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Identification of distinct LRC- and Fc receptor complex-like chromosomal regions in fish supports that teleost leukocyte immune-type receptors are distant relatives of mammalian Fc receptor-like molecules

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Abstract

Leukocyte immune-type receptors (LITRs) are a large family of immunoregulatory receptor-types originally identified in the channel catfish (Ictalurus punctatus (Ip)LITRs). Phylogenetic analyses of LITRs show that they share distant evolutionary relationships with important mammalian immunoregulatory receptors belonging to the Fc receptors family and the leukocyte receptor complex (LRC), but their syntenic relationships with these immunoglobulin superfamily members have not been investigated. To further examine the possible evolutionary connections between teleost LITRs and various mammalian immunoregulatory receptor-types, we surveyed the genomic databases of representative vertebrate taxa and our results show that teleost LITRs generally exist in large genomic clusters, which are linked to vangl2, arhgef11, and slam family genes, features that are also shared by amphibian and mammalian Fc receptor-like molecules (FCRLs). Moreover, detailed phylogenetic comparisons between the individual Ig-like domains of LITRs and mammalian FCRLs shows that these receptors share related Ig-like domains indicative of their common ancestry. However, contrary to our previous reports, no supportive evidence for phylogenetic relationships between the Ig-like domains of LITRs with the Ig-like domains of LRC-encoded mammalian immunoregulatory receptors was found. We also identified an LRC-like region in the zebrafish genome, but no expanded litr-related genes were located in this region. Similarly, no lilr-related genes were found in spotted gar, a representative basal ray-finned fish. Finally, two distantly related fcrls and an LRC-like gene were identified in the elephant shark genome, suggesting that the loss of an immunoregulatory receptor-containing LRC region may be unique to ray-finned fish.

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References

  • Akkaya M, Barclay AN (2013) How do pathogens drive the evolution of paired receptors? Eur J Immunol 43(2):303–313

    Article  CAS  PubMed  Google Scholar 

  • Akula S, Mohammadamin S, Hellman L (2014) Fc Receptors for Immunoglobulins and Their Appearance during Vertebrate Evolution. Plos One 9(5):e96903

  • Barrow A, Trowsdale J (2006) You say ITAM and I say ITIM, lets call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol 36(7):1646–1653

    Article  CAS  PubMed  Google Scholar 

  • Bakema JE, Egmond Mv (2011) The human immunoglobulin A Fc receptor FcαRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol 4(6):612–624

  • Barten R, Torkar M, Haude A, Trowsdale J, Wilson MJ (2001) Divergent and convergent evolution of NK-cell receptors. Trends Immunol 22(1):52–57

    Article  CAS  PubMed  Google Scholar 

  • Blackmon EL, Quiniou S, Wilson M, Bengten E (2018) Leukocyte immune-type receptor expressing cells increase in response to Edwardsiella ictaluri infection in Channel Catfish, Ictalurus punctatus. J Immun 59-4

  • Blasutig IM, New LA, Thanabalasuriar A, Dayarathna TK, Goudreault M, Quaggin SE, Li SS-C, Gruenheid S, Jones N, Pawson T (2008) Phosphorylated YDXV motifs and Nck SH2/SH3 adaptors act cooperatively to induce actin reorganization. Mol Cell Biol 28(6):2035–2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunet FG, Crollius HR, Paris M, Aury J, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23(9):1808–1816

    Article  CAS  PubMed  Google Scholar 

  • Campbell JA, Davis RS, Lilly LM, Fremont DH, French AR, Carayannopoulos LN (2010) Cutting edge: FcR-like 5 on innate B cells is targeted by a poxvirus MHC class I-like immunoevasin. J Immunol 185(1):28–32

    Article  CAS  PubMed  Google Scholar 

  • Catchen JM, Braasch I, Postlethwait JH (2011) Conserved synteny and the zebrafish genome. Methods Cell Biol 104:259–285

  • Chakraborty A, Dyer KF, Cascio M, Mietzner TA, Tweardy DJ (1999) Identification of a novel Stat3 recruitment and activation motif within the granulocyte colony-stimulating factor receptor. Blood 93(1):15–24

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Hurez V, Brockenbrough JS, Kubagawa H, Cooper MD (1999) Paternal monoallelic expression of the paired immunoglobulin-like receptors PIR-A and PIR-B. Proc Natl Acad Sci 96(12):6868–6872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conant GC (2020) The lasting after-effects of an ancient polyploidy on the genomes of teleosts. Plos One 15(4):e0231356

