Advertisement

Arthropoda: Pattern Recognition Proteins in Crustacean Immunity

  • Lage Cerenius
  • Kenneth Söderhäll
Chapter

Abstract

Crustaceans in general are able to mount a robust defense to microorganisms and parasites. They are equipped with pattern recognition proteins (PRPs) capable of binding microbial molecular patterns such as β-1,3-glucans and different bacterial cell wall components. A variety of different reactions are triggered such as prophenoloxidase activation, opsonin formation, phagocytosis, and encapsulation. The crustacean PRPs constitute a large group of proteins consisting of evolutionary highly conserved proteins with a wide presence in several phyla that act side by side with other PRPs that are possibly unique to crustaceans or even groups of crustaceans.

Keywords

β-1,3-Glucan Lipopolysaccharide Peptidoglycan Pattern recognition β-1,3-Glucan-binding protein Lectin Masquerade Glucanase Prophenoloxidase Serine protease homolog Ficolin Crayfish Shrimp 

References

  1. Alenton RR, Koiwai K, Miyaguchi K et al (2017) Pathogen recognition of a novel C-type lectin from Marsupenaeus japonicus reveals the divergent sugar-binding specificity of QAP motif. Sci Rep. https://doi.org/10.1038/srep45818
  2. Amparyup P, Sutthangkul J, Charoensapsri W et al (2012) Pattern recognition protein binds to lipopolysaccharide and β-1,3-glucan and activates shrimp prophenoloxidase system. J Biol Chem 287:10060–10069CrossRefPubMedPubMedCentralGoogle Scholar
  3. Angthong P, Watthanasurorot A, Klinbunga S et al (2010) Cloning and characterization of a melanisation inhibition protein (PmMIP) of the black tiger shrimp, Penaeus monodon. Fish Shellfish Immunol 29:464–468CrossRefGoogle Scholar
  4. Aspán A, Hall M, Söderhäll K (1990) The effect of endogeneous proteinase inhibitors on the prophenoloxidase activating enzyme, a serine proteinase from crayfish haemocytes. Insect Biochem 20:485–492CrossRefGoogle Scholar
  5. Barracco MA, Duvic B, Söderhäll K (1991) The β-1,3-glucan-binding protein from the crayfish Pacifastacus leniusculus, when reacted with a β-1,3-glucan, induces spreading and degranulation of crayfish granular cells. Cell Tissue Res 266:491–497CrossRefGoogle Scholar
  6. Bi WJ, Li DX, Xu YH et al (2015) Scavenger receptor B protects shrimp from bacteria by enhancing phagocytosis and regulating expression of antimicrobial peptides. Dev Comp Immunol 51:10–21CrossRefGoogle Scholar
  7. Brown GD, Gordon S (2001) Immune recognition: a new receptor for beta-glucans. Nature 413:36–37CrossRefPubMedPubMedCentralGoogle Scholar
  8. Canton J, Neculai D, Grinstein S et al (2013) Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 13:621–634CrossRefGoogle Scholar
  9. Cerenius L, Liang Z, Duvic B et al (1994) Structure and biological activity of a 1,3-beta-D-glucan-binding protein in crustacean blood. J Biol Chem 269:29462–29467Google Scholar
  10. Cerenius L, Luel BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chai YM, Zhu Q, Yu SS et al (2012) A novel protein with a fibrinogen-like domain involved in the innate immune response of Marsupenaeus japonicus. Fish Shellfish Immunol 32:307–315CrossRefGoogle Scholar
  12. Chaosomboon A, Phupet B, Rattanaporn O et al (2017) Lipopolysaccharide- and β-1,3-glucan-binding protein from Fenneropenaeus merguiensis functions as a pattern recognition receptor with a broad specificity for diverse pathogens in the defense against microorganisms. Dev Comp Immunol 67:434–444CrossRefGoogle Scholar
  13. Cheng WT, Liu CH, Tsai CH et al (2005) Molecular cloning and characterisation of a pattern recognition molecule, lipopolysaccharide- and beta-1,3-glucan binding protein (LGBP) from the white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 18:297–310CrossRefPubMedPubMedCentralGoogle Scholar
  14. Coelho JR, Bareto C, Silvera AS et al (2016) A hemocyte-expressed fibrinogen-related protein gene (LvFrep) from the shrimp Litopenaeus vannamei: expression analysis after microbial infection and during larval development. Fish Shellfish Immunol 56:123–126CrossRefGoogle Scholar
  15. Dimopoulos G, Richman A, Müller HM et al (1997) Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci U S A 94:11508–11513CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dunne DW, Resnick D, Grenberg J et al (1994) The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci U S A 91:1863–1867CrossRefPubMedPubMedCentralGoogle Scholar
