia on fish. However

the effects of hypoxia stress on apoptosis in

crocea

remain largely unknown. We investigated the effect of environmental hypoxia on apoptosis in

crocea

. Results show that hypoxia induced apoptosis in

crocea

both in vivo and in vitro. The mitochondrial membrane potential was significantly reduced in large yellow croaker fry (LYCF) cells. The expression levels of B-cell lymphoma/leukemia-2 (Bcl-2) mRNA and protein were also significantly decreased in the liver and LYCF cells during 96 h and 48 h of hypoxia stress

respectively

whereas the expression level of B

cl-2 associated X (

Bax

) mRNA

Casp3

mRNA

and activity of caspase-3/7/9 were significantly increased

indicating that hypoxia induced caspase-dependent intrinsic apoptosis in

crocea

. The expression level of the apoptosis-inducing factor (AIF) protein was significantly increased in the liver and LYCF cells. The level of AIF protein was significantly decreased in the cytoplasm but increased in the nuclei of

crocea

demonstrating that hypoxia induced the AIF-mediated caspase-independent intrinsic apoptosis. In addition

the activity of caspase-8 was significantly increased

indicating that hypoxia stress induced extrinsic apoptosis in

crocea

. Therefore

hypoxia induced apoptosis in

crocea

through both the intrinsic and extrinsic pathways. The present study accumulated basic biological information to help elucidate the mechanism of hypoxia response in marine fish.

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Keywords

references

Acehan D , Jiang X J , Morgan D G et al . 2002 . Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation . Molecular Cell , 9 ( 2 ): 423 - 432 . https://do 10.1016/s1097-2765(02)00442-2 http://dx.doi.org/10.1016/s1097-2765(02)00442-2

Ashkenazi A , Dixit V M . 1998 . Death receptors: signaling and modulation . Science , 281 ( 5381 ): 1305 - 1308 . https://do 10.1126/science.281.5381.1305 http://dx.doi.org/10.1126/science.281.5381.1305

Breitburg D , Levin L A , Oschlies A et al . 2018 . Declining oxygen in the global ocean and coastal waters . Science , 359 ( 6371 ): eaam7240 . https://do 10.1126/science.aam7240 http://dx.doi.org/10.1126/science.aam7240

Brukamp K , Jim B , Moeller M J et al . 2007 . Hypoxia and podocyte-specific Vhlh deletion confer risk of glomerular disease . American Journal of Physiology Renal Physiology , 293 ( 4 ): F1397 - F1407 . https://do 10.1152/ajprenal.00133.2007 http://dx.doi.org/10.1152/ajprenal.00133.2007

Cai M , He P , Fang D L . 2019 . Hypoxia‑induced mitochondrial translocation of DNM1L increases mitochondrial fission and triggers mPTP opening in HCC cells via activation of HK2 . Oncology Reports , 42 ( 3 ): 1125 - 1132 .

Cassidy-Stone A , Chipuk J E , Ingerman E et al . 2008 . Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization . Developmental Cell , 14 ( 2 ): 193 - 204 . https://do 10.1016/j.devcel.2007.11.019 http://dx.doi.org/10.1016/j.devcel.2007.11.019

Chao D T , Korsmeyer S J . 1998 . BCL-2 FAMILY: regulators of cell death . Annual Review of Immunology , 16 : 395 - 419 . https://do 10.1146/annurev.immunol.16.1.395 http://dx.doi.org/10.1146/annurev.immunol.16.1.395

Chao W , Shen Y , Li L et al . 2002 . Importance of FADD signaling in serum deprivation- and hypoxia-induced cardiomyocyte apoptosis . Journal of Biological Chemistry , 277 ( 35 ): 31639 - 31645 . https://do 10.1074/jbc.m204104200 http://dx.doi.org/10.1074/jbc.m204104200

Crompton M . 1999 . The mitochondrial permeability transition pore and its role in cell death . Biochemical Journal , 341 ( 2 ): 233 - 249 . https://do 10.1042/bj3410233 http://dx.doi.org/10.1042/bj3410233