  • Cortes HD, Montgomery BC, Verheijen K, García-García E, Stafford JL (2012) Examination of the stimulatory signaling potential of a channel catfish leukocyte immune-type receptor and associated adaptor. Dev Comp Immunol 36(1):62–73

    Article  CAS  PubMed  Google Scholar 

  • Cortes HD, Lillico DM, Zwozdesky MA, Pemberton JG, Obrien A, Montgomery BCS, Wiersma L, Stafford JL (2014) Induction of phagocytosis and intracellular signaling by an inhibitory channel catfish leukocyte immune-type receptor: evidence for immunoregulatory receptor functional plasticity in teleosts. J Innate Immun 6(4):435–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David L, Blum S, Feldman WM, Lavi U, Hillel J (2003) Recent Duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol Biol Evol 20(9):1425–1434

  • Davis RS (2007) Fc receptor-like molecules. Annu Rev Immunol 25(1):525–560

    Article  CAS  PubMed  Google Scholar 

  • Davis RS, Dennis G Jr, Odom MR, Gibson AW, Kimberly RP, Burrows PD, Cooper MD (2002) Fc receptor homologs: newest members of a remarkably diverse Fc receptor gene family. Immunol Rev 190(1):123–136

    Article  CAS  PubMed  Google Scholar 

  • Fayngerts SA, Najakshin AM, Taranin AV (2007) Species-specific evolution of the FcR family in endothermic vertebrates. Immunogenetics 59(6):493–506

    Article  CAS  PubMed  Google Scholar 

  • Fei C, Pemberton J, Lillico D, Zwozdesky M, Stafford J (2016) Biochemical and functional insights into the integrated regulation of innate immune cell responses by teleost leukocyte immune-type receptors. Biology 5(1):13

    Article  PubMed Central  CAS  Google Scholar 

  • Ferrier DE (2016) Evolution of homeobox gene clusters in animals: the giga-cluster and primary vs. secondary clustering. Front Ecol Evol 4:36

  • Franco A, Damdinsuren B, Ise T, Dement-Brown J, Li H, Nagata S, Tolnay M (2013) Human Fc receptor-like 5 binds intact IgG via mechanisms distinct from those of Fc-receptors. J Immunol 190(11):5739–5746

  • Fuente HD, Cibrián D, Sánchez-Madrid F (2012) Immunoregulatory molecules are master regulators of inflammation during the immune response. FEBS Lett 586(18):2897–2905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gillis C, Gouel-Cheron A, Jonsson F, Bruhns P (2014) Contribution of human FcγRs to disease with evidence from human polymorphisms and transgenic animal studies. Front Immunol 5:254

  • Guselnikov SV, Taranin AV (2019) Unraveling the LRC evolution in mammals: IGSF1 and A1BG provide the keys. Genome Biol Evol 11(6):1586–1601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guselnikov SV, Ramanayake T, Robert J, Taranin AV (2009) Diversity of the FcR- and KIR-related genes in an amphibian Xenopus. Front Biosci 14:130–140

  • Guselnikov S, Ershova S, Mechetina L, Najakshin A, Volkova O, Alabyev B, Taranin A (2002) A family of highly diverse human and mouse genes structurally links leukocyte FcR, gp42 and PECAM-1. Immunogenetics 54(2):87–95

    Article  CAS  PubMed  Google Scholar 

  • Guselnikov SV, Ramanayake T, Erilova AY, Mechetina LV, Najakshin AM, Robert J, Taranin AV (2008) The Xenopus FcR family demonstrates continually high diversification of paired receptors in vertebrate evolution. BMC Evol Biol 8(1):148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guselnikov SV, Reshetnikova ES, Najakshin AM, Mechetina LV, Robert J, Taranin AV (2010) The amphibians Xenopus levies and Silurana tropicalis possess a family of activating KIR-related immunoglobulin-like receptors. Dev Comp Immunol 34(3):308–315

    Article  CAS  PubMed  Google Scholar 

  • Hughes AL, Friedman R (2008) Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol 25(12):2681–2688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiyoshi M, Caaveiro JM, Kawai T, Tashiro S, Ide T, Asaoka Y, Hatayama K, Tsumoto K (2015) Structural basis for binding of human IgG1 to its high-affinity human receptor FcγRI. Nature Comms 6(1):1–11

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33(7):1870–1874

  • Li FJ, Won WJ, Becker EJ, Easlick JL, Tabengwa EM, Li R, Burrows PD, Davis RS (2014) Emerging roles for the FCRL family members in lymphocyte biology and disease. Fc Receptors. Springer, Cham 29–50

