Oyster studies reveal the duplication and functional diversification of Bivalvia caspase-8 genes

Shaoxi DENG; Tao QU; Guofan ZHANG; Fei XU

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Oyster studies reveal the duplication and functional diversification of Bivalvia caspase-8 genes

Biology | Updated：2024-10-12

- Oyster studies reveal the duplication and functional diversification of Bivalvia caspase-8 genes
- Journal of Oceanology and Limnology Vol. 41, Issue 3, Pages: 1109-1121(2023)
- Affiliations：
  
  1. CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  2. University of Chinese Academy of Sciences, Beijing 100049, China
  3. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China
  4. NHC Key Laboratory of Diagnosis and Therapy of Gastrointestinal Tumor, Gansu Provincial Hospital, Lanzhou 730000, China
- Author bio：
  
  xufei@qdio.ac.cn
- Funds：
- DOI：
  CLC：
- Received：20 March 2022，
  
  Published：01 May 2023
- Accepted：
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DENG Shaoxi,QU Tao,ZHANG Guofan,et al.Oyster studies reveal the duplication and functional diversification of Bivalvia caspase-8 genes[J].Journal of Oceanology and Limnology,2023,41(03):1109-1121.
DOI：

DENG Shaoxi,QU Tao,ZHANG Guofan,et al.Oyster studies reveal the duplication and functional diversification of Bivalvia caspase-8 genes[J].Journal of Oceanology and Limnology,2023,41(03):1109-1121. DOI：

摘要

Abstract

Caspase-8

first classified as a pro-apoptotic caspase

is considered to have arisen from duplication with caspase-10 and involves multiple immune and inflammatory responses in mammals. However

few are known on the phylogeny and function of caspase-8 in molluscs

one of the largest phyla in marine invertebrates. In this study

we conducted phylogenetic and functional analysis on molluscan caspase-8-like genes. Results indicate that duplication occurred in molluscan caspase-8-like genes

resulting in at least two caspase-8 copies in some groups of bivalves. Additional studies in Pacific oyster

Crassostrea gigas

showed diff

erent spatio-temporal expression patterns and subcellular localizations of

CgCaspase

and

CgCaspase

. While no interaction was observed between CgCaspase-8-2 and CgFADD

the adaptor molecule in apoptosis

yeast two-hybrid and co-immunoprecipitation assays suggested the interaction between CgCaspase-8-1 and CgFADD

indicating its pro-apoptotic function. In addition

CgCaspase-8-1 showed interaction with the CARD domain of CgRIG-I. Together with two NF-κB subunits (Cgp105 and CgRel)

their transcripts were up-regulated in response to poly(I:C) stimuli

supporting the immune function of both pro- and anti-inflammation. The results provide insight into the evolution and functional diversification of Bivalvia caspase-8 genes.

关键词

Keywords

references

Amé J C , Rolli V , Schreiber V et al . 1999 . PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase . Journal of Biological Chemistry , 274 ( 25 ): 17860 - 17868 , https://doi.org/10.1074/jbc.274.25.17860 https://doi.org/10.1074/jbc.274.25.17860 .

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

Benchoua A , Couriaud C , Gueágan C et al . 2002 . Active caspase-8 translocates into the nucleus of apoptotic cells to inactivate poly(ADP-ribose) polymerase-2 . Journal of Biological Chemistry , 277 ( 37 ): 34217 - 34222 , https://doi.org/10.1074/jbc.M203941200 https://doi.org/10.1074/jbc.M203941200 .

Besnault-Mascard L , Leprince C , Auffredou M T et al . 2005 . Caspase-8 sumoylation is associated with nuclear localization . Oncogene , 24 ( 20 ): 3268 - 3273 , https://doi.org/10.1038/sj.onc.1208448 https://doi.org/10.1038/sj.onc.1208448 .

Bjellqvist B , Basse B , Olsen E et al . 1994 . Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions . Electrophoresis , 15 ( 1 ): 529 - 539 , https://doi.org/10.1002/elps.1150150171 https://doi.org/10.1002/elps.1150150171 .

Bjellqvist B , Hughes G J , Pasquali C et al . 1993 . The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences . Electrophoresis , 14 ( 1 ): 1023 - 1031 , https://doi.org/10.1002/elps.11501401163 https://doi.org/10.1002/elps.11501401163 .

