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Cellular Immune Responses

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Principles of Fish Immunology

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Abstract

Generally speaking, cellular immune responses are comprised of innate and adaptive cell-based immune mechanisms in which all leukocyte subpopulations are involved. This includes effector functions such as phagocytosis, NETosis, and cell-mediated cytotoxicity. The main players are macrophages/monocytes, dendritic cells, granulocytes, NK cells, and cytotoxic T cells. These effector functions can only be executed and controlled through receptor/ligand interactions and by humoral factors produced by leukocytes or somatic cells. Thus, it is hard to draw a static line between cellular and humoral components of the immune systems since one system cannot exist independently from the other. Similarly, adaptive responses cannot be efficiently induced without innate triggers.

This chapter describes cellular immune mechanisms in teleost fish and relates them to mammalian immunology.

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Abbreviations

somatic cell::

bodies own cell

tissue::

aggregate of cells having the same structure and function

antigen::

from anti, Greek = against; gennan, Greek = produce; in the original sense: substances that the body recognizes as foreign via antibodies; in a broader sense: substances against which an immune response is mounted

aa:

amino acid

ADCC:

antibody-dependent cell-mediated cytotoxicity

APC:

antigen-presenting cell

CD:

cluster of differentiation

CMC:

cell-mediated cytotoxicity

CTL:

cytotoxic T cell

DC:

dendritic cell

HSC:

hematopoietic stem cell

IFN:

interferon

IL:

interleukin

MHC:

major histocompatibility complex

NET:

neutrophil extracellular trap

NK:

natural killer

PBL:

peripheral blood leukocytes

rb:

reviewed by

TCR:

T-cell receptor

Th:

T helper

References/Further Reading (Suggested Reviews in Bold)

  • Abel AM, Yang C, Thakar MS, Malarkannan S (2018) Natural killer cells: development, maturation, and clinical utilization. Front Immunol 9. doi: https://doi.org/10.3389/fimmu.2018.01869

  • Akula S, Mohammadamin S, Hellman L (2014) Fc receptors for immunoglobulins and their appearance during vertebrate evolution. PLoS One 9(5):e96903. https://doi.org/10.1371/journal.pone.0096903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alejo A, Tafalla C (2011) Chemokines in teleost fish species. Dev Comp Immunol 35(12):1215–1222

    CAS  PubMed  Google Scholar 

  • Aliahmad P, De La Torre B, Kaye J (2010) Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue–inducer cell and NK cell lineages. Nat Immunol 11(10):945–952

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D, Romagné F (2006) Human NK cell education by inhibitory receptors for MHC class I. Immunity 25(2):331–342

    CAS  PubMed  Google Scholar 

  • Bailey C, Segner H, Wahli T, Tafalla C (2020) Back from the brink: alterations in B- and T-cell responses modulate recovery of rainbow trout from chronic immunopathological Tetracapsuloides bryosalmonae infection. Front Immunol 11:1093. https://doi.org/10.3389/fimmu.2020.01093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajoghli B, Dick AM, Claasen A, Doll L, Aghaallaei N (2019) Zebrafish and medaka: two teleost models of T-Cell and thymic development. Int J Mol Sci 20:4179. https://doi.org/10.3390/ijms20174179

    Article  CAS  PubMed Central  Google Scholar 

  • Barrow AD, Martin CJ, Colonna M (2019) The natural cytotoxicity receptors in health and disease. Front Immunol 10:909. https://doi.org/10.3389/fimmu.2019.00909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielek E (1988) Ultrastructural analysis of leucocyte interaction with tumour targets in a teleost, Cyprinus carpio L. Dev Comp Immunol 12(4):809–821

    CAS  PubMed  Google Scholar 

  • Bird S, Tafalla C (2015) Teleost chemokines and their receptors. Biology 4(4):756–784

    Google Scholar 

  • Bishop GR, Taylor S, Jaso-Friedmann L, Evans DL (2002) Mechanisms of nonspecific cytotoxic cell regulation of apoptosis: cytokine-like activity of Fas ligand. Fish Shellfish Immunol 13(1):47–67

    CAS  PubMed  Google Scholar 

  • Boes KM, Durham AC (2017) Bone marrow, blood cells, and the lymphoid/lymphatic system. In: Zachary JF (ed) Pathologic basis of veterinary disease (6th edn). Elsevier. DOI: https://doi.org/10.1016/B978-0-323-35775-3.00013-8.

  • Boos MD, Yokota Y, Eberl G, Kee BL (2007) Mature natural killer cell and lymphoid tissue–inducing cell development requires Id2-mediated suppression of E protein activity. J Exp Med 204(5):1119–1130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt CS, Baratin M, Yi EC, Kennedy J, Gao Z, Fox B, Haldeman B, Ostrander CD, Kaifu T, Chabannon C, Moretta A (2009) The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 206(7):1495–1503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brillantes M, Beaulieu AM (2019) Transcriptional control of natural killer cell differentiation. Immunology 156(2):111–119

    CAS  PubMed  Google Scholar 

  • Carlson HC, Sweeny PR, Tokaryk JM (1968) Demonstration of phagocytic and trephocytic activities of chicken thrombocytes by microscopy and vital staining techniques. Avian Dis 12:700–715

    CAS  PubMed  Google Scholar 

  • Carmona SJ, Teichmann SA, Ferreira L, Macaulay IC, Stubbington MJ, Cvejic A, Gfeller D (2017) Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types. Gen Res 27(3):451–461

    CAS  Google Scholar 

  • Carotta S, Pang SHM, Nutt SL, Belz GT (2011) Identification of the earliest NK-cell precursor in the mouse BM. Blood 117(20):5449–5452

    CAS  PubMed  Google Scholar 

  • Carrillo-Bustamante P, Keşmir C, de Boer RJ (2016) The evolution of natural killer cell receptors. Immunogenetics 68(1):3–18

    CAS  PubMed  Google Scholar 

  • Castro R, Abós B, Pignatelli J, von Gersdorff JL, González Granja A, Buchmann K, Tafalla C (2014) Early immune responses in rainbow trout liver upon viral hemorrhagic septicemia virus (VHSV) infection. PLoS One 9(10):e111084. https://doi.org/10.1371/journal.pone.0111084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T (2009) Maturation of mouse NK cells is a 4-stage developmental program. Blood 113(22):5488–5496

