Immune-directed support of rich microbial communities in the gut has ancient roots

Developmental and Comparative Immunology

Volumn 47, Issue 1, 2014, Pages 36-51

  Dishaw, Larry J ^a   Cannon, John P ^a   Litman, Gary W ^a,b   Parker, William ^c  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

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

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Ciona intestinalis; Gut biofilms; Gut host microbe interactions; Gut immune effectors; Gut immune evolution; Mutualism

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; BACTERIAL COLONIZATION; CIONA INTESTINALIS; DIGESTIVE SYSTEM; DROSOPHILA; GENE EXPRESSION; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HYDRA; INNATE IMMUNITY; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIAL GROWTH; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STOMACH PH; SYMBIOSIS; ANIMAL; ANIMAL MODEL; CHORDATA; CNIDARIA; EVOLUTION; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; MAMMAL; MICROBIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; CHORDATA; CIONA INTESTINALIS; CNIDARIA; GASTROINTESTINAL TRACT; HUMANS; MAMMALS; MODELS, ANIMAL;

EID: 84904057761     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2014.06.011     Document Type: Review

References (295)

1. Abreu M.T. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 2010, 10:131-144.
2. Agostini S., Suzuki Y., Higuchi T., Casareto B.E., Yoshinaga K., Nakano Y., Fujimura H. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 2012, 31:147-156.
3. Amaro T., Witte H., Herndl G.J., Cunha M.R., Billett D.S.M. Deep-sea bacterial communities in sediments and guts of deposit-feeding holothurians in Portuguese canyons (NE Atlantic). Deep-Sea Res. I 2009, 56:1834-1843.
4. Andersson A.F., Lindberg M., Jakobsson H., Backhed F., Nyren P., Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 2008, 3:e2836.
5. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8:411-420.
6. Atarashi K., Umesaki Y., Honda K. Microbiotal influence on T cell subset development. Semin. Immunol. 2011, 23:146-153.
7. Augustin R., Fraune S., Franzenburg S., Bosch T.C. Where simplicity meets complexity: hydra, a model for host-microbe interactions. Adv. Exp. Med. Biol. 2012, 710:71-81.
8. Aychek T., Jung S. Immunology. The axis of tolerance. Science 2014, 343:1439-1440.
9. Azumi K., De Santis R., De Tomaso A., Rigoutsos I., Yoshizaki F., Pinto M.R., Marino R., Shida K., Ikeda M., Arai M., Inoue Y., Shimizu T., Satoh N., Rokhsar D.S., Du Pasquier L., Kasahara M., Satake M., Nonaka M. Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: "waiting for Godot". Immunogenetics 2003, 55:570-581.
10. Bachere E., Gueguen Y., Gonzalez M., de Lorgeril J., Garnier J., Romestand B. Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol. Rev. 2004, 198:149-168.
11. Baghdiguian S., Martinand-Mari C., Mangeat P. Using Ciona to study developmental programmed cell death. Semin. Cancer Biol. 2007, 17:147-153.
12. Bates J., Mittge E., Kuhlman J., Baden K., Cheesman S., Guillemin K. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 2006, 297:374-386.
13. Bickler S.W., DeMaio A. Western diseases: current concepts and implications for pediatric surgery research and practice. Pediatr. Surg. Int. 2008, 24:251-255.
14. Bilbo S.D., Wray G.A., Perkins S.E., Parker W. Reconstitution of the human biome as the most reasonable solution for epidemics of allergic and autoimmune diseases. Med. Hypotheses 2011, 77:494-504.
15. Blum J.E., Fischer C.N., Miles J., Handelsman J. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio 2013, 4. e00860-e00813.
16. Bodenmiller B., Malmstrom J., Gerrits B., Campbell D., Lam H., Schmidt A., Rinner O., Mueller L.N., Shannon P.T., Pedrioli P.G., Panse C., Lee H.K., Schlapbach R., Aebersold R. PhosphoPep-a phosphoproteome resource for systems biology research in Drosophila Kc167 cells. Mol. Syst. Biol. 2007, 3:139.
17. Boehm A.M., Khalturin K., Anton-Erxleben F., Hemmrich G., Klostermeier U.C., Lopez-Quintero J.A., Oberg H.H., Puchert M., Rosenstiel P., Wittlieb J., Bosch T.C. FoxO is a critical regulator of stem cell maintenance in immortal Hydra. Proc. Natl. Acad. Sci. USA 2012, 109:19697-19702.
18. Bollinger R.R., Everett M.L., Palestrant D., Love S.D., Lin S.S., Parker W. Human secretory immunoglobulin A may contribute to biofilm formation in the gut. Immunology 2003, 109:580-587.
19. Bollinger R.R., Everett M.L., Wahl S.D., Lee Y.H., Orndorff P.E., Parker W. Secretory IgA and mucin-mediated biofilm formation by environmental strains of Escherichia coli: role of type 1 pili. Mol. Immunol. 2006, 43:378-387.
20. Bosch T.C. Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu. Rev. Microbiol. 2013, 67:499-518.
21. Bosch T.C., Augustin R., Anton-Erxleben 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., Schroder J.M. Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 2009, 33:559-569.
22. Bosch T.C., McFall-Ngai M.J. Metaorganisms as the new frontier. Zoology 2011, 114:185-190.
23. Broderick N.A., Lemaitre B. Gut-associated microbes of Drosophila melanogaster. Gut Microbes 2012, 3:307-321.
24. Brown F.D., Prendergast A., Swalla B.J. Man is but a worm: chordate origins. Genesis 2008, 46:605-613.
25. Buchon N., Broderick N., Poidevin M., Pradervand S., Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 2009, 5:200-211.
26. Buchon N., Broderick N.A., Chakrabarti S., Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009, 23:2333-2344.
27. Buchon N., Broderick N.A., Lemaitre B. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 2013, 11:615-626.
28. Buchon N., Osman D., David F.P., Fang H.Y., Boquete J.P., Deplancke B., Lemaitre B. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 2013, 3:1725-1738.
29. Burighel P., Cloney R.A. Urochordata: Ascidiacea, Microscopic Anatomy of Invertebrates, vol. 15: Hemichordates, Chaetognatha, and the Invertebrate Chordates 1997, Wiley-Liss, pp. 221-347.
30. Byrne M. The morphology of autotomy structures in the sea cucumber Eupentacta quinquesemita before and during evisceration. J. Exp. Biol. 2001, 204:849-863.
31. Cabreiro F., Gems D. Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans. EMBO Mol. Med. 2013, 5:1300-1310.
32. Cameron C.B., Garey J.R., Swalla B.J. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc. Natl. Acad. Sci. USA 2000, 97:4469-4474.
33. Cañestro C., Bassham S., Postlethwait J. Seeing chordate evolution through the Ciona genome sequence. Genome Biol. 2003, 4:208.
34. Cario E., Brown D., McKee M., Lynch-Devaney K., Gerken G., Podolsky D.K. Commensal-associated molecular patterns induce selective toll-like receptor-trafficking from apical membrane to cytoplasmic compartments in polarized intestinal epithelium. Am. J. Pathol. 2002, 160:165-173.
35. Cario E., Podolsky D. Intestinal epithelial TOLLerance versus inTOLLerance of commensals. Mol. Immunol. 2005, 42:887-893.
36. Casali P., Schettino E.W. Structure and function of natural antibodies. Curr. Top. Microbiol. Immunol. 1996, 210:167-179.
