A basal chordate model for studies of gut microbial immune interactions

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages

  Dishaw, Larry J ^a   Flores Torres, Jaime A ^a   Mueller, M Gail ^a,b   Karrer, Charlotte R ^b   Skapura, Diana P ^b   Melillo, Daniela ^c   Zucchetti, Ivana ^c   De Santis, Rosaria ^c   Pinto, Maria Rosaria ^c   Litman, Gary W ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b JOHNS HOPKINS ALL CHILDREN S HOSPITAL   (United States)

^c STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

Ciona; Gut epitheliums; Innate immunity; Microbiota; Protochordate

Indexed keywords

EID: 84874177229     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00096     Document Type: Article

References (100)

1. Abreu, M. T. (2010). Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 10, 131-144.
2. Agrawal,A.,Eastman,Q. M.,and Schatz, D. G. (1998). Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system Nature 394, 744-751.
3. Arizza, V., and Parrinello, D. (2009). Inflammatory hemocytes in Ciona intestinalis innate immune response. Invertebrate Surviv. J. 6, S58-S66.
4. Arizza, V., Parrinello, D., Cammarata, M., Vazzana, M., Vizzini, A., Giaramita, F. T., and Parrinello, N. (2011). A lytic mechanism based on soluble phospholipases A2 (sPLA2) and beta-galactoside specific lectins is exerted by Ciona intestinalis (ascidian) unilocular refractile hemocytes against K562 cell line and mammalian erythrocytes. Fish Shellfish Immunol. 30, 1014-1023.
5. Artis, D. (2008). Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8, 411-420.
6. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., Taniguchi, T., Takeda, K., Hori, S., Ivanov, I. I., Umesaki, Y., Itoh, K., and Honda, K. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331, 337-341.
7. Azumi, K., De Santis, R., De Tomaso, A., Rigoutsos, I., Yoshizaki, F., Pinto, M. R., Marino, R., Shida, K., Ikeda, M., Ikeda, M., Arai, M., Inoue, Y., Shimizu, T., Satoh, N., Rokhsar, D. S., Du Pasquier, L., Kasahara, M., Satake, M., and 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.
8. Baghdiguian, S., Martinand-Mari, C., and Mangeat, P. (2007). Using Ciona to study developmental programmed cell death. Semin. Cancer Biol. 17, 147-153.
9. Bischoff, S. C. (2011). "Gut health": a new objective in medicine? BMC Med. 9, 24. doi:10.1186/1741-7015-9-24
10. Bonura, A., Vizzini, A., Salerno, G., Parrinello, N., Longo, V., and Colombo, P. (2009). Isolation and expression of a novel MBL-like collectin cDNA enhanced by LPS injection in the body wall of the ascidian Ciona intestinalis. Mol. Immunol. 46, 2389-2394.
11. Bosch, T. C., Augustin, R., AntonErxleben, F., Fraune, S., Hemmrich, G., Zill, H., Rosenstiel, P., Jacobs, G., Schreiber, S., Leippe, M., Stanisak, M., Grotzinger, J., Jung, S., Podschun, R., Bartels, J., Harder, J., and Schroder, J. M. (2009). Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 33, 559-569.
12. Bosch, T. C., and McFall-Ngai, M. J. (2011). Metaorganisms as the new frontier. Zoology (Jena) 114, 185-190.
13. Burighel, P., and Cloney, R. A. (1977). "Urochordata: Ascidiacea," in Microscopic Anatomy of Invertebrates, Vol. 15: Hemichordata, Chaetognatha and the Invertebrate Chordates,edsF.W. Harrison and E. E. Ruppert, 221-347.
14. Cammarata, M., Arizza, V., Cianciolo, C., Parrinello, D., Vazzana, M., Vizzini, A., Salerno, G., and Parrinello,N. (2008). The prophenoloxidase system is activated during the tunic inflammatory reaction of Ciona intestinalis. Cell Tissue Res. 333, 481-492.
15. Canestro, C., Bassham, S., and Postlethwait, J. H. (2003). Seeing chordate evolution through the Ciona genome sequence. Genome Biol. 4, 208.
16. Cannon, J. P., Haire, R. N., and Litman, G. W. (2002). Identification of diversified genes that contain immunoglobulin-like variable regionsinaprotochordate.Nat. Immunol. 3, 1200-1207.
17. Caputi, L., Andreakis, N., Mastrototaro, F., Cirino, P., Vassillo, M., and Sordino, P. (2007). Cryptic speciation in a model invertebrate chordate. Proc. Natl. Acad. Sci. U.S.A. 104, 9364-9369.