Bladon J , Taylor P C . 2006 . Extracorporeal photopheresis: a focus on apoptosis and cytokines . Journal of Dermatological Science , 43 ( 2 ): 85 - 94 , https://doi.org/10.1016/j.jdermsci.2006.05.004 https://doi.org/10.1016/j.jdermsci.2006.05.004 .

Boldin M P , Mett I L , Varfolomeev E E et al . 1995 . Self-association of the "death domains" of the p55 tumor necrosis factor (TNF) receptor and Fas/APO1 prompts signaling for TNF and Fas/APO1 effects . Journal of Biological Chemistry , 270 ( 1 ): 387 - 391 , https://doi.org/10.1074/jbc.270.1.387 https://doi.org/10.1074/jbc.270.1.387 .

Capella-Gutiérrez S , Silla-Martinez J M , Gabaldon T . 2009 . trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses . Bioinformatics , 25 ( 15 ): 1972 - 1973 , https://doi.org/10.1093/bioinformatics/btp348 https://doi.org/10.1093/bioinformatics/btp348 .

Chaudhary P M , Eby M T , Jasmin A et al . 2000 . Activation of the NF-κB pathway by caspase 8 and its homologs . Oncogene , 19 ( 39 ): 4451 - 4460 , https://doi.org/10.1038/sj.onc.1203812 https://doi.org/10.1038/sj.onc.1203812 .

Coon S L , Bonar D B , Weiner R M . 1986 . Chemical production of cultchless oyster spat using epinephrine and norepinephrine . Aquaculture , 58 ( 3-4 ): 255 - 262 , https://doi.org/10.1016/0044-8486(86)90090-6 https://doi.org/10.1016/0044-8486(86)90090-6 .

de Castro E , Sigrist C J A , Gattiker A et al . 2006 . ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins . Nucleic Acids Research , 34 ( S2 ): W362 - W365 , https://doi.org/10.1093/nar/gkl124 https://doi.org/10.1093/nar/gkl124 .

Fan T J , Han L H , Cong R S et al . 2005 . Caspase family proteases and apoptosis . Acta Biochimica et Biophysica Sinica , 37 ( 11 ): 719 - 727 , https://doi.org/10.1111/j.1745-7270.2005.00108.x https://doi.org/10.1111/j.1745-7270.2005.00108.x .

Fortier M E , Kent S , Ashdown H et al . 2004 . The viral mimic, polyinosinic: polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism . American Journal of Physiology-Regulatory, Integrative and Comparative Physiology , 287 ( 4 ): R759 - R766 , https://doi.org/10.1152/ajpregu.00293.2004 https://doi.org/10.1152/ajpregu.00293.2004 .

Galluzzi L , Maiuri M C , Vitale I et al . 2007 . Cell death modalities: classification and pathophysiological implications . Cell Death & Differentiation , 14 ( 7 ): 1237 - 1243 , https://doi.org/10.1038/sj.cdd.4402148 https://doi.org/10.1038/sj.cdd.4402148 .

Galluzzi L , Vitale I , Abrams J M et al . 2012 . Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012 . Cell Death & Differentiation , 19 ( 1 ): 107 - 120 , https://doi.org/10.1038/cdd.2011.96 https://doi.org/10.1038/cdd.2011.96 .

Gasteiger E , Hoogland C , Gattiker A et al . 2005 . Protein identification and analysis tools on the ExPASy server . In: Walker J M ed. The Proteomics Protocols Handbook . Humana, Totowa. p. 571 - 607 , https://doi.org/10.1385/1-59259-890-0:571 https://doi.org/10.1385/1-59259-890-0:571 .

Green D R , Llambi F . 2015 . Cell death signaling . Cold Spring Harbor Perspectives in Biology , 7 ( 12 ): a006080 , https://doi.org/10.1101/cshperspect.a006080 https://doi.org/10.1101/cshperspect.a006080 .

Hedgecock D , Gaffney P M , Goulletquer P et al . 2005 . The case for sequencing the Pacific oyster genome . Journal of Shellfish Research , 24 ( 2 ): 429 - 441 , https://doi.org/10.2983/0730-8000(2005)24 https://doi.org/10.2983/0730-8000(2005)24 [429:Tcfstp ] 2.0.Co; 2 .