37. Cavanaugh C.M., Gardiner S.L., Jones M.L., Jannasch H.W., Waterbury J.B. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 1981, 213:340-342.
38. Cebra J.J. Influences of microbiota on intestinal immune system development. Am. J. Clin. Nutr. 1999, 69:1046S-1051S.
39. Cebra J.J., Periwal S.B., Lee G., Lee F., Shroff K.E. Development and maintenance of the gut-associated lymphoid tissue (GALT): the roles of enteric bacteria and viruses. Dev. Immunol. 1998, 6:13-18.
40. Chan Y.K., Estaki M., Gibson D.L. Clinical consequences of diet-induced dysbiosis. Ann. Nutr. Metab. 2013, 63(Suppl 2):28-40.
41. Chandler J.A., Lang J.M., Bhatnagar S., Eisen J.A., Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 2011, 7:e1002272.
42. Charroux B., Royet J. Drosophila immune response: From systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract. Fly 2010, 4:40-47.
43. Choi K.Y., Chow L.N., Mookherjee N. Cationic host defence peptides: multifaceted role in immune modulation and inflammation. J. Innate Immun. 2012, 4:361-370.
44. Chow J., Mazmanian S. Getting the bugs out of the immune system: do bacterial microbiota "fix" intestinal T cell responses?. Cell Host Microbe 2009, 5:8-12.
45. Chow J., Mazmanian S.K. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 2010, 7:265-276.
46. Chung H., Pamp S.J., Hill J.A., Surana N.K., Edelman S.M., Troy E.B., Reading N.C., Villablanca E.J., Wang S., Mora J.R., Umesaki Y., Mathis D., Benoist C., Relman D.A., Kasper D.L. Gut immune maturation depends on colonization with a host-specific microbiota. Cell 2012, 149:1578-1593.
47. Clarke T., Davis K., Lysenko E., Zhou A., Yu Y., Weiser J. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 2010, 16:228-231.
48. Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science 2009, 326:1694-1697.
49. Cuomo A., Bonaldi T. Systems biology "on-the-fly": SILAC-based quantitative proteomics and RNAi approach in Drosophila melanogaster. Methods Mol. Biol. 2010, 662:59-78.
50. Dalmasso G., Nguyen H.T., Yan Y., Laroui H., Charania M.A., Ayyadurai S., Sitaraman S.V., Merlin D. Microbiota modulate host gene expression via microRNAs. PLoS ONE 2011, 6:e19293.
51. Davidson B. Ciona intestinalis as a model for cardiac development. Semin. Cell Dev. Biol. 2007, 18:16-26.
52. Davidson E.H. The sea urchin genome: where will it lead us?. Science 2006, 314:939-940.
53. de Morais Guedes S., Vitorino R., Domingues R., Tomer K., Correia A.J., Amado F., Domingues P. Proteomics of immune-challenged Drosophila melanogaster larvae hemolymph. Biochem. Biophys. Res. Commun. 2005, 328:106-115.
54. Dehal P., Satou Y., Campbell R., Chapman J., Degnan B., De Tomaso A., Davidson B., Di Gregorio A., Gelpke M., Goodstein D., Harafuji N., Hastings K., Ho I., Hotta K., Huang W., Kawashima T., Lemaire P., Martinez D., Meinertzhagen I., Necula S., Nonaka M., Putnam N., Rash S., Saiga H., Satake M., Terry A., Yamada L., Wang H., Awazu S., Azumi K., Boore J., Branno M., Chin-Bow S., DeSantis R., Doyle S., Francino P., Keys D., Haga S., Hayashi H., Hino K., Imai K., Inaba K., Kano S., Kobayashi K., Kobayashi M., Lee B., Makabe K., 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., Tassy O., Takatori N., Tokuoka M., Yagi K., Yoshizaki F., Wada S., Zhang C., Hyatt P., Larimer F., Detter C., Doggett N., Glavina T., Hawkins T., Richardson P., Lucas S., Kohara Y., Levine M., Satoh N., Rokhsar D. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298:2157-2167.
55. Deplancke B., Gaskins H.R. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr. 2001, 73:1131S-1141S.
56. Deppe U., Schierenberg E., Cole T., Krieg C., Schmitt D., Yoder B., von Ehrenstein G. Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1978, 75:376-380.
57. Derrien M., van Passel M.W., van de Bovenkamp J.H., Schipper R.G., de Vos W.M., Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 2010, 1:254-268.
58. Di Bella M.A., Fedders H., De Leo G., Leippe M. Localization of antimicrobial peptides in the tunic of Ciona intestinalis (Ascidiacea, Tunicata) and their involvement in local inflammatory-like reactions. Results Immunol. 2011, 1:70-75.
59. Diamond G., Beckloff N., Weinberg A., Kisich K.O. The roles of antimicrobial peptides in innate host defense. Curr. Pharm. Des. 2009, 15:2377-2392.
60. Dishaw L.J., Flores-Torres J., Lax S., Gemayel K., Leigh B., Melillo D., Mueller M.G., Natale L., Zucchetti I., De Santis R., Pinto M.R., Litman G.W., Gilbert J.A. The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS ONE 2014, 9:e93386.
61. Dishaw L.J., Flores-Torres J.A., Mueller M.G., Karrer C.R., Skapura D.P., Melillo D., Zucchetti I., De Santis R., Pinto M.R., Litman G.W. A basal chordate model for studies of gut microbial immune interactions. Front. Immunol. 2012, 3:96.
62. Dishaw L.J., Giacomelli S., Melillo D., Zucchetti I., Haire R.N., Natale L., Russo N.A., De Santis R., Litman G.W., Pinto M.R. A role for variable region-containing chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc. Natl. Acad. Sci. USA 2011, 108:16747-16752.
63. Dishaw L.J., Haire R.N., Litman G.W. The amphioxus genome provides unique insight into the evolution of immunity. Brief. Funct. Genomics 2012, 11:167-176.
64. Drake H.L., Horn M.A. As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu. Rev. Microbiol. 2007, 61:169-189.
65. Duerkop B.A., Vaishnava S., Hooper L.V. Immune responses to the microbiota at the intestinal mucosal surface. Immunity 2009, 31:368-376.
66. Duerr C.U., Hornef M.W. The mammalian intestinal epithelium as integral player in the establishment and maintenance of host-microbial homeostasis. Semin. Immunol. 2012, 24:25-35.
67. Eberl G. A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol. 2010, 3:450-460.
68. Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E., Relman D.A. Diversity of the human intestinal microbial flora. Science 2005, 308:1635-1638.
69. Edelman S., Kasper D. Symbiotic commensal bacteria direct maturation of the host immune system. Curr. Opin. Gastroenterol. 2008, 24:720-724.
70. Engel P., Martinson V.G., Moran N.A. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. USA 2012, 109:11002-11007.
71. Engstrom Y., Loseva O., Theopold U. Proteomics of the Drosophila immune response. Trends Biotechnol. 2004, 22:600-605.
72. Equileor M.d., Ottaviani E. The central role of immunity in the symbiotic event referred as parasitism. Invert. Surv. J. 2011, 8:227-230.
73. Eri R., Chieppa M. Messages from the inside. The dynamic environment that favors intestinal homeostasis. Front. Immunol. 2013, 4:323.
74. Ermak T.H. A comparison of cell proliferation patterns in the digestive tract of ascidians. J. Exp. Zool. 1981, 217:325-339.
