An Immune Effector System in the Protochordate Gut Sheds Light on Fundamental Aspects of Vertebrate Immunity

  • Assunta Liberti
  • Brittany Leigh
  • Rosaria De Santis
  • Maria Rosaria Pinto
  • John P. Cannon
  • Larry J. Dishaw
  • Gary W. Litman
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 57)

Abstract

A variety of germline and somatic immune mechanisms have evolved in vertebrate and invertebrate species to detect a wide array of pathogenic invaders. The gut is a particularly significant site in terms of distinguishing pathogens from potentially beneficial microbes. Ciona intestinalis, a filter-feeding marine protochordate that is ancestral to the vertebrate form, possesses variable region-containing chitin-binding proteins (VCBPs), a family of innate immune receptors, which recognize bacteria through an immunoglobulin-type variable region. The manner in which VCBPs mediate immune recognition appears to be related to the development and bacterial colonization of the gut, and it is likely that these molecules are critical elements in achieving overall immune and physiological homeostasis.

Keywords

Adaptive Immune System Versus Domain Beneficial Microbe Stomach Lumen Frequent Indels 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors would like to thank both the ASSEMBLE (Association of European Marine Biological Laboratories) program for collaborative support and Barbara Pryor for editorial assistance. LJD is supported by grants from the All Children’s Hospital Foundation and the University of South Florida College of Medicine Sponsored Research; GWL is supported by NIH R01 Al 23338.

