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Table of Contents
Vol. 3, No. 1, 2011
Issue release date: December 2010
Section title: Review
Free Access
J Innate Immun 2011;3:17–27
(DOI:10.1159/000321882)

The Primary Role of Fibrinogen-Related Proteins in Invertebrates Is Defense, Not Coagulation

Hanington P.C. · Zhang S.-M.
Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, N. Mex., USA
email Corresponding Author

Abstract

In vertebrates, the conversion of fibrinogen into fibrin is an essential process that underlies the establishment of the supporting protein framework required for coagulation. In invertebrates, fibrinogen-domain-containing proteins play a role in the defense response generated against pathogens; however, they do not function in coagulation, suggesting that this role has been recently acquired. Molecules containing fibrinogen motifs have been identified in numerous invertebrate organisms, and most of these molecules known to date have been linked to defense. Moreover, recent genome projects of invertebrate animals have revealed surprisingly high numbers of fibrinogen-like loci in their genomes, suggesting important and perhaps diverse functions of fibrinogen-like proteins in invertebrates. The ancestral role of molecules containing fibrinogen-related domains (FReDs) with immunity is the focus of this review, with emphasis on specific FReDs called fibrinogen-related proteins (FREPs) identified from the schistosome-transmitting mollusc Biomphalaria glabrata. Herein, we outline the range of invertebrate organisms FREPs can be found in, and detail the roles these molecules play in defense and protection against infection.

© 2010 S. Karger AG, Basel


  

Key Words

  • Biomphalaria
  • Coagulation
  • Defense
  • Fibrinogen
  • Fibrinogen-related protein
  • Fibrinogen-related domain
  • Invertebrate

References

  1. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D: The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008;451:783–788.
  2. Matsushita M, Fujita T: The role of ficolins in innate immunity. Immunobiology 2002; 205:490–497.
  3. Oren M, Escande ML, Paz G, Fishelson Z, Rinkevich B: Urochordate histoincompatible interactions activate vertebrate-like coagulation system components. PLoS ONE 2008;3:e3123.
  4. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS: The amphioxus genome and the evolution of the chordate karyotype. Nature 2008;453:1064–1071.
  5. Millar DA, Rateliffe NA: Invertebrate; in Turner RJ (ed): Immunology, a Comparative Approach. New York, Wiley, 1994, pp 29–60.
  6. Huang S, Yuan S, Guo L, Yu Y, Li J, Wu T, Liu T, Yang M, Wu K, Liu H, Ge J, Huang H, Dong M, Yu C, Chen S, Xu A: Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 2008;18:1112–1126.
  7. Doolittle RF: Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harb Symp Quant Biol 2009;74:35–40.
  8. Doolittle RF, Jiang Y, Nand J: Genomic evidence for a simpler clotting scheme in jawless vertebrates. J Mol Evol 2008;66:185–196.
  9. Osaki T, Kawabata S: Structure and function of coagulogen, a clottable protein in horseshoe crabs. Cell Mol Life Sci 2004;61:1257–1265.
  10. Cerenius L, Kawabata SI, Lee BL, Nonaka M, Soderhall K: Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 2010;35:575–583.
  11. Dushay MS: Insect hemolymph clotting. Cell Mol Life Sci 2009;66:2643–2650.
  12. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS: The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002;298:2157–2167.
  13. Okada K, Asai K: Expansion of signaling genes for adaptive immune system evolution in early vertebrates. BMC Genomics 2008;9:218.
  14. Kasahara M: The 2R hypothesis: an update. Curr Opin Immunol 2007;19:547–552.
  15. Telford MJ: Resolving animal phylogeny: a sledgehammer for a tough nut? Dev Cell 2008;14:457–459.
  16. Perovic-Ottstadt S, Adell T, Proksch P, Wiens M, Korzhev M, Gamulin V, Muller IM, Muller WE: A (1→3)-beta-D-glucan recognition protein from the sponge Suberites domuncula: mediated activation of fibrinogen-like protein and epidermal growth factor gene expression. Eur J Biochem 2004;271:1924–1937.
  17. Xu X, Doolittle RF: Presence of a vertebrate fibrinogen-like sequence in an echinoderm. Proc Natl Acad Sci USA 1990;87:2097–2101.
  18. Adema CM, Hertel LA, Loker ES: Evidence from two planorbid snails of a complex and dedicated response to digenean (echinostome) infection. Parasitology 1999;119:395–404.
  19. Adema CM, Hertel LA, Miller RD, Loker ES: A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 1997;94:8691–8696.
  20. Ramirez-Gomez F, Ortiz-Pineda PA, Rivera-Cardona G, Garcia-Arraras JE: LPS-induced genes in intestinal tissue of the sea cucumber Holothuria glaberrima. PLoS ONE 2009;4:e6178.
  21. Gorbushin AM, Iakovleva NV: A new gene family of single fibrinogen domain lectin in Mytilus. Fish Shellfish Immunol 2010 DOI: 10.1016/j.fsi.2010.10.002.

