Evolution and function of innate immune receptors - Insights from marine invertebrates

Journal of Innate Immunity

Volumn 1, Issue 4, 2009, Pages 291-300

  Rosenstiel, Philip ^a,b   Philipp, Eva E R ^a   Schreiber, Stefan ^a   Bosch, Thomas C G ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Asthma; Cnidaria; Crohn disease; Innate immunity; Nucleotide binding and oligomerization domain like receptor; Sea urchin; Toll like receptor

Indexed keywords

CARRIER PROTEIN; NUCLEOTIDE BINDING RECEPTOR; OLIGOMERIZATION DOMAIN LIKE RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; SCAVENGER RECEPTOR CYSTEINE RICH PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

GENETIC VARIABILITY; IMMUNE SYSTEM; INVERTEBRATE; LONGEVITY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; EVOLUTION, MOLECULAR; IMMUNITY, INNATE; INVERTEBRATES; RECEPTORS, IMMUNOLOGIC; TOLL-LIKE RECEPTORS;

EID: 69949084523     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000211193     Document Type: Review

References (84)

1. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I: The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 2007; 5: 355-362.
2. Schreiber S, Rosenstiel P, Albrecht M, Ha mpe J, Krawczak M: Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat Rev Genet 2005; 6:376-388.
3. Takeda K, Kaisho T, Akira S: Toll-like receptors. Annu Rev Immunol 2003; 21: 335 -376.
4. Inohara N, Chamaillard M, McDonald C, Nunez G: NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 2005; 74: 355- 383.
5. Sarrias MR, Gronlund J, Padilla O, Madsen J, Holmskov U, Lozano F: The scavenger receptor cysteine-rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit Rev Immunol 20 04; 24: 1-37.
6. Chisholm ST, Coaker G, Day B, Staskawicz BJ: Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006; 124:803-814.
7. Hashimoto C, Hudson KL, Anderson KV: The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 1988; 52:269-279.
8. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA: The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996; 86: 973 -983.
9. Janeway CA Jr, Medzhitov R: Innate immune recognition. Annu Rev Immunol 2002; 20: 197-216.
10. Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW: Genomic insights into the immune system of the sea urchin. Science 2006; 314:952-956.
11. Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, An-gerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, et al: The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006; 314: 941-952.
12. Qiu L, Song L, Xu W, Ni D, Yu Y: Molecular cloning and expression of a Toll receptor gene homologue from Zhikong Scallop, Chlamys farreri. Fish Shellfish Immunol 2007; 22: 451-466.
13. Rast JP, Messier-Solek C: Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol Bull 2008; 214: 274-283.
14. Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP: The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 2006; 300: 349-365.
15. Wiens M, Korzhev M, Perovic-Ottstadt S, Luthri nger B, Brandt D, K lein S, Mu l ler WE: Toll-like receptors are part of the innate immune defense system of sponges (Demo-spongiae: Porifera). Mol Biol Evol 2007; 24: 792-804.
16. Hemmrich G, Miller DJ, Bosch TC: The evolution of immunity: a low-life perspective. Trends Immunol 2007; 28:449-454.
17. Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TC: The innate immune repertoire in cnidaria - ancestral complexity and stochastic gene loss. Genome Biol 2007; 8:R59.
18. Bosch TC, 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 JM: Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev Comp Immunol 2009; 33: 559-569.
19. Tschopp J, Martinon F, Burns K: NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 2003; 4:95-104.
20. Ogura Y, Inohara N, Benito A, Chen FF, Yamaoka S, Nunez G: Nod2, a Nod1/Apaf-1 family member that is restricted to mono-cytes and activates NF-kappa B. J Biol Chem 2001; 276:4812-4818.
