Cite this paper:
Shasha WANG, Yingqiu ZHENG, Muyan CHEN, Kenneth B. STOREY. Ultrastructural variation and key ER chaperones response induced by heat stress in intestinal cells of sea cucumber Apostichopus japonicus[J]. Journal of Oceanology and Limnology, 2021, 39(1): 317-328

Ultrastructural variation and key ER chaperones response induced by heat stress in intestinal cells of sea cucumber Apostichopus japonicus

Shasha WANG1, Yingqiu ZHENG1, Muyan CHEN1, Kenneth B. STOREY2
1 Key Laboratory of Mariculture (Ocean University of China), Ministry of Education, Qingdao 266003, China;
2 Institute of Biochemistry, Carleton University, Ottawa ON K1S 5B6, Canada
Abstract:
The unfolded protein response (UPR) is an important protective and compensatory strategy used during endoplasmic reticulum stress caused by factors including glucose starvation, low pH, or heat shock. However, there is very little information on the possible role(s) of the UPR under adverse conditions experienced by marine invertebrates. We observed that rough endoplasmic reticulum (ER) was dramatically expanded and numerous autophagosomes were accumulated in the intestinal cells of sea cucumbers, Apostichopus japonicus, under heat stress (4 h at 25℃ compared with 15℃ controls). Moreover, heat stress led to sharp increases in the relative transcript and protein expression levels of two primary ER chaperones:the endoplasmic reticulum resident protein 29-like (ERP29) and protein disulfide-isomerase A6-like (PDIA6). These results suggest a potential adaptive mechanism to deal with heat-induced stress in sea cucumber intestine.
Key words:    Apostichopus japonicus|endoplasmic reticulum (ER)|unfolded protein response (UPR)|endoplasmic reticulum resident protein 29-like (ERP29)|protein disulfide-isomerase A6-like (PDIA6)   
Received: 2019-11-04   Revised: 2020-02-19
Tools
PDF (3087 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Shasha WANG
Articles by Yingqiu ZHENG
Articles by Muyan CHEN
Articles by Kenneth B. STOREY
References:
Asha P S, Muthiah P. 2005. Effects of temperature, salinity and pH on larval growth, survival and development of the sea cucumber Holothuria spinifera Theel. Aquaculture, 250(3-4):823-829, https://doi.org/10.1016/j.aquaculture. 2005.04.075.
Back S H, Schröder M, Lee K, Zhang K Z, Kaufman R J. 2005.ER stress signaling by regulated splicing:IRE1/HAC1/XBP1. Methods, 35(4):395-416, https://doi.org/10.1016/j.ymeth.2005.03.001.
Bánhegyi G, Baumeister P, Benedetti A, Dong D Z, Fu Y, Lee A S, Li J Z, Mao C H, Margittai E, Ni M, Paschen W, Piccirella S, Senesi S, Sitia R, Wang M, Yang W. 2007.Endoplasmic reticulum stress. Annals of the New York Academy of Sciences, 1113(1):58-71, https://doi.org/10.1196/annals.1391.007.
Bello S A, Abreu-Irizarry R J, García-Arrarás J E. 2015.Primary cell cultures of regenerating holothurian tissues.In:Nelson C M ed. Tissue Morphogenesis. Humana Press, New York. p.283-297, https://doi.org/10.1007/978-1-4939-1164-6_19.
Chen C, Dudenhausen E E, Pan Y X, Zhong C, Kilberg M S. 2004. Human CCAAT/enhancer-binding protein β gene expression is activated by endoplasmic reticulum stress through an unfolded protein response element downstream of the protein coding sequence. Journal of Biological Chemistry, 279(27):27 948-27 956, https://doi.org/10.1074/jbc.M313920200.
Chen M Y, Li X K, Zhu A J, Storey K B, Sun L N, Gao T X, Wang T M. 2016. Understanding mechanism of sea cucumber Apostichopus japonicus aestivation:insights from TMT-based proteomic study. Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 19:78-89, https://doi.org/10.1016/j.cbd. 2016.06.005.
Chen M Y, Wang S S, Li X K, Storey K B, Zhang X M. 2018.The potential contribution of miRNA-200-3p to the fatty acid metabolism by regulating AjEHHADH during aestivation in sea cucumber. PeerJ, 6:e5703, https://doi.org/10.7717/peerj.5703.
Chen M Y, Zhang X M, Liu J N, Storey K B. 2013. Highthroughput sequencing reveals differential expression of miRNAs in intestine from sea cucumber during aestivation. PLoS One, 8(10):e76120, https://doi.org/10.1371/journal.pone.0076120.
Chen Y H, Lian Y Y, He H H, Yuan K, Zhang C Z, Yu G H, He J G. 2019. Functional characterization of an ER-stress responding Crustin gene in Litopenaeus vannamei. Fish & Shellfish Immunology, 84:541-550, https://doi.org/10.1016/j.fsi.2018.10.047.
