Invertebrate immune diversity

Developmental and Comparative Immunology

Volumn 35, Issue 9, 2011, Pages 959-974

  Ghosh, Julie ^a   Lun, Cheng Man ^a   Majeske, Audrey J ^a   Sacchi, Sandro ^a   Schrankel, Catherine S ^a,b   Smith, L Courtney ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Crustins; Dscam; Fester; FREPs; Fuhc; Gene family evolution; Immune diversification; Innate immunity; Penaeidins; PGRP; Sp185 333; Uncle fester; VCBP

Indexed keywords

BINDING PROTEIN; CELL ADHESION MOLECULE; CRUSTIN; DOWN SYNDROME CELL ADHESION MOLECULE; FESTER PROTEIN; FIBRINOGEN RELATED PROTEIN; FUHC PROTEIN; HYASTATIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; MEMBRANE PROTEIN; PEPTIDOGLYCAN RECOGNITION PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; SP185 333 PROTEIN; UNCLASSIFIED DRUG; VARIABLE DOMAIN CONTAINING CHITIN BINDING PROTEIN; WHEY ACIDIC PROTEIN;

ALTERNATIVE RNA SPLICING; ANTIGEN RECOGNITION; ANTIMICROBIAL ACTIVITY; ARTICLE; BRANCHIOSTOMA; COEVOLUTION; COMPLEMENT SYSTEM; COMPLEMENTARITY DETERMINING REGION; CRUSTACEA; FESTER GENE; FREP GENE; FUHC GENE; GENE; GENE CONVERSION; GENE DUPLICATION; GENE FREQUENCY; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HAPLOTYPE; IMMUNE RESPONSE; INSECT; INVERTEBRATE; MOLLUSC; NONHUMAN; PENAEIDAE; PGRP GENE; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA EDITING; SEA URCHIN; SINGLE NUCLEOTIDE POLYMORPHISM; SP185 333 GENE;

ARTHROPODA; CRUSTACEA; ECHINOIDEA; GASTROPODA; INVERTEBRATA;

EID: 79959223954     PISSN: 0145305X     EISSN: 0145305X     Source Type: Journal    
DOI: 10.1016/j.dci.2010.12.009     Document Type: Review

References (172)

1. Haldane J.B.S. Disease and evolution. La Ricerca Scientifica 1949, 19(suppl):68-75.
2. Ferrandon D., Imler J.L., Hetru C., Hoffmann J.A. The Drosophila systemic immune response: sensing and signaling during bacterial and fungal infections. Nature Reviews Immunology 2007, 7(11):862-874.
3. Peiser L., Gordon S. The function of scavenger receptors expressed by macrophages and their role in the regulation of inflammation. Microbes and Infection 2001, 3(2):149-159.
4. Cigana C., Curcuru L., Leone M.R., Ierano T., Lore N.I., Bianconi I., et al. Pseudomonas aeruginosa exploits lipid A and muropeptides modification as a strategy to lower innate immunity during cystic fibrosis lung infection. PLoS One 2009, 4(12):e8439.
5. Herrin B.R., Cooper M.D. Alternative adaptive immunity in jawless vertebrates. Journal of Immunology 2010, 185:1367-1374.
6. Tassanakajon A., Amparyup P., Somboonwiwat K., Supungul P. Cationic antimicrobial peptides in penaeid shrimp. Marine Biotechnology (NY) 2010, 12(5):487-505.
7. Brown K.L., Hancock R.E. Cationic host defense (antimicrobial) peptides. Current Opinion in Immunology 2006, 18(1):24-30.
8. Hancock R.E., Brown K.L., Mookherjee N. Host defence peptides from invertebrates-emerging antimicrobial strategies. Immunobiology 2006, 211(4):315-322.
9. Yang D., Biragyn A., Kwak L.W., Oppenheim J.J. Mammalian defensins in immunity: more than just microbicidal. Trends in Immunology 2002, 23(6):291-296.
10. Bulet P., Stocklin R., Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunological Reviews 2004, 198:169-184.
11. Bartlett T.C., Cuthbertson B.J., Shepard E.F., Chapman R.W., Gross P.S., Warr G.W. Crustins, homologues of an 11.5kDa antibacterial peptide, from two species of penaeid shrimp, Litopenaeus vannamei and Litopenaeus setiferus. Marine Biotechnology (NY) 2002, 4(3):278-293.
12. Cuthbertson B.J., Shepard E.F., Chapman R.W., Gross P.S. Diversity of the penaeidin antimicrobial peptides in two shrimp species. Immunogenetics 2002, 54(6):442-445.