    CAS  PubMed  Google Scholar 

  • Cuoghi B, Mola L (2007) Microglia of teleosts: facing a challenge in neurobiology. Eur J Histochem 51(4):231–240

    CAS  PubMed  Google Scholar 

  • Curtsinger JM, Schmidt CS, Mondino A, Lins DC, Kedl RM, Jenkins MK, Mescher MF (1999) Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J Immunol 162(6):3256–3262

    CAS  PubMed  Google Scholar 

  • Dejean AS, Joulia E, Walzer T (2019) The role of Eomes in human CD4 T-cell differentiation: a question of context. Eur J Immunol 49(1):38–41

    CAS  PubMed  Google Scholar 

  • Deshmukh S, Kania PW, Chettri JK, Skov J, Bojesen AM, Dalsgaard I, Buchmann K (2013) Insight from molecular, pathological, and immunohistochemical studies on cellular and humoral mechanisms responsible for vaccine-induced protection of rainbow trout against Yersinia ruckeri. Clin Vaccine Immunol 20(10):1623–1641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Di Vito C, Mikulak J, Mavilio D (2019) On the way to become a natural killer cell. Front Immunol 10:1812. https://doi.org/10.3389/fimmu.2019.01812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dijkstra JM, Takizawa F, Fischer U, Friedrich M, Soto-Lampe V, Lefevre C, Lenk M, Matsui T, Hasimoto K (2014) Identification of a gene for an ancient cytokine, interleukin 15-like, in mammals; interleukins 2 and 15 co-evolved with this third family member, all sharing binding motifs for IL-15Ralpha. Immunogenetics 66(2):93–103

    CAS  PubMed  Google Scholar 

  • Dogra P, Rancan C, Ma W, Toth M, Senda T, Carpenter DJ, Kubota M, Matsumoto R, Thapa P, Szabo PA, Poon MML (2020) Tissue determinants of human NK cell development, function, and residence. Cell 180(4):749–763

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dotiwala F, Mulik S, Polidoro RB, Ansara JA, Burleigh BA, Walch M, Gazzinelli RT, Lieberman J (2016) Killer lymphocytes use granulysin, perforin and granzymes to kill intracellular parasites. Nat Med 22(2):210–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esteban MÁ, Cuesta A, Chaves-Pozo E, Meseguer J (2015) Phagocytosis in teleosts. Implications of the new cells involved. Biology (Basel) 4(4):907–922

    Google Scholar 

  • Evans DL, Jaso-Friedmann L, Smith EE, St John A, Koren HS, Harris DT (1988) Identification of a putative antigen receptor on fish nonspecific cytotoxic cells with monoclonal antibodies. J Immunol 141(1):324–332

    CAS  PubMed  Google Scholar 

  • Evans DL, Leary JH III, Jaso-Friedmann L (1999) An antigen receptor (NCCRP-1) on nonspecific cytotoxic cells is a phosphoprotein associated with the JAK–STAT activation pathway. Cell Signal 11(4):287–292

    CAS  PubMed  Google Scholar 

  • Evans DL, Leary JH III, Jaso-Friedmann L (2001) Nonspecific cytotoxic cells and innate immunity: regulation by programmed cell death. Dev Comp Immunol 25(8–9):791–805

    CAS  PubMed  Google Scholar 

  • Faisal M, Ahmed II, Peters G, Cooper EL (1989) Natural cyto-toxicity of tilapia leukocytes. Dis Aquat Organ 7(1):17–22

    Google Scholar 

  • Fänge R (1992) Fish blood cells. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol XII, part B, The cardiovascular system. Academic, New York, pp 1–54

    Google Scholar 

  • Fischer U, Ototake M, Nakanishi T (1998) Killing of isogeneic erythrocytes by neutrophils in ginbuna crucian carp (Carassius auratus langsdorfii). Fish Shellfish Immunol 8:531–544

    Google Scholar 

  • Fischer U, Dijkstra JM, Köllner B, Kiryu I, Koppang EO, Hordvik I, Sawamoto Y, Ototake M (2005) The ontogeny of MHC class I expression in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 18:49–60

    CAS  PubMed  Google Scholar 

  • Fischer U, Koppang EO, Nakanishi T (2013) Teleost T and NK cell immunity. Fish Shellfish Immunol 35(2):197–206

    CAS  PubMed  Google Scholar 

  • Flajnik MF, Tlapakova T, Criscitiello MF, Krylov V, Ohta Y (2012) Evolution of the B7 family: co-evolution of B7H6 and NKp30, identification of a new B7 family member, B7H7, and of B7’s historical relationship with the MHC. Immunogenetics 64(8):571–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freud AG, Mundy-Bosse BL, Yu J, Caligiuri MA (2017) The broad spectrum of human natural killer cell diversity. Immunity 47(5):820–833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Germain R (2002) T-cell development and the CD4–CD8 lineage decision. Nat Rev Immunol 2:309–322

    CAS  PubMed  Google Scholar 

  • Goh W, Huntington ND (2017) Regulation of murine natural killer cell development. Front Immunol 8:130. https://doi.org/10.3389/fimmu.2017.00130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez Román VR, Murray JC, Weiner LM (2014) Chapter 1 - Antibody-dependent cellular cytotoxicity (ADCC). In: Ackerman ME, Nimmerjahn F (eds) Antibody Fc. Academic, pp 1–27

    Google Scholar 

  • Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S, Sun JC, Lindsten T, Reiner SL (2012) The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36(1):55–67

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gotthardt D, Sexl V (2017) STATs in NK-cells: the good, the bad, and the ugly. Front Immunol 7:694. https://doi.org/10.3389/fimmu.2016.00694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenlee AR, Brown RA, Ristow SS (1991) Nonspecific cytotoxic cells of rainbow trout (Oncorhynchus mykiss) kill YAC-1 targets by both necrotic and apoptic mechanisms. Dev Comp Immunol 15(3):153–164

    CAS  PubMed  Google Scholar 

  • Grégoire C, Chasson L, Luci C, Tomasello E, Geissmann F, Vivier E, Walzer T (2007) The trafficking of natural killer cells. Immunol Rev 220(1):169–182

    PubMed  PubMed Central  Google Scholar 

  • Griffith JW, Sokol CL, Luster AD (2014) Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol 32(1):659–702

