Research Advances on Fish Blood Cells and Immune Defense Functions

doi:10.11924/j.issn.1000-6850.casb2023-0736

Abstract

Abstract:

Fish blood cells are important part in fish body immunity. They participate in many physiological activities, such as body phagocytosis, secretion, damage repair, defense and others. They are sensitive to changes in their own physiological state as well as to the stimulation of external environmental factors. Blood cells play an important role in indicating and maintaining the physiological homeostasis of fish. Based on recent research reports of domestic and international developments, this paper investigated the progress of fish blood, blood cells and their immune defense functions, and reviewed the blood composition, blood cell genesis, differentiation and related immune defense mechanisms of fish. This review is helpful to deepen the understanding of fish blood immune defense system and its related molecular mechanism, and provides references for further exploration of molecular markers related to fish blood immune defense and screening of molecular phenotypes of fish disease and stress resistance.

Key words: fish, fish blood, blood cell, immune cell, cell differentiation, immune defense, physiological homeostasis, molecular mechanisms of action

ZHANG Meiyan, ZHU Weijuan, LIU Zhigang, CAO Jianmeng, WANG Zhang, LU Maixin, KE Xiaoli. Research Advances on Fish Blood Cells and Immune Defense Functions[J]. Chinese Agricultural Science Bulletin, 2024, 40(26): 144-153.

References 89

[1]	DONOGHUE P C, KEATING J N. Early vertebrate evolution[J]. Palaeontology, 2014, 57(5):879-893.
[2]	WIENS J J. Explaining large-scale patterns of vertebrate diversity[J]. Biology letters, 2015, 11(7):20150506.
[3]	KATHY HUGHES. The world’s forgotten fishes[M]. America: WWF international, 2021:7-39.
[4]	RUMMER J L, WANG S, STEFFENSEN J F, et al. Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems[J]. Journal of experimental biology, 2014, 217(5):751-757.
[5]	TORT L, BALASCH J, MACKENZIE S. Fish immune system. A crossroads between innate and adaptive responses[J]. Inmunología, 2003, 22(3):277-286.
[6]	VERMEULEN W, KAISER H. A note on the formation of red blood cells in rainbow trout vertebral bone marrow[J]. Journal of applied ichthyology, 2008, 24(5):621-622.
[7]	ARAMLI M, KALBASSI M, NAZARI R. Blood and seminal plasma enzyme values of Persian sturgeon, Acipenser persicus (Chordata:Osteichthyes)[J]. Italian journal of zoology, 2013, 80(4):490-493.
[8]	尾崎久(著), 许学龙, 熊国强, 缪圣赐(译). 鱼类血液与循环生理[M]. 上海: 上海科学技术出版社, 1982:6-26.
[9]	刘霞飞, 杨合霖, 丰超杰, 等. 达氏鳇血细胞的组成、发生及吞噬功能研究[J]. 水产学杂志, 2022, 35(2):28-34.
[10]	李坚, 段利芳, 徐刚, 等. 施氏魮 (Barbonymus schwanenfeldii)外周血液及造血器官血细胞发生的观察[J]. 河南科学, 2020, 38(3):376-385.
[11]	曹文芝, 刘云, 梁冰, 等. 斑马鱼外周血液及造血器官血细胞发生的观察[J]. 水产科学, 2014, 33(7):403-409.
[12]	袁仕取, 张永安, 姚卫建, 等. 鳜鱼外周血细胞显微和亚显微结构的观察[J]. 水生生物学报, 1998, 22(1):39-46.
[13]	LAWRENCE M J, RABY G D, TEFFER A K, et al. Best practices for non-lethal blood sampling of fish via the caudal vasculature[J]. Journal of fish biology, 2020, 97(1):4-15. doi: 10.1111/jfb.14339 pmid: 32243570
[14]	刘巧. 不同倍性鱼类血细胞研究[D]. 长沙: 湖南师范大学, 2005.
[15]	FANG J, CHEN K, CUI H, et al. Morphological and cytochemical studies of peripheral blood cells of Schizothorax prenanti[J]. Anatomia, histologia, embryologia, 2014, 43(5):386-394.
[16]	MITCHELL C D, CRISCITIELLO M F. Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture[J]. Fish & shellfish immunology, 2020, 107:435-443.