Diaz R J . 2001 . Overview of hypoxia around the world . Journal of Environmental Quality , 30 ( 2 ): 275 - 281 . https://do 10.2134/jeq2001.302275x http://dx.doi.org/10.2134/jeq2001.302275x

Ding C Y , Hu L S , Li Y et al . 2018 . Effects of hypoxia stress on cardiomyocyte apoptosis and the control for Bax , Bcl - 2 expressions in Hypophthalmichthys molitrix . Freshwater Fisheries , 48 ( 2 ): 10 - 15 . (in Chinese with English abstract)

Dong Y , Wu Y , Zhao G L et al . 2019 . Inhibition of autophagy by 3-MA promotes hypoxia-induced apoptosis in human colorectal cancer cells . European Review for Medical and Pharmacological Sciences , 23 ( 3 ): 1047 - 1054 .

Feng J Y , Tan W , Li T et al . 2020 . Human retinal pigment epithelial cells are protected against hypoxia by BNIP3 . Annals of Translational Medicine , 8 ( 22 ): 1502 . https://do 10.21037/atm-20-7145 http://dx.doi.org/10.21037/atm-20-7145

Goel G , Guo M , Ding J et al . 2010 . Combined effect of tumor necrosis factor (TNF)-α and heat shock protein (HSP)-70 in reducing apoptotic injury in hypoxia: a cell culture study . Neuroscience Letters , 483 ( 3 ): 162 - 166 . https://do 10.1016/j.neulet.2010.07.069 http://dx.doi.org/10.1016/j.neulet.2010.07.069

Green D R , Reed J C . 1998 . Mitochondria and apoptosis . Science , 281 ( 5381 ): 1309 - 1312 . https://do 10.1126/science.281.5381.1309 http://dx.doi.org/10.1126/science.281.5381.1309

Grilo A L , Mantalaris A . 2019 . Apoptosis: a mammalian cell bioprocessing perspective . Biotechnology Advances , 37 ( 3 ): 459 - 475 . https://do 10.1016/j.biotechadv.2019.02.012 http://dx.doi.org/10.1016/j.biotechadv.2019.02.012

Gurevich R M , Regula K M , Kirshenbaum L A . 2001 . Serpin protein CrmA suppresses hypoxia-mediated apoptosis of ventricular myocytes . Circulation , 103 ( 15 ): 1984 - 1991 . https://do 10.1161/01.cir.103.15.1984 http://dx.doi.org/10.1161/01.cir.103.15.1984

Halliwell B . 1992 . Reactive oxygen species and the central nervous system . Journal of Neurochemistry , 59 ( 5 ): 1609 - 1623 . https://do 10.1111/j.1471-4159.1992.tb10990.x http://dx.doi.org/10.1111/j.1471-4159.1992.tb10990.x

Hammond E M , Denko N C , Dorie M J et al . 2002 . Hypoxia links ATR and p53 through replication arrest . Molecular and Cellular Biology , 22 ( 6 ): 1834 - 1843 . https://do 10.1128/mcb.22.6.1834-1843.2002 http://dx.doi.org/10.1128/mcb.22.6.1834-1843.2002

Hausenloy D J , Duchen M R , Yellon D M . 2003 . Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury . Cardiovascular Research , 60 ( 3 ): 617 - 625 . https://do 10.1016/j.cardiores.2003.09.025 http://dx.doi.org/10.1016/j.cardiores.2003.09.025

Hu H L , Zhang Z X , Chen C S et al . 2010 . Effects of mitochondrial potassium channel and membrane potential on hypoxic human pulmonary artery smooth muscle cells . American Journal of Respiratory cell and Molecular Biology , 42 ( 6 ): 661 - 666 . https://do 10.1165/rcmb.2009-0017oc http://dx.doi.org/10.1165/rcmb.2009-0017oc

Kerr J F R , Wyllie A H , Currie A R . 1972 . Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics . British Journal of Cancer , 26 ( 4 ): 239 - 257 . https://do 10.1038/bjc.1972.33 http://dx.doi.org/10.1038/bjc.1972.33

Khurana P , Ashraf Q M , Mishra O P et al . 2002 . Effect of hypoxia on caspase-3 , - 8 , and -9 activity and expression in the cerebral cortex of newborn piglets. Neurochemical Research , 27 ( 9 ): 931 - 938 .