    CAS  PubMed  Google Scholar 

  • Gullberg U, Andersson E, Garwicz D, Lindmark A, Olsson I (1997) Biosynthesis, processing and sorting of neutrophil proteins: insight into neutrophil granule development. Eur J Haematol 58:137–153

    CAS  PubMed  Google Scholar 

  • Guslund NC, Solbakken MH, Brieuc MSO, Jentoft S, Jakobsen KS, Qiao S-W (2020) Single-cell transcriptome profiling of immune cell repertoire of the atlantic cod which naturally lacks the major histocompatibility class II system. Front Immunol 11:559555. https://doi.org/10.3389/fimmu.2020.559555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamdan TA, Lang PA, Lang KS (2020) The diverse functions of the ubiquitous Fcγ receptors and their unique constituent, FcRγ subunit. Pathogens 9(2):140. https://doi.org/10.3390/pathogens9020140

    Article  CAS  PubMed Central  Google Scholar 

  • Havixbeck JJ, Barreda DR (2015) Neutrophil development, migration, and function in teleost fish. Biology (Basel) 4(4):715–734

    Google Scholar 

  • Havixbeck JJ, Rieger AM, Churchill LJ, Barreda DR (2017) Neutrophils exert protection in early aeromonas veronii infections through the clearance of both bacteria and dying macrophages. Fish Shellfish Immunol 63:18–30

    CAS  PubMed  Google Scholar 

  • Hayakawa Y, Smyth MJ (2006) CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 176(3):1517–1524

    CAS  PubMed  Google Scholar 

  • Hayden BJ, Laux DC (1985) Cell-mediated lysis of murine target cells by nonimmune salmonid lymphoid preparations. Dev Comp Immunol 9(4):627–639

    CAS  PubMed  Google Scholar 

  • He Y, Tian Z (2017) NK cell education via nonclassical MHC and non-MHC ligands. Cell Mol Immunol 14(4):321–330

    CAS  PubMed  Google Scholar 

  • He S, Chen J, Jiang Y, Wu Y, Zhu L, Jin W, Zhao C, Yu T, Wang T, Wu S, Lin X, Qu JY, Wen Z, Zhang W, Xu J (2018) Adult zebrafish Langerhans cells arise from hematopoietic stem/progenitor cells. elife 7:e36131

    PubMed  PubMed Central  Google Scholar 

  • Heinecke RD, Chettri JK, Buchmann K (2014) Adaptive and innate immune molecules in developing rainbow trout, Oncorhynchus mykiss eggs and larvae: expression of genes and occurrence of effector molecules. Fish Shellfish Immunol 38:25–33

    CAS  PubMed  Google Scholar 

  • Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM (2008) IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J Immunol 181(12):8576–8584

    CAS  PubMed  Google Scholar 

  • Hewitt EW (2003) The MHC class I antigen presentation pathway: strategies for viral immune evasion. Immunology 110(2):163–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hodgkinson JW, Ge JQ, Katzenback BA, Havixbeck JJ, Barreda DR, Stafford JL, Belosevic M (2015) Development of an in vitro model system to study the interactions between Mycobacterium marinum and teleost neutrophils. Dev Comp Immunol 53(2):349–357

    CAS  PubMed  Google Scholar 

  • Hogan RJ, Stuge TB, Clem LW, Miller NW, Chinchar VG (1996) Anti-viral cytotoxic cells in the channel catfish (Ictalurus punctatus). Dev Comp Immunol 20(2):115–127

    CAS  PubMed  Google Scholar 

  • Hogan RJ, Taylor WR, Cuchens MA, Naftel JP, Clem LW, Miller NW, Chinchar VG (1999) Induction of target cell apoptosis by channel catfish cytotoxic cells. Cell Immunol 195(2):110–118

    CAS  PubMed  Google Scholar 

  • Höglund P, Brodin P (2010) Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol 10(10):724–734

    PubMed  Google Scholar 

  • Huang XZ, Li YW, Mai YZ, Luo XC, Dan XM, Li AX (2014) Molecular cloning of NCCRP-1 gene from orange-spotted grouper (Epinephelus coioides) and characterization of NCCRP-1+ cells post Cryptocaryon irritans infection. Dev Comp Immunol 46(2):267–278

    CAS  PubMed  Google Scholar 

  • Huntington ND, Vosshenrich CA, Di Santo JP (2007) Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat Rev Immunol 7(9):703–714

    CAS  PubMed  Google Scholar 

  • Jaeschke H, Hasegawa T (2006) Role of neutrophils in acute inflammatory liver injury. Liver Int 26(8):912–919

    CAS  PubMed  Google Scholar 

  • Jaso-Friedmann L, Leary JH III, Warren J, McGraw RA, Evans DL (1997) Molecular characterization of a protozoan parasite target antigen recognized by nonspecific cytotoxic cells. Cell Immunol 176(2):93–102

    CAS  PubMed  Google Scholar 

  • Jaso-Friedmann L, Leary JH III, Evans DL (2001) The non-specific cytotoxic cell receptor (NCCRP-1): molecular organization and signaling properties. Dev Comp Immunol 25(8–9):701–711

    CAS  PubMed  Google Scholar 

  • Kallio H, Tolvanen M, Jänis J, Pan PW, Laurila E, Kallioniemi A, Kilpinen S, Tuominen VJ, Isola J, Valjakka J (2011) Characterization of non-specific cytotoxic cell receptor protein 1: a new member of the lectin-type subfamily of F-box proteins. PLoS One 6(11):e27152. https://doi.org/10.1371/journal.pone.0027152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kärre K (2002) A perfect mismatch. Science 295(5562):2029–2031

    PubMed  Google Scholar 

  • Katzenback BA, Katakura F, Belosevic M (2012) Regulation of teleost macrophage and neutrophil cell development by growth factors and transcription factors, new advances and contributions to fish biology, Hakan Türker, IntechOpen, doi:https://doi.org/10.5772/53589. https://www.intechopen.com/books/new-advances-and-contributions-to-fish-biology/regulation-of-fish-macrophage-and-neutrophil-cell-development-by-growth-factors-and-transcription-fa

  • Kaufmann SHE, Dorhoi A (2016) Molecular determinants in phagocyte-bacteria interactions. Immunity 44(3):476–491

    CAS  PubMed  Google Scholar 

  • Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet 1(2):129–139. https://doi.org/10.1371/journal.pgen.0010027