Henry C M , Martin S J . 2017 . Caspase-8 acts in a non-enzymatic role as a scaffold for assembly of a Pro-inflammatory "FADDosome" complex upon TRAIL stimulation . Molecular Cell , 65 ( 4 ): 715 - 729.E5 , https://doi.org/10.1016/j.molcel.2017.01.022 https://doi.org/10.1016/j.molcel.2017.01.022 .

Hu W H , Johnson H , Shu H B . 2000 . Activation of NF-κB by FADD, Casper, and caspase-8 . Journal of Biological Chemistry , 275 ( 15 ): 10838 - 10844 , https://doi.org/10.1074/jbc.275.15.10838 https://doi.org/10.1074/jbc.275.15.10838 .

Huang B Y , Zhang L L , Xu F et al . 2019 . Oyster versatile IKKα/βs are involved in toll-like receptor and RIG-I-like receptor signaling for innate immune response . Frontiers in Immunology , 10 : 1826 , https://doi.org/10.3389/fimmu.2019.01826 https://doi.org/10.3389/fimmu.2019.01826 .

Katoh K , Standley D M . 2013 . MAFFT multiple sequence alignment software version 7: improvements in performance and usability . Molecular Biology and Evolution , 30 ( 4 ): 772 - 780 , https://doi.org/10.1093/molbev/mst010 https://doi.org/10.1093/molbev/mst010 .

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

Kruidering M , Evan G I . 2000 . Caspase-8 in apoptosis: the beginning of "the end"? IUBMB Life , 50 ( 2 ): 85 - 90 , https://doi.org/10.1080/713803693 https://doi.org/10.1080/713803693 .

Lacoste A , Cueff A , Poulet S A . 2002 . P35-sensitive caspases, MAP kinases and Rho modulate β-adrenergic induction of apoptosis in mollusc immune cells . Journal of Cell Science , 115 ( 4 ): 761 - 768 , https://doi.org/10.1242/jcs.115.4.761 https://doi.org/10.1242/jcs.115.4.761 .

Launay S , Hermine O , Fontenay M et al . 2005 . Vital functions for lethal caspases . Oncogene , 24 ( 33 ): 5137 - 5148 , https://doi.org/10.1038/sj.onc.1208524 https://doi.org/10.1038/sj.onc.1208524 .

Lavrik I , Golks A , Krammer P H . 2005 . Death receptor signaling . Journal of Cell Science , 118 ( 2 ): 265 - 267 , https://doi.org/10.1242/jcs.01610 https://doi.org/10.1242/jcs.01610 .

Letunic I , Khedkar S , Bork P . 2021 . SMART: recent updates, new developments and status in 2020 . Nucleic Acids Research , 49 ( D1 ): D458 - D460 , https://doi.org/10.1093/nar/gkaa937 https://doi.org/10.1093/nar/gkaa937 .

Li C Y , Qu T , Huang B Y et al . 2015 . Cloning and characterization of a novel caspase -8-like gene in Crassostrea gigas . Fish & Shellfish Immunology , 46 ( 2 ): 486 - 492 , https://doi.org/10.1016/j.fsi.2015.06.035 https://doi.org/10.1016/j.fsi.2015.06.035 .

Li H L , Zhu H , Xu C J et al . 1998 . Cleavage of BID by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis . Cell , 94 ( 4 ): 491 - 501 , https://doi.org/10.1016/s0092-8674(00)81590-1 https://doi.org/10.1016/s0092-8674(00)81590-1 .

Li Z X , Wang C , Jiang F J et al . 2016 . Characterization and expression of a novel caspase gene: evidence of the expansion of caspases in Crassostrea gigas . Comparative Biochemistry and Physiology Part B : Biochemistry and Molecular Biology , 201 : 37 - 45 , https://doi.org/10.1016/j.cbpb.2016.07.001 https://doi.org/10.1016/j.cbpb.2016.07.001 .

Liu F Y , Li Y L , Yu H W et al . 2021 . MolluscDB: an integrated functional and evolutionary genomics database for the hyper-diverse animal phylum Mollusca . Nucleic Acids Research , 49 ( D1 ): D988 - D997 , https://doi.org/10.1093/nar/gkaa918 https://doi.org/10.1093/nar/gkaa918 .

