Effect of hypoxia on immune system of bivalve molluscs
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Abstract
Over the past decades, research on bivalve immune system is focused on studying the effect of environmental factors on the basal status of defense systems. The immune system of bivalves is greatly affected by abiotic factors, and the most significant ones are water temperature, salinity, and level of dissolved oxygen. Hypoxia is widespread in the coastal waters of the World Ocean since the 1950s. Hypoxic zones (with dissolved oxygen concentration < 0.5 mL O2·L−1) occur in shelf areas for a long time corresponding to the life cycle of many hydrobionts. Being benthic organisms, bivalve molluscs often experience reduced dissolved oxygen concentrations. This group of aquatic invertebrates both plays an important role in aquatic ecosystem functioning and is actively used in aquaculture. The efficiency of bivalve cultivation directly depends on its immune status determining resistance to diseases. The immune system of bivalve molluscs is based on a complex of nonspecific reactions of cellular and humoral components. Hemocytes circulating in the hemolymph are the key effectors of the cellular immune response which, along with the barrier tissues of molluscs, synthesize humoral factors with a wide spectrum of antimicrobial activity. The hemolymph of various bivalve species contains different cell types differing by size, morphology, and granulation of cytoplasm. Most bivalve species have 2 types of hemocytes – granular and agranular ones; those can be subdivided into morphotypes depending on number and color of granules, size of the nucleus, and presence of organelles in the cytoplasm. Granulocytes are considered the main immune cells that perform phagocytosis and (or) encapsulation of infectious agents, as well as their subsequent neutralization by releasing reactive oxygen species, lysing enzymes, and humoral antimicrobial proteins. Moreover, the complex of defense systems includes an antioxidant system which is closely related to mollusc immunity since it neutralizes reactive oxygen species releasing during cellular immune mechanism activation. An excess of these compounds damages mollusc cells by oxidizing proteins, cytoplasmic membrane lipids, and DNA. This article provides data on an oxygen deficiency effect on the cellular and humoral components of the immune system, as well as the tissue antioxidant complex of bivalve molluscs.
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References
Гостюхина О. Л., Андреенко Т. И. Ферментное и низкомолекулярное звенья антиоксидантного комплекса двух видов черноморских моллюсков с разной устойчивостью к окислительному стрессу: Mytilus galloprovincialis Lam. и Anadara kagoshimensis (Tokunaga, 1906) // Журнал общей биологии. 2018. Т. 79, № 6. С. 482–492. [Gostyukhina O. L., Andreenko T. I. Enzymatic and low-molecular weight units of antioxidant complex in two species of the Black Sea mollusks with different resistance to oxidative stress: Mytilus galloprovincialis Lam. and Anadara kagoshimensis (Tokunaga, 1906). Zhurnal obshchei biologii, 2018, vol. 79, no. 6, pp. 482–492. (in Russ.)]. https://doi.org/10.1134/S0044459618060040
Довженко Н. В. Реакция антиоксидантной системы двустворчатых моллюсков на воздействие повреждающих факторов среды : автореф. … дис. канд. биол. наук : 03.00.16. Владивосток, 2006. 22 с. [Dovzhenko N. V. Reaktsiya antioksidantnoi sistemy dvustvorchatykh mollyuskov na vozdeistvie povrezhdayushchikh faktorov sredy : avtoref. … dis. kand. biol. nauk : 03.00.16. Vladivostok, 2006, 22 p. (in Russ.)]
Истомина А. А. Реакция антиоксидантной системы у массовых видов моллюсков залива Петра Великого в условиях дефицита кислорода и действия ионов Cu2+ : автореф. … дис. канд. биол. наук : 03.08.02. Владивосток, 2012. 18 с. [Istomina A. A. Reaktsiya antioksidantnoi sistemy u massovykh vidov mollyuskov zaliva Petra Velikogo v usloviyakh defitsita kisloroda i deistviya ionov Cu2+ : avtoref. … dis. kand. biol. nauk : 03.08.02. Vladivostok, 2012, 18 p. (in Russ.)]