Kim C H , Ko A R , Lee S Y et al . 2010 . Hypoxia switches glucose depletion-induced necrosis to phosphoinositide 3-kinase/Akt-dependent apoptosis in A549 lung adenocarcinoma cells . International Journal of Oncology , 36 ( 1 ): 117 - 124 . https://do 10.3892/ijo_00000482 http://dx.doi.org/10.3892/ijo_00000482

Kim Y , Kim Y S , Noh M Y et al . 2017 . Neuroprotective effects of a novel poly (ADP-ribose) polymerase-1 inhibitor, JPI-289, in hypoxic rat cortical neurons . Clinical and Experimental Pharmacology and Physiology , 44 ( 6 ): 671 - 679 . https://do 10.1111/1440-1681.12757 http://dx.doi.org/10.1111/1440-1681.12757

Knudson C M , Tung K S K , Tourtellotte W G et al . 1995 . Bax-deficient mice with lymphoid hyperplasia and male germ cell death . Science , 270 ( 5233 ): 96 - 99 . https://do 10.1126/science.270.5233.96 http://dx.doi.org/10.1126/science.270.5233.96

Kunz M , Ibrahim S , Koczan D et al . 2001 . Activation of c-Jun NH 2 -terminal kinase/stress-activated protein kinase (JNK/SAPK) is critical for hypoxia-induced apoptosis of human malignant melanoma . Cell Growth & Differentiation , 12 ( 3 ): 137 - 145 .

Kurpakus-Wheater M , Sexton R , McDermott M L et al . 2003 . Caspase-9 activation in hypoxic human corneal epithelial cells . Apoptosis , 8 ( 6 ): 681 - 688 . https://do 10.1023/a:1026164332473 http://dx.doi.org/10.1023/a:1026164332473

Li J Y , Dai H , Liu H et al . 2011 . Effects of scutellarin benzyl ester on the expressions of Bcl-2 and Bax in cardiomyocytes injured by acute hypoxia . Chinese Critical Care Medicine , 23 ( 6 ): 337 - 340 . (in Chinese with English abstract)

Li Y L , Xu G Y , Xiao J W et al . 2017 . Studies on the protective role of zebrafish HO1 in response to hypoxia . Acta Hydrobiologica Sinica , 41 ( 1 ): 43 - 49 . (in Chinese with English abstract)

Liu X S , Kim C N , Yang J et al . 1996 . Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c . Cell , 86 ( 1 ): 147 - 157 . https://do 10.1016/s0092-8674(00)80085-9 http://dx.doi.org/10.1016/s0092-8674(00)80085-9

Lohberger B , Steinecker-Frohnwieser B , Stuendl N et al . 2016 . The proteasome inhibitor bortezomib affects chondrosarcoma cells via the mitochondria-caspase dependent pathway and enhances death receptor expression and autophagy . PLoS One , 11 ( 12 ): e0168193 . https://do 10.1371/journal.pone.0168193 http://dx.doi.org/10.1371/journal.pone.0168193

Lu G , Mak Y T , Wai S M et al . 2005 . Hypoxia-induced differential apoptosis in the central nervous system of the sturgeon ( Acipenser shrenckii ) . Microscopy Research and Technique , 68 ( 5 ): 258 - 263 . https://do 10.1002/jemt.20243 http://dx.doi.org/10.1002/jemt.20243

Luo S Y , Gao X M , Ding J et al . 2019 . Transcriptome sequencing reveals the traits of spermatogenesis and testicular development in large yellow croaker ( Larimichthys crocea ) . Genes , 10 ( 12 ): 958 . https://do 10.3390/genes10120958 http://dx.doi.org/10.3390/genes10120958