75. Everett M.L., Palestrant D., Miller S.E., Bollinger R.B., Parker W. Immune exclusion and immune inclusion: a new model of host-bacterial interactions in the gut. Clin. Appl. Immunol. Rev. 2004, 5:321-332.
76. Falk P.G., Hooper L.V., Midtvedt T., Gordon J.I. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 1998, 62:1157-1170.
77. Fallucca F., Porrata C., Fallucca S., Pianesi M. Influence of diet on gut microbiota, inflammation and type 2 diabetes mellitus. First experience with macrobiotic Ma-Pi 2 diet. Diabetes Metab. Res. Rev. 2014, 30:48-54.
78. Faust K., Sathirapongsasuti J.F., Izard J., Segata N., Gevers D., Raes J., Huttenhower C. Microbial co-occurrence relationships in the human microbiome. PLoS Comp. Biol. 2012, 8:e1002606.
79. Fedders H., Leippe M. A reverse search for antimicrobial peptides in Ciona intestinalis: identification of a gene family expressed in hemocytes and evaluation of activity. Dev. Comp. Immunol. 2008, 32:286-298.
80. Fischbach M.A., Sonnenburg J.L. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 2011, 10:336-347.
81. Franzenburg S., Fraune S., Altrock P.M., Kunzel S., Baines J.F., Traulsen A., Bosch T.C. Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. ISME J. 2013, 7:781-790.
82. Franzenburg S., Walter J., Kunzel S., Wang J., Baines J.F., Bosch T.C., Fraune S. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl. Acad. Sci. USA 2013, 110:E3730-3738.
83. Fraune S., Abe Y., Bosch T.C. Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environ. Microbiol. 2009, 11:2361-2369.
84. Fraune S., Augustin R., Anton-Erxleben F., Wittlieb J., Gelhaus C., Klimovich V.B., Samoilovich M.P., Bosch T.C. In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proc. Natl. Acad. Sci. USA 2010, 107:18067-18072.
85. Fraune S., Bosch T.C. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc. Natl. Acad. Sci. USA 2007, 104:13146-13151.
86. Friman V., Adlerberth I., Connell H., Svanborg C., Hanson L.A., Wold A.E. Decreased expression of mannose-specific adhesins by Escherichia coli in the colonic microflora of immunoglobulin A-deficient individuals. Infect. Immun. 1996, 64:2794-2798.
87. Fujimura K., Slusher N., Cabana M., Lynch S. Role of the gut microbiota in defining human health. Expert. Rev. Anti. Infect. Ther. 2010, 8:435-454.
88. Fujita T., Endo Y., Nonaka M. Primitive complement system-recognition and activation. Mol. Immunol. 2004, 41:103-111.
89. Galili U., Wang L., LaTemple D.C., Radic M.Z. The natural anti-Gal antibody. Sub-Cell. Biochem. 1999, 32:79-106.
90. Garigan D., Hsu A.L., Fraser A.G., Kamath R.S., Ahringer J., Kenyon C. Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 2002, 161:1101-1112.
91. Gewirtz A.T., Navas T.A., Lyons S., Godowski P.J., Madara J.L. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 2001, 167:1882-1885.
92. Ghosh J., Buckley K.M., Nair S.V., Raftos D.A., Miller C., Majeske A.J., Hibino T., Rast J.P., Roth M., Smith L.C. Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev. Comp. Immunol. 2010, 34:235-245.
93. Gibbons S.M., Caporaso J.G., Pirrung M., Field D., Knight R., Gilbert J.A. Evidence for a persistent microbial seed bank throughout the global ocean. Proc. Natl. Acad. Sci. USA 2013, 110:4651-4655.
94. Gilbert D.G. DroSpeGe: rapid access database for new Drosophila species genomes. Nucleic Acids Res. 2007, 35:D480-485.
95. Gill S.R., Pop M., Deboy R.T., Eckburg P.B., Turnbaugh P.J., Samuel B.S., Gordon J.I., Relman D.A., Fraser-Liggett C.M., Nelson K.E. Metagenomic analysis of the human distal gut microbiome. Science 2006, 312:1355-1359.
96. Glittenberg M.T., Kounatidis I., Christensen D., Kostov M., Kimber S., Roberts I., Ligoxygakis P. Pathogen and host factors are needed to provoke a systemic host response to gastrointestinal infection of Drosophila larvae by Candida albicans. Dis. Model Mech. 2011, 4:515-525.
97. Goddard C.K., Hoggett A.K. Gut contents of the ascidian Pyura praeputialis: endogenous and exogenous components. J. Zool. 1982, 196:489-497.
98. Gordon H.A. The germ-free animal. Its use in the study of "physiologic" effects of the normal microbial flora on the animal host. Am. J. Dig. Dis. 1960, 5:841-867.
99. Gruenheid S., Le Moual H. Resistance to antimicrobial peptides in Gram-negative bacteria. FEMS Microbiol. Lett. 2012, 330:81-89.
100. Gusarov I., Gautier L., Smolentseva O., Shamovsky I., Eremina S., Mironov A., Nudler E. Bacterial nitric oxide extends the lifespan of C. elegans. Cell 2013, 152:818-830.
101. Gutsmann T., Hagge S.O., David A., Roes S., Bohling A., Hammer M.U., Seydel U. Lipid-mediated resistance of Gram-negative bacteria against various pore-forming antimicrobial peptides. J. Endotoxin Res. 2005, 11:167-173.
102. Hahn M.W., Han M.V., Han S.G. Gene family evolution across 12 Drosophila genomes. PLoS Genet. 2007, 3:e197.
103. Hammer J., Hammer K., Kletter K. Lipids infused into the jejunum accelerate small intestinal transit but delay ileocolonic transit of solids and liquids. Gut 1998, 43:111-116.
104. Hejnol A., Martindale M.Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 2008, 456:382-386.
105. Herndl G., Velimirov B. Bacteria in the coelenteron of Anthozoa: control of coelenteric bacterial density by the coelenteric fluid, Deuxieme colloque international de bacteriologie marine 1986, IFREMER, Brest, France, pp. 407-414.
106. Hibino T., Loza-Coll M., Messier C., Majeske A.J., Cohen A.H., Terwilliger D.P., Buckley K.M., Brockton V., Nair S.V., Berney K., Fugmann S.D., Anderson M.K., Pancer Z., Cameron R.A., Smith L.C., Rast J.P. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 2006, 300:349-365.
107. Hill D., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Ann. Rev Immunol. 2010, 28:623-667.
108. Hirano T., Nishida H. Developmental fates of larval tissues after metamorphosis in the ascidian, Halocynthia roretzi. II. Origin of endodermal tissues of the juvenile. Dev. Genes. Evol. 2000, 210:55-63.
109. Holland L.Z. Body-plan evolution in the Bilateria: early antero-posterior patterning and the deuterostome-protostome dichotomy. Curr. Opin. Genet. Dev. 2000, 10:434-442.
110. 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., Gibson-Brown 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., 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 J.K., Zhang Q., Zmasek C.M., de Jong P.J., Osoegawa K., Putnam N.H., Rokhsar D.S., Satoh N., Holland P.W. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 2008, 18:1100-1111.
111. Hooper L. Do symbiotic bacteria subvert host immunity?. Nat. Rev. Microbiol. 2009, 7:367-374.
112. Hooper L., Gordon J. Commensal host-bacterial relationships in the gut. Science 2001, 292:1115-1118.
113. Hooper L., Macpherson A. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010, 10:159-169.
114. Hooper L., Wong M., Thelin A., Hansson L., Falk P., Gordon J. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291:881-884.