Czechowski J. 1996. Conventional radiography and ultrasonography in the diagnosis of small bowel obstruction and strangulation. Acta Radiologica, 37(2):186-189, https://doi.org/10.1080/02841859609173442.
DeSesso J M, Williams A L. 2008. Contrasting the gastrointestinal tracts of mammals:factors that influence absorption. Annual Reports in Medicinal Chemistry, 43:353-371, https://doi.org/10.1016/S0065-7743(08)00021-3.
Dong Y W, Dong S L. 2008. Induced thermotolerance and expression of heat shock protein 70 in sea cucumber Apostichopus japonicus. Fisheries Science, 74(3):573-578, https://doi.org/10.1111/j.1444-2906.2008.01560.x.
Dong Y W, Ji T T, Dong S L. 2007. Stress responses to rapid temperature changes of the juvenile sea cucumber(Apostichopus japonicus Selenka). Journal of Ocean University of China, 6(3):275-280, https://doi.org/10.1007/s11802-007-0275-3.
Fonseca S G, Gromada J, Urano F. 2011. Endoplasmic reticulum stress and pancreatic β-cell death. Trends in Endocrinology & Metabolism, 22(7):266-274, https://doi.org/10.1016/j.tem.2011.02.008.
Freedman R B, Hirst T R, Tuite M F. 1994. Protein disulphide isomerase:building bridges in protein folding. Trends in Biochemical Sciences, 19(8):331-336, https://doi.org/10.1016/0968-0004(94)90072-8.
Gao L, Yuan Z H, Ma Z, Li Z, Yu S M, Li Y F, He C B. 2019.Genome-wide comparative analysis of the SHSP, HSP60/10 and HSP90 genes reveals differential heat stress responses in estivation of the sea cucumber Apostichopus japonicus. Aquaculture Research, 50(4):1 117-1 130, https://doi.org/10.1111/are.13986.
Harding H P, Zhang Y H, Zeng H, Novoa I, Lu P D, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl D F, Bell J C, Hettmann T, Leiden J M, Ron D. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molecular Cell, 11(3):619-633, https://doi.org/10.1016/S1097-2765(03)00105-9.
Hendrick J P, Hartl F U. 1995. The role of molecular chaperones in protein folding. FASEB Journal, 9(15):1 559-1 569, https://doi.org/10.1096/fasebj.9.15.8529835.
Iwata A, Christianson J C, Bucci M, Ellerby L M, Nukina N, Forno L S, Kopito R R. 2005. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proceedings of the National Academy of Sciences of the United States of America, 102(37):13 135-13 140, https://doi.org/10.1073/pnas. 0505801102.
Kabir M F, Kim H R, Chae H J. 2018. Endoplasmic reticulum stress and autophagy. In:Català A ed. Stress and Autophagy, Endoplasmic Reticulum. IntechOpen, London, https://doi.org/10.5772/intechopen.81381.
Kandasamy M K, Kristen U. 1989. Ultrastructural responses of tobacco pollen tubes to heat shock. Protoplasma, 153(1-2):104-110, https://doi.org/10.1007/BF01322470.
Kanter M, Aktas C, Erboga M. 2013. Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term:an immunohistochemical and ultrastructural study. Toxicology and Industrial Health, 29(2):99-113, https://doi.org/10.1177/0748233711425082.
Kozutsumi Y, Segal M, Normington K, Gething M J, Sambrook J. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucoseregulated proteins. Nature, 332(6163):462-464, https://doi.org/10.1038/332462a0.
Lai E, Teodoro T, Volchuk A. 2007. Endoplasmic reticulum stress:signaling the unfolded protein response.Physiology, 22(3):193-201, https://doi.org/10.1152/physiol.00050.2006.
Levine B, Klionsky D J. 2004. Development by self-digestion:molecular mechanisms and biological functions of autophagy. Developmental Cell, 6(4):463-477, https://doi.org/10.1016/S1534-5807(04)00099-1.
Liao Y L. 1997. Fauna Sinica:Phylum Echinodermata:Class Holothuroidea. Science Press, Beijing. p.148-150. (in Chinese)
Ma Y J, Hendershot L M. 2002. The mammalian endoplasmic reticulum as a sensor for cellular stress. Cell Stress & Chaperones, 7(2):222-229, https://doi.org/10.1379/1466-1268(2002)007<0222:tmeraa>2.0.co;2.
Ma Y J, Hendershot L M. 2004. ER chaperone functions during normal and stress conditions. Journal of Chemical Neuroanatomy, 28(1-2):51-65, https://doi.org/10.1016/j.jchemneu.2003.08.007.