  17. Duvic B, Söderhäll K (1990) Purification and characterization of a beta-1,3-glucan binding protein from plasma of the crayfish Pacifastacus leniusculus. J Biol Chem 265:9327–9332Google Scholar
  18. Duvic B, Söderhäll K (1992) Purification and partial characterization of a beta-1,3-glucan-binding-protein membrane receptor from blood cells of the crayfish Pacifastacus leniusculus. Eur J Biochem 207:223–228CrossRefGoogle Scholar
  19. Feng J, Huang J, Jin M et al (2016) A C-type lectin (MrLec) with high expression in intestine is involved in innate immune response of Macrobrachium rosenbergii. Fish Shellfish Immunol 59:345–350CrossRefGoogle Scholar
  20. Gollas-Galvan T, Sotelo-Mundo RR, Yepiz-Plascencia G et al (2003) Purification and characterization of alpha 2-macroglobulin from the white shrimp (Penaeus vannamei). Comp Biochem Physiol C 134:431–438Google Scholar
  21. Goncalves P, Vernal J, Rosa RD et al (2012) Evidence for a novel biological role for the multifunctional β-1,3-glucan binding protein in shrimp. Mol Immunol 51:363–367CrossRefPubMedGoogle Scholar
  22. Häll L, Söderhäll K (1984) Lipopolysaccharide-induced activation of prophenoloxidase activating system in crayfish hemocyte lysate. Biochim Biophys Acta 797:99–104CrossRefGoogle Scholar
  23. Hall M, Söderhäll K (1994) Crayfish α-macroglobulin as a substrate for transglutaminases. Comp Biochem Physiol B 108:65–72CrossRefGoogle Scholar
  24. Hall M, Vanheusden MC, Söderhäll K (1995) Identification of the major lipoproteins in crayfish hemolymph as proteins involved in immune recognition and clotting. Biochem Biophys Res Commun 216:939–946CrossRefGoogle Scholar
  25. Ho PY, Cheng CH, Cheng W (2009) Identification and cloning of the alpha2-macroglobulin of giant freshwater prawn Macrobrachium rosenbergii and its expression in relation with the molt stage and bacteria injection. Fish Shellfish Immunol 26:459–466CrossRefGoogle Scholar
  26. Hou F, Liu T, Wang Q et al (2017) Identification and characterization of two Croquemort homologues in penaeid shrimp Litopenaeus vannamei. Fish Shellfish Immunol 60:1–5CrossRefGoogle Scholar
  27. Huang TS, Wang H, Lee SY et al (2000) A cell adhesion protein from the crayfish Pacifastacus leniusculus, a serine proteinase homologue similar to Drosophila masquerade. J Biol Chem 275:9996–10001CrossRefGoogle Scholar
  28. Huang X, Feng JL, Jin M et al (2016) C-type lectin (MrCTL) from the giant freshwater prawn Macrobrachium rosenbergii participates in innate immunity. Fish Shellfish Immunol 58:136–144CrossRefGoogle Scholar
  29. Jearaphunt M, Noonin C, Jiravanichpaisal P et al (2014) Caspase-1-like regulation of the proPO-system and role of ppA and caspase-1-like cleaved peptides from proPO in innate immunity. Plos Pathog. https://doi.org/10.1371/journal.ppat.1004059 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jearaphunt M, Amparyup P, Sangsuriya P et al (2015) Shrimp serine proteinase homologues PmMasSPH-1 and -2 play a role in the activation of the prophenoloxidase system. PLoS One. https://doi.org/10.1371/journal.pone.0121073 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jitvaropas R, Amparyup P, Gross PS et al (2009) Functional characterization of a masquerade-like serine proteinase homologue from the black tiger shrimp Penaeus monodon. Comp Biochem Physiol B 153:236–243CrossRefGoogle Scholar
  32. Kao D, Lai AG, Stamataki E et al (2016) The genome of the crustacean Parhyale hawaiensis, a model for animal development, regeneration, immunity and lignocellulose digestion. elife 5:1. https://doi.org/10.7554/eLife.20062 CrossRefGoogle Scholar
  33. Lai AG, Aboobaker AA (2017) Comparative genomic analysis of innate immunity reveals novel and conserved components in crustacean food crop species. BMC Genomics 18:389. https://doi.org/10.1186/s12864-017-3769-4 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lee SY, Söderhäll K (2001) Characterization of a pattern recognition protein, a masquerade-like protein, in the freshwater crayfish Pacifastacus leniusculus. J Immunol 166:7319–7326CrossRefGoogle Scholar
  35. Lee WJ, Lee JD, Kravchenko VV et al (1996) Purification and cloning of an inducible Gram-negative bacteria-binding protein from the silk-worm Bombyx mori. Proc Natl Acad Sci U S A 93:7888–7893CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lee SY, Wang RG, Söderhäll K (2000) A lipopolysaccharide- and beta-1,3-glucan-binding protein from hemocytes of the freshwater crayfish Pacifastacus leniusculus. Purification, characterization, and cDNA cloning. J Biol Chem 275:1337–1343CrossRefGoogle Scholar