Истомина А. А., Довженко Н. В., Бельчева Н. Н., Челомин В. П. Активность антиоксидантных ферментов у разных видов моллюсков в условиях гипоксии/аноксии // Известия Самарского НЦ РАН. 2011. Т. 13, № 1 (5). С. 1106–1108. [Istomina A. A., Dovzhenko N. V., Belcheva N. N., Chelomin V. P. Activity of antioxidant enzymes at different kinds of molluscums in the hypoxia/anoxia condition. Izvestiya Samarskogo NTs RAN, 2011, vol. 131, no. 2, pp. 1106–1108. (in Russ.)]
Abele-Oeschger D., Oeschger R. Hypoxia-induced autoxidation of haemoglobin in the benthic invertebrates Arenicola marina (Polychaeta) and Astarte borealis (Bivalvia) and the possible effects of sulphide. Journal of Experimental Marine Biology and Ecology, 1995, vol. 187, iss. 1, pp. 63–80. https://doi.org/10.1016/0022-0981(94)00172-A
Anderson R. S. Reactive oxygen species and antimicrobial defenses of invertebrates: A bivalve model. In: Phylogenetic Perspectives on the Vertebrate Immune System / G. Beck, M. Sugumaran, E. L. Cooper (Eds). Boston, MA : Springer, 2001, pp. 131–139. (Advances in Experimental Medicine and Biology ; vol. 484). https://doi.org/10.1007/978-1-4615-1291-2_12
Andreyeva A. Y., Efremova E. S., Kukhareva T. A. Morphological and functional characterization of hemocytes in cultivated mussel (Mytilus galloprovincialis) and effect of hypoxia on hemocyte parameters. Fish & Shellfish Immunology, 2019, vol. 89, pp. 361–367. https://doi.org/10.1016/j.fsi.2019.04.017
Belcheva N. N., Dovzhenko N. V., Istomina A. A., Zhukovskaya A. F., Kukla S. P. The antioxidant system of the Gray’s mussel Crenomytilus grayanus (Dunker, 1853) and the Japanese scallop Mizuhopecten yessoensis (Jay, 1857) (Mollusca: Bivalvia). Russian Journal of Marine Biology, 2016, vol. 42, iss. 6, pp. 489–494. http://dx.doi.org/10.1134/S106307401606002X
Canesi L., Gallo G., Gavioli M., Pruzzo C. Bacteria–hemocyte interactions and phagocytosis in marine bivalves. Microscopy Research and Technique, 2002, vol. 57, iss. 6, pp. 469–476. https://doi.org/10.1002/jemt.10100
Chandel N. S., McClintock D. S., Feliciano C. E., Wood T. M., Melendez J. A., Rodriguez A. M., Schumacker P. T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: A mechanism of O2 sensing. Journal of Biological Chemistry, 2000, vol. 275, iss. 33, pp. 25130–25138. https://doi.org/10.1074/jbc.m001914200
Charlet M., Chernysh S., Philippe H., Hetru C., Hoffmann J. A., Bulet P. Innate immunity: Isolation of several cysteine-rich antimicrobial peptides from the blood of a mollusc, Mytilus edulis. Journal of Biological Chemistry, 1996, vol. 271, iss. 36, pp. 21808–21813. https://doi.org/10.1074/jbc.271.36.21808
Chen J., Mai K., Ma H., Wang X., Deng D., Liu X., Xu W., Liufu Z., Zhang W., Tan B., Ai Q. Effects of dissolved oxygen on survival and immune responses of scallop (Chlamys farreri Jones et Preston). Fish & Shellfish Immunology, 2007, vol. 22, iss. 3, pp. 272–281. https://doi.org/10.1016/j.fsi.2006.06.003
Chen X., Zhang R., Li C., Bao Y. Mercury exposure modulates antioxidant enzymes in gill tissue and hemocytes of Venerupis philippinarum. Invertebrate Survival Journal, 2014, vol. 11, no. 1, pp. 298–308.