    External Resources

  22. Wang X, Rocheleau TA, Fuchs JF, Hillyer JF, Chen CC, Christensen BM: A novel lectin with a fibrinogen-like domain and its potential involvement in the innate immune response of Armigeres subalbatus against bacteria. Insect Mol Biol 2004;13:273–282.
  23. Kurachi S, Song Z, Takagaki M, Yang Q, Winter HC, Kurachi K, Goldstein IJ: Sialic-acid-binding lectin from the slug Limax flavus: cloning, expression of the polypeptide, and tissue localization. Eur J Biochem 1998; 254:217–222.
  24. Rego RO, Kovar V, Kopacek P, Weise C, Man P, Sauman I, Grubhoffer L: The tick plasma lectin, Dorin M, is a fibrinogen-related molecule. Insect Biochem Mol Biol 2006;36:291–299.
  25. Rego RO, Hajdusek O, Kovar V, Kopacek P, Grubhoffer L, Hypsa V: Molecular cloning and comparative analysis of fibrinogen-related proteins from the soft tick Ornithodoros moubata and the hard tick Ixodes ricinus. Insect Biochem Mol Biol 2005;35:991–1004.
  26. Gokudan S, Muta T, Tsuda R, Koori K, Kawahara T, Seki N, Mizunoe Y, Wai SN, Iwanaga S, Kawabata S: Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci USA 1999;96:10086–10091.
  27. Kawasaki H, Nose T, Muta T, Iwanaga S, Shimohigashi Y, Kawabata S: Head-to-tail polymerization of coagulin, a clottable protein of the horseshoe crab. J Biol Chem 2000;275:35297–35301.
  28. Kairies N, Beisel HG, Fuentes-Prior P, Tsuda R, Muta T, Iwanaga S, Bode W, Huber R, Kawabata S: The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc Natl Acad Sci USA 2001;98:13519–13524.
  29. Zhang H, Wang LL, Song LS, Song XY, Wang B, Mu CK, Zhang Y: A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor. Fish Shellfish Immunol 2009;26:56–64.
  30. Middha S, Wang X: Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics 2008;9:260.
  31. Dong Y, Dimopoulos G: Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 2009;284:9835–9844.
  32. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G: Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 2010;34:387–395.
  33. Fan C, Zhang S, Li L, Chao Y: Fibrinogen-related protein from amphioxus Branchiostoma belcheri is a multivalent pattern recognition receptor with a bacteriolytic activity. Mol Immunol 2008;45:3338–3346.
  34. Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T: Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 2001;276:19959–19965.
  35. Li D, Graham LD: Epiphragmin, the major protein of epiphragm mucus from the vineyard snail, Cernuella virgata. Comp Biochem Physiol B Biochem Mol Biol 2007;148:192–200.
  36. Soderhall I, Wu C, Novotny M, Lee BL, Soderhall K: A novel protein acts as a negative regulator of prophenoloxidase activation and melanization in the freshwater crayfish Pacifastacus leniusculus. J Biol Chem 2009;284:6301–6310.
  37. Lee EC, Yu SY, Hu X, Mlodzik M, Baker NE: Functional analysis of the fibrinogen-related scabrous gene from Drosophila melanogaster identifies potential effector and stimulatory protein domains. Genetics 1998;150:663–673.
  38. Mlodzik M, Baker NE, Rubin GM: Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev 1990;4:1848–1861.
  39. Yamada S, Hotta K, Yamamoto TS, Ueno N, Satoh N, Takahashi H: Interaction of notochord-derived fibrinogen-like protein with Notch regulates the patterning of the central nervous system of Ciona intestinalis embryos. Dev Biol 2009;328:1–12.
  40. Powell PA, Wesley C, Spencer S, Cagan RL: Scabrous complexes with Notch to mediate boundary formation. Nature 2001;409:626–630.
  41. Lee EC, Hu X, Yu SY, Baker NE: The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol Cell Biol 1996;16:1179–1188.
  42. Chou YH, Chien CT: Scabrous controls ommatidial rotation in the Drosophila compound eye. Dev Cell 2002;3:839–850.
  43. Yamada L, Saito T, Taniguchi H, Sawada H, Harada Y: Comprehensive egg coat proteome of the ascidian Ciona intestinalis reveals gamete recognition molecules involved in self-sterility. J Biol Chem 2009;284:9402–9410.
  44. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E, Sawada H: Mechanism of self-sterility in a hermaphroditic chordate. Science 2008;320:548–550.
  45. Gorbushin AM, Panchin YV, Iakovleva NV: In search of the origin of FREPs: characterization of Aplysia californica fibrinogen-related proteins. Dev Comp Immunol 2010;34:465–473.
  46. King CH: Toward the elimination of schistosomiasis. N Engl J Med 2009;360:106–109.
