Cite this paper:
Shengyu LUO, Cheng LIU, Xinming GAO, Jingqian WANG, Yibo ZHANG, Jie DING, Congcong HOU, Junquan ZHU, Bao LOU, Weiliang SHEN, Xiongfei WU, Chundan ZHANG. Environmental hypoxia induces apoptosis in large yellow croaker Larimichthys crocea via both intrinsic and extrinsic pathways[J]. Journal of Oceanology and Limnology, 2023, 41(6): 2429-2443

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

Shengyu LUO1, Cheng LIU1, Xinming GAO1, Jingqian WANG1, Yibo ZHANG1, Jie DING1, Congcong HOU1, Junquan ZHU1, Bao LOU2, Weiliang SHEN3, Xiongfei WU3, Chundan ZHANG1
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
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 L. crocea remain largely unknown. We investigated the effect of environmental hypoxia on apoptosis in L. crocea. Results show that hypoxia induced apoptosis in L. 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 Bcl-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 L. 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 L. 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 L. crocea. Therefore, hypoxia induced apoptosis in L. 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.
Key words:    hypoxia|large yellow croaker|mitochondrial apoptosis pathway|death receptor apoptosis pathway   
Received: 2022-07-04   Revised:
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Articles by Shengyu LUO
Articles by Cheng LIU
Articles by Xinming GAO
Articles by Jingqian WANG
Articles by Yibo ZHANG
Articles by Jie DING
Articles by Congcong HOU
Articles by Junquan ZHU
Articles by Bao LOU
Articles by Weiliang SHEN
Articles by Xiongfei WU
Articles by Chundan ZHANG
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.
Ashkenazi A, Dixit V M.1998.Death receptors:signaling and modulation.Science, 281(5381):1305-1308.
Breitburg D, Levin L A, Oschlies A et al.2018.Declining oxygen in the global ocean and coastal waters.Science, 359(6371):eaam7240.
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.
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.
Chao D T, Korsmeyer S J.1998.BCL-2 FAMILY:regulators of cell death.Annual Review of Immunology, 16:395-419.
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.
Crompton M.1999.The mitochondrial permeability transition pore and its role in cell death.Biochemical Journal, 341(2):233-249.
Diaz R J.2001.Overview of hypoxia around the world.Journal of Environmental Quality, 30(2):275-281.
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.
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.
Green D R, Reed J C.1998.Mitochondria and apoptosis.Science, 281(5381):1309-1312.
Grilo A L, Mantalaris A.2019.Apoptosis:a mammalian cell bioprocessing perspective.Biotechnology Advances, 37(3):459-475.
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.
Halliwell B.1992.Reactive oxygen species and the central nervous system.Journal of Neurochemistry, 59(5):1609-1623.
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.
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.
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.
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.
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.
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.
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.
Kunz M, Ibrahim S, Koczan D et al.2001.Activation of c-Jun NH2-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.
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.
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.
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.
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.
Martínez M L, Raynard E L, Rees B B et al.2011.Oxygen limitation and tissue metabolic potential of the African fish Barbus neumayeri:roles of native habitat and acclimatization.BMC Ecology, 11(1):1-9.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Reed J C.2006.Proapoptotic multidomain Bcl-2/Bax-family proteins:mechanisms, physiological roles, and therapeutic opportunities.Cell Death & Differentiation, 13(8):1378-1386.
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.
Semenza G L.2011.Oxygen sensing, homeostasis, and disease.The New England Journal of Medicine, 365(6):537-547.
Sendoel A, Hengartner M O.2014.Apoptotic cell death under hypoxia.Physiology, 29(3):168-176.
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.
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.
Susin S A, Lorenzo H K, Zamzami N et al.1999.Molecular characterization of mitochondrial apoptosis-inducing factor.Nature, 397(6718):441-446.
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.
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.
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.
Tummers B, Green D R.2017.Caspase-8:regulating life and death.Immunological Reviews, 277(1):76-89.
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.
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.
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.
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.
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.
Yuan S J, Akey C W.2013.Apoptosome structure, assembly, and procaspase activation.Structure, 21(4):501-515.
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.
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.
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.
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