References

  1. Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol 280:G922–G929PubMedGoogle Scholar
  2. Azumi K, De Santis R, De Tomaso A, Rigoutsos I, Yoshizaki F, Pinto MR, Marino R, Shida K, Ikeda M, Ikeda M, Arai M, Inoue Y, Shimizu T, Satoh N, Rokhsar DS, Pasquier D, Kasahara L, Satake M, Nonaka M (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: “waiting for Godot”. Immunogenetics 55:570–581CrossRefPubMedGoogle Scholar
  3. Bainard JD, Gregory TR (2013) Genome size evolution: patterns, mechanisms, and methodological advances. Genome 56:Vii–ViiiCrossRefPubMedGoogle Scholar
  4. Berrill NJ (1947) The development and growth of Ciona. J Mar Biol Assoc UK 26:616–625Google Scholar
  5. Boehm T (2007) Two in one: dual function of an invertebrate antigen receptor. Nat Immunol 8:1031–1033CrossRefPubMedGoogle Scholar
  6. Bollinger RR, Everett ML, Palestrant D, Love SD, Lin SS, Parker W (2003) Human secretory immunoglobulin A may contribute to biofilm formation in the gut. Immunology 109:580–587PubMedCentralCrossRefPubMedGoogle Scholar
  7. Burighel P, Cloney RA (1997) Urochordata: Ascidiacea. In: Harrison FW, Ruppert EE (eds) Microscopic analysis of invertebrates. Wiley-Liss, New York, pp 221–347Google Scholar
  8. Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3:1200–1207CrossRefPubMedGoogle Scholar
  9. Cannon JP, Haire RN, Schnitker N, Mueller MG, Litman GW (2004) Individual protochordates have unique immune-type receptor repertoires. Curr Biol 14:R465–R466CrossRefPubMedGoogle Scholar
  10. Craig SW, Cebra JJ (1971) Peyer’s patches – enriched source of precursors for iga-producing immunocytes in rabbit. J Exp Med 134:188–200PubMedCentralCrossRefPubMedGoogle Scholar
  11. Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968CrossRefPubMedGoogle Scholar
  12. Dishaw LJ, Mueller MG, Gwatney N, Cannon JP, Haire RN, Litman RT, Amemiya CT, Ota T, Rowen L, Glusman G, Litman GW (2008) Genomic complexity of the variable region-containing chitin-binding proteins in amphioxus. BMC Genet 9:78PubMedCentralCrossRefPubMedGoogle Scholar
  13. Dishaw LJ, Ota T, Mueller MG, Cannon JP, Haire RN, Gwatney NR, Litman RT, Litman GW (2010) The basis for haplotype complexity in VCBPs, an immune-type receptor in amphioxus. Immunogenetics 62:623–631PubMedCentralCrossRefPubMedGoogle Scholar
  14. Dishaw LJ, Giacomelli S, Melillo D, Zucchetti I, Haire RN, Natale L, Russo NA, De Santis R, Litman GW, Pinto MR (2011) A role for variable region-containing chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc Natl Acad Sci USA 108:16747–16752PubMedCentralCrossRefPubMedGoogle Scholar
  15. Dishaw LJ, Flores-Torres JA, Mueller MG, Karrer CR, Skapura DP, Melillo D, Zucchetti I, De Santis R, Pinto MR, Litman GW (2012) A basal chordate model for studies of gut microbial immune interactions. Front Immunol 3:96PubMedCentralCrossRefPubMedGoogle Scholar
  16. Dishaw LJ, Cannon JP, Litman GW, Parker W (2014a) Immune-directed support of rich microbial communities in the gut has ancient roots. Dev Comp Immunol 47:36–51PubMedCentralCrossRefPubMedGoogle Scholar
  17. Dishaw LJ, Flores-Torres J, Lax S, Gemayel K, Leigh B, Melillo D, Mueller MG, Natale L, Zucchetti I, De Santis R, Pinto MR, Litman GW, Gilbert JA (2014b) The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9, e93386Google Scholar
  18. Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K (2010) Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu Rev Immunol 28:243–273CrossRefPubMedGoogle Scholar
  19. Ghosh J, Lun CM, Majeske AJ, Sacchi S, Schrankel CS, Smith LC (2011) Invertebrate immune diversity. Dev Comp Immunol 35:959–974CrossRefPubMedGoogle Scholar
  20. Gough NM, Bernard O (1981) Sequences of the joining region genes for immunoglobulin heavy chains and their role in generation of antibody diversity. Proc Natl Acad Sci USA 78:509–513PubMedCentralCrossRefPubMedGoogle Scholar
  21. Hernandez Prada JA, Haire RN, Allaire M, Jakoncic J, Stojanoff V, Cannon JP, Litman GW, Ostrov DA (2006) Ancient evolutionary origin of diversified variable regions demonstrated by crystal structures of an immune-type receptor in amphioxus. Nat Immunol 7:875–882PubMedCentralCrossRefPubMedGoogle Scholar
  22. Hirano T, Nishida H (2000) Developmental fates of larval tissues after metamorphosis in ascidian Halocynthia roretziI. II. Origin of endodermal tissues of the juvenile. Dev Genes Evol 210:55–63CrossRefPubMedGoogle Scholar
  23. Holland LZ, Albalat R, Azumi K, Benito-Gutierrez E, Blow MJ, Bronner-Fraser M, Brunet F, Butts T, Candiani S, Dishaw LJ, Ferrier DE, Garcia-Fernandez J, Gibson-Brown JJ, Gissi C, Godzik A, Hallbook F, Hirose D, Hosomichi K, Ikuta T, Inoko H, Kasahara M, Kasamatsu J, Kawashima T, Kimura A, Kobayashi M, Kozmik Z, Kubokawa K, Laudet V, Litman GW, McHardy AC, Meulemans D, Nonaka M, Olinski RP, Pancer Z, Pennacchio LA, Pestarino M, Rast JP, Rigoutsos I, Robinson-Rechavi M, Roch G, Saiga H, Sasakura Y, Satake M, Satou Y, Schubert M, Sherwood N, Shiina T, Takatori N, Tello J, Vopalensky P, Wada S, Xu A, Ye Y, Yoshida K, Yoshizaki F, Yu JK, Zhang Q, Zmasek CM, de Jong PJ, Osoegawa K, Putnam NH, Rokhsar DS, Satoh N, Holland PW (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18:1100–1111PubMedCentralCrossRefPubMedGoogle Scholar
  24. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118CrossRefPubMedGoogle Scholar
  25. Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10:159–169CrossRefPubMedGoogle Scholar
  26. Jeuniaux C, Vossfoucart MF (1991) Chitin biomass and production in the marine-environment. Biochem Syst Ecol 19:347–356CrossRefGoogle Scholar
  27. Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 105:15064–15069PubMedCentralCrossRefPubMedGoogle Scholar
  28. Lang TA, Hansson GC, Samuelsson T (2007) Gel-forming mucins appeared early in metazoan evolution. Proc Natl Acad Sci USA 104:16209–16214PubMedCentralCrossRefPubMedGoogle Scholar
  29. Lee CG (2009) Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med J 50:22–30PubMedCentralCrossRefPubMedGoogle Scholar
  30. Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768–1773PubMedCentralCrossRefPubMedGoogle Scholar
  31. Liberti A, Melillo D, Zucchetti I, Natale L, Dishaw LJ, Litman GW, De Santis R, Pinto MR (2014) Expression of Ciona intestinalis variable region-containing chitin-binding proteins during development of the gastrointestinal tract and their role in host-microbe interactions. PLoS One 9, e94984Google Scholar
  32. Macpherson AJ, Mccoy KD, Johansen FE, Brandtzaeg P (2008) The immune geography of IgA induction and function. Mucosal Immunol 1:11–22CrossRefPubMedGoogle Scholar
  33. McFall-Ngai M (2007) Adaptive immunity: care for the community. Nature 445:153CrossRefPubMedGoogle Scholar
  34. Mostov KE, de Bruyn KA, Deitcher DL (1986) Deletion of the cytoplasmic tail of the polymeric immunoglobulin receptor prevents basolateral localization and endocytosis. Cell 47:359–364CrossRefPubMedGoogle Scholar
  35. Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295CrossRefPubMedGoogle Scholar
  36. Steward GF, Montiel JL, Azam F (2000) Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45:1697–1706CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Assunta Liberti
    • 1
  • Brittany Leigh
    • 2
  • Rosaria De Santis
    • 1
  • Maria Rosaria Pinto
    • 1
  • John P. Cannon
    • 3
  • Larry J. Dishaw
    • 3
  • Gary W. Litman
    • 3
  1. 1.Department of Animal Physiology and EvolutionStazione Zoologica Anton DohrnNapoliItaly
  2. 2.Department of Marine SciencesUniversity of South Florida St. PetersburgSt PetersburgUSA
  3. 3.Department of PediatricsUniversity of South Florida College of MedicineSt PetersburgUSA

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