    Article  CAS  PubMed  Google Scholar 

  • Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, Astemborski J, Cheng J, Goedert JJ, Vlahov D, Hilgartner M, Cox S (2004) HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305(5685):872–874

    CAS  PubMed  Google Scholar 

  • Kobayashi I, Katakura F, Moritomo T (2016) Isolation and characterization of hematopoietic stem cells in teleost fish. Dev Comp Immunol 58:86–94

    CAS  PubMed  Google Scholar 

  • Korhonen R, Lahti A, Kankaanranta H, Moilanen E (2005) Nitric oxide production and signaling in inflammation. Curr Drug Targets Inflamm Allergy 4(4):471–479

    CAS  PubMed  Google Scholar 

  • Kortum AN, Rodriguez-Nunez I, Yang J, Shim J, Runft D, O’Driscoll ML, Haire RN, Cannon JP, Turner PM, Litman RT, Kim CH (2014) Differential expression and ligand binding indicate alternative functions for zebrafish polymeric immunoglobulin receptor (pIgR) and a family of pIgR-like (PIGRL) proteins. Immunogenetics 66(4):267–279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Dikshit M (2019) Metabolic insight of neutrophils in health and disease. Front Immunol 10:2099. https://doi.org/10.3389/fimmu.2019.02099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari J, Bøgwald J, Dalmo RA (2013) Eomesodermin of Atlantic salmon: an important regulator of cytolytic gene and interferon gamma expression in spleen lymphocytes. PLoS One 8(2):e55893. https://doi.org/10.1371/journal.pone.0055893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurata O, Okamoto N, Ikeda Y (1995) Neutrophilic granulocytes in carp, Cyprinus carpio, possess a spontaneous cytotoxic activity. Dev Comp Immunol 19:315–325

    CAS  PubMed  Google Scholar 

  • Leal E, Granja AG, Zarza C, Tafalla C (2016) Distribution of T cells in rainbow trout (Oncorhynchus mykiss) skin and responsiveness to viral infection. PLoS One 11(1):e0147477. https://doi.org/10.1371/journal.pone.0147477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonard WJ, Lin JX, O'Shea JJ (2019) The γc family of cytokines: basic biology to therapeutic ramifications. Immunity 50(4):832–850

    CAS  PubMed  Google Scholar 

  • Li W (2012) Eat-me signals: keys to molecular phagocyte biology and “appetite” control. J Cell Physiol 227(4):1291–1297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, Lapatra S, Tort L, Sunyer JO (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124

    CAS  PubMed  Google Scholar 

  • Li Z, Zhang N, Ma L, Zhang L, Meng G, Xia C (2020) The mechanism of β2m molecule-induced changes in the peptide presentation profile in a bony fish. iScience 23(5):101119. https://doi.org/10.1016/j.isci.2020.101119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Kuick R, Hanash S, Richardson B (2009) DNA methylation inhibition increases T cell KIR expression through effects on both promoter methylation and transcription factors. Clin Immunol 130(2):213–224

    CAS  PubMed  Google Scholar 

  • Long EO (2008) Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev 224(1):70–84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lukácsi S, Mácsik-Valent B, Nagy-Baló Z, Kovács KG, Kliment K, Bajtay Z, Erdei A (2020) Utilization of complement receptors in immune cell-microbe interaction. FEBS Lett 594(16):2695–2713

    PubMed  Google Scholar 

  • Ma D, Wei Y, Liu F (2013) Regulatory mechanisms of thymus and T cell development. Dev Comp Immunol 39/1–2(102):91

    Google Scholar 

  • Male V, Nisoli I, Kostrzewski T, Allan DS, Carlyle JR, Lord GM, Wack A, Brady HJ (2014) The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J Exp Med 211(4):635–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Malek TR, Bayer AL (2004) Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol 4(9):665–674

    CAS  PubMed  Google Scholar 

  • Martínez-Riaño A, Bovolenta ER, Mendoza P, Oeste CL, Martín-Bermejo MJ, Bovolenta P, Turner M, Martínez-Martín N, Alarcón B (2018) Antigen phagocytosis by B cells is required for a potent humoral response. EMBO Rep 19(9):e46016

    PubMed  PubMed Central  Google Scholar 

  • McKinney EC, Schmale MC (1997) Damselfish with neurofibromatosis exhibit cytotoxicity towards retrovirus-infected cells. Dev Comp Immunol 21(3):287–298

    CAS  PubMed  Google Scholar 

  • Meazza R, Azzarone B, Orengo AM, Ferrini S (2011) Role of common-gamma chain cytokines in NK cell development and function: perspectives for immunotherapy. J Biomed Biotechnol 2011:861920. https://doi.org/10.1155/2011/861920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, Hammerbeck CD, Popescu F, Xiao Z (2006) Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 211:81–92

    CAS  PubMed  Google Scholar 

  • Meseguer J, Esteban MA, Lopez-ruiz A, Bielek E (1994) Ultrastructure of nonspecific cytotoxic cells in teleosts. I. Effector-target cell binding in a marine and a freshwater species (Seabream: Sparus aurata L., and Carp: Cyprinus carpio L.). Anat Rec 239(4):468–474

    CAS  PubMed  Google Scholar 

  • Meseguer J, Esteban MA, Rodríguez A (2002) Are thrombocytes and platelets true phagocytes? Microsc Res Tech 57(6):491–497

    PubMed  Google Scholar 

  • Metchnikoff E (1883) Untersuchungen ueber die mesodermalen Phagocyten einiger Wirbeltiere. Biologisches Centralblatt 3:560–565

    Google Scholar 

  • Moller AM, Korytar T, Kollner B, Schmidt-Posthaus H, Segner H (2014) The teleostean liver as an immunological organ: Intrahepatic immune cells (IHICs) in healthy and benzo[a]pyrene challenged rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 46:518–529

    CAS  PubMed  Google Scholar 

  • Moore FE, Garcia EG, Lobbardi R, Jain E, Tang Q, Moore JC, Cortes M, Molodtsov A, Kasheta M, Luo CC, Garcia AJ (2016) Single-cell transcriptional analysis of normal, aberrant, and malignant hematopoiesis in zebrafish. J Exp Med 213(6):979–992