115. Hooper L.V., Bry L., Falk P.G., Gordon J.I. Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. BioEssays 1998, 20:336-343.
116. Huang S., Yuan S., Guo L., Yu Y., Li J., Wu T., Liu T., Yang M., Wu K., Liu H., Ge J., Yu Y., Huang H., Dong M., Yu C., Chen S., Xu A. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res. 2008, 18:1112-1126.
117. Hughes A., Friedman R. Loss of ancestral genes in the genomic evolution of Ciona intestinalis. Evol. Dev. 2005, 7:196-200.
118. Human Microbiome Project, C. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
119. Idowu A.B., Edema M.O., Adeyi A.O. Gut microflora and microfauna of earthworm species in the soilds of the research farms of the university of agriculture, Abeokuta, Nigeria. Biol. Agric. Hort. 2008, 25:185-200.
120. 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., Littman D.R. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
121. Johansson M.E. Fast renewal of the distal colonic mucus layers by the surface goblet cells as measured by in vivo labeling of mucin glycoproteins. PLoS ONE 2012, 7:e41009.
122. Johansson M.E., Ambort D., Pelaseyed T., Schutte A., Gustafsson J.K., Ermund A., Subramani D.B., Holmen-Larsson J.M., Thomsson K.A., Bergstrom J.H., van der Post S., Rodriguez-Pineiro A.M., Sjovall H., Backstrom M., Hansson G.C. Composition and functional role of the mucus layers in the intestine. Cell. Mol. Life Sci. 2011, 68:3635-3641.
123. Johansson M.E., Larsson J.M., Hansson G.C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. USA 2011, 108(Suppl 1):4659-4665.
124. Johansson M.E., Phillipson M., Petersson J., Velcich A., Holm L., Hansson G.C. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA 2008, 105:15064-15069.
125. Juge N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 2012, 20:30-39.
126. Kanther M., Rawls J. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 2010, 22:10-19.
127. Kashyap P.C., Marcobal A., Ursell L.K., Larauche M., Duboc H., Earle K.A., Sonnenburg E.D., Ferreyra J.A., Higginbottom S.K., Million M., Tache Y., Pasricha P.J., Knight R., Farrugia G., Sonnenburg J.L. Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 2013, 144:967-977.
128. Kashyap P.C., Marcobal A., Ursell L.K., Smits S.A., Sonnenburg E.D., Costello E.K., Higginbottom S.K., Domino S.E., Holmes S.P., Relman D.A., Knight R., Gordon J.I., Sonnenburg J.L. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proc. Natl. Acad. Sci. USA 2013, 110:17059-17064.
129. Katz M.J. Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biol. Bull. 1983, 164:1-27.
130. Khomiakov N.V., Kharin S.A., Nechitailo T., Golyshin P.N., Kurakov A.V., Byzov B.A., Zviagintsev D.G. Reaction of microorganisms to the digestive fluid of the earthworms. Mikrobiologiia 2007, 76:55-65.
131. Kim S.H., Lee W.J. Role of DUOX in gut inflammation: lessons from model of gut-microbiota interactions. Front. Cell Infect. Microbiol. 2014, 3:116.
132. Kimura A., Sakaguchi E., Nonaka M. Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 2009, 214:165-178.
133. King G.M., Judd C., Kuske C.R., Smith C. Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS One 2012, 7:e51475.
134. Kingsolver M.B., Huang Z., Hardy R.W. Insect antiviral innate immunity: pathways, effectors, and connections. J. Mol. Biol. 2013, 425:4921-4936.
135. Koren O., Knights D., Gonzalez A., Waldron L., Segata N., Knight R., Huttenhower C., Ley R.E. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comp. Biol. 2013, 9:e1002863.
136. Koropatnick T.A., Engle J.T., Apicella M.A., Stabb E.V., Goldman W.E., McFall-Ngai M.J. Microbial factor-mediated development in a host-bacterial mutualism. Science 2004, 306:1186-1188.
137. Koyama H., Taneda Y., Ishii T. The postbranchial digestive tract of the ascidian, Polyandrocarpa misakiensis (Tunicata: Ascidiacea). 2. Stomach Zool. Sci. 2012, 29:97-110.
138. Kubo A., Imai K.S., Satou Y. Gene-regulatory networks in the Ciona embryos. Brief. Funct. Gen. Prot. 2009, 8:250-255.
139. Kuraishi T., Binggeli O., Opota O., Buchon N., Lemaitre B. Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2011, 108:15966-15971.
140. Kuraishi T., Hori A., Kurata S. Host-microbe interactions in the gut of Drosophila melanogaster. Front. Physiol. 2013, 4:375.
141. Kvell K., Cooper E.L., Engelmann P., Bovari J., Nemeth P. Blurring borders: innate immunity with adaptive features. Clin. Dev. Immunol. 2007, 2007:83671.
142. Lee K.A., Kim S.H., Kim E.K., Ha E.M., You H., Kim B., Kim M.J., Kwon Y., Ryu J.H., Lee W.J. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 2013, 153:797-811.
143. Lee W.J. Bacterial-modulated host immunity and stem cell activation for gut homeostasis. Genes Dev. 2009, 23:2260-2265.
144. Lee Y.H., Su K.Y., Wyse A., Barbas A., Palestrandt D., Shieh K., Everett M.L., Devalapalli A., Orndorff P.E., Bollinger R.R., Parker W. Incorporation of secretory immunoglobulin A into biofilms can decrease their resistance to ciprofloxacin. Microbiol. Immunol. 2011, 55:174-183.
145. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
146. Lemaitre B., Miguel-Aliaga I. The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 2013, 47:377-404.
147. Lentle R.G., Janssen P.W. Physical characteristics of digesta and their influence on flow and mixing in the mammalian intestine: a review. J. Comp. Physiol. B. 2008, 178:673-690.
148. Lentle R.G., Janssen P.W., Deloubens C., Lim Y.F., Hulls C., Chambers P. Mucosal microfolds augment mixing at the wall of the distal ileum of the brushtail possum. Neurogastroenterol. Motil. 2013, 25. 881-e700.
149. Ley R.E., Lozupone C.A., Hamady M., Knight R., Gordon J.I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 2008, 6:776-788.
150. Ley R.E., Peterson D.A., Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124:837-848.
151. Li M., Yang H., Gu J.D. Phylogenetic diversity and axial distribution of microbes in the intestinal tract of the polychaete Neanthes glandicincta. Microb. Ecol. 2009, 58:892-902.
152. Liberti A., Melillo D., Zucchetti I., Natale L., Dishaw L.J., Litman G.W., De Santis R., Pinto M.R. 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 2014, 9:e94984.
153. Lilley K.S., Griffiths D.R. Proteomics in Drosophila melanogaster. Brief. Funct. Gen. Prot. 2003, 2:106-113.
154. Loker E.S. Macroevolutionary immunology: a role for immunity in the diversification of animal life. Front. Immunol. 2012, 3:25.
155. Loker E.S., Adema C.M., Zhang S.M., Kepler T.B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol. Rev. 2004, 198:10-24.
156. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489:220-230.
157. Lu Y., Zhuang Y., Liu J. Mining antimicrobial peptides from small open reading frames in Ciona intestinalis. J. Pept. Sci. 2014, 20:25-29.
