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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 57))

Abstract

Jawless vertebrates represented by lampreys and hagfish mount antigen-specific immune responses using variable lymphocyte receptors. These receptors generate diversity comparable to that of T-cell and B-cell receptors by assembling multiple leucine-rich repeat modules with highly variable sequences. Although it is true that jawed and jawless vertebrates have structurally unrelated antigen receptors, their adaptive immune systems have much in common. Most notable is the conservation of lymphocyte lineages. It appears that specialized lymphocyte lineages emerged in a common vertebrate ancestor and that jawed and jawless vertebrates co-opted different antigen receptors within the context of such lymphocyte lineages.

This chapter is dedicated to the memory of Dr. Zeev Pancer who passed away on April 20, 2014.

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References

  • Acton RT, Weinheimer PF, Hildemann WH, Evans EE (1969) Induced bactericidal response in the hagfish. J Bacteriol 99:626–628

    PubMed Central  CAS  PubMed  Google Scholar 

  • Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z (2005) Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–1973

    Article  CAS  PubMed  Google Scholar 

  • Alder MN, Herrin BR, Sadlonova A, Stockard CR, Grizzle WE, Gartland LA, Gartland GL, Boydston JA, Turnbough CL Jr, Cooper MD (2008) Antibody responses of variable lymphocyte receptors in the lamprey. Nat Immunol 9:319–327

    Article  CAS  PubMed  Google Scholar 

  • Anderson MK, Sun X, Miracle AL, Litman GW, Rothenberg EV (2001) Evolution of hematopoiesis: Three members of the PU.1 transcription factor family in a cartilaginous fish, Raja eglanteria. Proc Natl Acad Sci USA 98:553–558

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ardavin CF, Zapata A (1987) Ultrastructure and changes during metamorphosis of the lympho-hemopoietic tissue of the larval anadromous sea lamprey Petromyzon marinus. Dev Comp Immunol 11:79–93

    Article  CAS  PubMed  Google Scholar 

  • Bajoghli B, Aghaallaei N, Hess I, Rode I, Netuschil N, Tay BH, Venkatesh B, Yu JK, Kaltenbach SL, Holland ND, Diekhoff D, Happe C, Schorpp M, Boehm T (2009) Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138:186–197

    Article  CAS  PubMed  Google Scholar 

  • Bajoghli B, Guo P, Aghaallaei N, Hirano M, Strohmeier C, McCurley N, Bockman DE, Schorpp M, Cooper MD, Boehm T (2011) A thymus candidate in lampreys. Nature 470:90–94

    Article  CAS  PubMed  Google Scholar 

  • Boehm T (2011) Design principles of adaptive immune systems. Nat Rev Immunol 11:307–317

    Article  CAS  PubMed  Google Scholar 

  • Boehm T, Iwanami N, Hess I (2012a) Evolution of the immune system in the lower vertebrates. Annu Rev Genomics Hum Genet 13:127–149

    Article  CAS  PubMed  Google Scholar 

  • Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD (2012b) VLR-based adaptive immunity. Annu Rev Immunol 30:203–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cerenius L, Kawabata S, Lee BL, Nonaka M, Soderhall K (2010) Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 35:575–583

    Article  CAS  PubMed  Google Scholar 

  • Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124:815–822

    Article  CAS  PubMed  Google Scholar 

  • Cruikshank WW, Kornfeld H, Center DM (2000) Interleukin-16. J Leukoc Biol 67:757–766

    CAS  PubMed  Google Scholar 

  • Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3, e314

    Article  PubMed Central  PubMed  Google Scholar 

  • Deng L, Velikovsky CA, Xu G, Iyer LM, Tasumi S, Kerzic MC, Flajnik MF, Aravind L, Pancer Z, Mariuzza RA (2010) A structural basis for antigen recognition by the T cell-like lymphocytes of sea lamprey. Proc Natl Acad Sci USA 107:13408–13413

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deng L, Luo M, Velikovsky A, Mariuzza RA (2013) Structural insights into the evolution of the adaptive immune system. Annu Rev Biophys 42:191–215

    Article  CAS  PubMed  Google Scholar 

  • Du Pasquier L (2000) The phylogenetic origin of antigen-specific receptors. Curr Top Microbiol Immunol 248:160–185

    PubMed  Google Scholar 

  • Du Pasquier L, Zucchetti I, De Santis R (2004) Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol Rev 198:233–248

    Article  PubMed  Google Scholar 

  • Finstad J, Good RA (1964) The evolution of the immune response. III. Immunologic responses in the lamprey. J Exp Med 120:1151–1168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flajnik MF (2002) Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2:688–698