McCullough K D, Martindale J L, Klotz L O, Aw T Y, Holbrook N J. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Molecular and Cellular Biology, 21(4):1 249-1 259, https://doi.org/10.1128/MCB.21.4.1249-1259.2001.
Mkrtchian S, Fang C, Hellman U, Ingelman-Sundberg M A. 1998. A stress-inducible rat liver endoplasmic reticulum protein, ERp29. European Journal of Biochemistry, 251(1-2):304-313, https://doi.org/10.1046/j.1432-1327.1998.2510304.x.
Noiva R, Lennarz W J. 1992. Protein disulfide isomerase. A multifunctional protein resident in the lumen of the endoplasmic reticulum. Journal of Biological Chemistry, 267(6):3 553-3 556.
Odintsova N A, Dolmatov I Y, Mashanov V S. 2005.Regenerating holothurian tissues as a source of cells for long-term cell cultures. Marine Biology, 146(5):915-921, https://doi.org/10.1007/s00227-004-1495-3.
Ono K, Suzuki T A, Toyoshima Y, Suzuki T, Tsutsui S, Odaka K, Miyadai T, Nakamura O. 2018. SJL-1, a C-type lectin, acts as a surface defense molecule in Japanese sea cucumber, Apostichopus japonicus. Molecular Immunology, 97:63-70, https://doi.org/10.1016/j.molimm.2018.03.009.
Park S, You K H, Shong M, Goo T W, Yun E Y, Kang S W, Kwon O Y. 2005. Overexpression of ERP29 in the thyrocytes of FRTL-5 cells. Molecular Biology Reports, 32(1):7-13, https://doi.org/10.1007/s11033-004-3069-3.
Saito M, Kunisaki N, Urano N, Kimura S. 2002. Collagen as the major edible component of sea cucumber (Stichopus japonicus). Journal of Food Science, 67(4):1 319-1 322, https://doi.org/10.1111/j.1365-2621.2002.tb10281.x.
Scheel A A, Pelham H R B. 1996. Purification and characterization of the human KDEL receptor.Biochemistry, 35(31):10 203-10 209, https://doi.org/10.1021/bi960807x.
Schröder M, Kaufman R J. 2005. The mammalian unfolded protein response. Annual Review of Biochemistry, 74:739-789, https://doi.org/10.1146/annurev.biochem.73.011303.074134.
Schröder M. 2006. The unfolded protein response. Molecular Biotechnology, 34(2):279-290, https://doi.org/10.1385/MB:34:2:279.
Schubert U, Antón L C, Gibbs J, Norbury C C, Yewdell J W, Bennink J R. 2000. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature, 404(6779):770-774, https://doi.org/10.1038/35008096.
Senft D, Ronai Z A. 2015. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends in Biochemical Sciences, 40(3):141-148, https://doi.org/10.1016/j.tibs.2015.01.002.
Shao Y N, Li C H, Chen X C, Zhang P J, Li Y, Li T W, Jiang J B. 2015. Metabolomic responses of sea cucumber Apostichopus japonicus to thermal stresses. Aquaculture, 435:390-397, https://doi.org/10.1016/j.aquaculture.2014.10.023.
Tu B P, Weissman J S. 2004. Oxidative protein folding in eukaryotes. Journal of Cell Biology, 164(3):341-346, https://doi.org/10.1083/jcb.200311055.
Ullman E, Fan Y, Stawowczyk M, Chen H M, Yue Z, Zong W X. 2008. Autophagy promotes necrosis in apoptosisdeficient cells in response to ER stress. Cell Death & Differentiation, 15(2):422-425, https://doi.org/10.1038/sj.cdd.4402234.
Wang F Y, Yang H S, Gao F, Liu G B. 2008. Effects of acute temperature or salinity stress on the immune response in sea cucumber, Apostichopus japonicus. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 151(4):491-498, https://doi.org/10.1016/j.cbpa.2008.06.024.
Wang H H, Li C H, Wang Z H, Shao Y N, Lv Z M, Zhang W W. 2016. p44/42MAPK and p90RSK modulate thermal stressed physiology response in Apostichopus japonicus.Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 196-197:57-66, https://doi.org/10.1016/j.cbpb.2016.02.008.
Wang H H, Shao Y N, Zhang W W, Li C H, Lv Z M, Jin C H. 2015. Molecular characterization of two novel molecular chaperones in bacterial-challenged Apostichopus japonicus. Gene, 570(1):141-149, https://doi.org/10.1016/j.gene.2015.06.024.
Wang S S, Chen M Y, Yin Y C, Storey K B. 2019. MiR-200-3p is potentially involved in cell cycle arrest by regulating cyclin A during aestivation in Apostichopus japonicus.Cells, 8(8):843, https://doi.org/10.3390/cells8080843.