    PubMed  PubMed Central  Google Scholar 

  • Muire PJ, Hanson LA, Wills R, Petrie-Hanson L (2017) Differential gene expression following TLR stimulation in rag1−/−mutant zebrafish tissues and morphological descriptions of lymphocyte-like cell populations. PLoS One 12(9):e0184077. https://doi.org/10.1371/journal.pone.0184077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy K, Weaver C (2017) Janeway’s immunobiology (9th edn). Taylor & Francis; Garland Science. ISBN 10: 0815345054 ISBN 13: 9780815345053

    Google Scholar 

  • Nagasawa T, Nakayasu C, Rieger AM, Barreda DR, Somamoto T, Nakao M (2014) Phagocytosis by thrombocytes is a conserved innate immune mechanism in lower vertebrates. Front Immunol 5:445. https://doi.org/10.3389/fimmu.2014.00445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakanishi T, Ototake M (1999) The graft-versus-host reaction (GVHR) in the ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 23(1):15–26

    CAS  PubMed  Google Scholar 

  • Nakanishi T, Shibasaki Y, Matsuura Y (2015) T cells in fish. Biology (Basel) 4(4):640–663

    CAS  Google Scholar 

  • Nelson BH (2004) IL-2, regulatory T cells, and tolerance. J Immunol 172(7):3983–3988

    CAS  PubMed  Google Scholar 

  • Neumann A, Brogden G, von Köckritz-Blickwede M (2020) Extracellular traps: an ancient weapon of multiple kingdoms. Biology (Basel) 9(2):34. https://doi.org/10.3390/biology9020034

    Article  CAS  Google Scholar 

  • Ohashi K, Takizawa F, Tokumaru N, Nakayasu C, Toda H, Fischer U, Moritomo T, Hashimoto K, Nakanishi T, Dijkstra JM (2010) A molecule in teleost fish, related with human MHC-encoded G6F, has a cytoplasmic tail with ITAM and marks the surface of thrombocytes and in some fishes also of erythrocytes. Immunogenetics 62(8):543–559

    CAS  PubMed  Google Scholar 

  • Oliveira THC, Marques PE, Proost P, Teixeira MMM (2018) Neutrophils: a cornerstone of liver ischemia and reperfusion injury. Lab Investig 98(1):51–62

    PubMed  Google Scholar 

  • Ouyang W, O'Garra A (2019) IL-10 family cytokines IL-10 and IL-22: from basic science to clinical translation. Immunity 50(4):871–891

    CAS  PubMed  Google Scholar 

  • Palić D, Ostojić J, Andreasen CB, Roth JA (2007) Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev Comp Immunol 31:805–816

    PubMed  Google Scholar 

  • Paolini R, Bernardini G, Molfetta R, Santoni A (2015) NK cells and interferons. Cytokine Growth Factor Rev 26(2):113–120

    CAS  PubMed  Google Scholar 

  • Parra D, Rieger AM, Li J, Zhang YA, Randall LM, Hunter CA, Barreda DR, Sunyer JO (2012) Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. J Leukoc Biol 91(4):525–536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pegram HJ, Andrews DM, Smyth MJ, Darcy PK, Kershaw MH (2011) Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol 89(2):216–224

    PubMed  Google Scholar 

  • Philip AM, Wang Y, Mauro A, El-Rass S, Marshall JC, Lee WL, Slutsky AS, dosSantos CC, Wen XY (2017) Development of a zebrafish sepsis model for high-throughput drug discovery. Mol Med 23:134–148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Picchietti S, Guerra L, Buonocore F, Randelli E, Fausto AM, Abelli L (2009) Lymphocyte differentiation in sea bass thymus: CD4 and CD8-alpha gene expression studies. Fish Shellfish Immunol 27(1):50–56

    CAS  PubMed  Google Scholar 

  • Pignatelli J, Castro R, González Granja A, Abós B, González L, Jensen LB, Tafalla C (2014) Immunological characterization of the teleost adipose tissue and its modulation in response to viral infection and fat-content in the diet. PLoS One 9(10):e110920. https://doi.org/10.1371/journal.pone.0110920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pijanowski L, Golbach L, Kolaczkowska E, Scheer M, Verburg-van Kemenade BML, Chadzinska M (2013) Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways. Fish Shellfish Immunol 34:1244–1252

    CAS  PubMed  Google Scholar 

  • Pipkin M, Sacks JA, Cruz-Guilloty F, Lichtenheld MG, Bevan MJ, Rao A (2010) Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32(1):79–90

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prager I, Watzl C (2019) Mechanisms of natural killer cell-mediated cellular cytotoxicity. J Leukoc Biol 105(6):1319–1329

    CAS  PubMed  Google Scholar 

  • Prajsnar TK, Hamilton R, Garcia-Lara J, McVicker G, Williams A, Boots M, Foster SJ, Renshaw SA (2012) A privileged intraphagocyte niche is responsible for disseminated infection of Staphylococcus aureus in a zebrafish model. Cell Microbiol 14(10):1600–1619

    CAS  PubMed  PubMed Central  Google Scholar 

  • Praveen K, Evans DL, Jaso-Friedmann L (2004) Evidence for the existence of granzyme-like serine proteases in teleost cytotoxic cells. J Mol Evol 58(4):449–459

    CAS  PubMed  Google Scholar 

  • Praveen K, Leary Iii JH, Evans DL, Jaso-Friedmann L (2006) Nonspecific cytotoxic cells of teleosts are armed with multiple granzymes and other components of the granule exocytosis pathway. Mol Immunol 43(8):1152–1162

    CAS  PubMed  Google Scholar 

  • Pritchard GH, Kedl RM, Hunter CA (2019) The evolving role of T-bet in resistance to infection. Nat Rev Immunol 19(6):398–410

    CAS  PubMed  PubMed Central  Google Scholar 

  • Purdy AK, Campbell KS (2009) Natural killer cells and cancer: regulation by the killer cell Ig-like receptors (KIR). Cancer Biol Ther 8(23):2209–2218

    CAS  Google Scholar 

  • Rahim MM, Tu MM, Mahmoud AB, Wight A, Abou-Samra E, Lima PD, Makrigiannis AP (2014) Ly49 receptors: innate and adaptive immune paradigms. Front Immunol 5:145. https://doi.org/10.3389/fimmu.2014.00145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiners KS, Topolar D, Henke A, Simhadri VR, Kessler J, Sauer M, Bessler M, Hansen HP, Tawadros S, Herling M, Krönke M (2013) Soluble ligands for NK cell receptors promote evasion of chronic lymphocytic leukemia cells from NK cell anti-tumor activity. Blood 121(18):3658–3665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riley JL, June CH (2005) The CD28 family: A T-cell rheostat for therapeutic control of T-cell activation. Blood 105(1):13–21