Martínez M L , Raynard E L , Rees B B et al . 2011 . Oxygen li mitation and tissue metabolic potential of the African fish Barbus neumayeri : roles of native habitat and acclimatization . BMC Ecology , 11 ( 1 ): 1 - 9 . https://do 10.1186/1472-6785-11-2 http://dx.doi.org/10.1186/1472-6785-11-2

Mishra O P , Delivoria-Papadopoulos M . 2006 . Effect of neuronal nitric oxide synthase inhibition on caspase-9 activity during hypoxia in the cerebral cortex of newborn piglets . Neuroscience Letters , 401 ( 1-2 ): 81 - 85 . https://do 10.1016/j.neulet.2006.02.070 http://dx.doi.org/10.1016/j.neulet.2006.02.070

Mishra O P , Randis T , Ashraf Q M et al . 2006 . Hypoxia-induced Bax and Bcl-2 protein expression, caspase-9 activation, DNA fragmentation, and lipid peroxidation in mitochondria of the cerebral cortex of newborn piglets: the role of nitric oxide . Neuroscience , 141 ( 3 ): 1339 - 1349 . https://do 10.1016/j.neuroscience.2006.05.005 http://dx.doi.org/10.1016/j.neuroscience.2006.05.005

Murphy A N , Fiskum G , Beal M F . 1999 . Mitochondria in neurodegeneration: bioenergetic function in cell life and death . Journal of Cerebral Blood Flow & Metabolism , 19 ( 3 ): 231 - 245 . https://do 10.1097/00004647-199903000-00001 http://dx.doi.org/10.1097/00004647-199903000-00001

Nagarajah N S , Vigneswaran N , Zacharias W . 2004 . Hypoxia-mediated apoptosis in oral carcinoma cells occurs via two independent pathways . Molecular Cancer , 3 ( 1 ): 38 . https://do 10.1186/1476-4598-3-38 http://dx.doi.org/10.1186/1476-4598-3-38

Ondricek K , Thomas P . 2018 . Effects of hypoxia exposure on apoptosis and expression of membrane steroid receptors, ZIP9, mPRα, and GPER in Atlantic croaker ovaries . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 224 : 84 - 92 . https://do 10.1016/j.cbpa.2018.07.002 http://dx.doi.org/10.1016/j.cbpa.2018.07.002

Ow Y L P , Green D R , Hao Z Y et al . 2008 . Cytochrome c : functions beyond respiration . Nature Reviews Molecular Cell Biology , 9 ( 7 ): 532 - 542 . https://do 10.1038/nrm2434 http://dx.doi.org/10.1038/nrm2434

Pan W L , Wong J H , Fang E F et al . 2014 . Preferential cytotoxicity of the type I ribosome inactivating protein alpha-momorcharin on human nasopharyngeal carcinoma cells under normoxia and hypoxia . Biochemical Pharmacology , 89 ( 3 ): 329 - 339 . https://do 10.1016/j.bcp.2014.03.004 http://dx.doi.org/10.1016/j.bcp.2014.03.004

Poli A , Beraudi A , Villani L et al . 2003 . Group II metabotropic glutamate receptors regulate the vulnerability to hypoxic brain damage . The Journal of Neuroscience , 23 ( 14 ): 6023 - 6029 . https://do 10.1523/jneurosci.23-14-06023.2003 http://dx.doi.org/10.1523/jneurosci.23-14-06023.2003

Quignard S , Mosser G , Boissière M et al . 2012 . Long-term fate of silica nanoparticles interacting with human dermal fibroblasts . Biomaterials , 33 ( 17 ): 4431 - 4442 . https://do 10.1016/j.biomaterials.2012.03.004 http://dx.doi.org/10.1016/j.biomaterials.2012.03.004

Reed J C . 2006 . Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities . Cell Death & Differentiation , 13 ( 8 ): 1378 - 1386 . https://do 10.1038/sj.cdd.4401975 http://dx.doi.org/10.1038/sj.cdd.4401975

Ren G X , Guo W , Ye D X et al . 2006 . A study on the mechanism of inducing apoptosis of Tca8113 cells by means of ultrasound hyperthermia . Shanghai Journal of Stomatology , 15 ( 5 ): 507 - 511 . (in Chinese with English abstract)