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF (2014) Re-evaluation of the immunological big bang. Curr Biol 24:R1060–R1065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15:351–362

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M (2010) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11:47–59

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fried C, Prohaska SJ, Stadler PF (2003) Independent Hox-cluster duplications in lampreys. J Exp Zool B Mol Dev Evol 299:18–25

    Article  PubMed  Google Scholar 

  • Fugmann SD (2010) The origins of the Rag genes—from transposition to V(D)J recombination. Semin Immunol 22:10–16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujii T, Nakagawa H, Murakawa S (1979) Immunity in lamprey. I. Production of haemolytic and haemagglutinating antibody to sheep red blood cells in Japanese lampreys. Dev Comp Immunol 3:441–451

    Article  CAS  PubMed  Google Scholar 

  • Fujita T (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat Rev Immunol 2:346–353

    Article  CAS  PubMed  Google Scholar 

  • Furlong RF, Holland PW (2002) Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci 357:531–544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Girardi M (2006) Immunosurveillance and immunoregulation by γδ T cells. J Invest Dermatol 126:25–31

    Article  CAS  PubMed  Google Scholar 

  • Guo P, Hirano M, Herrin BR, Li J, Yu C, Sadlonova A, Cooper MD (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796–802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haire RN, Miracle AL, Rast JP, Litman GW (2000) Members of the Ikaros gene family are present in early representative vertebrates. J Immunol 165:306–312

    Article  CAS  PubMed  Google Scholar 

  • Haruta C, Suzuki T, Kasahara M (2006) Variable domains in hagfish: NICIR is a polymorphic multigene family expressed preferentially in leukocytes and is related to lamprey TCR-like. Immunogenetics 58:216–225

    Article  CAS  PubMed  Google Scholar 

  • Hayday AC (2000) γδ cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975–1026

    Article  CAS  PubMed  Google Scholar 

  • Herrin BR, Alder MN, Roux KH, Sina C, Ehrhardt GR, Boydston JA, Turnbough CL Jr, Cooper MD (2008) Structure and specificity of lamprey monoclonal antibodies. Proc Natl Acad Sci USA 105:2040–2045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hildemann WH, Thoenes GH (1969) Immunological responses of Pacific hagfish. I. Skin transplantation immunity. Transplantation 7:506–521

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Das S, Guo P, Cooper MD (2011) The evolution of adaptive immunity in vertebrates. Adv Immunol 109:125–157

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Guo P, McCurley N, Schorpp M, Das S, Boehm T, Cooper MD (2013) Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435–438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holland PWH, Garcia-Fernandez J, Williams NA, Sidow A (1994) Gene duplications and the origins of vertebrate development. Development 1994(Suppl):125–133

    Google Scholar 

  • Holland SJ, Gao M, Hirano M, Iyer LM, Luo M, Schorpp M, Cooper MD, Aravind L, Mariuzza RA, Boehm T (2014) Selection of the lamprey VLRC antigen receptor repertoire. Proc Natl Acad Sci USA 111:14834–14839

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Honjo T, Muramatsu M, Fagarasan S (2004) AID: How does it aid antibody diversity? Immunity 20:659–668

    Article  CAS  PubMed  Google Scholar 

  • Hsu E (2011) The invention of lymphocytes. Curr Opin Immunol 23:156–162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janvier P (2006) Palaeontology: modern look for ancient lamprey. Nature 443:921–924

    Article  CAS  PubMed  Google Scholar 

  • Kanda R, Sutoh Y, Kasamatsu J, Maenaka K, Kasahara M, Ose T (2014) Crystal structure of the lamprey variable lymphocyte receptor C reveals an unusual feature in its N-terminal capping module. PLoS One 9, e85875

    Article  PubMed Central  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3, e181

    Article  PubMed Central  PubMed  Google Scholar 

  • Kasahara M (2007) The 2R hypothesis: an update. Curr Opin Immunol 19:547–552

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M (2010) Genome duplication and T cell immunity. Prog Mol Biol Transl Sci 92:7–36

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M (2013a) Deja vu: the identity of a third lineage of lymphocytes in lampreys. Immunol Cell Biol 91:599–600

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M (2013b) Impact of whole-genome duplication on vertebrate development and evolution. Semin Cell Dev Biol 24:81–82

    Article  PubMed  Google Scholar 

  • Kasahara M, Sutoh Y (2014) Two forms of adaptive immunity in vertebrates: similarities and differences. Adv Immunol 122:59–90

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M, Suzuki T, DuPasquier L (2004) On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25:105–111

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M, Kasamatsu J, Sutoh Y (2008) Two types of antigen receptor systems in vertebrates. Zool Sci 25:969–975