De Zoysa M., Whang I., Lee Y., Lee S., Lee J. S., Lee J. Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2009, vol. 154, iss. 4, pp. 387–395. https://doi.org/10.1016/j.cbpb.2009.08.002
Diaz R. J., Breitburg D. L. The hypoxic environment. In: Hypoxia / J. G. Richards, A. P. Farell, C. J. Brauner (Eds). New York ; London ; Oxford ; Boston ; San Diego : Academic Press, 2009, chap. 1, pp. 1–23. (Fish Physiology ; vol. 27). https://doi.org/10.1016/S1546-5098(08)00001-0
Donaghy L., Kraffe E., Le Goïc N., Lambert C., Volety A. K., Soudant P. Reactive oxygen species in unstimulated hemocytes of the Pacific oyster Crassostrea gigas: A mitochondrial involvement. PLoS One, 2012, vol. 7, iss. 10, art. no. e46594 (10 p.). https://doi.org/10.1371/journal.pone.0046594
Donaghy L., Artigaud S., Sussarellu R., Lambert C., Le Goïc N., Hégaret H., Soudant P. Tolerance of bivalve mollusc hemocytes to variable oxygen availability: A mitochondrial origin? Aquatic Living Resources, 2013, vol. 26, no. 3, pp. 257–261. https://doi.org/10.1051/alr/2013054
Dorrington T., Villamil L., Gómez-Chiarri M. Upregulation in response to infection and antibacterial activity of oyster histone H4. Fish & Shellfish Immunology, 2011, vol. 30, iss. 1, pp. 94–101. https://doi.org/10.1016/j.fsi.2010.09.006
Ellis R. P., Parry H., Spicer J. I., Hutchinson T. H., Pipe R. K., Widdicombe S. Immunological function in marine invertebrates: Responses to environmental perturbation. Fish & Shellfish Immunology, 2011, vol. 30, iss. 6, pp. 1209–1222. https://doi.org/10.1016/j.fsi.2011.03.017
Gallo N. D., Levin L. A. Fish ecology and evolution in the world’s oxygen minimum zones and implications of ocean deoxygenation. Advances in Marine Biology, 2016, vol. 74, pp. 117–198. https://doi.org/10.1016/bs.amb.2016.04.001
Giannetto A., Maisano M., Cappello T., Oliva S., Parrino V., Natalotto A., De Marco G., Fasulo S. Effects of oxygen availability on oxidative stress biomarkers in the Mediterranean mussel Mytilus galloprovincialis. Marine Biotechnology, 2017, vol. 19, no. 6, pp. 614–626. https://doi.org/10.1007/s10126-017-9780-6
Gostyukhina O. L., Andreenko T. I. Tissue metabolism and the state of the antioxidant complex in the Black Sea mollusks Anadara kagoshimensis (Tokunaga, 1906) and Mytilus galloprovincialis Lamarck, 1819 with different tolerances to oxidative stress. Russian Journal of Marine Biology, 2019, vol. 45, no. 3, pp. 211–220. https://doi.org/10.1134/S1063074019030039
Gu Z., Wei H., Cheng F., Wang A., Liu C. Effects of air exposure time and temperature on physiological energetics and oxidative stress of winged pearl oyster (Pteria penguin). Aquaculture Reports, 2020, vol. 17, art. no. 100384 (9 p.). https://doi.org/10.1016/j.aqrep.2020.100384
Hartmann J. T., Beggel S., Auerswald K., Stoeckle B. C., Geist J. Establishing mussel behavior as a biomarker in ecotoxicology. Aquatic Toxicology, 2016, vol. 170, pp. 279–288. https://doi.org/10.1016/j.aquatox.2015.06.014
Hermes-Lima M. Oxygen in biology and biochemistry: Role of free radicals. In: Functional Metabolism: Regulation and Adaptation / K. B. Storey (Ed.). Holoken, NJ : Wiley-Liss, 2004, chap. 12, pp. 319–368. https://doi.org/10.1002/047167558X.ch12
Hicks D. W., McMahon R. F. Effects of temperature on chronic hypoxia tolerance in the non-indigenous brown mussel, Perna perna (Bivalvia: Mytilidae) from the Texas Gulf of Mexico. Journal of Molluscan Studies, 2005, vol. 71, iss. 4, pp. 401–408. https://doi.org/10.1093/mollus/eyi042