21. Strober W, Murray PJ, Kitani A, Watanabe T: Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 2006; 6:9-20.
22. Kim HM, Park BS, Kim JI, Kim SE, Lee J, Oh SC, Enkhbayar P, Matsushima N, Lee H, Yoo OJ, Lee JO: Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 2007; 130:906-917.
23. Brodsky I, Medzhitov R: Two modes of li-gand recognition by TLRs. Cell 2007; 130: 979-981.
24. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H: HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006; 26:174-179.
25. Tsung A, Klune JR, Zhang X, Jeyabalan G, Cao Z, Peng X, Stolz DB, Geller DA, Rosengart MR, Billiar TR: HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 2007; 204:2913-2923.
26. Biragyn A, Ruffini PA, Leifer CA, Klyush-nenkova E, Shakhov A, Chertov O, Shiraka-wa AK, Farber JM, Segal DM, Oppenheim JJ, Kwak LW: Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002; 298: 1025 -1029.
27. Chamaillard M, Hashimoto M, Horie Y, Ma-sumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, Fukase K, Kusumoto S, Valvano MA, Foster SJ, Mak TW, Nunez G, Inohara N: An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopi-melic acid. Nat Immunol 2003; 4: 702-707.
28. Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, Viala J, Tedin K, Taha MK, Labigne A, Zahringer U, Coyle AJ, Di Stefano PS, Bertin J, Sansonetti PJ, Philpott DJ: Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 2003; 300: 1584 -1587.
29. Girardin SE, Boneca IG, Viala J, Chamail-lard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ: Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 2003; 278: 8869-8872.
30. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, Fukase K, Inamura S, Kusumoto S, Hashimoto M, Foster SJ, Moran AP, Fernandez-Luna JL, Nunez G: Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem 2003; 278:5509- 5512.
31. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J: Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008; 320: 674-677.
32. Martinon F, Agostini L, Meylan E, Tschopp J: Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol 20 04; 14: 1929 -1934.
33. Mariathasan S, Weiss DS, Newton K, Mc-Bride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM: Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440:228-232.
34. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J: Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440:237-241.
35. Kanneganti TD, Lamkanfi M, Kim YG, Chen G, Park JH, Franchi L, Vandenabeele P, Nunez G: Pannexin-1-mediated recognition of bacterial molecules activates the cryo-pyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007; 26: 433-443.
36. Ting JP, Davis BK: CATERPILLER: a novel gene family important in immunity, cell death, and diseases. Annu Rev Immunol 2005; 23:387-414.
37. Rosenstiel P, Jacobs G, Till A, Schreiber S: NOD-like receptors: ancient sentinels of the innate immune system. Cell Mol Life Sci 200; 65:1361-1377.
38. Park HH, Lo YC, Lin SC, Wang L, Yang JK, Wu H: The death domain superfamily in in-tracellular signaling of apoptosis and inflammation. Annu Rev Immunol 2007; 25: 561-586.
39. Watanabe T, Kitani A, Murray PJ, Strober W: NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat Immunol 2004; 5:800-808.
40. Fritz JH, Le Bourhis L, Sellge G, Magalhaes JG, Fsihi H, Kufer TA, Collins C, Viala J, Fer-rero RL, Girardin SE, Philpott DJ: Nod1-me-diated innate immune recognition of pepti-doglycan contributes to the onset of adaptive immunity. Immunity 2007; 26:445-459.
41. Magalhaes JG, Fritz JH, Le Bourhis L, Sellge G, Travassos LH, Selvanantham T, Girardin SE, Gommerman JL, Philpott DJ: Nod2-de-pendent Th2 polarization of antigen-specific immunit y. J Immunol 2008; 181: 7925-7935.
42. Rosenstiel P, Fantini M, Brautigam K, Kuh-bacher T, Waetzig GH, Seegert D, Schreiber S: TNF-alpha and IFN-gamma regulate the expression of the NOD2 (CARD15) gene in human intestinal epithelial cells. Gastroenterology 2003; 124:1001-1009.
43. Hisamatsu T, Suzuki M, Reinecker HC, Nadeau WJ, McCormick BA, Podolsky DK: CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 2003; 124: 993-1000.
44. Hisamatsu T, Suzuki M, Po dolsk y DK: Inter-feron-gamma augments CARD4/NOD1 gene and protein expression through inter-feron regulatory factor-1 in intestinal epithelial cells. J Biol Chem 2003; 278:32962- 32968.
45. Kim JG, Lee SJ, Kagnoff MF: Nod1 is an essential signal transducer in intestinal epithelial cells infected with bacteria that avoid recognition by toll-like receptors. Infect Im-mun 2004; 72: 1487 - 1495.
46. Rosenstiel P, Hellmig S, Hampe J, Ott S, Till A, Fischbach W, Sahly H, Lucius R, Folsch UR, Philpott D, Schreiber S: Influence of polymorphisms in the NOD1/CARD4 and NOD2/CARD15 genes on the clinical out-come of Helicobacter pylori infection. Cell Microbiol 2006; 8:1188-1198.
47. Viala J, Chaput C, Boneca IG, Cardona A, Gi-rardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, Distefano PS, Sanso-netti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL: Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 2004; 5: 1166 -1174.
48. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaef-feler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr, Fellermann K, Ganz T, Stange EF, Bevins CL: Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci USA 2005; 102:18129- 18134.
49. Wehkamp J, Harder J, Weichenthal M, Schwab M, Schaffeler E, Schlee M, Herr-linger KR, Stallmach A, Noack F, Fritz P, Schroder JM, Bevins CL, Fellermann K, Stange EF: NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 2004; 53:1658-1664.
50. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nunez G, Flavell RA: Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307:731-734.
51. Freeman M, Ashkenas J, Rees DJ, Kingsley DM, Copeland NG, Jenkins NA, Krieger M: An ancient, highly conserved family of cys-teine-rich protein domains revealed by cloning type I and type II murine macrophage scavenger receptors. Proc Natl Acad Sci USA 1990 ; 87: 8810-8814.
52. Bikker FJ, Ligtenberg AJ, End C, Renner M, Bla ich S, Lyer S, Wittig R, va n't Hof W, Veer-man EC, Nazmi K, de Blieck-Hogervorst JM, Kioschis P, Nieuw Amerongen AV, Poustka A, Mollenhauer J: Bacteria binding by DMBT1/SAG/gp-340 is confined to the VEVLXXXXW motif in its scavenger receptor cysteine-rich domains. J Biol Chem 2004; 279:47699-47703.
53. Rosenstiel P, Sina C, End C, Renner M, Lyer S, Till A, Hellmig S, Nikolaus S, Folsch UR, Helmke B, Autschbach F, Schirmacher P, Ki-oschis P, Hafner M, Poustka A, Mollenhauer J, Schreiber S: Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J Immunol 2007; 178:8203-8211.
54. Pancer Z, Rast JP, Davidson EH: Origins of immunity: transcription factors and homo-logues of effector genes of the vertebrate immune system expressed in sea urchin coelo-mocytes. Immunogenetics 1999; 49: 773- 786.
55. Pancer Z: Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci USA 2000; 97: 13156 -13161.
56. Pancer Z: Individual-specific repertoires of immune cells SRCR receptors in the purple sea urchin (S. purpuratus). Adv Exp Med Biol 2001; 484:31- 40.
57. Steindler L, Schuster S, Ilan M, Avni A, Cer-rano C, Beer S: Differential gene expression in a marine sponge in relation to its symbiotic state. Mar Biotechnol (NY) 2007; 9:543- 549.
58. Hooper LV, Gordon JI: Commensal host-bacterial relationships in the gut. Science 2001; 292: 1115 -1118.
59. Macpherson AJ, Harris NL: Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004; 4: 478-485.
60. Rakoff-Nahoum S, Paglino J, Eslami-Var-zaneh F, Edberg S, Medzhitov R: Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004; 11 8: 229-241.
61. Alley CD, Kiyono H, McGhee JR: Murine bone marrow IgA responses to orally administered sheep erythrocytes. J Immunol 1986; 136: 4414-4419.
62. Fanaro S, Chierici R, Guerrini P, Vigi V: Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl 2003; 91: 48-55.
63. Dai D, Walker WA: Protective nutrients and bacterial colonization in the immature human gut. Adv Pediatr 1999; 46: 353-382.
64. Walker WA: Role of nutrients and bacterial colonization in the development of intestinal host defense. J Pediatr Gastroenterol Nutr 2000; 30:S2-S7.
65. Smith S, Vaughan EE, De Vos WM: Quorum sensing within the gut. Microbial Ecol Health Dis 2000; 2(suppl):81-92.
66. Falcao JP, Sharp F, Sperandio V: Cell-to-cell signaling in intestinal pathogens. Curr Issues Intest Microbiol 2004; 5: 9-17.
67. Mazmanian SK, Kasper DL: The love-hate relationship between bacterial polysaccha-rides and the host immune system. Nat Rev Immunol 2006; 6:849-858.
68. Mazmanian SK: Capsular polysaccharides of symbiotic bacteria modulate immune responses during experimental colitis. J Pedi-atr Gastroenterol Nutr 2008; 46(suppl 1): E11-E12.
69. Ruby EG, McFall-Ngai MJ: A squid that glows in the night: development of an animal-bacterial mutualism. J Bacteriol 1992; 174:4865-4870.
70. Nyholm SV, McFall-Ngai MJ: Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl Environ Microbiol 2003; 69:3932-3937.
71. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ: Microbial factor-mediated development in a host-bacterial mutualism. Science 2004; 306: 1186 -1188.
72. Magalhaes JG, Philpott DJ, Nahori MA, Je-hanno M, Fritz J, Bourhis LL, Viala J, Hugot JP, Giovannini M, Bertin J, Lepoivre M, Mengin-Lecreulx D, Sansonetti PJ, Girardin SE: Murine Nod1 but not its human ortho-logue mediates innate immune detection of tracheal cytotoxin. EMBO Rep 2005; 6:1201- 1207.
73. Rahat M, Dimentman C: Cultivation of bacteria-free Hydra viridis: missing budding factor in nonsymbiotic hydra. Science 1982; 216: 67-68.
74. Ziuganov VV: Arctic and southern freshwater pearl mussel Margaritifera margaritifera with long and short life span as a model system for testing longevity mechanisms. Adv Gerontol 2004; 14 : 21-3 0.
75. Taylor AC, Brand AR: A comparative study of the respiratory responses of the bivalves Arctica islandica (L.) and Mytilus edulis L. to declining oxygen tension. Proc R Soc Lond B Biol Sci 1975; 190:443-456.
76. Abele D, Strahl J, Brey T, Philipp EE: Imperceptible senescence: ageing in the ocean qua-hog Arctica islandica. Free Radic Res 2008; 42: 474- 480.
77. Sauvage C, Bierne N, Lapegue S, Boudry P: Single nucleotide polymorphisms and their relationship to codon usage bias in the Pa-cif ic oyster Crassostrea gigas. Gene 2007;406: 13-22.
78. Franceschi C , Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G: Inflamm-aging. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 2000; 908: 244 -254 .
79. Franceschi C, Olivieri F, Marchegiani F, Cardelli M, Cavallone L, Capri M, Salvioli S, Valensin S, De Benedictis G, Di Iorio A, Caruso C, Paolisso G, Monti D: Genes involved in immune response/inflammation, IGF1/ insulin pathway and response to oxidative stress play a major role in the genetics of human longevity: the lesson of centenarians. Mech Ageing Dev 2005; 126:351-361.
80. Walford RL: The Immunologic Theory of Aging. Copenhagen, Munksgaard, 1969.
81. Rosenstiel P, Derer S, Till A, Hasler R, Eber-stein H, Bewig B, Nikolaus S, Nebel A, Schreiber S: Systematic expression profiling of innate immune genes defines a complex pattern of immunosenescence in peripheral and intestinal leukocytes. Genes Immun 2008; 9:103-114.
82. Gent AE, Hellier MD, Grace RH, Swarbrick ET, Coggon D: Inflammatory bowel disease and domestic hygiene in infancy. Lancet 1994; 343: 766-767.
83. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI: Host-bacterial mutualism in the human intestine. Science 2005; 307:1915- 1920.
84. Croucher PJ, Mascheretti S, Hampe J, Huse K, Frenzel H, Stoll M, Lu T, Nikolaus S, Yang SK, Krawczak M, Kim WH, Schreiber S: Haplotype structure and association to Crohn's disease of CARD15 mutations in two ethnically divergent populations. Eur J Hum Genet 2003; 11:6-16.