    Article  CAS  PubMed  Google Scholar 

  • Kasamatsu J, Suzuki T, Ishijima J, Matsuda Y, Kasahara M (2007) Two variable lymphocyte receptor genes of the inshore hagfish are located far apart on the same chromosome. Immunogenetics 59:329–331

    Article  CAS  PubMed  Google Scholar 

  • Kasamatsu J, Sutoh Y, Fugo K, Otsuka N, Iwabuchi K, Kasahara M (2010) Identification of a third variable lymphocyte receptor in the lamprey. Proc Natl Acad Sci USA 107:14304–14308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kato L, Stanlie A, Begum NA, Kobayashi M, Aida M, Honjo T (2012) An evolutionary view of the mechanism for immune and genome diversity. J Immunol 188:3559–3566

    Article  CAS  PubMed  Google Scholar 

  • Kishishita N, Matsuno T, Takahashi Y, Takaba H, Nishizumi H, Nagawa F (2010) Regulation of antigen-receptor gene assembly in hagfish. EMBO Rep 11:126–132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klein J, Sato A, Mayer WE (2000) Jaws and AIS. In: Kasahara M (ed) Major histocompatibility complex: evolution, structure, and function. Springer, Tokyo, pp 3–26

    Chapter  Google Scholar 

  • Kuraku S (2013) Impact of asymmetric gene repertoire between cyclostomes and gnathostomes. Semin Cell Dev Biol 24:119–127

    Article  CAS  PubMed  Google Scholar 

  • Kuraku S, Meyer A, Kuratani S (2009) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol Biol Evol 26:47–59

    Article  CAS  PubMed  Google Scholar 

  • Li J, Das S, Herrin BR, Hirano M, Cooper MD (2013) Definition of a third VLR gene in hagfish. Proc Natl Acad Sci USA 110:15013–15018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Linthicum DS, Hildemann WH (1970) Immunologic responses of Pacific hagfish. III. Serum antibodies to cellular antigens. J Immunol 105:912–918

    CAS  PubMed  Google Scholar 

  • Litman GW, Finstad FJ, Howell J, Pollara BW, Good RA (1970) The evolution of the immune response. III. Structural studies of the lamprey immunoglobulin. J Immunol 105:1278–1285

    CAS  PubMed  Google Scholar 

  • Litman GW, Anderson MK, Rast JP (1999) Evolution of antigen binding receptors. Annu Rev Immunol 17:109–147

    Article  CAS  PubMed  Google Scholar 

  • Marchalonis JJ, Edelman GM (1968) Phylogenetic origins of antibody structure. III. Antibodies in the primary immune response of the sea lamprey, Petromyzon marinus. J Exp Med 127:891–914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsushita M, Matsushita A, Endo Y, Nakata M, Kojima N, Mizuochi T, Fujita T (2004) Origin of the classical complement pathway: lamprey orthologue of mammalian C1q acts as a lectin. Proc Natl Acad Sci USA 101:10127–10131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mayer WE, O’hUigin C, Tichy H, Terzic J, Saraga-Babic M (2002) Identification of two Ikaros-like transcription factors in lamprey. Scand J Immunol 55:162–170

    Article  CAS  PubMed  Google Scholar 

  • Mehta TK, Ravi V, Yamasaki S, Lee AP, Lian MM, Tay BH, Tohari S, Yanai S, Tay A, Brenner S, Venkatesh B (2013) Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum). Proc Natl Acad Sci USA 110:16044–16049

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagawa F, Kishishita N, Shimizu K, Hirose S, Miyoshi M, Nezu J, Nishimura T, Nishizumi H, Takahashi Y, Hashimoto S, Takeuchi M, Miyajima A, Takemori T, Otsuka AJ, Sakano H (2007) Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat Immunol 8:206–213

    Article  CAS  PubMed  Google Scholar 

  • Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Book  Google Scholar 

  • Ohno S (1999) Gene duplication and the uniqueness of vertebrate genomes circa 1970–1999. Semin Cell Dev Biol 10:517–522

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Cooper MD (2006) The evolution of adaptive immunity. Annu Rev Immunol 24:497–518

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD (2004a) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–180

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Mayer WE, Klein J, Cooper MD (2004b) Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc Natl Acad Sci USA 101:13273–13278

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pancer Z, Saha NR, Kasamatsu J, Suzuki T, Amemiya CT, Kasahara M, Cooper MD (2005) Variable lymphocyte receptors in hagfish. Proc Natl Acad Sci USA 102:9224–9229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pollara B, Litman GW, Finstad J, Howell J, Good RA (1970) The evolution of the immune response. VII. Antibody to human “O” cells and properties of the immunoglobulin in lamprey. J Immunol 105:738–745