13. Destoumieux D., Bulet P., Loew D., Van Dorsselaer A., Rodriguez J., Bachere E. Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). Journal of Biological Chemistry 1997, 272(45):28398-28406.
14. Destoumieux D, Munoz M., Bulet P., Bachere E. Penaeidins, a family of antimicrobial peptides from penaeid shrimp (Crustacea, Decapoda). Cellular and Molecular Life Sciences 2000, 57(8-9):1260-1271.
15. Gueguen Y., Garnier J., Robert L., Lefranc M.P., Mougenot I., de Lorgeril J., et al. the shrimp antimicrobial peptide penaeidin database: sequence-based classification and recommended nomenclature. Developmental and Comparative Immunology 2006, 30(3):283-288.
16. O'Leary N.A., Gross P.S. Genomic structure and transcriptional regulation of the penaeidin gene family from Litopeneaus vannamei. Gene 2006, 371(1):75-83.
17. Cuthbertson B.J., Yang Y., Bachere E., Bullesbach E.E., Gross P.S., Aumelas A. Solution structure of synthetic penaeidin-4 with structural and functional comparisons with penaeidin-3. Journal of Biological Chemistry 2005, 280(16):16009-16018.
18. Yang Y., Poncet J., Garnier J., Zatylny C., Bachere E., Aumelas A. Solution structure of the recombinant penaeidin-3, a shrimp antimicrobial peptide. Journal of Biological Chemistry 2003, 278(38):36859-36867.
19. Yamada K, Takabatake T., Takeshima K. Isolation and characterization of three novel serine protease genes from Xenopus laevis. Gene 2000, 252(1-2):209-216.
20. Cuthbertson B.J., Deterding L.J., Williams J.G., Tomer K.B., Etienne K., Blackshear P.J., et al. Diversity in penaeidin antimicrobial peptide form and function. Developmental and Comparative Immunology 2008, 32(3):167-181.
21. Kang C., Xue J., Liu N., Zhao X., Wang J. Characterization and expression of a new subfamily member of penaeidin antimicrobial peptides (penaeidin 5) form Fenneropennawus chinensis. Molecular Immunology 2007, 44:1535-1543.
22. Cuthbertson B.J., Bullesbach E.E., Fievet J., Bachere E., Gross P.S. A new class (penaeidin class 4) of antimicrobial peptides from the Atlantic white shrimp (Litopenaeus setiferus) exhibits target specificity and an independent proline-rich-domain function. Biochemistry Journal 2004, 381(Pt 1):79-86.
23. Cuthbertson B.J., Bullesbach E.E., Gross P.S. Discovery of synthetic penaeidin activity against antibiotic-resistant fungi. Chemistry and Biology of Drug Design 2006, 68(2):120-127.
24. Sperstad S.V., Haug T., Vasskog T., Stensvag K. Hyastatin, a glycine-rich multi-domain antimicrobial peptide isolated from the spider crab (Hyas araneus) hemocytes. Molecular Immunology 2009, 46(13):2604-2612.
25. Sperstad S.V., Haug T., Paulsen V., Rode T.M., Strandskog G., Solem S.T., et al. Characterization of crustins from the hemocytes of the spider crab, Hyas araneus, and the red king crab, Paralithodes camtschaticus. Developmental and Comparative Immunology 2009, 33(4):583-591.
26. Padhi A., Verghese B., Otta S.K., Varghese B., Ramu K. Adaptive evolution after duplication of penaeidin antimicrobial peptides. Fish and Shellfish Immunology 2007, 23(3):553-566.
27. Brockton V., Hammond J.A., Smith V.J. Gene characterization, isoforms and recombinant expression of carcinin, an antibacterial protein from the shore crab, Carcinus maenas. Molecular Immunology 2007, 44(5):943-949.
28. Relf J.M., Chisholm J.R., Kemp G.D., Smith V.J. Purification and characterization of a cysteine-rich 11.5kDa antibacterial protein from the granular haemocytes of the shore crab Carcinus maenas. European Journal of Biochemistry 1999, 264(2):350-357.
29. Smith V.J., Chisholm J.R. Antimicrobial proteins in crustaceans. Advances in Experimental Medicine and Biology 2001, 484:95-112.
30. Gross P.S., Bartlett T.C., Browdy C.L., Chapman R.W., Warr G.W. Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the Pacific White Shrimp, Litopenaeus vannamei, and the Atlantic White Shrimp, L. setiferus. Developmental and Comparative Immunology 2001, 25(7):565-577.