158. Luckey D., Gomez A., Murray J., White B., Taneja V. Bugs & us: The role of the gut in autoimmunity. Indian J. Med. Res. 2013, 138:732-743.
159. Macdonald T., Monteleone G. Immunity, inflammation, and allergy in the gut. Science 2005, 307:1920-1925.
160. MacDonald T.T., Pettersson S. Bacterial regulation of intestinal immune responses. Inflamm. Bowel Dis. 2000, 6:116-122.
161. Macfarlane G.T., Macfarlane S. Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. Suppl. 1997, 222:3-9.
162. Majeske A.J., Oleksyk T.K., Smith L.C. The Sp185/333 immune response genes and proteins are expressed in cells dispersed within all major organs of the adult purple sea urchin. Innate Immun. 2013, 19:569-587.
163. Mallo G.V., Kurz C.L., Couillault C., Pujol N., Granjeaud S., Kohara Y., Ewbank J.J. Inducible antibacterial defense system in C. elegans. Curr. Biol. 2002, 12:1209-1214.
164. Marchiando A.M., Graham W.V., Turner J.R. Epithelial barriers in homeostasis and disease. Ann. Rev. Pathol. 2010, 5:119-144.
165. Marcobal A., Southwick A.M., Earle K.A., Sonnenburg J.L. A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 2013, 23:1038-1046.
166. Marino R., Kimura Y., De Santis R., Lambris J.D., Pinto M.R. Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 2002, 53:1055-1064.
167. Marsh E.K., May R.C. Caenorhabditis elegans, a model organism for investigating immunity. Appl. Environ. Microbiol. 2012, 78:2075-2081.
168. Martens E.C., Chiang H.C., Gordon J.I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 2008, 4:447-457.
169. Martinson V.G., Danforth B.N., Minckley R.L., Rueppell O., Tingek S., Moran N.A. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 2011, 20:619-628.
170. Mashanov V.S., Garcia-Arraras J.E. Gut regeneration in holothurians: a snapshot of recent developments. Biol. Bull. 2011, 221:93-109.
171. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122:107-118.
172. Mazmanian S.K. Capsular polysaccharides of symbiotic bacteria modulate immune responses during experimental colitis. J. Pediatr. Gastroenterol. Nutr. 2008, 46(Suppl 1):E11-12.
173. Mazmanian S.K., Kasper D.L. The love-hate relationship between bacterial polysaccharides and the host immune system. Nat. Rev. Immunol. 2006, 6:849-858.
174. Mazmanian S.K., Round J.L., Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008, 453:620-625.
175. McFall-Ngai M. Unseen forces: the influence of bacteria on animal development. Dev. Biol. 2002, 242:1-14.
176. McFall-Ngai M., Hadfield M.G., Bosch T.C., Carey H.V., Domazet-Loso T., Douglas A.E., Dubilier N., Eberl G., Fukami T., Gilbert S.F., Hentschel U., King N., Kjelleberg S., Knoll A.H., Kremer N., Mazmanian S.K., Metcalf J.L., Nealson K., Pierce N.E., Rawls J.F., Reid A., Ruby E.G., Rumpho M., Sanders J.G., Tautz D., Wernegreen J.J. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 2013, 110:3229-3236.
177. Medzhitov R. Innate immunity: quo vadis?. Nat. Immunol. 2010, 11:551-553.
178. Meinertzhagen I.A., Okamura Y. The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci. 2001, 24:401-410.
179. Meziti A., Kormas K.A., Pancucci-Papadopoulou M.-A., Thessalou-Legaki M. Bacterial phylotypes associated with the digestive tract of the sea urchin Paracentrotus lividus and the ascidian Microcosmus sp. Russian J. Marine Biol. 2007, 33:84-91.
180. Micchelli C.A. The origin of intestinal stem cells in Drosophila. Dev. Dyn. 2012, 241:85-91.
181. Micchelli C.A., Sudmeier L., Perrimon N., Tang S., Beehler-Evans R. Identification of adult midgut precursors in Drosophila. Gene Expr. Patterns 2011, 11:12-21.
182. Mondot S., de Wouters T., Dore J., Lepage P. The human gut microbiome and its dysfunctions. Dig. Dis. 2013, 31:278-285.
183. Mortha A., Chudnovskiy A., Hashimoto D., Bogunovic M., Spencer S.P., Belkaid Y., Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014, 343:1249288.
184. Mukherjee S., Vaishnava S., Hooper L.V. Multi-layered regulation of intestinal antimicrobial defense. Cell. Mol. Life Sci. 2008, 65:3019-3027.
185. Munn C. Marine Microbiology, Ecology and Applications 2011, Garland Science, New York, NY. 2nd Edition.
186. Nakazawa K., Yamazawa T., Moriyama Y., Ogura Y., Kawai N., Sasakura Y., Saiga H. Formation of the digestive tract in Ciona intestinalis includes two distinct morphogenic processes between its anterior and posterior parts. Dev. Dyn. 2013, 242:1172-1183.
187. Neish A.S. Microbes in gastrointestinal health and disease. Gastroenterology 2009, 136:65-80.
188. Neish A.S. Mucosal immunity and the microbiome. Ann. Am. Thor. Soc. 2014, 11(Suppl 1):S28-32.
189. Noah T.K., Donahue B., Shroyer N.F. Intestinal development and differentiation. Exp. Cell Res. 2011, 317:2702-2710.
190. Nyholm S.V., Graf J. Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat. Rev. Microbiol. 2012, 10:815-827.
191. Nyholm S.V., Song P., Dang J., Bunce C., Girguis P.R. Expression and putative function of innate immunity genes under in situ conditions in the symbiotic hydrothermal vent tubeworm Ridgeia piscesae. PLoS ONE 2012, 7:e38267.
192. O'Hara A., Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006, 7:688-693.
193. Ortega-Cava C.F., Ishihara S., Rumi M.A., Kawashima K., Ishimura N., Kazumori H., Udagawa J., Kadowaki Y., Kinoshita Y. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J. Immunol. 2003, 170:3977-3985.
194. Ottaviani E., Ventura N., Mandrioli M., Candela M., Franchini A., Franceschi C. Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 2011, 12:599-609.
195. Pacha J. Development of intestinal transport function in mammals. Physiol. Rev. 2000, 80:1633-1667.
196. Paris M., Laudet V. The history of a developmental stage: metamorphosis in chordates. Genesis 2008, 46:657-672.
197. Parker W., Lesher A.P. In pursuit of xenoreactive antibodies: where has it gotten us?. Immunol. Cell Biol. 2005, 83:413-417.
198. Parker W., Lin S.S., Yu P.B., Sood A., Nakamura Y.C., Song A., Everett M.L., Platt J.L. Naturally occurring anti-alpha-galactosyl antibodies: relationship to xenoreactive anti-alpha-galactosyl antibodies. Glycobiology 1999, 9:865-873.
199. Parker W., Ollerton J. Evolutionary biology and anthropology suggest biome reconstitution as a necessary approach toward dealing with immune disorders. Evol. Med. Publ. Health 2013, 2013:89-103.
200. Parker W., Perkins S.E., Harker M., Muehlenbein M.P. A prescription for clinical immunology: the pills are available and ready for testing. Curr. Med. Res. Opin. 2012, 28:1193-1202.
201. Parrinello N., Vizzini A., Arizza V., Salerno G., Parrinello D., Cammarata M., Giaramita F., Vazzana M. Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res. 2008, 334:305-317.