[17]	KONDERA E. Haematopoiesis and haematopoietic organs in fish[J]. Rocz nauk pol tow zootech, 2019, 15:9-16.
[18]	TEMMINK J, BAYNE C. Ultrastructural characterization of leucocytes in the pronephros of carp (Cyprinus carpio, L.)[J]. Developmental & comparative immunology, 1987, 11(1):125-137.
[19]	SOLDATOV A. Peculiarities of organization and functioning of the fish red blood system[J]. Journal of evolutionary biochemistry and physiology, 2005, 41(3):272-281.
[20]	FREITAS I, FRACCHIOLLA S, BARNI S, et al. Hemopoiesis in the liver of adult tumor-bearing mice[J]. Italian journal of anatomy and embryology = Archivio italiano di anatomia ed embriologia, 2001, 106(2 Suppl 1):295-302.
[21]	MURAYAMA E, KISSA K, ZAPATA A, et al. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development[J]. Immunity, 2006, 25(6):963-975. pmid: 17157041
[22]	BELOSEVIC M, HANINGTON P C, BARREDA D R. Development of goldfish macrophages in vitro[J]. Fish & shellfish immunology, 2006, 20(2):152-171.
[23]	ALIKO V, QIRJO M, SULA E, et al. Antioxidant defense system, immune response and erythron profile modulation in gold fish, Carassius auratus, after acute manganese treatment[J]. Fish & shellfish immunology, 2018, 76:101-109.
[24]	LAHNSTEINER F. Erythrocyte morphometry in teleost fish-species-specific, inter-individual and environmental-related differences[J]. Acta zoologica, 2021, 102(3):237-249.
[25]	MARTINS B O, FRANCO-BELUSSI L, SIQUEIRA M S, et al. The evolution of red blood cell shape in fishes[J]. Journal of evolutionary biology, 2021, 34(3):537-548. doi: 10.1111/jeb.13757 pmid: 33484056
[26]	PASSANTINO L, ALTAMURA M, CIANCIOTTA A, et al. Maturation of fish erythrocytes coincides with changes in their morphology, enhanced ability to interact with Candida albicans and release of cytokine-like factors active upon autologous macrophages[J]. Immunopharmacology and immunotoxicology, 2004, 26(4):573-585.
[27]	GLOMSKI C A, TAMBURLIN J, CHAINANI M. The phylogenetic odyssey of the erythrocyte. iii. fish, the lower vertebrate experience[J]. Histology and histopathology, 1992, 7(3):501-528. pmid: 1504472
[28]	ZEXIA G, WEIMIN W, YI Y, et al. Morphological studies of peripheral blood cells of the chinese sturgeon, Acipenser sinensis[J]. Fish physiology and biochemistry, 2007, 33(3):213-222.
[29]	SEKHON S S, BEAMS H. Fine structure of the developing trout erythrocytes and thrombocytes with special reference to the marginal band and the cytoplasmic organelles[J]. American journal of anatomy, 1969, 125(3):353-373. pmid: 5790998
[30]	GRANT K R. Fish hematology and associated disorders[J]. Veterinary clinics:exotic animal practice, 2015, 18(1):83-103.
[31]	JI-MIN JEONG, CHEUL MIN AN, MU-CHAN KIM, et al. Cooperation of erythrocytes with leukocytes in immune response of a teleost Oplegnathus fasciatus[J]. Genes & genomics, 2016, 38(10):931-938.
[32]	SHEN Y, WANG D, ZHAO J, et al. Fish red blood cells express immune genes and responses[J]. Aquaculture and fisheries, 2018, 3(1):14-21.
[33]	NOMBELA I, ORTEGA-VILLAIZAN M D M. Nucleated red blood cells:Immune cell mediators of the antiviral response[J]. Plos pathogens, 2018, 14(4):e1006910.
[34]	LU Z, YANG M, ZHANG K, et al. Aeromonas hydrophila infection activates death receptor apoptosis pathway in the red blood cells of grass carp (Ctenopharyngodon idellus)[J]. Aquaculture, 2021, 532:735956.