  47. Loker ES, Adema CM: Schistosomes, Echinostomes and snails: comparative immunobiology. Parasitology Today 1995;11:120–124.
  48. Adema CM, Hanington PC, Lun CM, Rosenberg GH, Aragon AD, Stout BA, Lennard Richard ML, Gross PS, Loker ES: Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 2010;47:849–860.
  49. Hanington PC, Lun CM, Adema CM, Loker ES: Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. Int J Parasitol 2010;40:819–831.
  50. Monroy FP, Loker ES: Production of heterogeneous carbohydrate-binding proteins by the host snail Biomphalaria glabrata following exposure to Echinostoma paraensei and Schistosoma mansoni. J Parasitol 1993;79:416–423.
  51. Hertel LA, Stricker SA, Monroy FP, Wilson WD, Loker ES: Biomphalaria glabrata hemolymph lectins: binding to bacteria, mammalian erythrocytes, and to sporocysts and rediae of Echinostoma paraensei. J Invertebr Pathol 1994;64:52–61.
  52. Leonard PM, Adema CM, Zhang SM, Loker ES: 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;269:155–165.
  53. Zhang SM, Leonard PM, Adema CM, Loker ES: Parasite-responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 2001;53:684–694.
  54. Zhang SM, Loker ES: The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Fibrinogen-related proteins. Dev Comp Immunol 2003;27:175–187.
  55. Zhang SM, Nian H, Zeng Y, Dejong RJ: Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev Comp Immunol 2008;32:1119–1130.
  56. Zhang SM, Loker ES: 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;341:255–266.
  57. Zhang SM, Adema CM, Kepler TB, Loker ES: Diversification of Ig superfamily genes in an invertebrate. Science 2004;305:251–254.
  58. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010;329:1353–1355.
  59. Stout BA, Adema CM, Zhang S-M, Loker ES: Biology of FREPs: diversified lectins with fibrinogen-related domains from the freshwater snail Biomphalaria glabrata; in Vasta GR, Ahmed H (eds): Animal Lectins: A Functional View. Boca Raton, CRC Press, 2009, pp 475–491.
  60. Cooper MD, Alder MN: The evolution of adaptive immune systems. Cell 2006;124:815–822.
  61. Litman GW, Cannon JP, Rast JP: New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 2005;87:209–236.
  62. Litman GW, Dishaw LJ, Cannon JP, Haire RN, Rast JP: Alternative mechanisms of immune receptor diversity. Curr Opin Immunol 2007;19:526–534.
  63. Herrin BR, Cooper MD: Alternative adaptive immunity in jawless vertebrates. J Immunol 2010;185:1367–1374.
  64. Jones JD, Dangl JL: The plant immune system. Nature 2006;444:323–329.
  65. Kurtz J, Armitage SA: Alternative adaptive immunity in invertebrates. Trends Immunol 2006;27:493–496.
  66. Loker ES, Adema CM, Zhang SM, Kepler TB: Invertebrate immune systems: not homogeneous, not simple, not well understood. Immunol Rev 2004;198:10–24.
  67. Sun SC, Lindstrom I, Boman HG, Faye I, Schmidt O: Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 1990;250:1729–1732.
  68. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D: Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005;309:1874–1878.
  69. Dong Y, Taylor HE, Dimopoulos G: AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 2006;4:e229.
  70. Zhang SM, Zeng Y, Loker ES: Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun 2008;14:175–189.
  71. Hertel LA, Adema CM, Loker ES: Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 2005;29:295–303.
  72. Roger E, Gourbal B, Grunau C, Pierce RJ, Galinier R, Mitta G: Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Mol Biochem Parasitol 2008;157:217–227.
  73. Roger E, Grunau C, Pierce RJ, Hirai H, Gourbal B, Galinier R, Emans R, Cesari IM, Cosseau C, Mitta G: Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Negl Trop Dis 2008;2:e330.
  74. Mone Y, Gourbal B, Duval D, Du Pasquier L, Keiffer-Jaquinod S, Mitta G: A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 2010;4:e813.
  75. Richards CS: Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 1975;70:231–241.
  76. Theron A, Coustau C: Are Biomphalaria snails resistant to Schistosoma mansoni? J Helminthol 2005;79:187–191.
  77. Agrawal AF, Lively CM: Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics. Proc Royal Soc Lond B Biol Sci 2003;270:323–334.
  78. Agrawal A, Lively CM: Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 2002;4:79–90.
  79. Hanington PC, Forys MA, Dragoo JW, Zhang SM, Adema CM, Loker ES: A role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc Natl Acad Sci USA 2010, in press.