Hine P. M. The inter-relationships of bivalve haemocytes. Fish & Shellfish Immunology, 1999, vol. 9, iss. 5, pp. 367–385. https://doi.org/10.1006/fsim.1998.0205
Ikuta T., Tame A., Saito M., Aoki Y., Nagai Y., Sugimura M., Inoue K., Fujikura K., Ohishi K., Maruyama T., Yoshida T. Identification of cells expressing two peptidoglycan recognition proteins in the gill of the vent mussel, Bathymodiolus septemdierum. Fish & Shellfish Immunology, 2019, vol. 93, pp. 815–822. https://doi.org/10.1016/j.fsi.2019.08.022
Irato P., Piccinni E., Cassini A., Santovito G. Antioxidant responses to variations in dissolved oxygen of Scapharca inaequivalvis and Tapes philippinarum, two bivalve species from the lagoon of Venice. Marine Pollution Bulletin, 2007, vol. 54, iss. 7, pp. 1020–1030. https://doi.org/10.1016/j.marpolbul.2007.01.020
Katsumiti A., Gilliland D., Arostegui I., Cajaraville M. P. Mechanisms of toxicity of Ag nanoparticles in comparison to bulk and ionic Ag on mussel hemocytes and gill cells. PLoS One, 2015, vol. 10, iss. 6, art. no. e0129039 (30 p.). https://doi.org/10.1371/journal.pone.0129039
Lambert A. J., Brand M. D. Superoxide production by NADH: Ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochemical Journal, 2004, vol. 382, iss. 2, pp. 511–517. https://doi.org/10.1042/BJ20040485
Liu S., Jiang X., Hu X., Gong J., Hwang H., Mai K. Effects of temperature on non‐specific immune parameters in two scallop species: Argopecten irradians (Lamarck 1819) and Chlamys farreri (Jones & Preston 1904). Aquaculture Research, 2004, vol. 35, iss. 7, pp. 678–682. https://doi.org/10.1111/j.1365-2109.2004.01065.x
Livingstone D. R. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 2001, vol. 42, iss. 8, pp. 656–666. https://doi.org/10.1016/s0025-326x(01)00060-1
Matozzo V., Monari M., Foschi J., Papi T., Cattani O., Marin M. G. Exposure to anoxia of the clam Chamelea gallina: I. Effects on immune responses. Journal of Experimental Marine Biology and Ecology, 2005, vol. 325, iss. 2, pp. 163–174. https://doi.org/10.1016/j.jembe.2005.04.030
Michiels C., Minet E., Mottet D., Raes M. Regulation of gene expression by oxygen: NF-κB and HIF-1, two extremes. Free Radical Biology and Medicine, 2002, vol. 33, iss. 9, pp. 1231–1242. https://doi.org/10.1016/S0891-5849(02)01045-6
Mitta G., Hubert F., Dyrynda E. A., Boudry P., Roch P. Mytilin B and MGD2, two antimicrobial peptides of marine mussels: Gene structure and expression analysis. Developmental & Comparative Immunology, 2000, vol. 24, iss. 4, pp. 381–393. https://doi.org/10.1016/S0145-305X(99)00084-1
Monari M., Matozzo V., Foschi J. M., Marin M. G., Cattani O. Exposure to anoxia of the clam, Chamelea gallina: II: Modulation of superoxide dismutase activity and expression in haemocytes. Journal of Experimental Marine Biology and Ecology, 2005, vol. 325, iss. 2, pp. 175–188. https://doi.org/10.1016/j.jembe.2005.05.001
Monari M., Matozzo V., Foschi J., Cattani O., Serrazanetti G. P., Marin M. G. Effects of high temperatures on functional responses of haemocytes in the clam Chamelea gallina. Fish & Shellfish Immunology, 2007, vol. 22, iss. 1–2, pp. 98–114. https://doi.org/10.1016/j.fsi.2006.03.016
Mosca F., Narcisi V., Calzetta A., Gioia L., Finoia M. G., Latini M., Tiscar P. G. Effects of high temperature and exposure to air on mussel (Mytilus galloprovincialis, Lmk 1819) hemocyte phagocytosis: Modulation of spreading and oxidative response. Tissue and Cell, 2013, vol. 45, iss. 3, pp. 198–203. https://doi.org/10.1016/j.tice.2012.12.002