[35]	MINASYAN H. Erythrocyte and blood antibacterial defense[J]. European journal of microbiology and immunology, 2014, 4(2):138-143. doi: 10.1556/EuJMI.4.2014.2.7 pmid: 24883200
[36]	PUENTE-MARIN S, NOMBELA I, CIORDIA S, et al. In silico functional networks identified in fish nucleated red blood cells by means of transcriptomic and proteomic profiling[J]. Genes, 2018, 9(4):202.
[37]	NIKINMAA M. Environmental regulation of the function of circulating erythrocytes via changes in age distribution in teleost fish: Possible mechanisms and significance[J]. Marine genomics, 2020, 49:100717.
[38]	DALMO R, INGEBRIGTSEN K, BØGWALD J. Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES)[J]. Journal of fish diseases, 1997, 20(4):241-273.
[39]	汤绮桐, 曹伏君, 叶宁. 珍珠龙胆石斑鱼血细胞发生的研究[J]. 水产科学, 2021, 40(2):210-217.
[40]	CHEN H, YUAN G, SU J, et al. Hematological analysis of Ctenopharyngodon idella, Megalobrama amblycephala and Pelteobagrus fulvidraco: Morphology, ultrastructure, cytochemistry and quantification of peripheral blood cells[J]. Fish & shellfish immunology, 2019, 90:376-384.
[41]	NAKANISHI T, SHIBASAKI Y, MATSUURA Y. T cells in fish[J]. Biology, 2015, 4(4):640-663.
[42]	TAFALLA C, LEAL E, YAMAGUCHI T, et al. T cell immunity in the teleost digestive tract[J]. Developmental & comparative immunology, 2016, 64:167-177.
[43]	YAMAGUCHI T, TAKIZAWA F, FURIHATA M, et al. Teleost cytotoxic T cells[J]. Fish & shellfish immunology, 2019, 95:422-439.
[44]	ASHFAQ H, SOLIMAN H, SALEH M, et al. CD4: A vital player in the teleost fish immune system[J]. Veterinary research, 2019, 50(1):1-11. doi: 10.1186/s13567-018-0620-0 pmid: 30616664
[45]	WU L, LI L, GAO A, et al. Antimicrobial roles of phagocytosis in teleost fish:phagocytic B cells vs professional phagocytes[J]. Aquaculture and fisheries, 2024, 9(2):105-114.
[46]	LUCKHEERAM R V, ZHOU R, VERMA A D, et al. CD4⁺ T cells:differentiation and functions[J]. Clinical and developmental immunology, 2012, 2012:925135.
[47]	FLAJNIK M F, KASAHARA M. Origin and evolution of the adaptive immune system:genetic events and selective pressures[J]. Nature reviews genetics, 2010, 11(1):47-59.
[48]	ESTEBAN M Á, CUESTA A, CHAVES-POZO E, et al. Phagocytosis in teleosts. Implications of the new cells involved[J]. Biology, 2015, 4(4):907-922.
[49]	CARMONA S J, TEICHMANN S A, FERREIRA L, et al. Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types[J]. Genome research, 2017, 27(3):451-461. doi: 10.1101/gr.207704.116 pmid: 28087841
[50]	HOHN C, PETRIE-HANSON L. Rag1^-/- mutant zebrafish demonstrate specific protection following bacterial re-exposure[J]. Plos one, 2012, 7(9):e44451.
[51]	MUIRE P J, HANSON L A, WILLS R, et al. Differential gene expression following TLR stimulation in rag1^-/-mutant zebrafish tissues and morphological descriptions of lymphocyte-like cell populations[J]. PloS one, 2017, 12(9):e0184077.
[52]	FEJER G, SHARMA S, GYORY I. Self-renewing macrophages-a new line of enquiries in mononuclear phagocytes[J]. Immunobiology, 2015, 220(2):169-174.
[53]	HUME D A, IRVINE K M, PRIDANS C. The mononuclear phagocyte system:the relationship between monocytes and macrophages[J]. Trends in immunology, 2019, 40(2):98-112.
[54]	ABARIKE E D, KUEBUTORNYE F K, JIAN J, et al. Influences of immunostimulants on phagocytes in cultured fish:a mini review[J]. Reviews in aquaculture, 2019, 11(4):1219-1227.