  

Author Contacts

Dr. Si-Ming Zhang
Center for Evolutionary and Theoretical Immunology
Department of Biology, MSC03 2020, University of New Mexico
Albuquerque, NM 87131 (USA)
Tel. +1 505 277 4589, Fax +1 505 277 0304, E-Mail zhangsm@unm.edu

  

Article Information

Received: August 31, 2010
Accepted after revision: October 8, 2010
Published online: November 9, 2010
Number of Print Pages : 11
Number of Figures : 1, Number of Tables : 1, Number of References : 79

  

Publication Details

Journal of Innate Immunity

Vol. 3, No. 1, Year 2011 (Cover Date: December 2010)

Journal Editor: Herwald H. (Lund), Egesten A. (Lund)
ISSN: 1662-811X (Print), eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

In vertebrates, the conversion of fibrinogen into fibrin is an essential process that underlies the establishment of the supporting protein framework required for coagulation. In invertebrates, fibrinogen-domain-containing proteins play a role in the defense response generated against pathogens; however, they do not function in coagulation, suggesting that this role has been recently acquired. Molecules containing fibrinogen motifs have been identified in numerous invertebrate organisms, and most of these molecules known to date have been linked to defense. Moreover, recent genome projects of invertebrate animals have revealed surprisingly high numbers of fibrinogen-like loci in their genomes, suggesting important and perhaps diverse functions of fibrinogen-like proteins in invertebrates. The ancestral role of molecules containing fibrinogen-related domains (FReDs) with immunity is the focus of this review, with emphasis on specific FReDs called fibrinogen-related proteins (FREPs) identified from the schistosome-transmitting mollusc Biomphalaria glabrata. Herein, we outline the range of invertebrate organisms FREPs can be found in, and detail the roles these molecules play in defense and protection against infection.

© 2010 S. Karger AG, Basel


  

Author Contacts

Dr. Si-Ming Zhang
Center for Evolutionary and Theoretical Immunology
Department of Biology, MSC03 2020, University of New Mexico
Albuquerque, NM 87131 (USA)
Tel. +1 505 277 4589, Fax +1 505 277 0304, E-Mail zhangsm@unm.edu

  

Article Information

Received: August 31, 2010
Accepted after revision: October 8, 2010
Published online: November 9, 2010
Number of Print Pages : 11
Number of Figures : 1, Number of Tables : 1, Number of References : 79

  

Publication Details

Journal of Innate Immunity

Vol. 3, No. 1, Year 2011 (Cover Date: December 2010)

Journal Editor: Herwald H. (Lund), Egesten A. (Lund)
ISSN: 1662-811X (Print), eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


Article / Publication Details

First-Page Preview
Abstract of Review

Received: 8/31/2010
Accepted: 10/8/2010
Published online: 11/9/2010
Issue release date: December 2010