31. Smith V.J., Fernandes J.M., Kemp G.D., Hauton C. Crustins: enigmatic WAP domain-containing antibacterial proteins from crustaceans. Developmental and Comparative Immunology 2008, 32(7):758-772.
32. Supungul P., Tang S., Maneeruttanarungroj C., Rimphanitchayakit V., Hirono I., Aoki T., et al. Cloning, expression and antimicrobial activity of crustinPm1, a major isoform of crustin, from the black tiger shrimp Penaeus monodon. Developmental and Comparative Immunology 2008, 32(1):61-70.
33. Amparyup P., Kondo H., Hirono I., Aoki T., Tassanakajon A. Molecular cloning, genomic organization and recombinant expression of a crustin-like antimicrobial peptide from black tiger shrimp Penaeus monodon. Molecular Immunology 2008, 45(4):1085-1093.
34. Zhang J., Li F., Wang Z., Xiang J. Cloning and recombinant expression of a crustin-like gene from Chinese shrimp Fenneropenaeus chinensis. Journal of Biotechnology 2007, 127(4):605-614.
35. Zhang J., Li F., Wang Z., Xiang J. Expression, purification, and characterization of recombinant Chinese shrimp crustin-like protein (CruFc) in Pichia pastoris. Biotechnology Letters 2007, 29(5):813-817.
36. Brockton V., Smith V.J. Crustin expression following bacterial injection and temperature change in the shore crab Carcinus maenas. Developmental and Comparative Immunology 2008, 32(9):1027-1033.
37. Hauton C., Brockton V., Smith V.J. Cloning of a crustin-like, single whey-acidic-domain, antibacterial peptide from the haemocytes of the European lobster, Homarus gammarus, and its response to infection with bacteria. Molecular Immunology 2006, 43(9):1490-1496.
38. Jiravanichpaisal P., Lee S.Y., Kim Y.A., Andren T., Soderhall I. Antibacterial peptides in hemocytes and hematopoietic tissue from freshwater crayfish Pacifastacus leniusculus: characterization and expression pattern. Developmental and Comparative Immunology 2007, 31(5):441-455.
39. Shockey J.E., O'Leary N.A., de la Vega E., Browdy C.L., Baatz J.E., Gross P.S. The role of crustins in Litopenaeus vannamei in response to infection with shrimp pathogens: an in vivo approach. Developmental and Comparative Immunology 2009, 33(5):668-673.
40. Chen J.Y., Chen J.C., Lin S.H., Pan C.Y., Kuo C.M. Organization and promoter analysis of a tiger shrimp Penaeus monodon sing WAP domain-containing protein gene. Fisheries Science 2006, 72:1086-1095.
41. Vatanavicharn T., Supungul P., Puanglarp N., Yingvilasprasert W., Tassanakajon A. Genomic structure, expression pattern and functional characterization of crustinPm5, a unique isoform of crustin from Penaeus monodon. Comparative Biochemistry and Physiology B Biochemistry and Molecular Biology 2009, 153(3):244-252.
42. Tassanakajon A., Vatanavicharn T., Supungul P., Tang S., Amparyup P., Somboonwiwat K., et al. Biotechnology of marine invertebrates - recent advances in shrimp and shellfish. Memorial book of the 5th World Fisheries Congress 2008 2008, TERRAPUB, Tokyo.
43. Manni L., Zaniolo G., Cima F., Burighel P., Ballarin L. Botryllus schlosseri: a model ascidian for the study of asexual reproduction. Developmental Dynamics 2007, 236(2):335-352.
44. Oka H., Watanabe H. Colony specificity in compound ascidians as tested by fusion experiments. Proceedings of the Japanese Academy of Science 1957, 33:657-664.
45. Oka H., Watanabe H. Problems of colony specificity in compound ascidians. Bulletin of the Biology Station at Asamushi 1960, 10:153-155.
46. Sabbadin A. Le basi genetiche della capacita di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Atti Accad Naz Lincei Rend 1962, 32:1031-1035.
47. Sabbadin A. The compound ascidian Botryllus schlosseri in the field and in the laboratory. Pubbl Staz Zool Napoli 1969, 37(Suppl):62-72.
48. Rinkevich B., Weissman I.L., De Tomaso A.W. Transplantation of Fu/HC-incompatible zooids in Botryllus schlosseri results in chimerism. Biological Bulletin 1998, 195(2):98-106.
49. Ballarin L., Cima F., Sabbadin A. Morula cells and histocompatibility in the colonial ascidian Botryllus schlosseri. Zoological Science 1995, 12(6):757-764.