Wang S S, Li X K, Chen M Y, Storey K B, Wang T M. 2018. A potential antiapoptotic regulation:the interaction of heat shock protein 70 and apoptosis-inducing factor mitochondrial 1 during heat stress and aestivation in sea cucumber. Journal of Experimental Zoology Part A:Ecological and Integrative Physiology, 329(3):103-111, https://doi.org/10.1002/jez.2180.
Xu C Y, Bailly-Maitre B, Reed J C. 2005. Endoplasmic reticulum stress:cell life and death decisions. The Journal of Clinical Investigation, 115(10):2 656-2 664, https://doi.org/10.1172/JCI26373.
Xu D X, Sun L N, Liu S L, Zhang L B, Yang H S. 2014.Polymorphisms of heat shock protein 90 (Hsp90) in the sea cucumber Apostichopus japonicus and their association with heat-resistance. Fish & Shellfish Immunology, 41(2):428-436, https://doi.org/10.1016/j.fsi.2014.09.025.
Xu D X, Sun L N, Liu S L, Zhang L B, Yang H S. 2015.Histological, ultrastructural and heat shock protein 70(HSP70) responses to heat stress in the sea cucumber Apostichopus japonicus. Fish & Shellfish Immunology, 45(2):321-326, https://doi.org/10.1016/j.fsi.2015.04.015.
Xu D X, Sun L N, Liu S L, Zhang L B, Yang H S. 2016.Understanding the heat shock response in the sea cucumber Apostichopus japonicus, using iTRAQ-based proteomics. International Journal of Molecular Sciences, 17(2):150, https://doi.org/10.3390/ijms17020150.
Xu D X, Zhou S, Yang H S. 2017. Carbohydrate and amino acids metabolic response to heat stress in the intestine of the sea cucumber Apostichopus japonicus. Aquaculture Research, 48:5 883-5 891, https://doi.org/10.1111/are.13411.
Xu K, Yu Q H, Zhang J S, Lv Z M, Fu W D, Wang T M. 2018.Cell loss by apoptosis is involved in the intestinal degeneration that occurs during aestivation in the sea cucumber Apostichopus japonicus. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 216:25-31, https://doi.org/10.1016/j.cbpb.2017.11.004.
Yewdell J W, Nicchitta C V. 2006. The DRiP hypothesis decennial:support, controversy, refinement and extension.Trends in Immunology, 27(8):368-373, https://doi.org/10.1016/j.it.2006.06.008.
Yin H C, Zhao L L, Jiang X J, Li S Q, Huo H, Chen H Y. 2017.DEV induce autophagy via the endoplasmic reticulum stress related unfolded protein response. PLoS One, 12(12):e0189704, https://doi.org/10.1371/journal.pone.0189704.
Yorimitsu T, Klionsky D J. 2005. Autophagy:molecular machinery for self-eating. Cell Death & Differentiation, 12 Suppl 2:1 542-1 552, https://doi.org/10.1038/sj.cdd.4401765.
Yorimitsu T, Nair U, Yang Z F, Klionsky D J. 2006.Endoplasmic reticulum stress triggers autophagy. Journal of Biological Chemistry, 281(40):30 299-30 304, https://doi.org/10.1074/jbc.M607007200.
Zhang P, Lu Y L, Li C H, Su X R, Wang Z H, Jin C H, Li Y, Li T W. 2013. Identification of differential expressed proteins and characterization their mRNA expression in thermally stressed Apostichopus japonicus. Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 8(3):194-200, https://doi.org/10.1016/j.cbd.2013.05.001.
Zhang X j, Sun L N, Yuan J B, Sun Y M, Gao Y, Zhang L B, Li S H, Dai H, Hamel J F, Liu C Z, Yu Y, Liu S L, Lin W C, Guo K M, Jin S J, Xu P, Storey K B, Huan P, Zhang T, Zhou Y, Zhang J Q, Lin C G, Li X N, Xing L L, Huo D, Sun M Z, Wang L, Mercier A, Li F H, Yang H S, Xiang J H. 2017. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. Plos Biology, 15(10):e2003790, https://doi.org/10.1371/journal.pbio.2003790.
Zhao H, Yang H S, Zhao H L, Chen M Y, Wang T M. 2011. The molecular characterization and expression of heat shock protein 90 (Hsp90) and 26 (Hsp26) cDNAs in sea cucumber (Apostichopus japonicus). Cell Stress and Chaperones, 16(5):481, https://doi.org/10.1007/s12192-011-0260-z.
Zhao Y, Chen M Y, Wang T M, Sun L N, Xu D X, Yang H S. 2014. Selection of reference genes for qRT-PCR analysis of gene expression in sea cucumber Apostichopus japonicus during aestivation. Chinese Journal of Oceanology and Limnology, 32(6):1 248-1 256, https://doi.org/10.1007/s00343-015-4004-2.
Copyright © Haiyang Xuebao