Liu W Z , Xie Y B , Ma J Y et al . 2015 . IBS: an illustrator for the presentation and visualization of biological sequences . Bioinformatics , 31 ( 20 ): 3359 - 3361 , https://doi.org/10.1093/bioinformatics/btv362 https://doi.org/10.1093/bioinformatics/btv362 .

Lu G X , Yu Z C , Lu M M et al . 2017 . The self-activation and LPS binding activity of executioner caspase-1 in oyster Crassostrea gigas . Developmental & Comparative Immunology , 77 : 330 - 339 , https://doi.org/10.1016/j.dci.2017.09.002 https://doi.org/10.1016/j.dci.2017.09.002 .

Matsuda I , Matsuo K , Matsushita Y et al . 2014 . The C-terminal domain of the long form of cellular FLICE-inhibitory protein (c-FLIP L ) inhibits the interaction of the caspase 8 prodomain with the receptor-interacting protein 1 (RIP1) death domain and regulates caspase 8-dependent nuclear factor κB (NF-κB) activation . Journal of Biological Chemistry , 289 ( 7 ): 3876 - 3887 , https://doi.org/10.1074/jbc.M113.506485 https://doi.org/10.1074/jbc.M113.506485 .

Micheau O , Tschopp J . 2003 . Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes . Cell , 114 ( 2 ): 181 - 190 , https://doi.org/10.1016/s0092-8674(03)00521-x https://doi.org/10.1016/s0092-8674(03)00521-x .

Philip N H , DeLaney A , Peterson L W et al . 2016 . Activity of uncleaved caspase-8 controls anti-bacterial immune defense and TLR-induced cytokine production independent of cell death . PLoS Pathogens , 12 ( 10 ): e1005910 , https://doi.org/10.1371/journal.ppat.1005910 https://doi.org/10.1371/journal.ppat.1005910 .

Puente X S , Sánchez L M , Overall C M et al . 2003 . Human and mouse proteases: a comparative genomic approach . Nature Reviews Genetics , 4 ( 7 ): 544 - 558 , https://doi.org/10.1038/nrg1111 https://doi.org/10.1038/nrg1111 .

Qin Y P , Zhang Y H , Li X Y et al . 2020 . Characterization and functional analysis of a caspase 3 gene: evidence that ChCas 3 participates in the regulation of apoptosis in Crassostrea hongkongensis . Fish & Shellfish Immunology , 98 : 122 - 129 , https://doi.org/10.1016/j.fsi.2020.01.007 https://doi.org/10.1016/j.fsi.2020.01.007 .

Qu T , Huang B Y , Zhang L L et al . 2014 . Identification and functional characterization of two executioner caspases in Crassostrea gigas . PLoS One , 9 ( 2 ): e89040 , https://doi.org/10.1371/journal.pone.0089040 https://doi.org/10.1371/journal.pone.0089040 .

Rajput A , Kovalenko A , Bogdanov K et al . 2011 . RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein . Immunity , 34 ( 3 ): 340 - 351 , https://doi.org/10.1016/j.immuni.2010.12.018 https://doi.org/10.1016/j.immuni.2010.12.018 .

Ren J , Wen L P , Gao X J et al . 2009 . DOG 1.0: illustrator of protein domain structures . Cell Research , 19 ( 2 ): 271 - 273 , https://doi.org/10.1038/cr.2009.6 https://doi.org/10.1038/cr.2009.6 .

Romero A , Novoa B , Figueras A . 2015 . The complexity of apoptotic cell death in mollusks: an update . Fish & Shellfish Immunology , 46 ( 1 ): 79 - 87 , https://doi.org/10.1016/j.fsi.2015.03.038 https://doi.org/10.1016/j.fsi.2015.03.038 .

Ronquist F , Teslenko M , van der Mark P et al . 2012 . MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space . Systematic Biology , 61 ( 3 ): 539 - 542 , https://doi.org/10.1093/sysbio/sys029 https://doi.org/10.1093/sysbio/sys029 .

Roth S , Ruland J . 2011 . Caspase-8: clipping off RIG-I signaling . Immunity , 34 ( 3 ): 283 - 285 , https://doi.org/10.1016/j.immuni.2011.03.011 https://doi.org/10.1016/j.immuni.2011.03.011 .