18. Cebra, J. J. (1999). Influences of microbiota on intestinal immune system development. Am. J. Clin. Nutr. 69, 1046S-1051S.
19. Cebra, J. J., Periwal, S. B., Lee, G., Lee, F., and Shroff, K. E. (1998). Development and maintenance of the gut-associated lymphoid tissue (GALT): the roles of enteric bacteria and viruses. Dev. Immunol. 6, 13-18.
20. Chow, J., and Mazmanian, S. K. (2010). A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7, 265-276.
21. Christiaen, L., Wagner, E., Shi, W., and Levine, M. (2009). Isolation of individual cells and tissues from electroporated sea squirt (Ciona) embryos by fluorescence-activated cell sorting (FACS). Cold Spring Harb. Protoc. 2009, pdb.prot5349.
22. Chung, H., and Kasper, D. L. (2010). Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr. Opin. Immunol. 22, 455-460.
23. Cirino, P., Toscano, A., Caramiello, D., Macina, A., Miraglia, V., and Monte, A. (2002). Laboratory culture of the ascidian Ciona intestinalis (L.): a model system for molecular developmental biology research. Mar. Mod. Elec. Rec. [serial online]. Available at: http://www.mbl.edu/html/BB/MMER/CIR/CirTit. html
24. Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., and Weiser, J. N. (2010). Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16, 228-231.
25. Cooper, M. D., and Alder, M. N. (2006). The evolution of adaptive immune systems. Cell 124, 815-822.
26. Davidson, B. (2007). Ciona intestinalis as a model for cardiac development. Semin. Cell Dev. Biol. 18, 16-26.
27. Dehal, P., Satou, Y., Campbell, R. K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio,A., Gelpke, M., Goodstein, D. M., Harafuji, N., Hastings, K. E. M., Ho, I., Hotta, K., Huang, W., Kawashima, T., Lamaire, P., Martinez, D., Meinertzhagan, I. A., Necula, S., Nonaka, M., Putnam, N., Rash, S., Salga, H., Sataka, M., Terry, A., Yamada, L., Wang, H.-G., Awazu, S., Azumi, K., Boore, J., Branno, M., Chin-bow, S., DeSantis, R., Doyle, S., Francino, P., Keys, D. N., Haga, S., Hayashi, H., Hino, K., Imai, K. S., Inaba, K., Kano, S., Kobayashi, K., Kobayashi, M., Lee, B.-I., Makabe, K. W., Manohar, C., Matassi, G., Medina, M., Mochizuki, Y., Mount, S., Morishita, T., Miura, S., Nakayama, A., Nishizaka, S., Nomoto, H., Ohta, F., Oishi, K., Rigoutsos, I., Sano, M., Sasaki, A., Sasakura, Y., Shoguchi, E., Shin-i, T., Spagnuolo,A., Stainier, D., Suzuki, M. M., Tassy, O., Takatori, N., Tokuoka, M., Yagi, K., Yoshizaki, F., Wada, S., Zhang, C., Hyatt, P. D., Larimer, F., Detter, C., Doggett, N., Glavina, T., Hawkins, T., Richardson, P., Lucas, S., Kohara, Y., Levine, M., Satoh, N., and Rokhsar, D. S. (2002). The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298, 2157-2160.
28. Denoeud, F., Henriet, S., Mungpakdee, S., Aury, J. M., Da Silva, C., Brinkmann, H., Mikhaleva, J., Olsen, L. C., Jubin, C., Canestro, C., Bouquet, J. M., Danks, G., Poulain, J., Campsteijn, C., Adamski, M., Cross, I., Yadetie, F., Muffato, M., Louis, A., Butcher, S., Tsagkogeorga, G., Konrad, A., Singh, S., Jensen, M. F., Cong, E. H., Eikeseth-Otteraa, H., Noel, B., Anthouard, V., Porcel, B. M., Kachouri-Lafond, R., Nishino, A., Ugolini, M., Chourrout, P., Nishida, H., Aasland, R., Huzurbazar, S., Westhof, E., Delsuc, F., Lehrach, H., Reinhardt, R., Weissenbach, J., Roy, S. W., Artiguenave, F., Postlethwait, J. H., Manak, J. R., Thompson, E. M., Jaillon, O., Du Pasquier, L., Boudinot, P., Liberles, D. A., Volff, J. N., Philippe, H., Lenhard, B., Crollius, H. R.,Wincker, P., and Chourrout, D. (2010). Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330, 1381-1385.
29. Di Bella, M. A., and De Leo, G. (2000). Hemocyte migration during inflammatory-like reaction of Ciona intestinalis (Tunicata, Ascidiacea). J Invertebr. Pathol. 76, 105-111.
