Skip to main content

New Approaches Towards an Understanding of Deuterostome Immunity

  • Chapter
Book cover Origin and Evolution of the Vertebrate Immune System

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 248))

Abstract

The vertebrate immune system is distinguished by an unusual propensity for genetic invention. For example, three forms of programmed somatic DNA recombination (V-D-J recombination, class switching and a highly targeted form of gene conversion) have arisen entirely independently in the course of immunoglobulin (Ig) heavy-chain gene evolution. Similar phenomena are virtually unknown in other metazoan genetic systems. Genes that mediate immunity are further characterized by accelerated sequence divergence rates when compared to nonimmune genes in studies of mouse and human gene orthologs (Hughes 1997; Murphy 1993). Both of these attributes, the tendency towards mechanistic novelty and a high rate of sequence evolution, may emerge from the dynamic nature of host-pathogen interactions and thus be a universal characteristic of immune systems. To investigate this possibility it is necessary to characterize immunity in animal phyla where the vertebrate forms of adaptive immunity are absent. A number of molecular advances have been made in recent years in the study of arthropod immunity (e.g., Hoffmann et al. 1996; Iwanaga and Kawabata 1998). As these data accumulate, in combination with similar work on an invertebrate deuterostome that is described here, a more general understanding of immunity will emerge.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAGI and RAG2 and its implications for the evolution of the immune system Nature 394: 744–751

    CAS  Google Scholar 

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387: 489–493

    Article  PubMed  CAS  Google Scholar 

  • Al-Sharif WZ, Sunyer JO, Lambris JD, Smith LC (1998) Sea urchin coelomocytes specifically express a homologue of the complement component C3. J Immunol 160: 2983–2997

    PubMed  CAS  Google Scholar 

  • Amemiya CT, Ota T, Litman GW (1996) Construction of PI Artificial Chromosome (PAC) libraries from lower vertebrates. In: Birren, B and Lai, E (ed) Nonmammalian Genomic Analysis: A practical Guide. Academic Press, New York, pp 223–256

    Chapter  Google Scholar 

  • Bailey WJ, Kim J, Wagner GP, Ruddle FH (1997) Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol Evol 14: 843–853

    PubMed  CAS  Google Scholar 

  • Balavoine G (1997) The early emergence of platyhelminths is contradicted by the agreement between 18 s rRNA and Hox genes data. C R Acad Sci III 320: 83–94

    Article  Google Scholar 

  • Balavoine G, Adoutte A (1998) One or three Cambrian radiations? Science 280: 397–398

    Article  CAS  Google Scholar 

  • Carroll RL (1988) Vertebrate Paleontology and Evolution. Freeman, New York

    Google Scholar 

  • Castresana J, Feldmaier-Fuchs G, Yokobori S, Satoh N, Paabo S (1998) The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria. Genetics 150: 1115–1123

    PubMed  CAS  Google Scholar 

  • Coffman JA, Kirchhamer CV, Harrington MG, Davidson EH (1996) SpRunt-1, a new member of the runt domain family of transcription factors, is a positive regulator of the aboral ectoderm-specific CyIIIA gene in sea urchin embryos. Dev Biol 174: 43–54

    Article  PubMed  CAS  Google Scholar 

  • Davidson EH (1994) Stepwise evolution of major functional systems in vertebrates, including the immune system. In: Hoffmann JA, Janeway CA, Shunji N (ed) Phylogenetic Perspectives in Immunity: the Insect Host Defense. R.G. Landes Company, Austin, pp 133–142

    Google Scholar 

  • Davidson EH, Cameron RA, Ransick A (1998) Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125: 3269–3290

    PubMed  CAS  Google Scholar 

  • Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270: 1319–1325

    Article  PubMed  CAS  Google Scholar 

  • Eernisse DJ (1997) Arthropod and annelid relationships re-examined. In: Fortey, RA and Thomas, RH (ed) Arthropod Relationships, Systematics Association Special Volume Series 55. Chapman and Hall, London, pp 43–56