    CAS  PubMed  Google Scholar 

  • Rosales C (2017) Fcγ receptor heterogeneity in leukocyte functional responses. Front Immunol 8:280. https://doi.org/10.3389/fimmu.2017.00280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosental B, Brusilovsky M, Hadad U, Oz D, Appel MY, Afergan F, Yossef R, Rosenberg LA, Aharoni A, Cerwenka A, Campbell KS (2011) Proliferating cell nuclear antigen is a novel inhibitory ligand for the natural cytotoxicity receptor NKp44. J Immunol 187(11):5693–5702

    CAS  PubMed  Google Scholar 

  • Saalmüller A, Reddehase MJ, Bühring HJ, Jonjić S, Koszinowski UH (1987) Simultaneous expression of CD4 and CD8 antigens by a substantial proportion of resting porcine T lymphocytes. Eur J Immunol 17(9):1297–1301

    PubMed  Google Scholar 

  • Sakata H, Savan R, Sogabe R, Kono T, Taniguchi K, Gunimaladevi I, Tassakka AC, Sakai M (2005) Cloning and analysis of non-specific cytotoxic cell receptor (NCCRP)-1 from common carp Cyprinus carpio L. Comp Biochem Physiol C Toxicol Pharmacol 140(3–4):287–294

    PubMed  Google Scholar 

  • Santourlidis S, Trompeter HI, Weinhold S, Eisermann B, Meyer KL, Wernet P, Uhrberg M (2002) Crucial role of DNA methylation in determination of clonally distributed killer cell Ig-like receptor expression patterns in NK cells. J Immunol 169(8):4253–4261

    CAS  PubMed  Google Scholar 

  • Sasaki Y, Maita M, Okamoto N (2002) Rainbow trout neutrophils are responsible for non-specific cytotoxicity. Fish Shellfish Immunol 12(3):243–252

    PubMed  Google Scholar 

  • Sepahi A, Tacchi L, Casadei E, Takizawa F, LaPatra SE, Salinas I (2017) CK12a, a CCL19-like chemokine that orchestrates both nasal and systemic antiviral immune responses in rainbow trout. J Immunol 199(11):3900–3913

    CAS  PubMed  Google Scholar 

  • Sepahi A, Kraus A, Casadei E, Johnston CA, Galindo-Villegas J, Kelly C, García-Moreno D, Muñoz P, Mulero V, Huertas M, Salinas I (2019) Olfactory sensory neurons mediate ultrarapid antiviral immune responses in a TrkA-dependent manner. Proc Natl Acad Sci U S A 116(25):12428–12436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen L, Stuge TB, Zhou H, Khayat M, Barker KS, Quiniou SM, Wilson M, Bengtén E, Chinchar VG, Clem LW, Miller NW (2002) Channel catfish cytotoxic cells: a mini-review. Dev Comp Immunol 26(2):141–149

    CAS  PubMed  Google Scholar 

  • Shen L, Stuge TB, Evenhuis JP, Bengtén E, Wilson M, Chinchar VG, Clem LW, Miller NW (2003) Channel catfish NK-like cells are armed with IgM via a putative FcμR. Dev Comp Immunol 27(8):699–714

    CAS  PubMed  Google Scholar 

  • Shen L, Stuge TB, Bengtén E, Wilson M, Chinchar VG, Naftel JP, Bernanke JM, Clem LW, Miller NW (2004) Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev Comp Immunol 28(2):139–152

    CAS  PubMed  Google Scholar 

  • Shen XF, Cao K, Jiang JP, Guan WX, Du JF (2017) Neutrophil dysregulation during sepsis: an overview and update. J Cell Mol Med 21:1687–1697

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shibasaki Y, Toda H, Kobayashi I, Moritomo T, Nakanishi T (2010) Kinetics of CD4+ and CD8alpha+ T-cell subsets in graft-versus-host reaction (GVHR) in ginbuna crucian carp Carassius auratus langsdorfii. Dev Comp Immunol 34(10):1075–1081

    CAS  PubMed  Google Scholar 

  • Shifrin N, Raulet DH, Ardolino M (2014). NK cell self tolerance, responsiveness and missing self recognition. In Seminars in immunology (Vol. 26(2), pp. 138-144). Academic.

    Google Scholar 

  • Shwartz A, Goessling W, Yin C (2019) Macrophages in zebrafish models of liver diseases. Front Immunol 10:2840. https://doi.org/10.3389/fimmu.2019.02840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sim GC, Radvanyi L (2014) The IL-2 cytokine family in cancer immunotherapy. Cytokine Growth Factor Rev 25(4):377–390

    CAS  PubMed  Google Scholar 

  • Simonetta F, Pradier A, Roosnek E (2016) T-bet and eomesodermin in NK cell development, maturation, and function. Front Immunol 7:241. https://doi.org/10.3389/fimmu.2016.00241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh NK, Riley TP, Baker SCB, Borrman T, Weng Z, Baker BM (2017) Emerging concepts in TCR specificity: rationalizing and (maybe) predicting outcomes. J Immunol 199(7):2203–2213

    CAS  PubMed  Google Scholar 

  • Somamoto T, Kondo M, Nakanishi T, Nakao M (2014) Helper function of CD4(+) lymphocytes in antiviral immunity in ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 44(1):111–115

    CAS  PubMed  Google Scholar 

  • Soong J, Soni N (2012) Sepsis: recognition and treatment. Clin Med (Lond) 12(3):276–280

    CAS  Google Scholar 

  • Stafford JL, Wilson M, Nayak D, Quiniou SM, Clem LW, Miller NW, Bengtén E (2006) Identification and characterization of a FcR homolog in an ectothermic vertebrate, the channel catfish (Ictalurus punctatus). J Immunol 177(4):2505–2517

    CAS  PubMed  Google Scholar 

  • Stosik M, Tokarz-Deptuła B, Deptuła W (2019) Characterisation of thrombocytes in osteichthyes. J Vet Res 63(1):123–131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stuge TB, Miller NW, Clem LW (1995) Channel catfish cytotoxic effector cells from peripheral blood and pronephroi are different. Fish Shellfish Immunol 5(6):469–471