Mydlarz L. D., Jones L. E., Harvell C. D. Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annual Review of Ecology, Evolution, and Systematics, 2006, vol. 37, pp. 251–288. https://doi.org/10.1146/annurev.ecolsys.37.091305.110103
Nogueira L., Mello D. F., Trevisan R., Garcia D., da Silva Acosta D., Dafre A. L., de Almeida E. A. Hypoxia effects on oxidative stress and immunocompetence biomarkers in the mussel Perna perna (Mytilidae, Bivalvia). Marine Environmental Research, 2017, vol. 126, pp. 109–115. https://doi.org/10.1016/j.marenvres.2017.02.009
Pampanin D. M., Ballarin L., Carotenuto L., Marin M. G. Air exposure and functionality of Chamelea gallina haemocytes: Effects on haematocrit, adhesion, phagocytosis and enzyme contents. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2002, vol. 131, iss. 3, pp. 605–614. https://doi.org/10.1016/S1095-6433(01)00512-8
Parisi M. G., Vizzini A., Toubiana M., Sarà G., Cammarata M. Identification, cloning and environmental factors modulation of a αβ defensin from the Lessepsian invasive mussel Brachidontes pharaonis (Bivalvia: Mytilidae). Invertebrate Survival Journal, 2015, vol. 12, no. 1, pp. 264–273.
Pauletto M., Milan M., Moreira R., Novoa B., Figueras A., Babbucci M., Patarnello T., Bargelloni L. Deep transcriptome sequencing of Pecten maximus hemocytes: A genomic resource for bivalve immunology. Fish & Shellfish Immunology, 2014, vol. 37, iss. 1, pp. 154–165. https://doi.org/10.1016/j.fsi.2014.01.017
Rodrigues J., Brayner F. A., Alves L. C., Dixit R., Barillas-Mury C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science, 2010, vol. 329, iss. 5997, pp. 1353–1355. https://doi.org/10.1126/science.1190689
Shen Y., Huang Z., Liu G., Ke C., You W. Hemolymph and transcriptome analysis to understand innate immune responses to hypoxia in Pacific abalone. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 2019, vol. 30, pp. 102–112. https://doi.org/10.1016/j.cbd.2019.02.001
Sokolov E. P., Markert S., Hinzke T., Hirschfeld C., Becher D., Ponsuksili S., Sokolova I. M. Effects of hypoxia-reoxygenation stress on mitochondrial proteome and bioenergetics of the hypoxia-tolerant marine bivalve Crassostrea gigas. Journal of Proteomics, 2019, vol. 194, pp. 99–111. https://doi.org/10.1016/j.jprot.2018.12.009
Soldatov A. A., Gostyukhina O. L., Golovina I. V. Functional states of antioxidant enzymatic complex of tissues of Mytilus galloprovincialis Lam. under conditions of oxidative stress. Journal of Evolutionary Biochemistry and Physiology, 2014, vol. 50, iss. 3, pp. 206–214. https://doi.org/10.1134/S0022093014030028
Suárez-Ulloa V., Fernández-Tajes J., Manfrin C., Gerdol M., Venier P., Eirín-López J. M. Bivalve omics: State of the art and potential applications for the biomonitoring of harmful marine compounds. Marine Drugs, 2013, vol. 11, no. 11, pp. 4370–4389. https://doi.org/10.3390/md11114370
Sui Y., Hu M., Shang Y., Wu F., Huang X., Dupont S., Storch D., Pörtner H.-O., Li J., Lu W., Wang Y. Antioxidant response of the hard shelled mussel Mytilus coruscus exposed to reduced pH and oxygen concentration. Ecotoxicology and Environmental Safety, 2017, vol. 137, pp. 94–102. https://doi.org/10.1016/j.ecoenv.2016.11.023