    Google Scholar 

  • Eppig JT, Nadeau JH (1995) Comparative maps: the mammalian jigsaw puzzle. Curr Opin Genet Dev 5: 709–716

    Article  PubMed  CAS  Google Scholar 

  • Forey P, Janvier P (1993) Agnathans and the origin of jawed vertebrates, Nature 361: 129–134

    Article  Google Scholar 

  • Ghosh S, May MJ, Kopp EB (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225–260

    Article  PubMed  CAS  Google Scholar 

  • Giribet G, Ribera C (1998) The position of arthropods in the animal kingdom: A search for a reliable outgroup for internal arthropod phylogeny. Mol Phylogenet Evol 9: 481–488

    Article  PubMed  CAS  Google Scholar 

  • Gress TM, Hoheisel JD, Lennon GG, Zehetner G, Lehrach H (1992) Hybridization fingerprinting of high-density cDNA-library arrays with cDNA pools derived from whole tissues. Mamm Genome 3: 609–619

    Article  PubMed  CAS  Google Scholar 

  • Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18 sribosomal DNA that the lophophorates are protostome animals. Science 267: 1641–1643

    Article  PubMed  CAS  Google Scholar 

  • Hedges SB, Parker PH, Sibley CG, Kumar S (1996) Continental breakup and the ordinal diversification of birds and mammals. Nature 381: 226–229

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann JA, Reichhart JM, Hetru C (1996) Innate immunity in higher insects. Curr Opin Immunol 8: 8–13

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL (1997) Rapid evolution of immunoglobulin superfamily C2 domains expressed in immune system cells. Mol Biol Evol 14: 1–5

    PubMed  CAS  Google Scholar 

  • Hughes AL (1998a) Protein phylogenies provide evidence of a radical discontinuity between arthropod and vertebrate immune systems. Immunogenetics 47: 283–296

    Article  CAS  Google Scholar 

  • Hughes AL (1998b) Phylogenetic tests of the hypothesis of block duplication of homologous genes on human chromosomes. 6:9, and 1. Mol Biol Evol 15: 854–870

    CAS  Google Scholar 

  • Iwanaga S, Kawabata S (1998) Evolution and phylogeny of defense molecules associated with innate immunity in horseshoe crab. Front Biosci 3: 973–984

    Google Scholar 

  • Kandil E, Namikawa C, Nonaka M, Greenberg AS, Flajnik MF, Ishibashi T, Kasahara M (1996) Isolation of low molecular mass polypeptide complementary DNA clones from primitive vertebrates. Implications for the origin of MHC class I-restricted antigen presentation. J Immunol 156: 4245–4253

    PubMed  CAS  Google Scholar 

  • Kasahara M, Hayashi M, Tanaka K, Inoko H, Sugaya K, Ikemura T, Ishibashi T (1996) Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. Proc Natl Acad Sci USA 93: 9096–9101

    Article  PubMed  CAS  Google Scholar 

  • Kasahara M, Nakaya J, Satta Y, Takahata N (1997) Chromosomal duplication and the emergence of the adaptive immune system. Trends Genet 13: 90–92

    Article  PubMed  CAS  Google Scholar 

  • Katsanis N, Fitzgibbon J, Fisher EMC (1996) Paralogy mapping: identification of a region in the human MHC triplicated onto human chromosomes I and 9 allows the prediction and isolation of novel PBX and NOTCH loci. Genomics 35: 101–108

    Article  PubMed  CAS  Google Scholar 

  • Litman GW, Anderson MK, Rast JR (1999) Evolution of antigen binding receptors. Annual Review of Immunology 17: 109–147

    Article  PubMed  CAS  Google Scholar 

  • Lundin LG (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16: 1–19

    Article  PubMed  CAS  Google Scholar 

  • Mallatt J, Sullivan J (1998) 28 s and 18 s rDNA sequences support the monophyly of lampreys and hagfishes. Mol Biol Evol 15: 1706–1718