    Google Scholar 

  • Stuge TB, Wilson MR, Zhou H, Barker KS, Bengtén E, Chinchar G, Miller NW, Clem LW (2000) Development and analysis of various clonal alloantigen-dependent cytotoxic cell lines from channel catfish. J Immunol 164(6):2971–2977

    CAS  PubMed  Google Scholar 

  • Sun JC, Lanier LL (2011) NK cell development, homeostasis and function: parallels with CD8+ T cells. Nat Rev Immunol 11(10):645–657

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tafalla C, Granja AG (2018) Novel insights on the regulation of B cell functionality by members of the tumor necrosis factor superfamily in jawed fish. Front Immunol 9:1285. https://doi.org/10.3389/fimmu.2018.01285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takizawa F, Dijkstra JM, Kotterba P, Korytár T, Kock H, Köllner B, Jaureguiberry B, Nakanishi T, Fischer U (2011) The expression of CD8α discriminates distinct T cell subsets in teleost fish. Dev Comp Immunol 35(7):752–763

    CAS  PubMed  Google Scholar 

  • Takizawa F, Araki K, Ohtani M, Toda H, Saito Y, Lampe VS, Dijkstra JM, Ototake M, Moritomo T, Nakanishi T, Fischer U (2014) Transcription analysis of two Eomesodermin genes in lymphocyte subsets of two teleost species. Fish Shellfish Immunol 36(1):215–222

    CAS  PubMed  Google Scholar 

  • Takizawa F, Magadan S, Parra D, Xu Z, Korytář T, Boudinot P, Sunyer JO (2016) Novel teleost CD4-bearing cell populations provide insights into the evolutionary origins and primordial roles of CD4+ lymphocytes and CD4+ macrophages. J Immunol 196(11):4522–4535

    CAS  PubMed  Google Scholar 

  • Tang Q, Iyer S, Lobbardi R, Moore JC, Chen H, Lareau C, Hebert C, Shaw ML, Neftel C, Suva ML, Ceol CJ (2017) Dissecting hematopoietic and renal cell heterogeneity in adult zebrafish at single-cell resolution using RNA sequencing. J Exp Med 214(10):2875–2887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor EB, Moulana M, Stuge TB, Quiniou SM, Bengten E, Wilson M (2016) A leukocyte immune-type receptor subset is a marker of antiviral cytotoxic cells in channel catfish, Ictalurus punctatus. J Immunol 196(6):2677–2689

    CAS  PubMed  Google Scholar 

  • Taylor EB, Chinchar VG, Quiniou SMS, Wilson M, Bengtén E (2020) Cloning and characterization of antiviral cytotoxic T lymphocytes in channel catfish, Ictalurus punctatus. Virology 540:184–194

    CAS  PubMed  Google Scholar 

  • Toda H, Saito Y, Koike T, Takizawa F, Araki K, Yabu T, Somamoto T, Suetake H, Suzuki Y, Ototake M, Moritomo T, Nakanishi T (2011) Conservation of characteristics and functions of CD4 positive lymphocytes in a teleost fish. Dev Comp Immunol 35(6):650–660

    CAS  PubMed  Google Scholar 

  • Torraca V, Otto NA, Tavakoli-Tameh A, Meijer AH (2017) The inflammatory chemokine Cxcl18b exerts neutrophil-specific chemotaxis via the promiscuous chemokine receptor Cxcr2 in zebrafish. Dev Comp Immunol 67:57–65

    CAS  PubMed  Google Scholar 

  • Ueno N, Wilson ME (2012) Receptor-mediated phagocytosis of Leishmania: implications for intracellular survival. Trends Parasitol 28(8):335–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van AP, Álvarez de Haro N, Bron JE, Desbois AP (2020) Chromatin extracellular trap release in rainbow trout, Oncorhynchus mykiss (Walbaum, 1792). Fish Shellfish Immunol 99:227–238

    Google Scholar 

  • Virella G (2007) Medical immunology. Informa Healthcare USA Inc. edited by Gabriel Virella. ISBN-13: 978-0-8493-9696-0.

    Google Scholar 

  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9(5):503–510

    CAS  PubMed  Google Scholar 

  • Voskoboinik I, Whisstock J, Trapani J (2015) Perforin and granzymes: function, dysfunction and human pathology. Nat Rev Immunol 15:388–400

    CAS  PubMed  Google Scholar 

  • Walch M, Dotiwala F, Mulik S, Thiery J, Kirchhausen T, Clayberger C, Krensky AM, Martinvalet D, Lieberman J (2014) Cytotoxic cells kill intracellular bacteria through granulysin-mediated delivery of granzymes. Cell 157(6):1309–1323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waldhauer I, Steinle A (2008) NK cells and cancer immunosurveillance. Oncogene 27(45):5932–5943

    CAS  PubMed  Google Scholar 

  • Waldmann TA (2006) The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 6(8):595–601

    CAS  PubMed  Google Scholar 

  • Walzer T, Chiossone L, Chaix J, Calver A, Carozzo C, Garrigue-Antar L, Jacques Y, Baratin M, Tomasello E, Vivier E (2007) Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat Immunol 8(12):1337–1344

    CAS  PubMed  Google Scholar 

  • Wang G, Pan L, Zhang Y (2011a) Approaches to improved targeting of DNA vaccines. Hum Vaccin 7(12):1271–1281

    CAS  PubMed  Google Scholar 

  • Wang T, Diaz-Rosales P, Costa MM, Campbell S, Snow M, Collet B, Martin SAM, Secombes CJ (2011b) Functional characterization of a nonmammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 upregulates the expression of the Th cell signature cytokines IFN-gamma, IL-10, and IL-22. J Immunol 186(2):708–721

    CAS  PubMed  Google Scholar 

  • Wang W, Erbe AK, Hank JA, Morris ZS, Sondel PM (2015) NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy. Front Immunol 6:368. https://doi.org/10.3389/fimmu.2015.00368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhang N, Wang Z, Yanan W, Zhang L, Xia C (2018a) Structural insights into the evolution feature of a bony fish CD8αα homodimer. Mol Immunol 97:109–116