    CAS  PubMed  Google Scholar 

  • Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071

    Article  CAS  PubMed  Google Scholar 

  • Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, Pavlov YI, Aravind L, Pancer Z (2007) Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 8:647–656

    Article  CAS  PubMed  Google Scholar 

  • Shimeld SM, Donoghue PC (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139:2091–2099

    Article  CAS  PubMed  Google Scholar 

  • Shintani S, Terzic J, Sato A, Saraga-Babic M, O’hUigin C, Tichy H, Klein J (2000) Do lampreys have lymphocytes? The Spi evidence. Proc Natl Acad Sci USA 97:7417–7422

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell MS, Yandell MD, Manousaki T, Meyer A, Bloom OE, Morgan JR, Buxbaum JD, Sachidanandam R, Sims C, Garruss AS, Cook M, Krumlauf R, Wiedemann LM, Sower SA, Decatur WA, Hall JA, Amemiya CT, Saha NR, Buckley KM, Rast JP, Das S, Hirano M, McCurley N, Guo P, Rohner N, Tabin CJ, Piccinelli P, Elgar G, Ruffier M, Aken BL, Searle SM, Muffato M, Pignatelli M, Herrero J, Jones M, Brown CT, Chung-Davidson YW, Nanlohy KG, Libants SV, Yeh CY, McCauley DW, Langeland JA, Pancer Z, Fritzsch B, de Jong PJ, Zhu B, Fulton LL, Theising B, Flicek P, Bronner ME, Warren WC, Clifton SW, Wilson RK, Li W (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45:415–421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stadler PF, Fried C, Prohaska SJ, Bailey WJ, Misof BY, Ruddle FH, Wagner GP (2004) Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Mol Phylogenet Evol 32:686–694

    Article  CAS  PubMed  Google Scholar 

  • Sutoh Y, Kasahara M (2014) Copy number and sequence variation of leucine-rich repeat modules suggests distinct functional constraints operating on variable lymphocyte receptors expressed by agnathan T cell-like and B cell-like lymphocytes. Immunogenetics 66:403–409

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Shin IT, Kohara Y, Kasahara M (2004) Transcriptome analysis of hagfish leukocytes: a framework for understanding the immune system of jawless fishes. Dev Comp Immunol 28:993–1003

    Article  PubMed  Google Scholar 

  • Suzuki T, Shin-I T, Fujiyama A, Kohara Y, Kasahara M (2005) Hagfish leukocytes express a paired receptor family with a variable domain resembling those of antigen receptors. J Immunol 174:2885–2891

    Article  CAS  PubMed  Google Scholar 

  • Takaba H, Imai T, Miki S, Morishita Y, Miyashita A, Ishikawa N, Nishizumi H, Sakano H (2013) A major allogenic leukocyte antigen in the agnathan hagfish. Sci Rep 3:1716

    Article  PubMed Central  PubMed  Google Scholar 

  • Uinuk-Ool T, Mayer WE, Sato A, Dongak R, Cooper MD, Klein J (2002) Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc Natl Acad Sci USA 99:14356–14361

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vantourout P, Hayday A (2013) Six-of-the-best: unique contributions of γδ T cells to immunology. Nat Rev Immunol 13:88–100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, Hoon S, Gangu V, Roy SW, Irimia M, Korzh V, Kondrychyn I, Lim ZW, Tay BH, Tohari S, Kong KW, Ho S, Lorente-Galdos B, Quilez J, Marques-Bonet T, Raney BJ, Ingham PW, Tay A, Hillier LW, Minx P, Boehm T, Wilson RK, Brenner S, Warren WC (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu F, Chen L, Liu X, Wang H, Su P, Han Y, Feng B, Qiao X, Zhao J, Ma N, Liu H, Zheng Z, Li Q (2013) Lamprey variable lymphocyte receptors mediate complement-dependent cytotoxicity. J Immunol 190:922–930

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Takamune K, Kondo M, Takahashi Y, Kato-Unoki Y, Nakao M, Sano N, Fujii T (2014) Hagfish C1q: Its unique binding property. Dev Comp Immunol 43:47–53

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Experimental work in my laboratory has been supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan. I thank Dr. Yoichi Sutoh for his kind help with the preparation of figures.

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Correspondence to Masanori Kasahara .

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Kasahara, M. (2015). Variable Lymphocyte Receptors: A Current Overview. In: Hsu, E., Du Pasquier, L. (eds) Pathogen-Host Interactions: Antigenic Variation v. Somatic Adaptations. Results and Problems in Cell Differentiation, vol 57. Springer, Cham. https://doi.org/10.1007/978-3-319-20819-0_8

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