Number of Print Pages: 11
Number of Figures: 1
Number of Tables: 1

ISSN: 1662-811X (Print)
eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D: The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008;451:783–788.
  2. Matsushita M, Fujita T: The role of ficolins in innate immunity. Immunobiology 2002; 205:490–497.
  3. Oren M, Escande ML, Paz G, Fishelson Z, Rinkevich B: Urochordate histoincompatible interactions activate vertebrate-like coagulation system components. PLoS ONE 2008;3:e3123.
  4. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS: The amphioxus genome and the evolution of the chordate karyotype. Nature 2008;453:1064–1071.
  5. Millar DA, Rateliffe NA: Invertebrate; in Turner RJ (ed): Immunology, a Comparative Approach. New York, Wiley, 1994, pp 29–60.
  6. Huang S, Yuan S, Guo L, Yu Y, Li J, Wu T, Liu T, Yang M, Wu K, Liu H, Ge J, Huang H, Dong M, Yu C, Chen S, Xu A: Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 2008;18:1112–1126.
  7. Doolittle RF: Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harb Symp Quant Biol 2009;74:35–40.
  8. Doolittle RF, Jiang Y, Nand J: Genomic evidence for a simpler clotting scheme in jawless vertebrates. J Mol Evol 2008;66:185–196.
  9. Osaki T, Kawabata S: Structure and function of coagulogen, a clottable protein in horseshoe crabs. Cell Mol Life Sci 2004;61:1257–1265.
  10. Cerenius L, Kawabata SI, Lee BL, Nonaka M, Soderhall K: Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 2010;35:575–583.
  11. Dushay MS: Insect hemolymph clotting. Cell Mol Life Sci 2009;66:2643–2650.
  12. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS: The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002;298:2157–2167.
  13. Okada K, Asai K: Expansion of signaling genes for adaptive immune system evolution in early vertebrates. BMC Genomics 2008;9:218.
  14. Kasahara M: The 2R hypothesis: an update. Curr Opin Immunol 2007;19:547–552.
  15. Telford MJ: Resolving animal phylogeny: a sledgehammer for a tough nut? Dev Cell 2008;14:457–459.
  16. Perovic-Ottstadt S, Adell T, Proksch P, Wiens M, Korzhev M, Gamulin V, Muller IM, Muller WE: A (1→3)-beta-D-glucan recognition protein from the sponge Suberites domuncula: mediated activation of fibrinogen-like protein and epidermal growth factor gene expression. Eur J Biochem 2004;271:1924–1937.
  17. Xu X, Doolittle RF: Presence of a vertebrate fibrinogen-like sequence in an echinoderm. Proc Natl Acad Sci USA 1990;87:2097–2101.
  18. Adema CM, Hertel LA, Loker ES: Evidence from two planorbid snails of a complex and dedicated response to digenean (echinostome) infection. Parasitology 1999;119:395–404.
  19. Adema CM, Hertel LA, Miller RD, Loker ES: A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 1997;94:8691–8696.
  20. Ramirez-Gomez F, Ortiz-Pineda PA, Rivera-Cardona G, Garcia-Arraras JE: LPS-induced genes in intestinal tissue of the sea cucumber Holothuria glaberrima. PLoS ONE 2009;4:e6178.
  21. Gorbushin AM, Iakovleva NV: A new gene family of single fibrinogen domain lectin in Mytilus. Fish Shellfish Immunol 2010 DOI: 10.1016/j.fsi.2010.10.002.