Ren Q Y , Zhang M Z , Li M et al . 2018 . Differential induction of gene expressions, protein contents and enzyme activities involved in hypoxic responsive in liver tissues of mudskipper Boleophthalmus pectinirostris exposed to acute hypoxia . Oceanologia et Limnologia Sinica , 49 ( 4 ): 889 - 896 . (in Chinese with English abstract)

Schulte P M . 2014 . What is environmental stress? Insights from fish living in a variable environment . Journal of Experimental Biology , 217 ( 1 ): 23 - 34 . https://do 10.1242/jeb.089722 http://dx.doi.org/10.1242/jeb.089722

Semenza G L . 2011 . Oxygen sensing, homeostasis, and disease . The New England Journal of Medicine , 365 ( 6 ): 537 - 547 . https://do 10.1056/nejmra1011165 http://dx.doi.org/10.1056/nejmra1011165

Sendoel A , Hengartner M O . 2014 . Apoptotic cell death under hypoxia . Physiology , 29 ( 3 ): 168 - 176 . https://do 10.1152/physiol.00016.2013 http://dx.doi.org/10.1152/physiol.00016.2013

Sollid J , De Angelis P , Gundersen K et al . 2003 . Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills . Journal of Experimental Biology , 206 ( 20 ): 3667 - 3673 . https://do 10.1242/jeb.00594 http://dx.doi.org/10.1242/jeb.00594

Sun C F , Tao Y , Jiang X Y et al . 2011 . IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp ( Ctenopharyngodon idellus ) embryos . General and Comparative Endocrinology , 172 ( 3 ): 409 - 415 . https://do 10.1016/j.ygcen.2011.04.005 http://dx.doi.org/10.1016/j.ygcen.2011.04.005

Susin S A , Lorenzo H K , Zamzami N et al . 1999 . Molecular characterization of mitochondrial apoptosis-inducing factor . Nature , 397 ( 6718 ): 441 - 446 . https://do 10.1038/17135 http://dx.doi.org/10.1038/17135

Tamatani M , Ogawa S , Tohyama M . 1998 . Roles of Bcl-2 and caspases in hypoxia-induced neuronal cell death: a possible neuroprotective mechanism of peptide growth factors . Molecular Brain Research , 58 ( 1-2 ): 27 - 39 . https://do 10.1016/s0169-328x(98)00095-3 http://dx.doi.org/10.1016/s0169-328x(98)00095-3

Tse A C K , Li J W , Chan T F et al . 2015 . Hypoxia induces miR-210, leading to anti-apoptosis in ovarian follicular cells of marine medaka Oryzias melastigma . Aquatic Toxicology , 165 : 189 - 196 . https://do 10.1016/j.aquatox.2015.06.002 http://dx.doi.org/10.1016/j.aquatox.2015.06.002

Tsukahara S , Yamamoto S , Shwe T T W et al . 2006 . Inhalation of low-level formaldehyde increases the Bcl-2/Bax expression ratio in the hippocampus of immunologically sensitized mice . Neuroimmunomodulation , 13 ( 2 ): 63 - 68 . https://do 10.1159/000094829 http://dx.doi.org/10.1159/000094829

Tummers B , Green D R . 2017 . Caspase-8: regulating life and death . Immunological Reviews , 277 ( 1 ): 76 - 89 . https://do 10.1111/imr.12541 http://dx.doi.org/10.1111/imr.12541

Vuori K A M , Soitamo A , Vuorinen P J et al . 2004 . Baltic salmon ( Salmo salar ) yolk-sac fry mortality is associated with disturbances in the function of hypoxia-inducible transcription factor (HIF-1α) and consecutive gene expression . Aquatic Toxicology , 68 ( 4 ): 301 - 313 . https://do 10.1016/j.aquatox.2004.03.019 http://dx.doi.org/10.1016/j.aquatox.2004.03.019

Wang J C , Xue Z M , Hua C T et al . 2020a . Metabolomic analysis of the ameliorative effect of enhanced proline metabolism on hypoxia-induced injury in cardiomyocytes . Oxidative Medicine and Cellular Longevity , 2020 : 8866946 .