[55]	SHA Z, WANG L, SUN L, et al. Isolation and characterization of monocyte/macrophage from peripheral blood of half smooth tongue sole (Cynoglossus semilaevis)[J]. Fish & shellfish immunology, 2017, 100(65):256-266.
[56]	WIEGERTJES G F, WENTZEL A S, SPAINK H P, et al. Polarization of immune responses in fish:The ‘macrophages first’point of view[J]. Molecular immunology, 2016, 100(69):146-156.
[57]	GRAYFER L, KERIMOGLU B, YAPARLA A, et al. Mechanisms of fish macrophage antimicrobial immunity[J]. Frontiers in immunology, 2018, 9:1105. doi: 10.3389/fimmu.2018.01105 pmid: 29892285
[58]	LEIRO J, IGLESIAS R, PARAMA A, et al. Effect of tetramicra brevifilum (Microspora) infection on respiratory-burst responses of turbot (Scophthalmus maximus L.) phagocytes[J]. Fish & shellfish immunology, 2001, 11(7):639-652.
[59]	KIM J-H, OGAWA K, WAKABAYASHI H. Respiratory burst assay of head kidney macrophages of ayu, Plecoglossus altivelis, stimulated with Glugea plecoglossi (Protozoa:Microspora) spores[J]. The journal of parasitology, 1998, 84(3):552-556.
[60]	FORLENZA M, FINK I R, RAES G, et al. Heterogeneity of macrophage activation in fish[J]. Developmental & comparative immunology, 2011, 35(12):1246-1255.
[61]	Hodgkinson J W, Grayfer L, Belosevic M. Biology of bony fish macrophages[J]. Biology, 2015, 4(4):881-906.
[62]	MONTERO J, GÓMEZ-ABELLÁN V, ARIZCUN M, et al. Prostaglandin E2 promotes M2 polarization of macrophages via a cAMP/CREB signaling pathway and deactivates granulocytes in teleost fish[J]. Fish & shellfish immunology, 2016, 55:632-641.
[63]	KUMAR J, KUMAR M, SHARMA S, et al. Th1-Th2 and M1-M2 interplay sculpt Aeromonas hydrophila pathogenesis in zebrafish (Danio rerio)[J]. Fish & shellfish immunology, 2022, 127:357-365.
[64]	ODAKA T, SUETAKE H, MAEDA T, et al. Teleost basophils have IgM-dependent and dual Ig-independent degranulation systems[J]. The journal of immunology, 2018, 200(8):2767-2776.
[65]	HAVIXBECK J J, RIEGER A M, WONG M E, et al. Neutrophil contributions to the induction and regulation of the acute inflammatory response in teleost fish[J]. Journal of leukocyte biology, 2016, 99(2):241-252. doi: 10.1189/jlb.3HI0215-064R pmid: 26292979
[66]	HAVIXBECK J J, BARREDA D R. Neutrophil development, migration, and function in teleost fish[J]. Biology, 2015, 4(4):715-734.
[67]	SOEHNLEIN O, ZERNECKE A, WEBER C. Neutrophils launch monocyte extravasation by release of granule proteins[J]. Thrombosis and haemostasis, 2009, 102(8):198-205.
[68]	CAPILLO G, ZACCONE G, CUPELLO C, et al. Expression of acetylcholine, its contribution to regulation of immune function and O₂ sensing and phylogenetic interpretations of the African butterfly fish Pantodon buchholzi (Osteoglossiformes, Pantodontidae)[J]. Fish & shellfish immunology, 2021, 111:189-200.
[69]	HUIZINGA H. Anti-parasitic mechanisms of the eosinophilic leukocyte of the goldfish[C]. American zoologist, 1980, 20(4):795-795.
[70]	CHOI K-M, JOO M-S, KANG G, et al. First report of eosinophil peroxidase in starry flounder (Platichthys stellatus): Gene identification and gene expression profiling[J]. Fish & shellfish immunology, 2021, 118:155-159.
[71]	YAMANISHI Y, MIYAKE K, IKI M, et al. Recent advances in understanding basophil-mediated Th2 immune responses[J]. Immunological reviews, 2017, 278(1):237-245. doi: 10.1111/imr.12548 pmid: 28658549
[72]	HE Y, ZHU W, XU T, et al. Identification and immune responses of thrombocytes in bacterial and viral infections in grass carp (Ctenopharyngodon idella)[J]. Fish & shellfish immunology, 2022, 123:314-323.