Salvesen G S , Dixit V M . 1997 . Caspases: intracellular signaling by proteolysis . Cell , 91 ( 4 ): 443 - 446 , https://doi.org/10.1016/s0092-8674(00)80430-4 https://doi.org/10.1016/s0092-8674(00)80430-4 .

Schütze S , Tchikov V , Schneider-Brachert W . 2008 . Regulation of TNFR1 and CD95 signalling by receptor compartmentalization . Nature Reviews Molecular Cell Biology , 9 ( 8 ): 655 - 662 , https://doi.org/10.1038/nrm2430 https://doi.org/10.1038/nrm2430 .

Subramanian B , Gao S H , Lercher M J et al . 2019 . Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees . Nucleic Acids Research , 47 ( W1 ): W270 - W275 , https://doi.org/10.1093/nar/gkz357 https://doi.org/10.1093/nar/gkz357 .

Takeuchi O , Akira S . 2010 . Pattern recognition receptors and inflammation . Cell , 140 ( 6 ): 805 - 820 , https://doi.org/10.1016/j.cell.2010.01.022 https://doi.org/10.1016/j.cell.2010.01.022 .

Vogeler S , Carboni S , Li X X et al . 2021 . Phylogenetic analysis of the caspase family in bivalves: implications for programmed cell death, immune response and development . BMC Genomics , 22 ( 1 ): 80 , https://doi.org/10.1186/s12864-021-07380-0 https://doi.org/10.1186/s12864-021-07380-0 .

Wajant H . 2002 . The Fas signaling pathway: more than a paradigm . Science , 296 ( 5573 ): 1635 - 1636 , https://doi.org/10.1126/science.1071553 https://doi.org/10.1126/science.1071553 .

Wang J , Chun H J , Wong W et al . 2001 . Caspase-10 is an initiator caspase in death receptor signaling . Proceedings of the National Academy of Sciences of the United States of America , 98 ( 24 ): 13884 - 13888 , https://doi.org/10.1073/pnas.241358198 https://doi.org/10.1073/pnas.241358198 .

Wang K , Yin X M , Chao D T et al . 1996 . BID: a novel BH3 domain-only death agonist . Genes & Development , 10 ( 22 ): 2859 - 2869 , https://doi.org/10.1101/gad.10.22.2859 https://doi.org/10.1101/gad.10.22.2859 .

Xiang Z M , Qu F F , Qi L et al . 2013 . Cloning, characterization and expression analysis of a caspase-8 like gene from the Hong Kong oyster, Crassostrea hongkongensis . Fish & Shellfish Immunology , 35 ( 6 ): 1797 - 1803 , https://doi.org/10.1016/j.fsi.2013.08.026 https://doi.org/10.1016/j.fsi.2013.08.026 .

Yang B Y , Li L L , Pu F et al . 2015 . Molecular cloning of two molluscan caspases and gene functional analysis during Crassostrea angulata (Fujian oyster) larval metamorphosis . Molecular Biology Reports , 42 ( 5 ): 963 - 975 , https://doi.org/10.1007/s11033-014-3833-y https://doi.org/10.1007/s11033-014-3833-y .

Yoneyama M , Fujita T . 2009 . RNA recognition and signal transduction by RIG-I-like receptors . Immunological Reviews , 227 ( 1 ): 54 - 65 , https://doi.org/10.1111/j.1600-065X.2008.00727.x https://doi.org/10.1111/j.1600-065X.2008.00727.x .

Zhang G F , Fang X D , Guo X M et al . 2012 . The oyster genome reveals stress adaptation and complexity of shell formation . Nature , 490 ( 7418 ): 49 - 54 , https://doi.org/10.1038/nature11413 https://doi.org/10.1038/nature11413 .

Zhang L L , Li L , Zhang G F . 2011 . Gene discovery, comparative analysis and expression profile reveal the complexity of the Crassostrea gigas apoptosis system . Developmental & Comparative Immunology , 35 ( 5 ): 603 - 610 , https://doi.org/10.1016/j.dci.2011.01.005 https://doi.org/10.1016/j.dci.2011.01.005 .

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Related Institution

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Innovation Center for Marine Bio-Industry Technology of Jiangsu Province

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