50. Ballarin L., Cima F., Sabbadin A. Phenoloxidase and cytotoxicity in the compound ascidian Botryllus schlosseri. Developmental and Comparative Immunology 1998, 22(5-6):479-492.
51. Scofield V.L., Nagashima L.S. Morphology and genetics of rejection reactions between oozooids from the tunicate Botryllus schlosseri. Biological Bulletin 1983, 165(3):733-744.
52. De Tomaso A.W., Nyholm S.V., Palmeri K.J., Ishizuka K.J., Ludington W.B., Mitchel K., et al. Isolation and characterization of a protochordate histocompatibility locus. Nature 2005, 438(7067):454-945.
53. De Tomaso A.W., Saito Y., Ishizuka K.J., Palmeri K.J., Weissman I.L. Mapping the genome of a model protochordate, I. A low resolution genetic map encompassing the fusion/histocompatibility (Fu/HC) locus of Botryllus schlosseri. Genetics 1998, 149(1):277-287.
54. De Tomaso A.W., Weissman I.L. Construction and characterization of large-insert genomic libraries (BAC and fosmid) from the ascidian Botryllus schlosseri and initial physical mapping of a histocompatibility locus. Marine Biotechnology (NY) 2003, 5(2):103-115.
55. De Tomaso A.W., Weissman I.L. Initial characterization of a protochordate histocompatibility locus. Immunogenetics 2003, 55(7):480-490.
56. Grosberg R.K., Quinn J.F. The genetic-control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 1986, 322(6078):456-459.
57. McKitrick T.R., De Tomaso A.W. Molecular mechanisms of allorecognition in a basal chordate. Seminar in Immunology 2010, 22(1):34-38.
58. Rinkevich B., Porat R., Goren M. Allorecognition elements on a urochordate histocompatibility locus indicate unprecedented extensive polymorphism. Proceedings of the Royal Society London B Biology 1995, 259(1356):319-324.
59. Scofield V.L., Schlumpberger J.M., West L.A., Weissman I.L. Protochordate allorecognition is controlled by a MHC-like gene system. Nature 1982, 295(5849):499-502.
60. Nyholm S.V., Passegue E., Ludington W.B., Voskoboynik A., Mitchel K., Weissman I.L., et al. fester, a candidate allorecognition receptor from a primitive chordate. Immunity 2006, 25(1):163-173.
61. De Tomaso A.W. Sea squirts and immune tolerance. Disease Models and Mechanisms 2009, 2(9-10):440-445.
62. Lanier L.L. NK cell recognition. Annual Review of Immunology 2005, 23:225-274.
63. Aguilera A., Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nature Reviews Genetics 2008, 9(3):204-217.
64. Dishaw L.J., Litman G.W. Invertebrate allorecognition: the origins of histocompatibility. Current Biology 2009, 19(7):R286-R288.
65. Dehal P., Satou Y., Campbell R.K., Chapman J., Degnan B., De Tomaso A., et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298(5601):2157-2167.
66. Nicotra M.L., Powell A.E., Rosengarten R.D., Moreno M., Grimwood J., Lakkis F.G., et al. A hypervariable invertebrate allodeterminant. Current Biology 2009, 19(7):583-589.
67. Weissman I.L., Saito Y., Rinkevich B. Allorecognition histocompatibility in a protochordate species - is the relationship to MHC somatic or structural?. Immunological Reviews 1990, 113:227-241.
68. Burnet F.M. Self-recognition in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 1971, 232(5308):230-235.
69. Flajnik M.F., Du Pasquier L. Evolution of innate and adaptive immunity: can we draw a line?. Trends in Immunology 2004, 25(12):640-644.
70. Yamakawa K., Huot Y.K., Haendelt M.A., Hubert R., Chen X.N., Lyons G.E., et al. DSCAM: a novel member of the immunoglobulin superfamily maps in a Down syndrome region and is involved in the development of the nervous system. Human Molecular Genetics 1998, 7(2):227-237.
71. Holt R.A., Subramanian G.M., Halpern A., Sutton G.G., Charlab R., Nusskern D.R., et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298(5591):129-149.
72. Schmucker D., Clemens J.C., Shu H., Worby C.A., Xiao J., Muda M., et al. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 2000, 101(6):671-684.
73. Graveley B.R., Kaur A., Gunning D., Zipursky S.L., Rowen L., Clemens J.C. The organization and evolution of the dipteran and hymenopteran Down syndrome cell adhesion molecule (Dscam) genes. RNA 2004, 10(10):1499-1506.