    PubMed  Google Scholar 

  • Wang T, Hu Y, Wangkahart E, Liu F, Wang A, Zahran E, Maisey KR, Liu M, Xu Q, Imarai M, Secombes CJ (2018b) Interleukin (IL)-2 is a key regulator of T helper 1 and T helper 2 cytokine expression in fish: functional characterization of two divergent IL2 paralogs in salmonids. Front Immunol 9:1683. https://doi.org/10.3389/fimmu.2018.01683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Wang J, Lei L, Xu J, Qin Y, Gao Q, Zou J (2020) Characterisation of IL-15 and IL-2Rβ in grass carp: IL-15 upregulates cytokines and transcription factors of type 1 immune response and NK cell activation. Fish Shellfish Immunol 107(A):104–117

    CAS  PubMed  Google Scholar 

  • Wcisel DJ, Yoder JA (2016) The confounding complexity of innate immune receptors within and between teleost species. Fish Shellfish Immunol 53:24–34

    CAS  PubMed  Google Scholar 

  • Wei S, Zhou JM, Chen X, Shah RN, Liu J, Orcutt TM, Traver D, Djeu JY, Litman GW, Yoder JA (2007) The zebrafish activating immune receptor Nitr9 signals via Dap12. Immunogenetics 59(10):813–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilk AJ, Blish CA (2018) Diversification of human NK cells: lessons from deep profiling. J Leukoc Biol 103(4):629–641

    CAS  PubMed  Google Scholar 

  • Witten PE, Huysseune A (2009) A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev Camb Philos Soc 84(2):315–346

    PubMed  Google Scholar 

  • Wu Y, Tian Z, Wei H (2017) Developmental and functional control of natural killer cells by cytokines. Front Immunol 8:930. https://doi.org/10.3389/fimmu.2017.00930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing J, Ma J, Tang X, Sheng X, Zhan W (2017) Characterizations of CD4-1, CD4-2 and CD8β T cell subpopulations in peripheral blood leucocytes, spleen and head kidney of Japanese flounder (Paralichthys olivaceus). Mol Immunol 85:155–165

    CAS  PubMed  Google Scholar 

  • Xing J, Wang L, Zhen M, Tang X, Zhan W (2018) Variations of T and B lymphocytes of flounder (Paralichthys olivaceus) after Hirame novirhabdovirus infection and immunization. Mol Immunol 96:19–27

    CAS  PubMed  Google Scholar 

  • Yamaguchi T, Dijkstra JM (2019) Major Histocompatibility complex (MHC) genes and disease resistance in fish. Cell 8(4):378. doi: https://doi.org/10.3390/cells8040378

  • Yamaguchi T, Takizawa F, Furihata M, Soto-Lampe V, Dijkstra JM, Fischer U (2019a) Teleost cytotoxic T cells. Fish Shellfish Immunol 95:422–439

    Google Scholar 

  • Yamaguchi T, Quillet E, Boudinot P, Fischer U (2019b) What could be the mechanisms of immunological memory in fish? Fish Shellfish Immunol 85:3–8

    Google Scholar 

  • Yamaguchi T, Chang CJ, Karger AK, Keller M, Pfaff F, Wangkahart E, Wang T, Secombes CJ, Kimoto A, Furihata M, Hashimoto K, Fischer U, Dijkstra JM (2020) Ancient cytokine interleukin 15-like (IL-15L) induces a type 2 immune response. Front Immunol 11:2384. https://doi.org/10.3389/fimmu.2020.549319

    Article  CAS  Google Scholar 

  • Yamasaki M, Araki K, Nakanishi T, Nakayasu C, Yamamoto A (2014) Role of CD4(+) and CD8α(+) T cells in protective immunity against Edwardsiella tarda infection of ginbuna crucian carp, Carassius auratus langsdorfii. Fish Shellfish Immunol 36(1):299–304

    CAS  PubMed  Google Scholar 

  • Yoder JA, Litman GW (2011) The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 63(3):123–141

    CAS  PubMed  Google Scholar 

  • Yoshida SH, Stuge TB, Miller NW, Clem LW (1995) Phylogeny of lymphocyte heterogeneity: cytotoxic activity of channel catfish peripheral blood leukocytes directed against allogeneic targets. Dev Comp Immunol 19(1):71–77

    CAS  PubMed  Google Scholar 

  • Yu J, Freud AG, Caligiuri MA (2013) Location and cellular stages of natural killer cell development. Trends Immunol 34(12):573–582

    CAS  PubMed  Google Scholar 

  • Zhang YA, Hikima JI, Li J, LaPatra SE, Luo YP, Sunyer JO (2009) Conservation of structural and functional features in a primordial CD80/86 molecule from rainbow trout (Oncorhynchus mykiss), a primitive teleost fish. J Immunol 183(1):83–96

    CAS  PubMed  Google Scholar 

  • Zhao ML, Chi H, Sun L (2017) Neutrophil extracellular traps of Cynoglossus semilaevis: production characteristics and antibacterial effect. Front Immunol 8:290. https://doi.org/10.3389/fimmu.2017.00290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu LY, Lin AF, Shao T, Nie L, Dong WR, Xiang LX, Shao JZ (2014) B cells in teleost fish act as pivotal initiating APCs in priming adaptive immunity: an evolutionary perspective on the origin of the B-1 cell subset and B7 molecules. J Immunol 192(6):2699–2714

    CAS  PubMed  Google Scholar 

  • Zook EC, Li ZY, Xu Y, de Pooter RF, Verykokakis M, Beaulieu A, Lasorella A, Maienschein-Cline M, Sun JC, Sigvardsson M, Kee BL (2018) Transcription factor ID2 prevents E proteins from enforcing a naïve T lymphocyte gene program during NK cell development. Sci Immunol 3(22):eaao2139. https://doi.org/10.1126/sciimmunol.aao2139

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr Kimberly Veenstra for critical reading the manuscript of this book chapter.

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Authors and Affiliations

  1. Institute of Infectology, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany

    Uwe Fischer

  2. Faculty of Marine Science and Technology, Fukui Prefectural University, Fukui, Japan

    Fumio Takizawa

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Correspondence to Uwe Fischer .

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  1. Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C, Denmark

    Kurt Buchmann

  2. Scottish Fish Immunology Research Centre, University of Aberdeen, Aberdeen, UK

    Christopher J. Secombes

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Fischer, U., Takizawa, F. (2022). Cellular Immune Responses. In: Buchmann, K., Secombes, C.J. (eds) Principles of Fish Immunology . Springer, Cham. https://doi.org/10.1007/978-3-030-85420-1_4

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