30. Dishaw, L. J., Giacomelli, S., Melillo, D., Zucchetti, I., Haire, R. N., Natale, L., Russo, N. A., De Santis, R., Litman, G. W., and Pinto, M. R. (2011). A role for variable regioncontaining chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc. Natl. Acad. Sci. U.S.A. 108, 16747-16752.
31. Dreyfus, D. H. (1992). Evidence suggesting an evolutionary relationship between transposable elements and immune system recombination sequences. Mol. Immunol. 29, 807-810.
32. Duerkop, B. A., Vaishnava, S., and Hooper, L. V. (2009). Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31, 368-376.
33. Edelman, S. M., and Kasper, D. L. (2008). Symbiotic commensal bacteria direct maturation of the host immune system. Curr. Opin. Gastroenterol. 24, 720-724.
34. Ermak, T. H. (1981). A comparison of cell proliferation patterns in the digestive track of ascidians. J. Exp. Zool. 217, 325-339.
35. Fedders, H., and Leippe, M. (2008). A reverse search for antimicrobial peptides in Ciona intestinalis: identification of a gene family expressed in hemocytes and evaluation of activity. Dev. Comp. Immunol. 32, 286-298.
36. Feng, T., and Elson, C. O. (2011). Adaptive immunity in the host-microbiota dialog. Mucosal Immunol. 4, 15-21.
37. Flajnik, M. F., and Kasahara, M. (2010). Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11, 47-59.
38. Fujimura, K. E., Slusher, N. A., Cabana, M. D., and Lynch, S. V. (2010). Role of the gut microbiota in defining human health. Expert Rev. Anti Infect. Ther. 8, 435-454.
39. Fujita, T., Endo, Y., and Nonaka, M. (2004). Primitive complement system-recognition and activation. Mol. Immunol. 41, 103-111.
40. Holland, L. Z., Albalat, R., Azumi, K., Benito-Gutierrez, E., Blow, M. J., Bronner-Fraser,M.,Brunet,F.,Butts, T., Candiani, S., Dishaw, L. J., Ferrier, D. E., Garcia-Fernandez, J., GibsonBrown, J. J., 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, G. W., McHardy, A. C., Meulemans, D.,Nonaka,M.,Olinski,R. P.,Pancer, Z., Pennacchio, L. A., Pestarino, M., Rast, J. P., Rigoutsos, I., RobinsonRechavi, 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, J. K., Zhang, Q., Zmasek, C. M., de Jong, P. J., Osoegawa, K., Putnam, N. H., Rokhsar, D. S., Satoh, N., and Holland, P. W. (2008). The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100-1111.
41. Hooper, L. V., and Gordon, J. I. (2001). Commensal host-bacterial relationships in the gut. Science 292, 1115-1118.
42. Hooper, L. V., and Macpherson, A. J. (2010). Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10, 159-169.
43. Hughes, A. L., and Friedman, R. (2005). Loss of ancestral genes in the genomic evolution of Ciona intestinalis. Evol. Dev. 7, 196-200.
44. Ikuta,T.,Satoh,N.,and Saiga,H. (2010). Limited functions of Hox genes in the larval development of the ascidian Ciona intestinalis. Development 137, 1505-1513.
45. Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., and Littman, D. R. (2009). Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498.
46. Joly, J., Kano, S., Matsuoka, T., Auger, H., Hirayama, K., Satoh, N., Awazu, S., Legendre, L., and Sasakura, Y. (2007). Culture of Ciona intestinalis in closed systems. Dev. Dyn. 236, 1832-1840.
47. Kanther, M., and Rawls, J. F. (2010). Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 22, 10-19.
48. Katz, M. J. (1983). Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biol. Bull. 164, 1-27.
49. Kubo, A., Suzuki, N., Yuan, X., Nakai, K., Satoh, N., Imai, K. S., and Satou, Y. (2010). Genomic cis-regulatory networks in the early Ciona intestinalis embryo. Development 137, 1613-1623.
50. Lathrop, S. K., Bloom, S. M., Rao, S. M., Nutsch, K., Lio, C. W., Santacruz, N., Peterson, D. A., Stappenbeck, T. S., and Hsieh, C. S. (2011). Peripheral education of the immune system by colonic commensal microbiota. Nature 478, 250-254.
51. Lavelle, E. C., Murphy, C., O'Neill, L. A., and Creagh, E. M. (2010). The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol. 3, 17-28.
52. Lee, Y. K., and Mazmanian, S. K. (2010). Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330, 1768-1773.
53. Lemaire, P., Smith, W. C., and Nishida, H. (2008). Ascidians and the plasticity of the chordate developmental program. Curr. Biol. 18, R620-R631.