74. Watson F.L., Puttmann-Holgado R., Thomas F., Lamar D.L., Hughes M., Kondo M., et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005, 309(5742):1874-1878.
75. Brites D., McTaggart S., Morris K., Anderson J., Thomas K., Colson I., et al. The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Molecular Biology and Evolution 2008, 25(7):1429-1439.
76. Crayton M.E., Powell B.C., Vision T.J., Giddings M.C. Tracking the evolution of alternatively spliced exons within the Dscam family. BMC Evolutionary Biology 2006, 6:16.
77. Celotto A.M., Graveley B.R. Alternative splicing of the Drosophila Dscam pre-mRNA is both temporally and spatially regulated. Genetics 2001, 159(2):599-608.
78. Lee C., Kim N., Roy M., Graveley B.R. Massive expansions of Dscam splicing diversity via staggered homologous recombination during arthropod evolution. RNA 2010, 16(1):91-105.
79. Graveley B.R. Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 2005, 123(1):65-73.
80. Kreahling J.M., Graveley B.R. The iStem, a long-range RNA secondary structure element required for efficient exon inclusion in the Drosophila Dscam pre-mRNA. Molecular and Cellular Biology 2005, 25(23):10251-10260.
81. Olson S., Blanchette M., Park J., Sawa Y., Yeo G.W., Yakkley J.M., et al. A regulator of Dscam mutually exclusive splicing fidelity. Nature Structural and Molecular Biology 2007, 14:1134-1140.
82. Schmucker D., Chen B. Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes and Development 2009, 23:147-156.
83. Dong Y., Taylor H.E., Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biology 2006, 4(7):e229.
84. Dziarski R., Gupta D. The peptidoglycan recognition proteins (PGRPs). Genealogy 2006, 7(8):232.
85. Lemaitre B., Hoffmann J.A. The host defense of Drosophila melanogaster. Annual Review of Immunology 2007, 25:697-743.
86. Kurata S. Extracellular and intracellular pathogen recognition by Drosophila PGRP-LE and PGRP-LC. International Immunology 2010, 22(3):143-148.
87. Mellroth P., Karlsson J., Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. The Journal of Biological Chemistry 2003, 278(9):7059-7064.
88. Bischoff V., Vignal C., Boneca I.G., Michel T., Hoffmann J.A., Royet J. Function of the Drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nature Immunology 2004, 5(11):1175-1180.
89. Riddell C., Adams S., Schimd-Hempel P., Mallon E.B. Differential expression of immune defences is associated with specific host-parasite interactions in insects. PLoS One 2009, 4(10):e7621.
90. Kaneko T., Yano T., Aggarwal K., Lim J.H., Ueda K., Oshima Y., et al. PGRP-LC and PGRP-LE have essential yet distinct functions in the Drosophila immune response to monomeric DAP-type peptidoglycan. Nature Immunology 2006, 7(7):715-723.
91. Leulier F., Parquet C., Pili-Floury S., Ryu J.H., Caroff M., Lee W.J., et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunology 2003, 4(5):478-484.
92. Lemaitre B. The road to Toll. Nature Reviews Immunology 2004, 4(7):521-527.
93. Werner T., Liu G., Kang D., Ekengren S., Steiner H., Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proceedings of National Academy of Science United States of America 2000, 97(25):13772-13777.
94. Charroux B., Rival T., Narbonne-Reveau K., Royet J. Bacterial detection by Drosophila peptidoglycan recognition proteins. Microbes and Infection 2009, 11(6-7):631-636.
95. Loker E.S., Adema C.M., Zhang S.-M., Kepler T.B. Invertebrate immune systems - not homogeneous, not simple, not well understood. Immunological Reviews 2004, 198(1):10-24.
96. Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal of Parasitology 2003, 33(7):733-755.
97. Loker E.S. Gastropod immunobiology. Invertebrate immunity 2010, Landes Bioscience and Spring Science Business Media. K. Soderhall (Ed.).
98. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nature Reviews Immunology 2002, 2(7):499-511.
99. Adema C.M., Hertel L.A., Miller R.D., Loker E.S. A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proceedings of National Academy of Science United States of America 1997, 94(16):8691-8696.
100. Leonard P.M., Adema C.M., Zhang S.M., Loker E.S. Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene 2001, 269(1-2):155-165.
101. Stout B.A., Adema C.M., Zhang S.M., Loker E.S. The biology of FREPs: diversified lectins with fibrinogen-related domains from the freshwater snail Biomphalaria glabrata. Animal lectins: A functional view 2009, 475-491. CRC Press, Taylor & Francis. V.A. Ahmen (Ed.).
102. Adema C.M., Hanington P.C., Lun C.M., Rosenberg G.H., Aragon A.D., Stout B.A., et al. Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea. Platyhelminthes). Molecular Immunology 2010, 47(4):849-860.
103. Hanington P.C., Lun C.M., Adema C.M., Loker E.S. Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. International Journal of Parasitology 2010, 40(7):819-831.
104. Zhang S.M., Zeng Y., Loker E.S. Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Journal of Innate Immunity 2008, 14(3):175-189.
105. Uttenweiler-Joseph S, Moniatte M., Lagueux M., Van Dorsselaer A., Hoffmann J.A., Bulet P. Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study. Proceedings of National Academy of Science United States of America 1998, 95(19):11342-11347.
106. Hertel L.A., Stricker S.A., Monroy F.P., Wilson W.D., Loker E.S. Biomphalaria glabrata hemolymph lectins: binding to bacteria, mammalian erythrocytes, and to sporocysts and rediae of Echinostoma paraensei. Journal of Invertebrate Pathology 1994, 64(1):52-61.
107. Humphries J.E, Yoshino T.P. Regulation of hydrogen peroxide release in circulating hemocytes of the planorbid snail Biomphalaria glabrata. Developmental and Comparative Immunology 2008, 32(5):554-562.
108. Zhang S.M., Adema C.M., Kepler T.B., Loker E.S. Diversification of Ig superfamily genes in an invertebrate. Science 2004, 305(5681):251-254.
109. Zhang S.M., Loker E.S. The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Developmental and Comparative Immunology 2003, 27(3):175-187.
110. Zhang S.M., Leonard P.M., Adema C.M., Loker E.S. Parasite-responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 2001, 53(8):684-694.
111. Zhang S.M., Loker E.S. Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 2004, 341:255-566.
112. Renwrantz L., Schancke W., Harm H., Erl H., Liebsch H., Gercken J. Discrimative ability and function of the immunobiological recognition system of the snail Helix pomatic. Journal of Comparative Physiology B 1981, 141:477-488.
113. Zhang S.M., Nian H., Zeng Y., Dejong R.J. Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Developmental and Comparative Immunology 2008, 32(10):1119-1130.
114. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., et al. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Developmental and Comparative Immunology 2005, 29(5):393-407.
115. Friedman A.R., Baker B.J. The evolution of resistance genes in multi-protein plant resistance systems. Current Opinion in Genetics and Development 2007, 17:493-499.
116. Gorbushin A.M., Panchin Y.V., Iakovleva N.V. In search of the origin of FREPs: characterization of Aplysia californica bifrinogen-related proteins. Developmental and Comparative Immunology 2009, 34(4):465-473.
117. Dong Y., Dimopoulos G. Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. Journal of Biological Chemistry 2009, 284(15):9835-9844.
118. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316(5832):1738-1743.
119. Wang X., Zhao Q., Christensen B.M. Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes. BMC Genomics 2005, 6(1):114.
120. Strong S.J., Mueller M.G., Litman R.T., Hawke N.A., Haire R.N., Miracle A.L., et al. A novel multigene family encodes diversified variable regions. Proceedings of National Academy of Science United States of America 1999, 96(26):15080-15085.
121. Yoder J.A., Mueller M.G., Wei S., Corliss B.C., Prather D.M., Willis T., et al. Immune-type receptor genes in zebrafish share genetic and functional properties with genes encoded by the mammalian leukocyte receptor cluster. Proceedings of National Academy of Science United States of America 2001, 98(12):6771-6776.
122. Cannon J.P., Haire R.N., Litman G.W. Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nature Immunology 2002, 3(12):1200-1207.
123. Cannon J.P., Haire R.N., Schnitker N., Mueller M.G., Litman G.W. Individual protochordates possess unique immune-type receptor repertoires. Current Biology 2004, 14:R465-R466.
124. Hernandez Prada J.A., Haire R.N., Allaire M., Jakoncic J., Stojanoff V., Cannon J.P., et al. Ancient evolutionary origin of diversified variable regions demonstrated by crystal structures of an immune-type receptor in amphioxus. Nature Immunology 2006, 7(8):875-882.
125. Cannon J.P., Dishaw L.J., Haire R.N., Litman R.T., Ostrov D.A., Litman G.W. Recognition of additional roles for immunoglobulin domains in immune function. Seminars in Immunology 2010, 22(1):17-24.
126. Litman G.W., Rast J.P., Fugmann S.D. The origins of vertebrate adaptive immunity. Nature Reviews Immunology 2010, 10:543-553.
127. Litman G.W., Dishaw L.J., Cannon J.P., Haire R.N., Rast J.P. Alternative mechanisms of immune receptor diversity. Current Opinion in Immunology 2007, 19:526-534.
128. Huang G., Liu H., Han Y., Fan L., Zhang Q., Liu J., et al. Profile of acute immune response in Chinese amphioxus upon Staphylococcus aureus and Vibrio parahaemolyticus infection. Developmental and Comparative Immunology 2007, 31(10):1013-1023.
129. Dishaw L.J., Mueller M.G., Gwatney N., Cannon J.P., Haire R.N., Litman R.T., et al. Genomic complexity of the variable region-containing chitin-binding proteins in amphioxus. BMC Genetics 2008, 9(1):78.
130. Dishaw L., Ota T., Mueller M., Cannon J., Haire R., Gwatney N., et al. The basis for haplotype complexity in VCBPs, an immune-type receptor in amphioxus. Immunogenetics 2010, 1-9.
131. Ghosh J.G., Buckley K.M., Nair S.V., Raftos D.A., Miller C.A., Majeske A.J., et al. Sp185/333: A novel family of genes and proteins involved in the purple sea urchin immune response. Developmental and Comparative Immunology 2010, 34:235-245.
132. Smith L.C., Ghosh J., Buckley K.M., Clow L.A., Dheilly N.M., Haug T., et al. Echinoderm immunity. Invertebrate immunity 2010, Landes Bioscience and Spring Science+Business Media. K. Soderhall (Ed.).
133. Rast J.P, Pancer Z., Davidson E.H. New approaches towards an understanding of deuterostome immunity. Current Topics in Microbiology and Immunology 2000, 248:3-16.
134. Smith L.C., Chang L., Britten R.J., Davidson E.H. Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Complement homologues and other putative immune response genes suggest immune system homology within the deuterostomes. Journal of Immunology 1996, 156(2):593-602.
135. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., Smith L.C. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin, Identification of unexpected immune diversity in an invertebrate. Physiological Genomics 2005, 22(1):33-47.
136. Terwilliger D.P., Buckley K.M., Brockton V., Ritter N.J., Smith L.C. Distinctive expression patterns of 185/333 genes in the purple sea urchin, Strongylocentrotus purpuratus: an unexpectedly diverse family of transcripts in response to LPS, beta-1,3-glucan, and dsRNA. BMC Molecular Biology 2007, 8:16.
137. Dheilly N.M., Nair S.V., Smith L.C., Raftos D.A. Highly variable immune-response proteins (185/333) from the sea urchin Strongylocentrotus purpuratus: proteomic analysis identifies diversity within and between individuals. Journal of Immunology 2009, 182:2203-2212.
138. Terwilliger D.P., Buckley K.M., Mehta D., Moorjani P.G., Smith L.C. Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpuratus. Physiological Genomics 2006, 26(2):134-144.
139. Buckley K.M., Munshaw S., Kepler T.B., Smith L.C. The 185/333 gene family is a rapidly diversifying host-defense gene cluster in the purple sea urchin, Strongylocentrotus purpuratus. Journal of Molecular Biology 2008, 379:912-928.
140. Buckley K.M., Smith L.C. Extraordinary diversity among members of the large gene family, 185/333, from the purple sea urchin, Strongylocentrotus purpuratus. BMC Molecular Biology 2007, 8:68.
141. Gilad Y., Man O., Paabo S., Lancet D. Human specific loss of olfactory receptor genes. Proceedings of National Academy of Science United States of America 2003, 100(6):3324-3327.
142. Rast J.P., Messier-Solek C. Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biological Bulletin 2008, 214:274-283.
143. Brockton V., Henson J.H., Raftos D.A., Majeske A.J., Kim Y.O., Smith L.C. Localization and diversity of 185/333 proteins from the purple sea urchin - unexpected protein-size range and protein expression in a new coelomocyte type. Journal of Cell Science 2008, 121(3):339-348.
144. Buckley K.M., Terwilliger D.P., Smith L.C. Sequence variations between the 185/333 genes and messages from the purple sea urchin suggest post-transcriptional modifications. Journal of Immunology 2008, 181(12):2203-2212.
145. Hibino T., Loza-Coll M., Messier C., Majeske A.J., Cohen A., Terwilliger D.P., et al. The immune gene repertoire encoded in the purple sea urchin genome. Developmental Biology 2006, 300:349-365.
146. Chester A., Scott J., Anant S., Navaratnam N. RNA editing: cytidine to uridine conversion in apolipoprotein B mRNA. Biochimica et Biophysica Acta 2000, 1494(1-2):1-13.