202. Parthasarathi K., Ranganathan L.S., Anandi V., Zeyer J. Diversity of microflora in the gut and casts of tropical composting earthworms reared on different substrates. J. Environ. Biol. 2007, 28:87-97.
203. Pearson C., Uhlig H.H., Powrie F. Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol. 2012, 33:289-296.
204. Pedros-Alio C. Marine microbial diversity: can it be determined?. Trends Microbiol. 2006, 14:257-263.
205. Pedros-Alio C. The rare bacterial biosphere. Ann. Rev. Marine Sci. 2012, 4:449-466.
206. Peterson D.A., McNulty N.P., Guruge J.L., Gordon J.I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007, 2:328-339.
207. Petrof E.O., Claud E.C., Gloor G.B., Allen-Vercoe E. Microbial ecosystems therapeutics: a new paradigm in medicine?. Benef. Microbes 2013, 4:53-65.
208. Portal-Celhay C., Bradley E.R., Blaser M.J. Control of intestinal bacterial proliferation in regulation of lifespan in Caenorhabditis elegans. BMC Microbiol. 2012, 12:49.
209. Pott J., Hornef M. Innate immune signalling at the intestinal epithelium in homeostasis and disease. EMBO Rep. 2012, 13:684-698.
210. Power S.E., O'Toole P.W., Stanton C., Ross R.P., Fitzgerald G.F. Intestinal microbiota, diet and health. Br. J. Nutr. 2014, 111:387-402.
211. Pradel E., Zhang Y., Pujol N., Matsuyama T., Bargmann C.I., Ewbank J.J. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2007, 104:2295-2300.
212. Pulido D., Nogues M.V., Boix E., Torrent M. Lipopolysaccharide neutralization by antimicrobial peptides: a gambit in the innate host defense strategy. J. Innate Immunol. 2012, 4:327-336.
213. Qin J., Li R., Raes J., Arumugam M., Burgdorf K., Manichanh C., Nielsen T., Pons N., Levenez F., Yamada T., Mende D., Li J., Xu J., Li S., Li D., Cao J., Wang B., Liang H., Zheng H., Xie Y., Tap J., Lepage P., Bertalan M., Batto J., Hansen T., Le Paslier D., Linneberg A., Nielsen H., Pelletier E., Pelletier E., Renault P., Sicheritz-Ponten T., Turner K., Zhu H., Zhu H., Yu C., Jian M., Zhou Y., Li Y., Zhang X., Qin N., Yang H., Wang J., Brunak S., Brunak S., Doré J., Guarner F., Kristiansen K., Pedersen O., Parkhill J., Weissenbach J., Bork P., Ehrlich S., Consortium M. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
214. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
215. Rast J.P., Smith L.C., Loza-Coll M., Hibino T., Litman G.W. Genomic insights into the immune system of the sea urchin. Science 2006, 314:952-956.
216. Rawls J.F., Samuel B.S., Gordon J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 2004, 101:4596-4601.
217. Rawls J., Mahowald M., Ley R., Gordon J. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 2006, 127:423-433.
218. Rinkevich Y., Douek J., Haber O., Rinkevich B., Reshef R. Urochordate whole body regeneration inaugurates a diverse innate immune signaling profile. Dev. Biol. 2007, 312:131-146.
219. Roeder T., Stanisak M., Gelhaus C., Bruchhaus I., Grotzinger J., Leippe M. Caenopores are antimicrobial peptides in the nematode Caenorhabditis elegans instrumental in nutrition and immunity. Dev. Comp. Immunol. 2010, 34:203-209.
220. Rook G.A., Brunet L.R. Microbes, Immunoregulation, and the Gut. Gut 2005, 54:317-320.
221. Rosa R.D., de Lorgeril J., Tailliez P., Bruno R., Piquemal D., Bachere E. A hemocyte gene expression signature correlated with predictive capacity of oysters to survive Vibrio infections. BMC Genomics 2012, 13:252.
222. Rosenberg E., Sharon G., Atad I., Zilber-Rosenberg I. The evolution of animals and plants via symbiosis with microorganisms. Environ. Microbiol. Rep. 2010, 2:500-506.
223. Rost-Roszkowska M.M., Undrul A. Fine structure and differentiation of the midgut epithelium of Allacma fusca (Insecta: Collembola: Symphypleona). Zool. Stud. 2008, 47:200-206.
224. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9:313-323.
225. Round J., O'Connell R., Mazmanian S. Coordination of tolerogenic immune responses by the commensal microbiota. J. Autoimmun. 2010, 34:J220-225.
226. Round J.L., Mazmanian S.K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2010, 107:12204-12209.
227. Round J.L., O'Connell R.M., Mazmanian S.K. Coordination of tolerogenic immune responses by the commensal microbiota. J. Autoimmun. 2010, 34:J220-225.
228. Rubin G.M. Around the genomes: the Drosophila genome project. Genome Res. 1996, 6:71-79.
229. Rudi K., Odegard K., Lokken T.T., Wilson R. A feeding induced switch from a variable to a homogenous state of the earthworm gut microbiota within a host population. PLoS ONE 2009, 4:e7528.
230. Ryu J.H., Ha E.M., Lee W.J. Innate immunity and gut-microbe mutualism in Drosophila. Dev. Comp. Immunol. 2010, 34:369-376.
231. Saenz S.A., Taylor B.C., Artis D. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol. Rev. 2008, 226:172-190.
232. Salem H., Kreutzer E., Sudakaran S., Kaltenpoth M. Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ. Microbiol. 2013, 15:1956-1968.
233. Sasaki N., Ogasawara M., Sekiguchi T., Kusumoto S., Satake H. Toll-like receptors of the ascidian Ciona intestinalis: prototypes with hybrid functionalities of vertebrate Toll-like receptors. J. Biol. Chem. 2009, 284:27336-27343.
234. Sasakura Y., Inaba K., Satoh N., Kondo M., Akasaka K. Ciona intestinalis and Oxycomanthus japonicus, representatives of marine invertebrates. Exp. Anim. 2009, 58:459-469.
235. Savage D.C. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 1977, 31:107-133.
236. Schalen C. Prevalence of IgA receptors in clinical isolates of Streptococcus pyogenes and Streptococcus agalactiae: serologic distinction between the receptors by blocking antibodies. FEMS Immunol. Med. Microbiol. 1993, 7:39-45.
237. Schmitt P., Rosa R.D., Duperthuy M., de Lorgeril J., Bachere E., Destoumieux-Garzon D. The antimicrobial defense of the pacific oyster, Crassostrea gigas. How diversity may compensate for scarcity in the regulation of resident/pathogenic microflora. Front. Microbiol. 2012, 3:160.
238. Schreiber S., Rosenstiel P., Albrecht M., Hampe J., Krawczak M. Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat. Rev. Genet. 2005, 6:376-388.
239. Scott M.G., Dullaghan E., Mookherjee N., Galvas N., Waldbrook M., Thompson A., Wang A., Lee K., Doria S., Hamill P., Yu J.J., Li Y., Donini O., Guarna M.M., Finlay B.B., North J.R., Hancock R.E. An anti-infective peptide that selectively modulates the innate immune response. Nat. Biotechnol. 2007, 25:465-472.