54. Leulier, F., and Lemaitre, B. (2008). Tolllike receptors -taking an evolutionary approach. Nat. Rev. Genet. 9, 165-178.
55. Litman, G. W., Rast, J. P., and Fugmann, S. D. (2010). Origins of vertebrate adaptive immunity. Nat. Rev. Immunol. 10, 543-553.
56. Lotz, M., Gutle, D., Walther, S., Menard, S., Bogdan, C., and Hornef, M. W. (2006). Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J. Exp. Med. 203, 973-984.
57. Lyczak, J. B. (2003). Commensal bacteria increase invasion of intestinal epithelium by Salmonella enterica serovar Typhi. Infect. Immun. 71, 6610-6614.
58. Maldonado-Contreras, A. L., and McCormick, B. A. (2011). Intestinal epithelial cells and their role in innate mucosal immunity. Cell Tissue Res. 343, 5-12.
59. Mans, J. J., von Lackum, K., Dorsey, C., Willis, S., Wallet, S. M., Baker, H. V., Lamont, R. J., and Handfield, M. (2009). The degree of microbiome complexity influences the epithelial response to infection. BMC Genomics 10, 380. doi:10.1186/1471-2164-10-380
60. Marchiando, A. M., Graham, W. V., and Turner, J. R. (2010). Epithelial barriers in homeostasis and disease. Annu. Rev. Pathol. 5, 119-144.
61. Marino, R., Kimura, Y., De Santis, R., Lambris, J. D., and Pinto, M. R. (2002). Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53, 1055-1064.
62. Maslowski, K. M., and Mackay, C. R. (2011). Diet, gut microbiota and immune responses. Nat. Immunol. 12, 5-9.
63. Matsunaga, T., and Rahman, A. (1998). What brought the adaptive immune system to vertebrates? -The jaw hypothesis and the seahorse. Immunol. Rev. 166, 177-186.
64. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., and Kasper, D. L. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107-118.
65. McFall-Ngai, M. (2007). Adaptive immunity: care for the community. Nature 445, 153-153.
66. Meinertzhagen, I. A., and Okamura, Y. (2001). The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci. 24, 401-410.
67. Melillo, D., Sfyroera, G., De Santis, R., Graziano, R., Marino, R., Lambris, J. D., and Pinto, M. R. (2006). First identification of a chemotactic receptor in an invertebrate species: structural and functional characterization of Ciona intestinalis C3a receptor. J. Immunol. 177, 4132-4140.
68. Messier-Solek, C., Buckley, K. M., and Rast, J. P. (2010). Highly diversified innate receptor systems and new forms of animal immunity. Semin. Immunol. 22, 39-47.
69. Millar, R. H. (1953). Ciona, Liverpool: University Press of Liverpool, 1-122.
70. Muller, C. A., Autenrieth, I. B., and Peschel, A. (2005). Innate defenses of the intestinal epithelial barrier. Cell. Mol. Life Sci. 62, 1297-1307.
71. Nell, S., Suerbaum, S., and Josenhans, C. (2010). The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat. Rev. Microbiol. 8, 564-577.
72. Nishida, H., Satoh, N., and Hirose, E. (2010). More diversity and more convergence in tunicate biology. Zool. Sci. 27, 67-68.
73. Ohland, C. L., and Macnaughton, W. K. (2010). Probiotic bacteria and intestinal epithelial barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G807-G819.
74. Parrinello, N. (2009). Focusing on Ciona intestinalis (tunicate) innate immune system. Evolutionary implications. Invertebrate Surviv. J. 6, S46-S57.
75. Parrinello, N., Arizza, V., Cammarata, M., Giaramita, F. T., Pergolizzi, M., Vazzana, M., Vizzini, A., and Parrinello, D. (2007). Inducible lectins with galectin properties and human IL1alpha epitopes opsonize yeast during the inflammatory response of the ascidian Ciona intestinalis. Cell Tissue Res. 329, 379-390.
76. Parrinello, N., Cammarata, M., and Arizza, V. (1996). Univacuolar refractile hemocytes from the tunicate Ciona intestinalis are cytotoxic for mammalian erythrocytes in vitro. Biol. Bull. 190, 418-425.
77. Parrinello, N., Vizzini, A., Arizza, V., Salerno, G., Parrinello, D., Cammarata, M., Giaramita, F. T., and Vazzana, M. (2008). Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res. 334, 305-317.
