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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
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–G929
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 55:570–581
Bainard JD, Gregory TR (2013) Genome size evolution: patterns, mechanisms, and methodological advances. Genome 56:Vii–Viii
Berrill NJ (1947) The development and growth of Ciona. J Mar Biol Assoc UK 26:616–625
Boehm T (2007) Two in one: dual function of an invertebrate antigen receptor. Nat Immunol 8:1031–1033
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 109:580–587
Burighel P, Cloney RA (1997) Urochordata: Ascidiacea. In: Harrison FW, Ruppert EE (eds) Microscopic analysis of invertebrates. Wiley-Liss, New York, pp 221–347
Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3:1200–1207
Cannon JP, Haire RN, Schnitker N, Mueller MG, Litman GW (2004) Individual protochordates have unique immune-type receptor repertoires. Curr Biol 14:R465–R466
Craig SW, Cebra JJ (1971) Peyer’s patches – enriched source of precursors for iga-producing immunocytes in rabbit. J Exp Med 134:188–200
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
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 9:78
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 62:623–631
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 108:16747–16752
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 3:96
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 47:36–51
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, e93386
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 28:243–273
Ghosh J, Lun CM, Majeske AJ, Sacchi S, Schrankel CS, Smith LC (2011) Invertebrate immune diversity. Dev Comp Immunol 35:959–974
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 78:509–513
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 7:875–882
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 210:55–63
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 18:1100–1111
Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118
Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10:159–169
Jeuniaux C, Vossfoucart MF (1991) Chitin biomass and production in the marine-environment. Biochem Syst Ecol 19:347–356
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 105:15064–15069
Lang TA, Hansson GC, Samuelsson T (2007) Gel-forming mucins appeared early in metazoan evolution. Proc Natl Acad Sci USA 104:16209–16214
Lee CG (2009) Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med J 50:22–30
Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768–1773
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, e94984
Macpherson AJ, Mccoy KD, Johansen FE, Brandtzaeg P (2008) The immune geography of IgA induction and function. Mucosal Immunol 1:11–22
McFall-Ngai M (2007) Adaptive immunity: care for the community. Nature 445:153
Mostov KE, de Bruyn KA, Deitcher DL (1986) Deletion of the cytoplasmic tail of the polymeric immunoglobulin receptor prevents basolateral localization and endocytosis. Cell 47:359–364
Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295
Steward GF, Montiel JL, Azam F (2000) Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45:1697–1706
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Liberti, A. et al. (2015). An Immune Effector System in the Protochordate Gut Sheds Light on Fundamental Aspects of Vertebrate Immunity. 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_7
Download citation
DOI: https://doi.org/10.1007/978-3-319-20819-0_7
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-20818-3
Online ISBN: 978-3-319-20819-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)