[73]	NAGASAWA T, NAKAYASU C, RIEGER A M, et al. Phagocytosis by thrombocytes is a conserved innate immune mechanism in lower vertebrates[J]. Frontiers in immunology, 2014, 5:445. doi: 10.3389/fimmu.2014.00445 pmid: 25278940
[74]	NAGASAWA T, SOMAMOTO T, NAKAO M. Carp thrombocyte phagocytosis requires activation factors secreted from other leukocytes[J]. Developmental & comparative immunology, 2015, 52(2):107-111.
[75]	FINK I R, RIBEIRO C M, FORLENZA M, et al. Immune-relevant thrombocytes of common carp undergo parasite-induced nitric oxide-mediated apoptosis[J]. Developmental & comparative immunology, 2015, 50(2):146-154.
[76]	COOKE S J, LAWRENCE M J, RABY G D, et al. Comment:practices for drawing blood samples from teleost fish[J]. North American journal of aquaculture, 2019, 81(4):424-426.
[77]	WITESKA M. Anemia in teleost fishes[J]. Bull eur assoc fish pathol, 2015, 35(4):148-160.
[78]	FAZIO F, PICCIONE G, ARFUSO F, et al. Peripheral blood and head kidney haematopoietic tissue response to experimental blood loss in mullet (Mugil cephalus)[J]. Marine biology research, 2015, 11(2):197-202.
[79]	JAN K, AHMED I. The influence of sex and season on some hematological and biochemical parameters of snow trout Schizothorax labiatus in the Indian Himalayan region[J]. Fisheries science, 2021, 87:39-54.
[80]	ONXAYVIENG K, PIRIA M, FUKA M M, et al. High stocking density alters growth performance, blood biochemical profiles, and hepatic antioxidative capacity in gibel carp (Carassius gibelio)[J]. Fish physiology and biochemistry, 2021, 47(2):203-212. doi: 10.1007/s10695-020-00905-6 pmid: 33405063
[81]	RIBAS J L C, ZAMPRONIO A R, SILVA DE ASSIS H C. Effects of trophic exposure to diclofenac and dexamethasone on hematological parameters and immune response in freshwater fish[J]. Environmental toxicology and chemistry, 2016, 35(4):975-982. doi: 10.1002/etc.3240 pmid: 27003719
[82]	ANDREYEVA A Y, SOLDATOV A A, KUKHAREVA T A. Black scorpionfish (Scorpaena porcus) hemopoiesis:analysis by flow cytometry and light microscopy[J]. The anatomical record, 2017, 300(11):1993-1999.
[83]	FREEN-VAN HEEREN J J, NICOLET B P, WOLKERS M C. Measuring T cell responses by flow cytometry-based fluorescence in situ hybridization[J]. Critical reviews™ in immunology, 2018, 38(2):131-143.
[84]	FAZIO F. Fish hematology analysis as an important tool of aquaculture:a review[J]. Aquaculture, 2019, 500:237-242.
[85]	SULA E, ALIKO V, PAGANO M, et al. Digital light microscopy as a tool in toxicological evaluation of fish erythrocyte morphological abnormalities[J]. Microscopy research and technique, 2020, 83(4):362-369. doi: 10.1002/jemt.23422 pmid: 31825143
[86]	BALL P. High-Resolution technique tracks blood flow in live fish[J]. Physics, 2020, 13:81.
[87]	CHAN J T, KADRI S, KÖLLNER B, et al. RNA-seq of single fish cells-seeking out the leukocytes mediating immunity in teleost fishes[J]. Frontiers in immunology, 2022, 13:798712.
[88]	YU H, REN Y, XU G, et al. Iso-seq combined with RNA-seq analysis provided insight into the molecular response to dietary oxidized fish oil in juvenile Amur sturgeon, Acipenser schrenckii[J]. Aquaculture, 2022, 552:737971.
[89]	MOSES L, PACHTER L. Museum of spatial transcriptomics[J]. Nature methods, 2022, 19(5):534-546. doi: 10.1038/s41592-022-01409-2 pmid: 35273392