  • Liu H, Li L, Voss C, Wang F, Liu J, Li SS (2015) A Comprehensive immunoreceptor phosphotyrosine-based signaling network revealed by reciprocal protein-peptide array screening. Mol Cell Proteomics 14(7):1846–1858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46(D1):D493–D496

  • Maeso I, Irimia M, Tena JJ, Casares F, Gómez-Skarmeta JL (2013) Deep conservation of cis -regulatory elements in metazoans. Philosophical Transactions of the Royal Society B: Biological Sciences 368(1632):20130020

    Article  CAS  Google Scholar 

  • Makino T, McLysaght A (2008) Interacting gene clusters and the evolution of the vertebrate immune system. Mol Biol Evol 25(12):2771–2771

    Article  CAS  Google Scholar 

  • Maltais LJ, Lovering RC, Taranin AV, Colonna M, Ravetch JV, Dalla-Favera R, Burrows PD, Cooper MD, Davis RS (2006) New nomenclature for Fc receptor–like molecules. Nat Immunol 7(5):431–432

    Article  CAS  PubMed  Google Scholar 

  • Martin AM, Kulski JK, Witt C, Pontarotti P, Christiansen FT (2002) Leukocyte Ig-like receptor complex (LRC) in mice and men. Trends Immunol 23(2):81–88

    Article  CAS  PubMed  Google Scholar 

  • Montgomery BC, Mewes J, Davidson C, Burshtyn DN, Stafford JL (2009) Cell surface expression of channel catfish leukocyte immune-type receptors (IpLITRs) and recruitment of both Src homology 2 domain-containing protein tyrosine phosphatase (SHP)-1 and SHP-2. Dev Comp Immunol 33(4):570–582

    Article  CAS  PubMed  Google Scholar 

  • Montgomery BC, Cortes HD, Burshtyn DN, Stafford JL (2012) Channel catfish leukocyte immune-type receptor mediated inhibition of cellular cytotoxicity is facilitated by SHP-1-dependent and -independent mechanisms. Dev Comp Immunol 37(1):151–163

    Article  CAS  PubMed  Google Scholar 

  • Morton HC, Pleass RJ, Storset AK, Dissen E, Williams JL, Brandtzaeg P, Woof JM (2004) Cloning and characterization of an immunoglobulin A Fc receptor from cattle. Immunology 111(2):204–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikolaidis N, Makalowska I, Chalkia D, Makalowski W, Klein J, Nei M (2005) Origin and evolution of the chicken leukocyte receptor complex. Proc Natl Acad Sci 102(11):4057–4062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oates AC, Wollberg P, Pratt SJ, Paw BH, Johnson SL, Ho RK, Postlethwait HJ, Zon IL, Wilks AF (1999) Zebrafishstat3 is expressed in restricted tissues during embryogenesis and stat1 rescues cytokine signaling in a STAT1-deficient human cell line. Dev Dyn 215(4):352–370

    Article  CAS  PubMed  Google Scholar 

  • Ohta Y, Kasahara M, O’Connor TD, Flajnik MF (2019) Inferring the “primordial immune complex”: origins of MHC class I and antigen receptors revealed by comparative genomics. J Immunol 203(7):1882–1896

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Nunez I, Wcisel DJ, Litman GW, Yoder JA (2014) Multigene families of immunoglobulin domain-containing innate immune receptors in zebrafish: deciphering the differences. Dev Comp Immunol 46(1):24–34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rostamzadeh D, Kazemi T, Amirghofran Z, Shabani M (2018) Update on Fc receptor-like (FCRL) family: New immunoregulatory players in health and diseases. Expert Opin Ther Targets 22(6):487–502

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Hashiguchi Y, Nishida M (2009) Temporal pattern of loss/persistence of duplicate genes involved in signal transduction and metabolic pathways after teleost-specific genome duplication. BMC Evol Biol 9(1):127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sambrook JG, Bashirova A, Andersen H, Piatak M, Vernikos GS, Coggill P, Lifson DJ, Carrington M, Beck S (2006) Identification of the ancestral killer immunoglobulin-like receptor gene in primates. BMC Genomics 7(1):1–8

  • Schreeder DM, Cannon JP, Wu J, Li R, Shakhmatov MA, Davis RS (2010) Cutting edge: FcR-Like 6 is an MHC class II receptor. J Immunol 185(1):23–27