Wang M X , Rong Y , Luo L . 2021 . Neuroprotective effects of icariin in neonatal hypoxia-ischemic brain damage via its anti-apoptotic property . Child's Nervous System , 37 ( 1 ): 39 - 46 . https://do 10.1007/s00381-020-04690-8 http://dx.doi.org/10.1007/s00381-020-04690-8

Wang X H , Li Q H , Mu P F et al . 2020b . Large yellow croaker peroxiredoxin IV protect cells against oxidative damage and apoptosis . Molecular Immunology , 127 : 150 - 156 .

Wang Y , Liu C X , Yi Y R et al . 2006 . Detection of apoptosis of the human hepatic carcinoma cells induced by bluetongus virus by PI and Annexin V/PI staining methods . Virologica Sinica , 21 ( 3 ): 253 - 256 . (in Chinese with English abstract)

Wei M C , Zong W X , Cheng E H Y et al . 2001 . Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death . Science , 292 ( 5517 ): 727 - 730 . https://do 10.1126/science.1059108 http://dx.doi.org/10.1126/science.1059108

Williams T A , Bergstrome J C , Scott J et al . 2017 . CRF and urocortin 3 protect the heart from hypoxia/reoxygenation-induced apoptosis in zebrafish . American Journal of Physiology-Regulatory, Integrative and Comparative Physiology , 313 ( 2 ): R91 - R100 . https://do 10.1152/ajpregu.00045.2017 http://dx.doi.org/10.1152/ajpregu.00045.2017

Wu X J , Chen N , Huang C X et al . 2016 . Effects of hypoxia on cardiomyocyte apoptosis and activity of antioxidant enzymes in Megalobrama amblycephala heart . Journal of Huazhong Agricultural University , 35 ( 3 ): 108 - 113 . (in Chinese with English abstract)

Youle R J , Strasser A . 2008 . The BCL-2 protein family: opposing activities that mediate cell death . Nature Reviews Molecular Cell Biology , 9 ( 1 ): 47 - 59 . https://do 10.1038/nrm2308 http://dx.doi.org/10.1038/nrm2308

Yuan S J , Akey C W . 2013 . Apoptosome structure, assembly, and procaspase activation . Structure , 21 ( 4 ): 501 - 515 . https://do 10.1016/j.str.2013.02.024 http://dx.doi.org/10.1016/j.str.2013.02.024

Yuan Z H , Liu S K , Yao J et al . 2016 . Expression of Bcl-2 genes in channel catfish after bacterial infection and hypoxia stress . Developmental & Comparative Immunology , 65 : 79 - 90 . https://do 10.1016/j.dci.2016.06.018 http://dx.doi.org/10.1016/j.dci.2016.06.018

Zhang S W , Zhao Y L , Xu M et al . 2013 . FoxO3a modulates hypoxia stress induced oxidative stress and apoptosis in cardiac microvascular endothelial cells . PLoS One , 8 ( 11 ): e80342 . https://do 10.1371/journal.pone.0080342 http://dx.doi.org/10.1371/journal.pone.0080342

Zhao J K , Liang H W , Zou G W et al . 2016 . Influence of hypoxic stress on apoptosis of hepatocyte and brain cells of silver carp ( Hypophthalmichthys molitrix ) . Journal of Northwest A&F University (Natural Science Edition) , 44 ( 7 ): 34 - 38 . (in Chinese with English abstract)

Zhao L L , Cui C , Liu Q et al . 2020 . Combined exposure to hypoxia and ammonia aggravated biological effects on glucose metabolism, oxidative stress, inflammation and apoptosis in largemouth bass ( Micropterus salmoides ) . Aquatic Toxicology , 224 : 105514 . https://do 10.1016/j.aquatox.2020.105514 http://dx.doi.org/10.1016/j.aquatox.2020.105514

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Environmental hypoxia induces apoptosis in large yellow croaker Larimichthyscrocea via both intrinsic and extrinsic pathways

DOI：

摘要

Abstract

关键词

Keywords

references