240. Sea Urchin Genome Sequencing, C., Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., Angerer L.M., Arnone M.I., Burgess D.R., Burke R.D., Coffman J.A., Dean M., Elphick M.R., Ettensohn C.A., Foltz K.R., Hamdoun A., Hynes R.O., Klein W.H., Marzluff W., McClay D.R., Morris R.L., Mushegian A., Rast J.P., Smith L.C., Thorndyke M.C., Vacquier V.D., Wessel G.M., Wray G., Zhang L., Elsik C.G., Ermolaeva O., Hlavina W., Hofmann G., Kitts P., Landrum M.J., Mackey A.J., Maglott D., Panopoulou G., Poustka A.J., Pruitt K., Sapojnikov V., Song X., Souvorov A., Solovyev V., Wei Z., Whittaker C.A., Worley K., Durbin K.J., Shen Y., Fedrigo O., Garfield D., Haygood R., Primus A., Satija R., Severson T., Gonzalez-Garay M.L., Jackson A.R., Milosavljevic A., Tong M., Killian C.E., Livingston B.T., Wilt F.H., Adams N., Belle R., Carbonneau S., Cheung R., Cormier P., Cosson B., Croce J., Fernandez-Guerra A., Geneviere A.M., Goel M., Kelkar H., Morales J., Mulner-Lorillon O., Robertson A.J., Goldstone J.V., Cole B., Epel D., Gold B., Hahn M.E., Howard-Ashby M., Scally M., Stegeman J.J., Allgood E.L., Cool J., Judkins K.M., McCafferty S.S., Musante A.M., Obar R.A., Rawson A.P., Rossetti B.J., Gibbons I.R., Hoffman M.P., Leone A., Istrail S., Materna S.C., Samanta M.P., Stolc V., Tongprasit W., Tu Q., Bergeron K.F., Brandhorst B.P., Whittle J., Berney K., Bottjer D.J., Calestani C., Peterson K., Chow E., Yuan Q.A., Elhaik E., Graur D., Reese J.T., Bosdet I., Heesun S., Marra M.A., Schein J., Anderson M.K., Brockton V., Buckley K.M., Cohen A.H., Fugmann S.D., Hibino T., Loza-Coll M., Majeske A.J., Messier C., Nair S.V., Pancer Z., Terwilliger D.P., Agca C., Arboleda E., Chen N., Churcher A.M., Hallbook F., Humphrey G.W., Idris M.M., Kiyama T., Liang S., Mellott D., Mu X., Murray G., Olinski R.P., Raible F., Rowe M., Taylor J.S., Tessmar-Raible K., Wang D., Wilson K.H., Yaguchi S., Gaasterland T., Galindo B.E., Gunaratne H.J., Juliano C., Kinukawa M., Moy G.W., Neill A.T., Nomura M., Raisch M., Reade A., Roux M.M., Song J.L., Su Y.H., Townley I.K., Voronina E., Wong J.L., Amore G., Branno M., Brown E.R., Cavalieri V., Duboc V., Duloquin L., Flytzanis C., Gache C., Lapraz F., Lepage T., Locascio A., Martinez P., Matassi G., Matranga V., Range R., Rizzo F., Rottinger E., Beane W., Bradham C., Byrum C., Glenn T., Hussain S., Manning G., Miranda E., Thomason R., Walton K., Wikramanayke A., Wu S.Y., Xu R., Brown C.T., Chen L., Gray R.F., Lee P.Y., Nam J., Oliveri P., Smith J., Muzny D., Bell S., Chacko J., Cree A., Curry S., Davis C., Dinh H., Dugan-Rocha S., Fowler J., Gill R., Hamilton C., Hernandez J., Hines S., Hume J., Jackson L., Jolivet A., Kovar C., Lee S., Lewis L., Miner G., Morgan M., Nazareth L.V., Okwuonu G., Parker D., Pu L.L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952.
241. Segata N., Haake S.K., Mannon P., Lemon K.P., Waldron L., Gevers D., Huttenhower C., Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012, 13:R42.
242. Semova I., Carten J.D., Stombaugh J., Mackey L.C., Knight R., Farber S.A., Rawls J.F. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 2012, 12:277-288.
243. Semple F., Dorin J.R. Beta-Defensins: multifunctional modulators of infection, inflammation and more?. J. Innate Immunol. 2012, 4:337-348.
244. Semple F., Webb S., Li H.N., Patel H.B., Perretti M., Jackson I.J., Gray M., Davidson D.J., Dorin J.R. Human beta-defensin 3 has immunosuppressive activity in vitro and in vivo. Eur. J. Immunol. 2010, 40:1073-1078.
245. Sharon G., Segal D., Zilber-Rosenberg I., Rosenberg E. Symbiotic bacteria are responsible for diet-induced mating preference in Drosophila melanogaster, providing support for the hologenome concept of evolution. Gut Microbes 2011, 2:190-192.
246. Shi W., Levine M., Davidson B. Unraveling genomic regulatory networks in the simple chordate. Ciona intestinalis. Genome Res. 2005, 15:1668-1674.
247. 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., Kasuya A. Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem. Biophys. Res. Commun. 2003, 302:207-218.
248. Shields J.W. The functional evolution of GALT: a review. Lymphology 2000, 33:47-57.
249. Shim J.O. Gut Microbiota in Inflammatory Bowel Disease. Pediatr. Gastroenterol. Hepatol. Nutr. 2013, 16:17-21.
250. Shimoda M., Inoue Y., Azuma N., Kanno C. Natural polyreactive immunoglobulin A antibodies produced in mouse Peyer's patches. Immunology 1999, 97:9-17.
251. Shin S.C., Kim S.H., You H., Kim B., Kim A.C., Lee K.A., Yoon J.H., Ryu J.H., Lee W.J. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 2011, 334:670-674.
252. Shivers R.P., Kooistra T., Chu S.W., Pagano D.J., Kim D.H. Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 2009, 6:321-330.
253. Skjoedt M.O., Palarasah Y., Rasmussen K., Vitved L., Salomonsen J., Kliem A., Hansen S., Koch C., Skjodt K. 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. 2010, 34:59-68.
254. Smith L.C., Ghosh J., Buckley K.M., Clow L.A., Dheilly N.M., Haug T., Henson J.H., Li C., Lun C.M., Majeske A.J., Matranga V., Nair S.V., Rast J.P., Raftos D.A., Roth M., Sacchi S., Schrankel C.S., Stensvag K. Echinoderm immunity. Adv. Exp. Med. Biol. 2010, 708:260-301.
255. So S., Tokumaru T., Miyahara K., Ohshima Y. Control of lifespan by food bacteria, nutrient limitation and pathogenicity of food in C. elegans. Mech. Ageing Dev. 2011, 132:210-212.
256. Sommer F., Backhed F. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11:227-238.
257. Song X., Goicoechea J.L., Ammiraju J.S., Luo M., He R., Lin J., Lee S.J., Sisneros N., Watts T., Kudrna D.A., Golser W., Ashley E., Collura K., Braidotti M., Yu Y., Matzkin L.M., McAllister B.F., Markow T.A., Wing R.A. The 19 genomes of Drosophila: a BAC library resource for genus-wide and genome-scale comparative evolutionary research. Genetics 2011, 187:1023-1030.
258. Sonnenburg J.L., Xu J., Leip D.D., Chen C.H., Westover B.P., Weatherford J., Buhler J.D., Gordon J.I. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 2005, 307:1955-1959.