Sui Y., Kong H., Shang Y., Huang X., Wu F., Hu M., Lin D., Lu W., Wang Y. Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Marine Pollution Bulletin, 2016, vol. 108, iss. 1–2, pp. 46–52. https://doi.org/10.1016/j.marpolbul.2016.05.001
Sun Y., Zhang X., Wang G., Lin S., Zeng X., Wang Y., Zhang Z. PI3K-AKT signaling pathway is involved in hypoxia/thermal-induced immunosuppression of small abalone Haliotis diversicolor. Fish & Shellfish Immunology, 2016, vol. 59, pp. 492–508. https://doi.org/10.1016/j.fsi.2016.11.011
Tomanek L. Proteomic responses to environmentally induced oxidative stress. Journal of Experimental Biology, 2015, vol. 218, pt. 12, pp. 1867–1879. https://doi.org/10.1242/jeb.116475
Valko M., Rhodes C., Moncol J., Izakovic M. M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions, 2006, vol. 160, iss. 1, pp. 1–40. https://doi.org/10.1016/j.cbi.2005.12.009
Wang S., Peatman E., Liu H., Bushek D., Ford S. E., Kucuktas H., Quilang J., Li P., Wallace R., Wang Y., Guo X., Liu Z. Microarray analysis of gene expression in eastern oyster (Crassostrea virginica) reveals a novel combination of antimicrobial and oxidative stress host responses after dermo (Perkinsus marinus) challenge. Fish & Shellfish Immunology, 2010, vol. 29, iss. 6, pp. 921–929. https://doi.org/10.1016/j.fsi.2010.07.035
Wang Q., Wang C., Mu C., Wu H., Zhang L., Zhao J. A novel C-type lysozyme from Mytilus galloprovincialis: Insight into innate immunity and molecular evolution of invertebrate C-type lysozymes. PLoS One, 2013, vol. 8, iss. 6, art. no. e67469 (12 p.). https://doi.org/10.1371/journal.pone.0067469
Wang W., Li M., Wang L., Chen H., Liu Z., Jia Z., Qiu L., Song L. The granulocytes are the main immunocompetent hemocytes in Crassostrea gigas. Developmental & Comparative Immunology, 2017, vol. 67, pp. 221–228. https://doi.org/10.1016/j.dci.2016.09.017
Wang Y., Hu M., Cheung S. G., Shin P. K. S., Lu W., Li J. Immune parameter changes of hemocytes in green-lipped mussel Perna viridis exposure to hypoxia and hyposalinity. Aquaculture, 2012, vols 356–357, pp. 22–29. https://doi.org/10.1016/j.aquaculture.2012.06.001
Wang Y., Hu M., Shin P. K., Cheung S. G. Immune responses to combined effect of hypoxia and high temperature in the green-lipped mussel Perna viridis. Marine Pollution Bulletin, 2011, vol. 63, iss. 5–12, pp. 201–208. https://doi.org/10.1016/j.marpolbul.2011.05.035
Wijsman J. W. M., Troost K., Fang J., Roncarati A. Global production of marine bivalves. Trends and challenges. In: Goods and Services of Marine Bivalves / A. Smaal, J. Ferreira, J. Grant, J. Petersen, Ø. Strand (Eds). Cham : Springer, 2019, pp. 7–26. https://doi.org/10.1007/978-3-319-96776-9_2
Woo S., Denis V., Won H., Shin K., Lee G., Lee T.-K., Yum S. Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zoological Studies, 2013, vol. 52, no. 1, art. no. 15 (8 p.). https://doi.org/10.1186/1810-522X-52-15
Wootton E. C., Dyrynda E. A., Ratcliffe N. A. Bivalve immunity: Comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua). Fish & Shellfish Immunology, 2003, vol. 15, iss. 3, pp. 195–210. https://doi.org/10.1016/S1050-4648(02)00161-4
Zhang X., Shi J., Sun Y., Habib Y. J., Yang H., Zhang Z., Wang Y. Integrative transcriptome analysis and discovery of genes involving in immune response of hypoxia/thermal challenges in the small abalone Haliotis diversicolor. Fish & Shellfish Immunology, 2019, vol. 84, pp. 609–626. https://doi.org/10.1016/j.fsi.2018.10.044