147. Miller C.A., Buckley K.M., Easley R.L., Smith L.C. An Sp185/333 gene cluster from the purple sea urchin and putative microsatellite-mediated gene diversification. BMC Genomics 2010, 11:575.
148. Smith L.C. Diversification of innate immune genes: lessons from the purple sea urchin. Disease Models and Mechanisms 2010, 3:274-279.
149. Massana R., Murray A.E., Preston C.M., DeLong E.F. Vertical distribution and phylogenetic characterization of marine palnktonic Archaea in the Santa Barbara Chanel. Applied and Environmental Microbiology 1997, 63(1):50-56.
150. Whitman W.B., Coleman D.C., Wiebe W.J. Prokaryotes: the unseen majority. Proceedings of National Academy of Science United States of America 1998, 95(12):6578-6583.
151. Llobet-Brossa E., Rossello-Mora R., Amann R. Microbial community composition of Wadden sea sediments as revealed by fluorescence in situ hybridization. Applied and Environmental Microbiology 1998, 64(7):2691-2696.
152. Suttle C.A. Marine viruses - major players in the global ecosystem. Nature reviews Microbiology 2007, 5:801-812.
153. Munn C.B. Viruses as pathogens of marine organisms - from bacteria to whales. Journal of the Marine Biological Association of the UK 2006, 86:453-467.
154. Woolhouse M.E.J., Webster J.P., Domingo E., Charlesworth B., Levin B.R. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics 2002, 32:569-577.
155. Van Valen L. A new evolutionary law. Evolutionary Theory 1973, 1:1-30.
156. Carroll L. Through the looking-glass and what Alice found there 1871, Macmillan and Co, London.
157. Carroll S.B., Grenier J.K., Weatherbee S.D. From DNA to diversity 2005, Blackwell Publishing, Malden MA, 258. Second ed.
158. Green B.M., Finn K.J., Li J.J. Loss of DNA replication control is a potent inducer of gene amplification. Science 2010, 329(5994):943-946.
159. Khalturin K., Anton-Erxleben F., Sassmann S., Wittlieb J., Hemmrich G., Bosch T.C. A novel gene family controls species-specific morphological traits in Hydra. PLoS Biology 2008, 6(11):e278.
160. Hemmrich G., Miller D.J., Bosch T.C.G. The evolution of immunity: a low-life perspective. Trends in Immunology 2007, 28(10):449-454.
161. Litman G.W., Cannon J.P., Dishaw L.J. Reconstructing immune phylogeny: new perspectives. Nature Reviews Immunology 2005, 5(11):866-879.
162. Zhang Q., Zmasek C.M., Godzik A. Domain architecture evolution of pattern-recognition receptors. Immunogenetics 2010, 62:263-272.
163. Kapitonov V.V., Jurka J. Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biology 2004, 23(5):311-324.
164. Kurata S. Recognition and elimination of diversified pathogens in insect defense systems. Molecular Diversity 2006, 10(4):599-605.
165. Miller, CA. Assembly and analysis of a Sp185/333 gene cluster from the sea urchin. Evidence for microsatellite-mediated gene and segmental duplication of this highly variable immune response gene family. MS thesis: Program in Genomics and Bioinformatics, George Washington University 2009.
166. Michel T., Reichhart J.M., Hoffmann J.A., Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 2001, 414(6865):756-759.
167. Royet J., Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nature Reviews Microbiology 2007, 5(4):264-277.
168. Mellroth P., Karlsson J., Hakansson J., Schultz N., Goldman W.E., Steiner H. Ligand-induced dimerization of Drosophila peptidoglycan recognition proteins in vitro. Proceedings of National Academy of Science United States of America 2005, 102(18):6455-6460.
169. Ramet M., Manfruelli P., Pearson A., Mathey-Prevot B., Ezekowitz R.A. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 2002, 416(6881):644-648.
170. Lim J.H., Kim M.S., Kim H.E., Yano T., Oshima Y., Aggarwal K., et al. Structural basis for preferential recognition of diaminopimelic acid-type peptidoglycan by a subset of peptidoglycan recognition proteins. Journal of Biological Chemistry 2006, 281(12):8286-8295.
171. Takehana A., Katsuyama T., Yano T., Oshima Y., Takada H., Aigaki T., et al. Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proceedings of National Academy of Science United States of America 2002, 99(21):13705-13710.
172. Maillet F., Bischoff V., Vignal C., Hoffmann J., Royet J. The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host and Microbe 2008, 3(5):293-303.