    Article  CAS  PubMed  Google Scholar 

  • Stafford JL, Bengtén E, Pasquier LD, Mcintosh RD, Quiniou SM, Clem LW, Miller WN, Wilson M (2006a) A novel family of diversified immunoregulatory receptors in teleosts is homologous to both mammalian Fc receptors and molecules encoded within the leukocyte receptor complex. Immunogenetics 58(9):758–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stafford JL, Bengtén E, Pasquier LD, Miller NW, Wilson M (2007) Channel catfish leukocyte immune-type receptors contain a putative MHC class I binding site. Immunogenetics 59(1):77–91

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Star B, Jentoft S (2012) Why does the immune system of Atlantic cod lack MHC II?. Bioessays 34(8):648–651

  • Takai T (2005) A novel recognition system for MHC class I molecules constituted by PIR. Adv Immunol 88:161–192

  • Takeda K, Nakamura A (2017) Regulation of immune and neural function via leukocyte Ig-like receptors. J Biochem 162(2):73–80

    Article  CAS  PubMed  Google Scholar 

  • Taylor AI, Gould HJ, Sutton BJ, Calvert RA (2007) The first avian Ig-like Fc receptor family member combines features of mammalian FcR and FCRL. Immunogenetics 59(4):323–328

    Article  CAS  PubMed  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 Immun 196(6):2677–2689

    Article  CAS  PubMed  Google Scholar 

  • Traub LM, Bonifacino JS (2013) Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol 5(11):a016790

  • Trowsdale J, Barten R, Haude A, Stewart CA, Beck S, Wilson MJ (2001) The genomic context of natural killer receptor extended gene families. Immunol Rev 181(1):20–38

    Article  CAS  PubMed  Google Scholar 

  • Viertlboeck BC, Habermann FA, Schmitt R, Groenen MA, Pasquier LD, Göbel TW (2005) The chicken leukocyte receptor complex: a highly diverse multigene family encoding at least six structurally distinct receptor types. J Immunol 175(1):385–393

    Article  CAS  PubMed  Google Scholar 

  • Viertlboeck BC, Schweinsberg S, Hanczaruk MA, Schmitt R, Pasquier LD, Herberg FW, Gobel TW (2007) The chicken leukocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor. PNAS 104(28):11718–11723

  • Viertlboeck BC, Schweinsberg S, Schmitt R, Herberg FW, Gobel TW (2009) The chicken leukocyte receptor complex encodes a family of different affinity Fcγ receptors. J Immunol 182(11):6985–6992

  • Wang J, Belosevic M, Stafford JL (2020) Identification of goldfish (Carassius auratus L.) leukocyte immune-type receptors shows alternative splicing as a potential mechanism for receptor diversification. Mol Immunol 125:83–94

    Article  CAS  PubMed  Google Scholar 

  • Wcisel DJ, Ota T, Litman GW, Yoder JA (2017) Spotted gar and the evolution of innate immune receptors. J Exp Zool B Mol Dev Evol 328(7):666–684

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson TJ, Fuchs A, Colonna M (2012) Cutting edge: human FcRL4 and FcRL5 are receptors for IgA and IgG. J Immunol 188(10):4741–4745

    Article  CAS  PubMed  Google Scholar 

  • Yu W, Pallen CJ, Tay A, Jirik FR, Brenner S, Tan YH, Venkatesh B (2001) Conserved synteny between the Fugu and human PTEN locus and the evolutionary conservation of vertebrate PTEN function. Oncogene 20(39):5554–5561

    Article  CAS  PubMed  Google Scholar 

  • Yuan J, He Z, Yuan X, Jiang X, Sun X, Zou S (2010) Speciation of polyploid Cyprinidae fish of common carp, crucian carp, and silver crucian carp derived from duplicated Hox genes. J Exp Zool B Mol Dev Evol 314B(6):445–456

    Article  CAS  Google Scholar 

  • Zwozdesky MA, Fei C, Lillico DME, Stafford JL (2017) Imaging flow cytometry and GST pulldown assays provide new insights into channel catfish leukocyte immune-type receptor-mediated phagocytic pathways. Dev Comp Immunol 67:126–138

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Funding

This work was supported by the Natural Sciences and Engineering Council of Canada (NSERC; Grant No. RGPIN-2014-06395) to MB. JW was supported by University of Alberta Recruitment Scholarship, a Research assistantship, and a Teaching Assistantship from Department of Biological Sciences of University of Alberta.

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Wang, J., Belosevic, M. & Stafford, J.L. Identification of distinct LRC- and Fc receptor complex-like chromosomal regions in fish supports that teleost leukocyte immune-type receptors are distant relatives of mammalian Fc receptor-like molecules. Immunogenetics 73, 93–109 (2021). https://doi.org/10.1007/s00251-020-01193-3

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