    External Resources

  22. Wang X, Rocheleau TA, Fuchs JF, Hillyer JF, Chen CC, Christensen BM: A novel lectin with a fibrinogen-like domain and its potential involvement in the innate immune response of Armigeres subalbatus against bacteria. Insect Mol Biol 2004;13:273–282.
  23. Kurachi S, Song Z, Takagaki M, Yang Q, Winter HC, Kurachi K, Goldstein IJ: Sialic-acid-binding lectin from the slug Limax flavus: cloning, expression of the polypeptide, and tissue localization. Eur J Biochem 1998; 254:217–222.
  24. Rego RO, Kovar V, Kopacek P, Weise C, Man P, Sauman I, Grubhoffer L: The tick plasma lectin, Dorin M, is a fibrinogen-related molecule. Insect Biochem Mol Biol 2006;36:291–299.
  25. Rego RO, Hajdusek O, Kovar V, Kopacek P, Grubhoffer L, Hypsa V: Molecular cloning and comparative analysis of fibrinogen-related proteins from the soft tick Ornithodoros moubata and the hard tick Ixodes ricinus. Insect Biochem Mol Biol 2005;35:991–1004.
  26. Gokudan S, Muta T, Tsuda R, Koori K, Kawahara T, Seki N, Mizunoe Y, Wai SN, Iwanaga S, Kawabata S: Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci USA 1999;96:10086–10091.
  27. Kawasaki H, Nose T, Muta T, Iwanaga S, Shimohigashi Y, Kawabata S: Head-to-tail polymerization of coagulin, a clottable protein of the horseshoe crab. J Biol Chem 2000;275:35297–35301.
  28. Kairies N, Beisel HG, Fuentes-Prior P, Tsuda R, Muta T, Iwanaga S, Bode W, Huber R, Kawabata S: The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc Natl Acad Sci USA 2001;98:13519–13524.
  29. Zhang H, Wang LL, Song LS, Song XY, Wang B, Mu CK, Zhang Y: A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor. Fish Shellfish Immunol 2009;26:56–64.
  30. Middha S, Wang X: Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics 2008;9:260.
  31. Dong Y, Dimopoulos G: Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 2009;284:9835–9844.
  32. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G: Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 2010;34:387–395.
  33. Fan C, Zhang S, Li L, Chao Y: Fibrinogen-related protein from amphioxus Branchiostoma belcheri is a multivalent pattern recognition receptor with a bacteriolytic activity. Mol Immunol 2008;45:3338–3346.
  34. Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T: Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 2001;276:19959–19965.
  35. Li D, Graham LD: Epiphragmin, the major protein of epiphragm mucus from the vineyard snail, Cernuella virgata. Comp Biochem Physiol B Biochem Mol Biol 2007;148:192–200.
  36. Soderhall I, Wu C, Novotny M, Lee BL, Soderhall K: A novel protein acts as a negative regulator of prophenoloxidase activation and melanization in the freshwater crayfish Pacifastacus leniusculus. J Biol Chem 2009;284:6301–6310.
  37. Lee EC, Yu SY, Hu X, Mlodzik M, Baker NE: Functional analysis of the fibrinogen-related scabrous gene from Drosophila melanogaster identifies potential effector and stimulatory protein domains. Genetics 1998;150:663–673.
  38. Mlodzik M, Baker NE, Rubin GM: Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev 1990;4:1848–1861.
  39. Yamada S, Hotta K, Yamamoto TS, Ueno N, Satoh N, Takahashi H: Interaction of notochord-derived fibrinogen-like protein with Notch regulates the patterning of the central nervous system of Ciona intestinalis embryos. Dev Biol 2009;328:1–12.
  40. Powell PA, Wesley C, Spencer S, Cagan RL: Scabrous complexes with Notch to mediate boundary formation. Nature 2001;409:626–630.
  41. Lee EC, Hu X, Yu SY, Baker NE: The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol Cell Biol 1996;16:1179–1188.
  42. Chou YH, Chien CT: Scabrous controls ommatidial rotation in the Drosophila compound eye. Dev Cell 2002;3:839–850.
  43. Yamada L, Saito T, Taniguchi H, Sawada H, Harada Y: Comprehensive egg coat proteome of the ascidian Ciona intestinalis reveals gamete recognition molecules involved in self-sterility. J Biol Chem 2009;284:9402–9410.
  44. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E, Sawada H: Mechanism of self-sterility in a hermaphroditic chordate. Science 2008;320:548–550.
  45. Gorbushin AM, Panchin YV, Iakovleva NV: In search of the origin of FREPs: characterization of Aplysia californica fibrinogen-related proteins. Dev Comp Immunol 2010;34:465–473.
  46. King CH: Toward the elimination of schistosomiasis. N Engl J Med 2009;360:106–109.