    PubMed  CAS  Google Scholar 

  • Miles C, Elgar G, Coles E, Kleinjan DJ, van Heyningen V, Hastie N (1998) Complete sequencing of the Fugu WAGR region from WTI to PAX6: dramatic compaction and conservation of synteny with human chromosome 11p13. Proc Natl Acad Set USA 95: 13068–13072

    Article  CAS  Google Scholar 

  • Murphy PM (1993) Molecular mimicry and the generation of host defense protein diversity. Cell 72: 823–826

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1970) Evolution by Gene Duplication. Springer-Verlag, Heidelberg

    Google Scholar 

  • Pancer Z, Rast JP, Davidson EH (1999) Origins of immunity: Transcription factors and homologs of effector genes of the vertebrate immune system expressed in sea urchin coelomocytes. Immunogenetics 49: 773–786

    Article  PubMed  CAS  Google Scholar 

  • Pebusque MJ, Coulier F, Birnbaum D, Pontarotti P (1998) Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Mol Biol Evol 15: 1145–1159

    PubMed  CAS  Google Scholar 

  • Peterson KJ (1995) A phylogenetic test of the calcichordate scenario. Lethaia 28: 25–38

    Article  Google Scholar 

  • Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: evolutionary and developmental significance. Bioessays 19: 623–631

    Article  PubMed  CAS  Google Scholar 

  • Smith LC, Britten RJ, Davidson EH (1995) Lipopolysaccharide activates the sea urchin immune system. Dev Comp Immunol 19: 217–224

    Article  PubMed  CAS  Google Scholar 

  • Smith LC, Chang L, Britten RJ, Davidson EH (1996) Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Complement homologues and other putative immune response genes suggest immune system homology within the deuterostomes. J Immunol 156: 593–602

    PubMed  CAS  Google Scholar 

  • Smith LC, Davidson EH (1992) The echinoid immune system and the phylogenetic occurrence of immune mechanisms in deuterostomes. Immunol Today 13: 356–362

    Article  PubMed  CAS  Google Scholar 

  • Smith LC, Davidson EH (1994) The echinoderm immune system. Characters shared with vertebrate immune systems and characters arising later in deuterostome phylogeny. Ann N Y Acad Sci 712: 213–226

    Article  PubMed  CAS  Google Scholar 

  • Smith LC, Shih CS, Dachenhausen SG (1998) Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J Immunol 161: 6784–6793

    PubMed  CAS  Google Scholar 

  • Stock DW, Whitt GS (1992) Evidence from 18 s ribosomal RNA sequences that lampreys and hagfishes form a natural group. Science 257: 787–789

    Article  PubMed  CAS  Google Scholar 

  • Tenen DG, Hromas R, Licht JD, Zhang DE (1997) Transcription factors, normal myeloid development, and leukemia. Blood 90: 489–519

    PubMed  CAS  Google Scholar 

  • Turbeville JM, Schultz JR, Raff RA (1994) Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. Mol Biol Evol 11: 648–655

    PubMed  CAS  Google Scholar 

  • Wada H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18 s rDNA. Proc Natl Acad Sci USA 91: 1801–1804

    Article  PubMed  CAS  Google Scholar 

  • Weiss MJ, Orkin SH (1995) GATA transcription factors: key regulators of hematopoiesis. Exo Hematol 23:99–107

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Rast, J.P., Pancer, Z., Davidson, E.H. (2000). New Approaches Towards an Understanding of Deuterostome Immunity. In: Du Pasquier, L., Litman, G.W. (eds) Origin and Evolution of the Vertebrate Immune System. Current Topics in Microbiology and Immunology, vol 248. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59674-2_1

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-59674-2_1

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64078-0

  • Online ISBN: 978-3-642-59674-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics