The ancestry and cumulative evolution of immune reactions
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The last two decades of study enriched greatly our knowledge of how the immune system originated and the sophisticated immune mechanisms of today's vertebrates and invertebrates developed. Even unicellular organisms possess mechanisms for pathogen destruction and self recognition. The ability to distinguish self from non-self is a prerequisite for recognition of sexual compatibility and ensuring survival. Molecules involved in these processes resemble those found in the phagocytic cells of higher organisms. Recognition of bacteria by scavenger receptors induces phagocytosis or endocytosis. The phagocytic mechanisms characterizing the amoeboid protozoans developed further during the evolution towards innate immunity. The scavenger receptor cysteine-rich domain SRCR is encoded in the genomes from the most primitive sponges to mammals. The immune system of sponges comprises signal transduction molecules which occur in higher metazoans as well. Sponges already possess recognition systems for pathogenic bacteria and fungi, based on membrane receptors (a lipopolysaccharide-interacting protein, a cell surface receptor recognizing β(1 → 3)-d-glucans of fungi). Perforin-like molecules and lysozymes are involved, among others, in defense in sponges. Reactive oxygen and nitrogen species function in the immunity of early metazoan. Genes encoding the family of reactive oxygen-generating NADPH oxidases (Noxes) are found in a variety of protists and plants. The NO synthases of cnidarians, mollusks, and chordates are conserved with respect to the mammalian NOS. The antimicrobial peptides of protozoans, amoebapores, are structural and functional analogs of the natural killer cell peptide, NK-lysin, of vertebrates. An ancestral S-type lectin has been found in sponges. Opsonizing properties of lectins and the ability to agglutinate cells justify their classification as primitive recognition molecules. Invertebrate cytokines are not homologous to those of vertebrate, and their functional convergence was presumably enabled by the general similarity of the lectin-like recognition domain three-dimensional structure. Sponges contain molecules with SCR/CCP domains that show high homology to the mammalian regulators of complement activation (RCA family). A multi-component complement system comprising at least the central molecule of the complement system, C3, Factor B, and MASP developed in the cnidarians and evolved into the multilevel cascade engaged in innate and acquired immunity of vertebrates. The adaptive immune system of mammals is also deeply rooted in the metazoan evolution. Some its precursors have been traced as deep as in sponges, namely, two classes of receptors that comprise Ig-like domains, the receptor tyrosine kinases (RTK), and the non-enzymic sponge adhesion molecules (SAM). The antibody-based immune system defined by the presence of the major histocompatibility complex (MHC), T-cell receptor (TCR), B-cell receptor (BCR) or recombination activating genes (RAGs) is known beginning from jawed fishes. However, genes closely resembling RAG1 and RAG2 have been uncovered in the genome of a see urchin. The ancestry of MHC gene remains unknown. Similarly, no homologue of the protein binding domain (PBD) in MHC molecules has been found in invertebrates. The pathway by which endogenous peptides are degraded for presentation with class I MHC molecules utilizes mechanisms similar to those involved in the normal turnover of intracellular proteins, apparently recruited to work also for the immune system. Several cDNAs coding for lysosomal enzymes, e.g., cathepsin, have been isolated from sponges. All chromosomal duplication events in the MHC region occurred after the origin of the agnathans but before the gnathostomes split from them. The V-domains of the subtype found in the receptors of T and B-cells are known from both agnathans and cephalochordates, although they do not rearrange. The rearrangement mechanism of the lymphocyte V-domains suggests its origin from a common ancestral domain existing before the divergence of the extant gnathostome classes. Activation-induced deaminase (AID) - homologous proteins have been found only in the gnathostomes. It appears thus that the adaptive immunity of vertebrates is a result of stepwise accumulation of small changes in molecules, cells and organs over almost half a billion years.
- Abi-Rached L, McDermott MF, Pontarotti P (1999) The MHC big bang. Immunol Rev 167: 33-44.
- Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394: 744-751.
- Akira K, Takahashi M, Matsushita M, Endo Y, Nakata M. Mizuochi T. Fujita T (2001) Cloning and characterization of novel ficolins from the solitary urochordate. Halocynthia roretzi. J Biol Chem 276: 19959-19965.
- Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
- Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z (2005) Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310: 1970-1973.
- Allen PG, Dawidowicz EA (1990) Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast. J Cell Physiol 145: 508-513.
- Amara U, Rittirsch D, Flierl M, Bruckner U, Klos A, Gebhard F, Lambris JD, Huber-Lang M (2008) Interaction between the coagulation and complement system. Adv Exp Med Biol 632: 71-79.
- Ambach A, Bonnekoh B, Nguyen M, Schön MP, Gollnick H (2004) Imiquimod, a Toll-like receptor-7 agonist, induces perforin in cytotoxic T lymphocytes in vitro. Mol Immunol 40: 1307-1314.
- Ariki S, Takahara S, Shibata T, Fukuoka T, Ozaki A, Endo Y, Fujita T, Koshiba T, Kawabata S (2008) Factor C acts as a lipopolysaccharide-responsive C3 convertase in horseshoe crab complement activation. J Immunol 181: 7994-8001.
- Armstrong PB (2006) Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 211: 263-281.
- Artavanis-Tsakonas K, Love JC, Ploegh HL, Vyas JM (2006) Recruitment of CD63 to Cryptococcus neoformans phagosomes requires acidification. Proc Natl Acad Sci USA 103: 15945-15950.
- Ayala FJ, Rzhetsky A, Ayala FJ (1998) Origin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc Natl Acad Sci USA 95: 606-611.
- Azumi K, De Santis R, De Tomaso A, Rigoutsos I, Yoshizaki F, Pinto MR, Marino R, Shida K, Ikeda I, Ikeda M, Arai M, Inoue Y, Shimizu T, Satoh N, Rokhsar DS, Du Pasquier L, Kasahara M, Satake M. Nonaka M (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: 'waiting for Godot'. Immunogenetics 55: 570
- Babior BM (1999) NADPH oxidase: an update. Blood 93: 1464-1476.
- Barwig B (1985) Isolation and characterization of plasma coagulogen of the cockroach Leucophaea maderae (Blattaria). J Comp Physiol (B) 155: 135-143.
- Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337: 585-596.
- Beck G, O'Brien RF, Habicht GS, Stillman DL, Cooper EL, Raftos DA (1993) Invertebrate cytokines. III: Invertebrate interleukin-1-like molecules stimulate phagocytosis by tunicate and echinoderm cells. Cell Immunol 146: 284-299.
- Beschin A, Bilej M, Torreele E, De Baetselier P (2001) On the existence of cytokines in invertebrates. Cell Mol Life Sci 58: 801-814.
- Beutler B, Rehli M (2002) Evolution of the TIR, tolls and TLRs: functional inferences from computational biology. Curr Top Microbiol Immunol 270: 1-21.
- Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463: 1042-1047.
- Blandin S, Levashina EA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40: 903-908.
- Blumbach B, Pancer Z, Diehl-Seifert B, Steffen R, Münkner J, Müller I, Müller WE (1998) The putative sponge aggregation receptor: isolation and characterization of a molecule composed of scavenger receptor cysteine-rich domains and short consensus repeats. J Cell Sci 111: 2635-2644.
- Blumbach B, Diehl-Seifert B, Seack J, Steffen R, Müller IM, Müller WEG (1999) Cloning and expression of novel receptors belonging to the immunoglobulin superfamily from the marine sponge Geodia cydonium. Immunogenetics 49: 751-763.
- Böhm M, Schröder HC, Müller IM, Müller WE, Gamulin V (2000) The mitogen-activated protein kinase p38 pathway is conserved in metazoans: cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol Cell 92: 95-104.
- Borth W (1992) Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J 6: 3345-3353
- Bouige P, Laurent D, Piloyan L, Dassa E (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr Protein Pept Sci 3: 541-559.
- Brehélin M (1979) Hemolymph coagulation in Locusta migratoria: evidence for a functional equivalent of fibrinogen. Comp Biochem Physiol (B) 62: 329-334.
- Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
- Buljan M, Bateman A (2009) The evolution of protein domain families. Biochem Soc Trans 37: 751-755.
- Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3: 1200-1207.
- Cannon JP, Haire RN, Rast JP, Litman GW (2004) The phylogenetic origins of the antigen-binding receptors and somatic diversification mechanisms. Immunol Rev 200: 12-22.
- Cardelli J (2001) Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic 2: 311-320.
- Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198: 116-126.
- Chen G, Zhuchenko O, Kuspa A (2007) Immune-like phagocyte activity in the social amoeba. Science 317: 678-681.
- Cho WL, Liu HF, Lee CH, Kuo CC, Chang TY, Liu CT, Chen CC (1998) Molecular cloning, characterization and tissue expression of prophenoloxidase cDNA from the mosquito Armigeres subalbatus innoculated with Dirofilaria immitis microfilariae. Insect Mol Biol 7: 31-40.
- Cooper EL, Mansour MH, Negm HI (1996) Marine invertebrate immunodefense responses: Molecular and cellular approaches in tunicates Ann Rev Fish Dis 6: 133-149.
- Cox RL, Mariano T, Heck DE, Laskin JD, Stegeman JJ (2001) Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comp Biochem Physiol B Biochem Mol Biol 130: 479-491.
- Daffre S, Kylsten P, Samakovlis C, Hultmark D (1994) The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol Gen Genet 242: 152-162.
- Danchin EG, Abi-Rached L, Gilles A, Pontarotti P (2003) Conservation of the MHC-like region throughout evolution. Immunogenetics 55: 141-148.
- Dangott LJ, Jordan JE, Bellet RA, Garbers DL (1989) Cloning of the mRNA for the protein that crosslinks to the egg peptide speract. Proc Natl Acad Sci USA 86: 2128-2132.
- Danilova N (2006) The evolution of immune mechanisms. J Exp Zool B Mol Dev Evol 306: 496-520.
- Davies B, Chattings LS, Edwards SW (1991) Superoxide generation during phagocytosis by Acanthamoeba castellanii: similarities to the respiratory burst of immune phagocytes. J Gen Microbiol 137: 705-710.
- De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, Weissman IL (2005) Isolation and characterization of a protochordate histocompatibility locus. Nature 438: 454-459.
- Decker H, Schweikardt T, Nillius D, Salzbrunn U, Jaenicke E, Tuczek F (2007) Similar enzyme activation and catalysis in hemocyanins and tyrosinases. Gene 398: 183-191.
- Dijkstra JM, Kiryu I, Kollner B, Yoshiura Y, Ototake M (2003) MHC class II invariant chain homologues in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 15: 91-105.
- Dodd RB, Drickamer K (2001) Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11: 71R-79R.
- Dodds AW, Law SK (1998) The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha 2-macroglobulin. Immunol Rev 166: 15-26.
- Dodds AW, Smith SL, Levine RP, Willis AC (1998) Isolation and initial characterisation of complement components C3 and C4 of the nurse shark and the channel catfish. Dev Comp Immunol 22: 207-216.
- Doolittle RF, Riley M (1990) The amino-terminal sequence of lobster fibrinogen reveals common ancestry with vitellogenins. Biochem Biophys Res Commun 167: 16-19.
- dos Remedios NJ, Ramsland PA, Hook JW, Raison RL (1999) Identification of a homologue of CD59 in a cyclostome: implications for the evolutionary development of the complement system. Dev Comp Immunol 23: 1-14.
- Dreyfus DH (2009) Paleo-immunology: evidence consistent with insertion of a primordial herpes virus-like element in the origins of acquired immunity. PLoS One 4: e5778.
- Du Pasquier L, Zucchetti I, De Santis R (2004) Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol Rev 198: 233-248.
- Dzik JM (2006) Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 53: 33-64.
- Dzik JM, Zieliński Z, Gołos B, Wałajtys-Rode E (2006) Trichinella spiralis infection affects p47(phox) protein expression in guinea-pig alveolar macrophages. Exp Parasitol 112: 158-163.
- Dzik JM, Zieliński Z, Cieśla J, Wałajtys-Rode E (2010) Trichinella spiralis infection enhances protein kinase C phosphorylation in guinea-pig alveolar macrophages. Parasite Immunol 32: 209-220.
- Elphick MR, Williams L, O'Shea M (1996) New features of the locust optic lobe: evidence of a role for nitric oxide in insect vision. J Exp Biol 199: 2395-2407.
- Endo Y, Takahashi M, Fujita T (2006) Lectin complement system and pattern recognition. Immunobiology 211: 283-293.
- Fautin DG, Mariscal RN (1991) Cnidaria: Anthozoa. Harrison FW, Westfall JA, eds. Microscopic Anatomy of Invertebrates, Placozoa, Porifera, Cnidaria, and Ctenophora, vol 2, pp 267-358. Wiley-Liss, Inc, New York and other cities.
- Fernàndez-Busquets X, Burger MM (1997) The main protein of the aggregation factor responsible for species-specific cell adhesion in the marine sponge Microciona prolifera is highly polymorphic. J Biol Chem 272: 27839-27847.
- Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15: 351-362.
- Fujii T, Nakamura T, Sekizawa A, Tomonaga S (1992) Isolation and characterization of a protein from hagfish serum that is homologous to the third component of the mammalian complement system. J Immunol 148: 117-123.
- Fujito NT, Sugimoto S, Nonaka M (2010) Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev Comp Immunol 34: 775-784.
- Fuller GM, Doolittle RF (1971) Studies of invertebrate fibrinogen. II. Transformation of lobster fibrinogen into fibrin. Biochemistry 10: 1311-1315.
- Gan X, Ma Z, Deng N, Wang J, Ding J, Li L (2004) Involvement of the C-terminal proline-rich motif of G protein-coupled receptor kinases in recognition of activated rhodopsin. J Biol Chem 279: 49741-49746.
- Garcia-Garcia E, Prado-Alvarez M, Novoa B, Figueras A, Rosales C (2008) Immune responses of mussel hemocyte subpopulations are differentially regulated by enzymes of the PI-3K, PKC, and ERK kinase families. Dev Comp Immunol 32: 637-653.
- Gauthier M, Degnan BM (2008) The transcription factor NF-κB in the demosponge Amphimedon queenslandica: insights on the evolutionary origin of the Rel homology domain. Dev Genes Evol 218: 23-32.
- Giovine M, Pozzolini M, Favre A, Bavestrello G, Cerrano C, Ottaviani F, Chiarantini L, Cerasi A, Cangiotti M, Zocchi E, Scarfì S, Sarà M, Benatti U (2001) Heat stress-activated, calcium-dependent nitric oxide synthase in sponges. Nitric Oxide 5: 427-431.
- Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA, Ferrandon D, Royet J (2002) The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416: 640-644.
- Guo P, Hirano M, Herrin BR, Li J, Yu C, Sadlonova A, Cooper MD (2009) Dual nature of the adaptive immune system in lampreys. Nature 459: 796-801.
- Ha EM, Lee KA, Park SH, Kim SH, Nam HJ, Lee HY, Kang D, Lee WJ (2009) Regulation of DUOX by the Galphaq-phospholipase Cβ-Ca2+ pathway in Drosophila gut immunity. Dev Cell 16: 386-397.
- Halaby DM, Mornon JP (1998) The immunoglobulin superfamily: an insight on its tissular, species, and functional diversity. J Mol Evol 46: 389-400.
- Hancock RE, Brown KL, Mookherjee N (2006) Host defence peptides from invertebrates - emerging antimicrobial strategies. Immunobiology 211: 315-322.
- Hanley PJ, Hook JW, Raftos DA, Gooley AA, Trent R, Raison RL (1992) Hagfish humoral defense protein exhibits structural and functional homology with mammalian complement components. Proc Natl Acad Sci USA 89: 7910-7914.
- Hartenstein V (2006) Blood cells and blood cell development in the animal kingdom. Annu Rev Cell Dev Biol 22: 677-712.
- Hemmrich G, Miller DJ, Bosch TC (2007) The evolution of immunity: a low-life perspective. Trends Immunol 28: 449-454.
- Hiltbold EM, Roche PA (2002) Trafficking of MHC class II molecules in the late secretory pathway. Curr Opin Immunol 14: 30-35.
- Hirabayashi J, Kusunoki T, Kasai K-I (1991) Complete primary structure of a galactose-specific lectin from the venom of the rattlesnake Crotalus atrox. J Biol Chem 266:: 2320-2326.
- Hirabayashi J, Satoh M, Kasai K-I (1992) Evidence that Caenorhabditis elegans 32-kDa β-galactoside-binding protein is homologous to vertebrate β-galactoside-binding lectins. J Biol Chem 267: 15485-15490.
- Hoffmann JA (2003) The immune response of Drosophila. Nature 426: 33-38.
- Hogan BL (1996) Bone morphogenetic proteins in development. Curr Opin Genet Dev 6: 432-438.
- Honjo T, Muramatsu M, Fagarasan S (2004) AID: how does it aid antibody diversity? Immunity 20: 659-668.
- Hood L, Kronenberg M, Hunkapiller T (1985) T cell antigen receptors and the immunoglobulin supergene family. Cell 40: 225-229.
- Hourcade D, Holers VM, Atkinson JP (1989) The regulators of complement activation (RCA) gene cluster. Adv Immunol 45: 381-416.
- 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 (2008) Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 18: 1112-1126.
- Hughes AL (1998) Protein phylogenies provide evidence of a radical discontinuity between arthropod and vertebrate immune systems. Immunogenetics 47: 283-296.
- Hughes AL (1999) Genomic catastrophism and the origin of vertebrate immunity. Arch Immunol Ther Exp (Warsz) 47: 347-353.
- Hughes AL, Nei M (1993) Evolutionary relationships of the classes of major histocompatibility complex genes. Immunogenetics 37: 337-346.
- Huising MO, Kruiswijk CP, Flik G (2006) Phylogeny and evolution of class-I helical cytokines. J Endocrinol 189: 1-25.
- Humphreys T, Reinherz EL (1994) Invertebrate immune recognition, natural immunity and the evolution of positive selection. Immunol Today 15: 316-320.
- Ikawa M, Wada I, Kominami K, Watanabe D, Toshimori K, Nishimune Y, Okabe M (1997) The putative chaperone calmegin is required for sperm fertility Nature 387: 607-611.
- Inamori K, Ariki S, Kawabata S (2004) A Toll-like receptor in horseshoe crabs. Immunol Rev 198: 106-115.
- Inoue Y, Ogasawara M, Moroi T, Satake M, Azumi K, Moritomo T, Nakanishi T (2005) Characteristics of NADPH oxidase genes (Nox2, p22, p47, and p67) and Nox4 gene expressed in blood cells of juvenile Ciona intestinalis. Immunogenetics 57: 520-534.
- Irazoqui JE, Urbach JM, Ausubel FM (2010) Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 10: 47-58.
- Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, Zachary D, Hoffmann JA, Hetru C, Meister M (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7: 335-350.
- Iwanga S, Kawabata S (1998) Evolution and phylogeny of defense molecules associated with innate immunity in horseshoe crab. Front Biosci 3: D973-D984.
- Jensen JA, Festa E, Smith DS, Cayer M (1981) The complement system of the nurse shark: hemolytic and comparative characteristics. Science 214: 566-569.
- Ji X, Azumi K, Sasaki M, Nonaka M (1997) Ancient origin of the complement lectin pathway revealed by molecular cloning of mannan binding protein-associated serine protease from a urochordate, the Japanese urochordate, Halocynthia roretzi. Proc Natl Acad Sci USA 94: 6340-6345.
- Kanzok SM, Hoa NT, Bonizzoni M, Luna C, Huang Y, Malacrida AR, Zheng L (2004) Origin of Toll-like receptor-mediated innate immunity. J Mol Evol 58: 442-448.
- Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PloS Biol 3: e181.
- Kasahara M, Flajnik MF, Ishibashi T, Natori T (1995) Evolution of the major histocompatibility complex: a current overview. Transpl Immunol 3: 1-20.
- Kasahara M, Nakaya J, Satta Y, Takahata N (1997) Chromosomal duplication and the emergence of the adaptive immune system. Trends Genet 13: 90-92.
- Kasahara M, Suzuki T, Pasquier LD (2004) On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25: 105-111.
- Kaur H, Jaso-Friedmann L, Evans DL (2003) Identification of a scavenger receptor homologue on nonspecific cytotoxic cells and evidence for binding to oligodeoxyguanosine. Fish Shellfish Immunol 15: 169-181.
- Kauschke E, Komiyama K, Moro I, Eue I, König S, Cooper EL (2001) Evidence for perforin-like activity associated with earthworm leukocytes. Zoology (Jena) 104: 13-24.
- Kawahara T, Lambeth JD (2007) Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol Biol 7: 178.
- Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T (2001) Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 276: 19959-19965.
- Khalturin K, Bosch TC (2007) Self/non-self discrimination at the basis of chordate evolution: limits on molecular conservation. Curr Opin Immunol 19: 4-9.
- Khalturin K, Becker M, Rinkevich B, Bosch TC (2003) Urochordates and the origin of natural killer cells: identification of a CD94/NKR-P1-related receptor in blood cells of Botryllus. Proc Natl Acad Sci USA 100: 622-627.
- Kimura Y, Inoue N, Fukui A, Oshiumi H, Matsumoto M, Nonaka M, Kuratani S, Fujita T, Nonaka M, Seya T (2004) A short consensus repeat-containing complement regulatory protein of lamprey that participates in cleavage of lamprey complement 3. J Immunol 173: 1118-1128.
- Kimura A, Sakaguchi E, Nonaka M (2009) Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone. Nematostella vectensis. Immunobiology 214: 165-178.
- Kindt TJ, Goldsby RA, Osborne BA (2007) Kuby Immunology. Sixth edn. W.H. Freeman and Company, New York.
- King N, Hittinger CT, Carroll SB (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361-363.
- Kingsley DM (1994) The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133-146.
- Klein J (1986) natural history of the major histocompatibility complex. Wiley Interscience. New York.
- Klein J (2006) The grapes of incompatibility. Dev Cell 10: 2-4.
- Klein J, O'hUigin C (1993) Composite origin of major histocompatibility complex genes. Curr Opin Genet Dev 3: 923-930.
- Klein J, Nikolaidis N (2005) The descent of the antibody-based immune system by gradual evolution. Proc Natl Acad Sci USA 102: 169-174.
- Kopacek P, Hall KM, Söderhäll K (1993) Characterization of a clotting protein, isolated from plasma of the freshwater crayfish Pacifastacus leniusculus. Eur J Biochem 213: 591-597.
- Krarup A, Wallis R, Presanis JS, Gál P, Sim RB (2007) Simultaneous activation of complement and coagulation by MBL-associated serine protease 2. PLoS One 2: e623.
- Krasko A, Gamulin V, Seack J, Steffen R, Schröder HC, Müller WEG (1997) Cathepsin, a major protease of the marine sponge Geodia cydonium: purification of the enzyme and molecular cloning of cDNA Mol Marine Biol Biotechnol 6: 296-307.
- Krause CD, Pestka S (2005) Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol Ther 106: 299-346.
- Krem MM, Di Cera E (2002) Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem Sci 27: 67-74.
- Krushkal J, Kemper C, Gigli I (1998) Ancient origin of human complement factor H. J Mol Evol 47: 625-630.
- Kusumoto H, Hirosawa S, Salier JP, Hagen FS, Kurachi K (1988) Human genes for complement components C1r and C1s in a close tail-to-tail arrangement. Proc Natl Acad Sci USA 85: 7307-7311.
- Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123: 1351-1360.
- Lardy B, Bof M, Aubry L, Paclet MH, Morel F, Satre M, Klein G (2005) NADPH oxidase homologs are required for normal cell differentiation and morphogenesis in Dictyostelium discoideum. Biochim Biophys Acta 1744: 199-212.
- Lazzaro BP (2005) Elevated polymorphism and divergence in the class C scavenger receptors of Drosophila melanogaster and D. simulans. Genetics 169: 2023-2034.
- Lee PH, Goetz FW (1998) Characterization of a novel cDNA obtained through differential-display PCR of phorbol ester-stimulated ovarian tissue from the brook trout (Salvelinus fontinalis). Mol Reprod Dev 49: 112-118.
- Leippe M (1995) Ancient weapons: NK-lysin, is a mammalian homolog to pore-forming peptides of a protozoan parasite. Cell 83: 17-18.
- Leippe M (1999) Antimicrobial and cytolytic polypeptides of ameboid protozoa - effector molecules of primitive phagocytes. Dev Comp Immunol 23: 267-279.
- Leippe M, Andrä J, Nickel R, Tannich E, Müller-Eberhard HJ (1994) Amoebapores, a family of membranolytic peptides from cytoplasmic granules of Entamoeba histolytica: isolation, primary structure, and pore formation in bacterial cytoplasmic membranes. Mol Microbiol 14: 895-904.
- Letterio JJ, Roberts AB (1998) Regulation of immune responses by TGF-β. Annu Rev Immunol 16: 137-161.
- Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in culture cells of the mosquito, Anopheles gambiae. Cell 104: 709-718.
- Li X, Namikawa-Yamada C, Nakanishi M, Sasaki M, Nonaka M (2000) Molecular cloning of complement factor B from a solidary ascidian: unique combination of domains and implicating ancient exon shufflings. Immunopharmacology 49: 43.
- Little KD, Hemler ME, Stipp CS (2004) Dynamic regulation of a GPCR-tetraspanin-G protein complex on intacT-cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Mol Biol Cell 15: 2375-2387.
- Lucas R, Magez S, De Leys R, Fransen L, Scheerlinck JP, Rampelberg M, Sablon E, De Baetselier P (1994) Mapping the lectin-like activity of tumor necrosis factor. Science 263: 814-817.
- Luckhart S, Rosenberg R (1999) Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232: 25-34.
- Luo C, Zheng L (2000) Independent evolution of Toll and related genes in insects and mammals. Immunogenetics 51: 92-98.
- Mah SA, Moy GW, Swanson WJ, Vacquier VD (2004) A perforin-like protein from a marine mollusk. Biochem Biophys Res Commun 316: 468-475.
- Mangel A, Leitão JM, Batel R, Zimmermann H, Müller WE, Schröder HC (1992) Purification and characterization of a pore-forming protein from the marine sponge Tethya lyncurium. Eur J Biochem 210: 499-507.
- Marmaras VJ, Charalambidis ND, Zervas CG (1996) Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch Insect Biochem Physiol 31: 119-133.
- Matsushita M, Takahashi M, Thiel S, Jensenius JC, Fujita T (1998) Distinct proteolytic activities of MASP-1 and MASP-2. Mol Immunol 35: 349-349.
- Matsushita M, Matsushita A, Endo Y, Nakata M, Kojima N, Mizuochi T, Fujita T (2004) Origin of the classical complement pathway: Lamprey orthologue of mammalian C1q acts as a lectin. Proc Natl Acad Sci USA 101: 10127-10131.
- Mayer WE, Tichy H (1995) A cDNA clone from the sea lamprey Petromyzon marinus coding for a scavenger receptor Cys-rich (SRCR) domain protein. Gene 164: 267-271.
- Meister M, Lagueux M (2003) Drosophila blood cells. Cell Microbiol 5: 573-580.
- Miller MM, Wang C, Parisini E, Coletta RD, Goto RM, Lee SY, Barral DC, Townes M, Roura-Mir C, Ford HL, Brenner MB, Dascher CC (2005) Characterization of two avian MHC-like genes reveals an ancient origin of the CD1 family Proc Natl Acad Sci USA 102: 8674-8679.
- Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TC (2007) The innate immune repertoire in cnidaria - ancestral complexity and stochastic gene loss. Genome Biol 8: 1-13.
- Minnick MF, Rupp RA, Spence KD (1986) A bacterial-induced lectin which triggers hemocyte coagulation in Manduca sexta. Biochem Biophys Res Commun 137: 729-735.
- Mondragon-Palomino M, Pinero D, Nicholson-Weller A, Laclette JP (1999) Phylogenetic analysis of the homologous proteins of the terminal complement complex supports the emergence of C6 and C7 followed by C8 and C9. J Mol Evol 49: 282-289.
- Morgan BP (1999) Regulation of the complement membrane attack pathway. Crit Rev Immunol 19: 173-198.
- Moscona AA (1968) Cell aggregation: properties of specific cell-ligands and their role in the formation of multicellular systems. Dev Biol 18: 250-277.
- Müller WE, Blumbach B, Müller IM (1999a) Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum (Porifera) and those in vertebrates. Transplantation 68: 1215-1227.
- Müller WE, Koziol C, Müller IM, Wiens M (1999b) Towards an understanding of the molecular basis of immune responses in sponges: the marine demosponge Geodia cydonium as a model. Microsc Res Tech 44: 219-236.
- Munford RS, Sheppard PO, O'Hara PJ (1995) Saposin-like proteins (SAPLIP) carry out diverse functions on a common backbone structure. J Lipid Res 36: 1653-1663.
- Muta T, Iwanaga S (1996) The role of hemolymph coagulation in innate immunity. Curr Opin Immunol 8: 41-47.
- Muta T, Miyata T, Misumi Y, Tokunaga F, Nakamura T, Toh Y, Ikehara Y, Iwanaga S (1991) Limulus factor C. An endotoxin-sensitive serine protease zymogen with a mosaic structure of complement-like, epidermal growth factor-like, and lectin-like domains. J Biol Chem 266: 6554-6561.
- Muta T, Seki N, Takaki Y, Hashimoto R, Oda T, Iwanaga A, Tokunaga F, Iwanaga S (1995) Purified horseshoe crab factor G. Reconstitution and characterization of the (1→3)-β-d-glucan-sensitive serine protease cascade. J Biol Chem 270: 892-897.
- Nagai T, Kawabata S (2000) A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J Biol Chem 275: 29264-29267.
- Nakao M, Osaka K, Kato Y, Fujiki K, Yano T (2001) Molecular cloning of the complement (C1r/C1s/MASP2-like serine proteases from the common carp (Cyprinus carpio). Immunogenetics 52: 255-263.
- Nakao M, Hisamatsu S, Nakahara M, Kato Y, Smith SL, Yano T (2003a) Molecular cloning of the complement regulatory factor I isotypes from the common carp (Cyprinus carpio). Immunogenetics 54: 801-806.
- Nakao M, Mutsuro J, Nakahara M, Kato Y, Yano T (2003b) Expansion of genes encoding complement components in bony fish: biological implications of the complement diversity. Dev Comp Immunol 27: 749-762.
- Nappi AJ, Ottaviani E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22: 469-480.
- Nappi AJ, Vass E, Frey F, Carton Y (1995) Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur J Cell Biol 68: 450-456.
- Nappi AJ, Vass E, Frey F, Carton Y (2000) Nitric oxide involvement in Drosophila Immunity Nitric Oxide 4: 423-430.
- Neuberger MS (2008) Antibody diversification by somatic mutation: from Burnet onwards. Immunol Cell Biol 86: 124-132.
- Niedermann G, Grimm R, Geier E, Maurer M, Realini C, Gartmann C, Soll J, Omura S, Rechsteiner MC, Baumeister W, Eichmann K (1997) Potential immunocompetence of proteolytic fragments produced by proteasomes before evolution of the vertebrate immune system. J Exp Med 186: 209-220.
- Nonaka M (2001) Evolution of the complement system. Curr Opin Immunol 13: 69-73.
- Nonaka M, Takahashi M (1992) Complete complementary DNA sequence of the third component of complement of lamprey. Implication for the evolution of thioester containing proteins. J Immunol 148: 3290-3295.
- Nonaka M, Miyazawa S (2002) Evolution of the initiating enzymes of the complement system. Genome Biol 3: Reviews 1001.
- Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58: 701-713.
- Nonaka M, Matsuda Y, Shiroishi T, Moriwaki K, Nonaka M, Natsuume-Sakai S (1993) Molecular cloning of the b subunit of mouse coagulation factor XIII and assignment of the gene to chromosome 1: close evolutionary relationship to complement factor H. Genomics 15: 535-542.
- Nonaka M, Takahashi M, Sasaki M (1994) Molecular cloning of a lamprey homologue of the mammalian MHC class III gene, complement factor B. J Immunol 152: 2263-2269.
- Nonaka M, Azumi K, Ji X, Namikawa-Yamada C, Sasaki M, Saiga H,. Dodds AW, Sekine H, Homma MK, Matsushita M, Endo Y, Fujita T (1999) Opsonic complement component C3 in the solitary urochordate, Halocynthia roretzi. J Immunol 162: 387-391.
- Nonaka M, Yamada-Namikawa C, Flajnik MF, Du Pasquier L (2000) Trans-species polymorphism of the major histocompatibility complex-encoded proteasome subunit LMP7 in an amphibian genus, Xenopus. Immunogenetics 51: 186-192.
- Nosanchuk JD, Casadevall A (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5: 203-223.
- Ohno S (1987) The ancestor of the adaptive immune system was the CAM system for organogenesis. Exp Clin Immunogenet 4: 181-192.
- Osaki T, Kawabata S (2004) Structure and function of coagulogen, a clottable protein in horseshoe crabs. Cell Mol Life Sci 61: 1257-1265.
- Ottaviani E, Franceschi C (1997) The invertebrate phagocytic immunocyte: clues to a common evolution of immune and neuroendocrine systems. Immunol Today 18: 169-174.
- Pahler S, Blumbach B, Muller I, Muller EW (1998) Putative multiadhesive protein from the marine sponge Geodia cydonium: cloning of the cDNA encoding a fibronectin-, an SRCR-, and a complement control protein module. J Exp Zool 282: 332-343.
- Pålsson-McDermott EM, O'Neill LA (2004) Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113: 153-162.
- Palumbo A (2005) Nitric oxide in marine invertebrates: A comparative perspective. Comp Biochem Physiol A Mol Integr Physiol 142: 241-248.
- Pancer Z (2000) Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci USA 97: 13156-13161.
- Pancer Z, Kruse M, Schäcke H, Scheffer U, Steffen R, Kovács P, Müller WE (1996a) Polymorphism in the immunoglobulin-like domains of the receptor tyrosine kinase from the sponge Geodia cydonium. Cell Adhes Commun 4: 327-339.
- Pancer Z, Scheffer U, Müller I, Müller WEG (1996b) Cloning of sponge (Geodia cydonium) and tunicate (Botryllus schlosseri) proteasome subunit epsilon (PRCE): implications about the evolution of the vertebrate MHC-encoded homologue LMP7 (PRCC). Biochem Biophys Res Commun 228: 406-410.
- Pancer Z, Münkner J, Müller I, Müller WEG (1997) A novel member of an ancient superfamily: sponge (Geodia cydonium, Porifera) putative protein that features scavenger receptor cysteine-rich repeats. Gene 193: 211-218.
- Pancer Z, Skorokhod A, Blumbach B, Müller WEG (1998) Multiple Ig-like featuring genes divergent within and among individuals of the marine sponge Geodia cydonium. Gene 207: 227-233.
- Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD (2004a) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430: 174-180.
- Pancer Z, Mayer WE, Klein J, Cooper MD (2004b) Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc Natl Acad Sci USA 101: 13273-13278.
- Peiseret L, Mukhopadhyay S, Gordon S (2002) Scavenger receptors in innate immunity. Curr Opin Immunol 14: 123-128.
- Peña SV, Hanson DA, Carr BA, Goralski TJ, Krensky AM (1997) Processing, subcellular localization, and function of 519 (granulysin), a human late T-cell activation molecule with homology to small, lytic, granule proteins. J Immunol 158: 2680-2688.
- Penna G, Vulcano M, Sozzani S, Adorini L (2002) Differential migration behavior and chemokine production by myeloid and plasmacytoid dendritic cells. Hum Immunol 63: 1164-1171.
- Pereira LS, Oliveira PL, Barja-Fidalgo C, Daffre S (2001) Production of reactive oxygen species by hemocytes from the cattle tick Boophilus microplus. Exp Parasitol 99: 66-72.
- Perović-Ottstadt S, Adell T, Proksch P, Wiens M, Korzhev M, Gamulin V, Müller IM, Müller WE (2004) A (1→3)-β-d-glucan recognition protein from the sponge Suberites domuncula. Mediated activation of fibrinogen-like protein and epidermal growth factor gene expression. Eur J Biochem 271: 1924-1937.
- Peskin AV, Labas YA, Tikhonov AN (1998) Superoxide radical production by sponges Sycon sp. FEBS Lett 434: 201-204.
- Pfeifer K, Haaseman M, Gamulin V, Bretting H, Fahrenholz F, Müller WEG (1993) S-Type lectins occur also in invertebrates: High conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydonium. Glycobiology 3: 179-184.
- Płonka PM, Grabacka M (2006) Melanin synthesis in microorganism - biotechnological and medical aspects. Acta Biochim Pol 53: 429-443.
- Podack ER, Olsen KJ, Lowrey DM, Lichtenheld M (1989) Structure and function of perforin. Curr Top Microbiol Immunol 140: 11-17.
- Powis SJ, Deverson EV, Coadwell WJ, Ciruela A, Huskisson NS, Smith H, Butcher GW, Howard JC (1992) Effect of polymorphism of an MHC-linked transporter on the peptides assembled in a class I molecule. Nature 357: 211-215.
- Prager EM (1996) Adaptive evolution of lysozyme: changes in amino acid sequence, regulation of expression and gene number. EXS 75: 323-345.
- Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, Tan MW, Ray KP, Solari R, Johnson CD, Ewbank JJ (2001) A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 11: 809-821.
- Qiu L, Song L, Xu W, Ni D, Yu Y (2007) Molecular cloning and expression of a Toll receptor gene homologue from Zhikong Scallop, Chlamys farreri. Fish Shellfish Immunol 22: 451-466.
- Raftos D (1996) Interactions of tunicate immunomodulatory proteins with mammalian cells. Immunol Cell Biol 74: 26-31.
- Rast JP, Litman GW (1994) T-cell receptor gene homologs are present in the most primitive jawed vertebrates. Proc Natl Acad Sci USA 91: 9248-9252.
- Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314: 952-956.
- Rathjen JP, Chang JH, Staskawicz BJ, Michelmore RW (1999) Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO J 18: 3232-3240.
- Reid KBM, Day AJ (1989) Structure-function relationship of the complement components. Immunol Today 10: 177-180.
- Resnick D, Pearson A, Krieger M (1994) The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 19: 5-8.
- Rhodes CP, Ratcliffe NA, Rowley AF (1982) Presence of coelomocytes in the primitive chordate amphioxus (Branchiostoma lanceolatum). Science 217: 263-265.
- Ribeiro JM, Hazzard JM, Nussenzveig RH, Champagne DE, Walker FA (1993) Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect. Science 260: 539-541.
- Rivero A (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol 22: 219-224.
- Ryan RO, van der Horst DJ (2000) Lipid transport biochemistry and its role in energy production. Annu Rev Entomol 45: 233-260.
- Rypniewski WR, Perrakis A, Vorgias CE, Wilson KS (1994) Evolutionary divergence and conservation of trypsin. Protein Eng 7: 57-64.
- Salomonsen J, Rathmann Sørensen M, Marston DA, Rogers SL, Collen T, van Hateren A, Smith AL, Beal RK, Skjødt K, Kaufman J (2005) Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC. Proc Natl Acad Sci USA 102: 8668-8673.
- Salter-Cid L, Flajnik MF (1995) Evolution and developmental regulation of the major histocompatibility complex. Crit Rev Immunol 15: 31-75.
- Salzet M, Tasiemski A, Cooper E (2006) Innate immunity in lophotrochozoans: the annelids. Curr Pharm Des 12: 3043-3050.
- Samal B, Sun Y, Stearns G, Xie C, Suggs S, McNiece I (1994) Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol Cell Biol 14: 1431-1437.
- Sato A, Mayer WE, Klein J (2003) A molecule bearing an immunoglobulin-like V region of the CTX subfamily in amphioxus. Immunogenetics 55: 423-427.
- Schluter SF, Bernstein RM, Marchalonis JJ (1997) Molecular origins and evolution of immunoglobulin heavy-chain genes of jawed vertebrates. Immunol Today 18: 543-549.
- Schröder HC, Ushijima H, Krasko A, Gamulin V, Thakur NL, Diehl-Seifert B, Müller IM, Müller WE (2003) Emergence and disappearance of an immune molecule, an antimicrobial lectin, in basal metazoa. A tachylectin-related protein in the sponge Suberites domuncula. J Biol Chem 278: 32810-32817.
- Sekine H, Kenjo A, Azumi K, Ohi G, Takahashi M, Kasukawa R, Ichikawa N, Nakata M, Mizuochi T, Matsushita M, Endo Y, Fujita T (2001) An ancient Lectin-Dependent Complement System in an Ascidian: Novel Lectin Isolated from the Plasma of the Solitary Ascidian, Halocynthia roretzi. J Immunol 167: 4504-4510.
- Shin DH, Webb B, Nakao M, Smith SL (2007) Molecular cloning, structural analysis and expression of complement component Bf/C2 genes in the nurse shark, Ginglymostoma cirratum. Dev Comp Immunol 31: 1168-1182.
- Sillo A, Bloomfield G, Balest A, Balbo A, Pergolizzi B, Peracino B, Skelton J, Ivens A, Bozzaro S (2008) Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9: 291.
- Smith SL (1998) Shark complement: an assessment. Immunol Rev 166: 67-78.
- Smith CL, DeLotto R (1992) A common domain within the proenzyme regions of the Drosophila snake and easter proteins and Tachypleus proclotting enzyme defines a new subfamily of serine proteases. Protein Sci 1: 1225-1226.
- Smith LC, Clow LA, Terwilliger DP (2001) The ancestral complement system in sea urchins. Immunol Rev 180: 16-34.
- Smolenaars MM, Madsen O, Rodenburg KW, Van der Horst DJ (2007) Molecular diversity and evolution of the large lipid transfer protein superfamily. J Lipid Res 48: 489-502.
- Söderhäll K, Cerenius L, Johansson MW (1994) The prophenoloxidase activating system and its role in invertebrate defence. Ann N Y Acad Sci 712: 155-161.
- Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS (1990) Sequence identity between the α2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 265: 17401-17404.
- Sumimoto H (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275: 3249-3277.
- Suzuki T, Shin-I T, Kohara Y, Kasahara M (2004) Transcriptome analysis of hagfish leukocytes: a framework for understanding the immune system of jawless fishes. Dev Comp Immunol 28: 993-1003.
- Takezaki N, Figueroa F, Zaleska-Rutczynska Z, Klein J (2003) Molecular phylogeny of early vertebrates: monophyly of the agnathans as revealed by sequences of 35 genes. Mol Biol Evol 20: 287-292.
- Tan MW, Ausubel FM (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3: 29-34.
- Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB (1999) Overexpression of Pto activates defense responses and confers broad resistance. PlanT-cell 11: 15-29.
- Tenor JL, Aballay A (2008) A conserved Toll-like receptor is required for Caenorhabditis elegans innate immunity. EMBO Rep 9: 103-109.
- Thiel S, Vorup-Jensen T, Stover CM, Schwaeble W, Laursen SB, Poulsen K, Willis AC, Eggleton P, Hansen S, Holmskov U, Reid KB, Jensenius JC (1997) A second serine protease associated with mannan-binding lectin that activates complement. Nature 386: 506-510.
- Travis J (2009) Origins. On the origin of the immune system. Science 324: 580-582.
- Trinité B, Voisine C, Yagita H, Josien R (2000) A subset of cytolytic dendritic cells in rat. J Immunol 165: 4202-4208.
- Uinuk-Ool T, Mayer WE, Sato A, Dongak R, Cooper MD, Klein J (2002) Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc Natl Acad Sci USA 99: 14356-14361.
- Uinuk-Ool TS, Mayer WE, Sato A, Takezaki N, Benyon L, Cooper MD, Klein J (2003a) Identification and characterization of a TAP-family gene in the lamprey. Immunogenetics 55: 38-48.
- Uinuk-Ool TS, Takezaki N, Kuroda N, Figueroa F, Sato A, Samonte IE, Mayer WE, Klein J (2003b) Phylogeny of antigen-processing enzymes: cathepsins of a cephalochordate, an agnathan and a bony fish. Scand J Immunol 58: 436-448.
- Utans U, Arceci RJ, Yamashita Y, Russell ME (1995) Cloning and characterization of allograft inflammatory factor-1: a novel macrophage factor identified in rat cardiac allografts with chronic rejection. J Clin Invest 95: 2954-2962.
- Van Endert PM (1999) Genes regulating MHC class I processing of antigen. Curr Opin Immunol 11: 82-88.
- Van Leuven F, Cassiman JJ, Van den Berghe H (1978) Uptake and degradation of α2-macroglobulin-protease complexes in human cells in culture. Exp Cell Res 117: 273-282.
- Varner J, Neame P, Litman GW (1991) A serum heterodimer from hagfish (Eptatretus stoutii) exhibits structural similarity and partial sequence identity with immunoglobulin. Proc Natl Acad Sci USA 88: 1746-1750.
- Vasta GR, Ahmed H, Fink NE, Elola MT, Marsh AG, Snowden A, Odom EW (1994) Animal lectins as self/non-self recognition molecules. Biochemical and genetic approaches to understanding their biological roles and evolution. Ann N Y Acad Sci 712: 55-73.
- Waddell DR, Duffy KT (1986) Breakdown of self/non-self recognition in cannibalistic strains of the predatory slime mold, Dictyostelium caveatum. J Cell Biol 102: 298-305.
- Watts C, Powis S (1999) Pathways of antigen processing and presentation. Rev Immunogenet 1: 60-74.
- Wiens M, Korzhev M, Krasko A, Thakur NL, Perović-Ottstadt S, Breter HJ,Ushijima H, Diehl-Seifert B, Müller IM, Müller WE (2005) Innate immune defense of the sponge Suberites domuncula against bacteria involves a MyD88-dependent signaling pathway. Induction of a perforin-like molecule. J Biol Chem 280: 27949-27959.
- Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.
- Whitten MMA, Ratcliffe Norman A (1999) In vitro superoxide activity in the haemolymph of the West Indian leaf cockroach, Blaberus discoidalis. J Insect Physiol 45: 667-675.
- Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WE (2007) Toll-like receptors are part of the innate immune system of sponges (demospongiae: Porifera) Mol Biol Evol 24: 792-804.
- Wiens M, Koziol C, Batel R, Müller WEG (1998) Phenylalanine hydroxylase from the sponge Geodia cydonium: implication for allorecognition and evolution of aromatic amino acid hydroxylases. Dev Comp Immunol 22: 469-478.
- Wimmer W, Blumbach B, Diehl-Seifert B, Koziol C, Batel R, Steffen R, Müller IM, Müller WE (1999) Increased expression of integrin and receptor tyrosine kinase genes during autograft fusion in the sponge Geodia cydonium. Cell Adhes Commun 7: 111-124.
- Wölfle U, Martin S, Emde M, Schempp C (2009) Dermatology in the Darwin anniversary. Part 2: Evolution of the skin-associated immune system. J Dtsch Dermatol Ges 7: 862-869.
- Xie K, Sowden MP, Dance GS, Torelli AT, Smith HC, Wedekind JE (2004) The structure of a yeast RNA-editing deaminase provides insight into the fold and function of activation-induced deaminase and APOBEC-1. Proc Natl Acad Sci USA 101: 8114-8119.
- Yeh FC, Wu SH, Lai CY, Lee CY (2006) Demonstration of nitric oxide synthase activity in crustacean hemocytes and anti-microbial activity of hemocyte-derived nitric oxide. Comp Biochem Physiol B Biochem Mol Biol 144: 11-17.
- Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T (2001) Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 291: 2135-2138.
- Zanetta JP, Vergoten G (2003) Lectin domains on cytokines. Adv Exp Med Biol 535: 107-124.
- Zarkadis IK, Mastellos D, Lambris JD (2001) Phylogenetic aspects of the complement system. Dev Comp Immunol 25: 745-762.
- Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
- Zhang F, Zhang W, Liu L, Fisher CL, Hui D, Childs S, Dorovini-Zis K, Ling V (2000) Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes. J Biol Chem 275: 23287-23294.
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