  47. Loker ES, Adema CM: Schistosomes, Echinostomes and snails: comparative immunobiology. Parasitology Today 1995;11:120–124.
  48. Adema CM, Hanington PC, Lun CM, Rosenberg GH, Aragon AD, Stout BA, Lennard Richard ML, Gross PS, Loker ES: Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 2010;47:849–860.
  49. Hanington PC, Lun CM, Adema CM, Loker ES: Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. Int J Parasitol 2010;40:819–831.
  50. Monroy FP, Loker ES: Production of heterogeneous carbohydrate-binding proteins by the host snail Biomphalaria glabrata following exposure to Echinostoma paraensei and Schistosoma mansoni. J Parasitol 1993;79:416–423.
  51. Hertel LA, Stricker SA, Monroy FP, Wilson WD, Loker ES: Biomphalaria glabrata hemolymph lectins: binding to bacteria, mammalian erythrocytes, and to sporocysts and rediae of Echinostoma paraensei. J Invertebr Pathol 1994;64:52–61.
  52. Leonard PM, Adema CM, Zhang SM, Loker ES: 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;269:155–165.
  53. Zhang SM, Leonard PM, Adema CM, Loker ES: Parasite-responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 2001;53:684–694.
  54. Zhang SM, Loker ES: The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Fibrinogen-related proteins. Dev Comp Immunol 2003;27:175–187.
  55. Zhang SM, Nian H, Zeng Y, Dejong RJ: Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev Comp Immunol 2008;32:1119–1130.
  56. Zhang SM, Loker ES: 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;341:255–266.
  57. Zhang SM, Adema CM, Kepler TB, Loker ES: Diversification of Ig superfamily genes in an invertebrate. Science 2004;305:251–254.
  58. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010;329:1353–1355.
  59. Stout BA, Adema CM, Zhang S-M, Loker ES: Biology of FREPs: diversified lectins with fibrinogen-related domains from the freshwater snail Biomphalaria glabrata; in Vasta GR, Ahmed H (eds): Animal Lectins: A Functional View. Boca Raton, CRC Press, 2009, pp 475–491.
  60. Cooper MD, Alder MN: The evolution of adaptive immune systems. Cell 2006;124:815–822.
  61. Litman GW, Cannon JP, Rast JP: New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 2005;87:209–236.
  62. Litman GW, Dishaw LJ, Cannon JP, Haire RN, Rast JP: Alternative mechanisms of immune receptor diversity. Curr Opin Immunol 2007;19:526–534.
  63. Herrin BR, Cooper MD: Alternative adaptive immunity in jawless vertebrates. J Immunol 2010;185:1367–1374.
  64. Jones JD, Dangl JL: The plant immune system. Nature 2006;444:323–329.
  65. Kurtz J, Armitage SA: Alternative adaptive immunity in invertebrates. Trends Immunol 2006;27:493–496.
  66. Loker ES, Adema CM, Zhang SM, Kepler TB: Invertebrate immune systems: not homogeneous, not simple, not well understood. Immunol Rev 2004;198:10–24.
  67. Sun SC, Lindstrom I, Boman HG, Faye I, Schmidt O: Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 1990;250:1729–1732.
  68. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D: Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005;309:1874–1878.
  69. Dong Y, Taylor HE, Dimopoulos G: AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 2006;4:e229.
  70. Zhang SM, Zeng Y, Loker ES: Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun 2008;14:175–189.
  71. Hertel LA, Adema CM, Loker ES: Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 2005;29:295–303.
  72. Roger E, Gourbal B, Grunau C, Pierce RJ, Galinier R, Mitta G: Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Mol Biochem Parasitol 2008;157:217–227.
  73. Roger E, Grunau C, Pierce RJ, Hirai H, Gourbal B, Galinier R, Emans R, Cesari IM, Cosseau C, Mitta G: Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Negl Trop Dis 2008;2:e330.
  74. Mone Y, Gourbal B, Duval D, Du Pasquier L, Keiffer-Jaquinod S, Mitta G: A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 2010;4:e813.
  75. Richards CS: Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 1975;70:231–241.
  76. Theron A, Coustau C: Are Biomphalaria snails resistant to Schistosoma mansoni? J Helminthol 2005;79:187–191.
  77. Agrawal AF, Lively CM: Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics. Proc Royal Soc Lond B Biol Sci 2003;270:323–334.
  78. Agrawal A, Lively CM: Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 2002;4:79–90.
  79. Hanington PC, Forys MA, Dragoo JW, Zhang SM, Adema CM, Loker ES: A role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc Natl Acad Sci USA 2010, in press.