259. Sonnenwirth A.C. Antibody response to anaerobic bacteria. Rev. Infect. Dis. 1979, 1:337-341.
260. Sorokin Y.I. On the feeding of some scleractinian corals with bacteria and dissolved organic matter. Limonol. Oceanogr. 1973, 18:380-385.
261. Storelli G., Defaye A., Erkosar B., Hols P., Royet J., Leulier F. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabol. 2011, 14:403-414.
262. Stowell S.R., Arthur C.M., Dias-Baruffi M., Rodrigues L.C., Gourdine J.P., Heimburg-Molinaro J., Ju T., Molinaro R.J., Rivera-Marrero C., Xia B., Smith D.F., Cummings R.D. Innate immune lectins kill bacteria expressing blood group antigen. Nat. Med. 2010, 16:295-301.
263. Stuart L.M., Boulais J., Charriere G.M., Hennessy E.J., Brunet S., Jutras I., Goyette G., Rondeau C., Letarte S., Huang H., Ye P., Morales F., Kocks C., Bader J.S., Desjardins M., Ezekowitz R.A. A systems biology analysis of the Drosophila phagosome. Nature 2007, 445:95-101.
264. Sudakaran S., Salem H., Kost C., Kaltenpoth M. Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol. Ecol. 2012, 21:6134-6151.
265. Swalla B.J., Cameron C.B., Corley L.S., Garey J.R. Urochordates are monophyletic within the deuterostomes. Syst. Biol. 2000, 49:52-64.
266. Swalla B.J., Smith A.B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:1557-1568.
267. Tagliabue A., Nencioni L., Villa L., Keren D.F., Lowell G.H., Boraschi D. Antibody-dependent cell-mediated antibacterial activity of intestinal lymphocytes with secretory IgA. Nature 1983, 306:184-186.
268. Tenor J.L., Aballay A. A conserved Toll-like receptor is required for Caenorhabditis elegans innate immunity. EMBO Rep. 2008, 9:103-109.
269. Territo M.C., Ganz T., Selsted M.E., Lehrer R. Monocyte-chemotactic activity of defensins from human neutrophils. J. Clin. Invest. 1989, 84:2017-2020.
270. Thakuria D., Schmidt O., Finan D., Egan D., Doohan F.M. Gut wall bacteria of earthworms: a natural selection process. ISME J. 2010, 4:357-366.
271. Thomas A.D., Parker W. Cultivation of epithelial-associated microbiota by the immune system. Fut. Microbiol. 2010, 5:1483-1492.
272. Thorsen M.S. Microbial activity, oxygen status and fermentation in the gut of the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Mar. Biol. 1998, 132:423-433.
273. Thorsen M.S., Wieland A., Ploug P., Kragelund C., Nielsen P.H. Distribution and activity of endosymbiotic sulfur bacteria in anoxic aggregates from the hindgut of the sea urchin Echinocardium cordatum. Marine Biol. Res. 2003, 57:1-12.
274. Tlaskalova-Hogenova H., Tuckova L., Lodinova-Zadnikova R., Stepankova R., Cukrowska B., Funda D.P., Striz I., Kozakova H., Trebichavsky I., Sokol D., Rehakova Z., Sinkora J., Fundova P., Horakova D., Jelinkova L., Sanchez D. Mucosal immunity: its role in defense and allergy. Int. Arch. Allergy Immunol. 2002, 128:77-89.
275. Umesaki Y., Setoyama H. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect. 2000, 2:1343-1351.
276. Vaishnava S., Behrendt C., Ismail A., Eckmann L., Hooper L. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc. Nat. Acad. Sci. USA 2008, 105:20858-20863.
277. Vidal-Dupiol J., Ladriere O., Destoumieux-Garzon D., Sautiere P.E., Meistertzheim A.L., Tambutte E., Tambutte S., Duval D., Foure L., Adjeroud M., Mitta G. Innate immune responses of a scleractinian coral to vibriosis. J. Biol. Chem. 2011, 286:22688-22698.
278. Vierstraete E., Verleyen P., De Loof A., Schoofs L. Differential proteomics for studying Drosophila immunity. Ann. N. Y. Acad. Sci. 2005, 1040:504-507.
279. Vijay-Kumar M., Aitken J., Carvalho F., Cullender T., Mwangi S., Srinivasan S., Sitaraman S., Knight R., Ley R., Gewirtz A. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010, 328:228-231.
280. Vijay-Kumar M., Aitken J.D., Gewirtz A.T. Toll like receptor-5: protecting the gut from enteric microbes. Semin. Immunopathol. 2008, 30:11-21.
281. Wagner R. Effects of microbiota on GI health: gnotobiotic research. Adv. Exp. Med. Biol. 2008, 635:41-56.
282. Wang L., Kounatidis I., Ligoxygakis P. As a model to study the role of blood cells in inflammation, innate immunity and cancer. Front. Cell. Infect. Microbiol. 2014, 3:113.
283. Wilkie I.C. Autotomy as a prelude to regeneration in echinoderms. Microbe. Res. Technol. 2001, 55:369-396.
284. Williams A.M., Probert C.S., Stepankova R., Tlaskalova-Hogenova H., Phillips A., Bland P.W. Effects of microflora on the neonatal development of gut mucosal T cells and myeloid cells in the mouse. Immunology 2006, 119:470-478.
285. Wold A.E., Adlerberth I. Breast feeding and the intestinal microflora of the infant-implications for protection against infectious diseases. Adv. Exp. Med. Biol. 2000, 478:77-93.
286. Wold A.E., Mestecky J., Tomana M., Kobata A., Ohbayashi H., Endo T., Eden C.S. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 1990, 58:3073-3077.
287. Wong A.C., Chaston J.M., Douglas A.E. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 2013, 7:1922-1932.
288. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., Heath A.C., Warner B., Reeder J., Kuczynski J., Caporaso J.G., Lozupone C.A., Lauber C., Clemente J.C., Knights D., Knight R., Gordon J.I. Human gut microbiome viewed across age and geography. Nature 2012, 486:222-227.
289. Zhang L., Li L., Zhu Y., Zhang G., Guo X. Transcriptome analysis reveals a rich gene set related to innate immunity in the Eastern Oyster (Crassostrea virginica). Marine Biotechnol. (NY) 2014, 16:17-33.
290. Zhang Q., Zmasek C.M., Dishaw L.J., Mueller M.G., Ye Y., Litman G.W., Godzik A. Novel genes dramatically alter regulatory network topology in amphioxus. Genome Biol. 2008, 9:R123.
291. Zhang R., Hou A. Host-microbe interactions in Caenorhabditis elegans. ISRN Microbiol. 2013, 2013:356451.
292. Zhang X., Nakahara T., Miyazaki M., Nogi Y., Taniyama S., Arakawa O., Inoue T., Kudo T. Diversity and function of aerobic culturable bacteria in the intestine of the sea cucumber Holothuria leucospilota. J. Gen. App. Microbiol. 2012, 58:447-456.
293. Zhang X., Nakahara T., Murase S., Nakata H., Inoue T., Kudo T. Physiological characterization of aerobic culturable bacteria in the intestine of the sea cucumber Apostichopus japonicus. J. Gen. App. Microbiol. 2013, 59:1-10.
294. Zhang Y., Lu H., Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 2005, 438:179-184.
295. Zucchetti I., De Santis R., Grusea S., Pontarotti P., Du Pasquier L. Origin and evolution of the vertebrate leukocyte receptors: the lesson from tunicates. Immunogenetics 2009, 61:463-481.