78. Parrinello, N., Vizzini, A., Salerno, G., Sanfratello, M. A., Cammarata, M., Arizza, V., Vazzana, M., and Parrinello, D. (2010). Inflamed adult pharynx tissues and swimming larva of Ciona intestinalis share CiTNFalpha-producing cells. Cell Tissue Res. 341, 299-311.
79. Pinto, M. R., Chinnici, C. M., Kimura, Y., Melillo, D., Marino, R., Spruce, L. A., De Santis, R., Parrinello, N., and Lambris, J. D. (2003). CiC3-1a-mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J. Immunol. 171, 5521-5528.
80. Rast, J. P., and Messier-Solek, C. (2008). Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol. Bull. 214, 274-283.
81. Rast, J. P., Smith, L. C., Loza-Coll, M., Hibino, T., and Litman, G. W. (2006). Genomic insights into the immune system of the sea urchin. Science 314, 952-956.
82. Rautava, S., and Walker, W. A. (2007). Commensal bacteria and epithelial cross talk in the developing intestine. Curr. Gastroenterol. Rep. 9, 385-392.
83. Rescigno, M., and Di, Sabatino, A. (2009). Dendritic cells in intestinal homeostasis and disease. J. Clin. Invest. 119, 2441-2450.
84. Round, J. L., and Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323.
85. Sasaki, N., Ogasawara, M., Sekiguchi, T., Kusumoto, S., and Satake, H. (2009). Toll-like receptors of the ascidian Ciona intestinalis: prototypes with hybrid functionalities of vertebrate Toll-like receptors. J. Biol. Chem. 284, 27336-27343.
86. Sasakura, Y., Inaba, K., Satoh, N., Kondo, M., and Akasaka, K. (2009). Ciona intestinalis and Oxycomanthus japonicus, representatives of marine invertebrates. Exp. Anim. 58, 459-469.
87. Sasakura, Y., Suzuki, M. M., Hozumi, A., Inaba, K., and Satoh, N. (2010). Maternal factor-mediated epigenetic gene silencing in the ascidian Ciona intestinalis. Mol. Genet. Genomics 283, 99-110.
88. Satoh, N., and Levine, M. (2005). Surfing with the tunicates into the post-genome era. Genes Dev. 19, 2407-2411.
89. Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annu.Rev.Microbiol.31, 107-133.
90. Sekirov, I., Russell, S. L., Antunes, L. C., and Finlay, B. B. (2010). Gut microbiota in health and disease. Physiol. Rev. 90, 859-904.
91. Shi, W., Levine, M., and Davidson, B. (2005). Unraveling genomic regulatory networks in the simple chordate, Ciona intestinalis. Genome Res. 15, 1668-1674.
92. Shida, K., Terajima, D., Uchino, R., Ikawa, S., Ikeda, M., Asano, K., Watanabe, T., Azumi, K., Nonaka, M., Satou, Y., Satoh, N., Satake, M., Kawazoe, Y., and Kasuya, A. (2003). Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem. Biophys. Res. Commun. 302, 207-218.
93. Skjoedt, M. O., Palarasah, Y., Rasmussen, K., Vitved, L., Salomonsen, J., Kliem, A., Hansen, S., Koch, C., and Skjodt, K. (2010). Two mannose-binding lectin homologues and an MBL-associated serine protease are expressed in the gut epithelia of the urochordate species Ciona intestinalis. Dev. Comp. Immunol. 34, 59-68.
94. Smith, V. J., and Peddie, C. M. (1992). Cell cooperation during host defense in the solitary tunicate Ciona intestinalis (L). Biol. Bull. 183, 211-219.
95. Terajima, D., Shida, K., Takada, N., Kasuya, A., Rokhsar, D., Satoh, N., Satake, M., and Wang, H. G. (2003). Identification of candidate genes encoding the core components of the cell death machinery in the Ciona intestinalis genome. Cell Death Differ. 10, 749-753.
96. Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809.
97. Usharauli, D. (2010). Chronic infection and the origin of adaptive immune system. Med. Hypotheses 75, 241-243.
98. Willing, B. P., Antunes, L. C., Keeney, K. M., Ferreira, R. B., and Finlay, B. B. (2011). Harvesting the biological potential of the human gut microbiome. Bioessays 33, 414-418.
99. Yonge, C. M. (1925). Studies on the comparative physiology of digestion. III. Secretion, digestion, and assimilation in the gut of Ciona intestinalis. J. Exp. Biol. 2, 373-388.
100. Zucchetti, I., De Santis, R., Grusea, S., Pontarotti, P., and Du Pasquier, L. (2009). Origin and evolution of the vertebrate leukocyte receptors: the lesson from tunicates. Immunogenetics 61, 463-481.