  37. Levashina EA, Moita LF, Blandin S et al (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104:709–718CrossRefGoogle Scholar
  38. Li M, Li C, Ma C et al (2014) Identification of a C-type lectin with antiviral and antibacterial activity from pacific white shrimp Litopenaeus vannamei. Dev Comp Immunol 46:231–240CrossRefGoogle Scholar
  39. Li CZ, Li HY, Xiao B et al (2017) Identification and functional analysis of a TEP gene from a crustacean reveals its transcriptional regulation mediated by NF-kappa B and JNK pathways and its broad protective roles against multiple pathogens. Dev Comp Immunol 70:45–58CrossRefGoogle Scholar
  40. Liu H, Wu C, Matsuda Y et al (2011) Peptidoglycan activation of the proPO-system without a peptidoglycan receptor protein (PGRP)? Dev Comp Immunol 35:51–61CrossRefGoogle Scholar
  41. Loker ES, Adema CM, Zhang SM et al (2004) Invertebrate immune systems – not homogenous, not simple, not well understood. Immunol Rev 198:10–24CrossRefPubMedPubMedCentralGoogle Scholar
  42. Luo T, Yang H, Li F et al (2006) Purification, characterization and cDNA cloning of a novel lipopolysaccharide-binding lectin from the shrimp Penaeus monodon. Dev Comp Immunol 30:607–617CrossRefGoogle Scholar
  43. Ma HM, Wang B, Zhang JQ et al (2010) Multiple forms of alpha-2 macroglobulin in shrimp Fenneropenaeus chinesis and their transcriptional response to WSSV or Vibrio pathogen infection. Dev Comp Immunol 34:677–684CrossRefGoogle Scholar
  44. McTaggart SJ, Conlon C, Colbourne JK et al (2009) The components of the Daphnia pulex immune system as revealed by complete genome sequencing. BMC Genomics 10:175. https://doi.org/10.1186/1471-2164-10-175 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mekata T, Okugawa S, Inada M et al (2011) Class B scavenger receptor, Croquemort from kuruma shrimp Marsupenaeus japonicus: molecular cloning and characterization. Mol Cell Probes 25:94–100CrossRefGoogle Scholar
  46. Pees B, Yang W, Zarate-Poles A et al (2016) High innate immune specificity through diversified C-type lectin-like domain proteins in invertebrates. J Innate Immun 8:129–142CrossRefPubMedPubMedCentralGoogle Scholar
  47. Perazzolo LM, Bachere E, Rosa RD et al (2011) Alpha2-macroglobulin from an Atlantic shrimp: biochemical characterization, sub-cellular localization and gene expression upon fungal challenge. Fish Shellfish Immunol 31:938–943CrossRefGoogle Scholar
  48. Ponprateep S, Vatanavicharn T, Lo CF et al (2017) Alpha-2-macroglobulin is a modulator of prophenoloxidase system in pacific white shrimp Litopenaeus vannamai. Fish Shellfish Immunol 62:68–74CrossRefGoogle Scholar
  49. Rattanachai A, Hirono I, Ohira T et al (2004) Molecular cloning and expression analysis of alpha 2-macroglobulin in the kuruma shrimp, Marsupenaeus japonicus. Fish Shellfish Immunol 16:599–611CrossRefGoogle Scholar
  50. Roux MM, Pain A, Klimpel KR et al (2002) The lipopolysaccharide and β-1,3-glucan binding protein gene is upregulated in white spot virus-infected shrimp (Penaeus stylirostris). J Virol 76:7140–7149CrossRefPubMedPubMedCentralGoogle Scholar
  51. Söderhäll K (1981) Fungal cell wall beta-1,3-glucans induce clotting and phenoloxidase attachment to foreign surfaces of crayfish hemocyte lysate. Dev Comp Immunol 5:565–573CrossRefGoogle Scholar
  52. Söderhäll K, Unestam T (1979) Activation of serum prophenoloxidase in arthropod immunity. The specificity of cell wall glucan activation and activation by purified fungal glycoproteins of crayfish phenoloxidase. Can J Microbiol 25:406–414CrossRefGoogle Scholar
  53. Sritunyalucksana K, Lee SY, Söderhäll K (2002) A beta-1,3-glucan binding protein from the black tiger shrimp, Penaeus monodon. Dev Comp Immunol 26:237–245CrossRefGoogle Scholar
  54. Stroschein-Stevenson SL, Foley E, O’Farrell PH et al (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. https://doi.org/10.1371/journal.pbio.0040004 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sun JJ, Lan JF, Shi XZ et al (2014) A fibrinogen-related protein (FREP) is involved in the antibacterial immunity of Marsupenaeus japonicas. Fish Shellfish Immunol 39:296–304CrossRefGoogle Scholar
  56. Thörnqvist PO, Johansson MW, Söderhäll K (1994) Opsonic activity of cell adhesion proteins and beta-1,3-glucan binding proteins from two crustaceans. Dev Comp Immunol 18:3–12CrossRefGoogle Scholar
  57. Udompetcharaporn A, Kingkamon J, Senapin S et al (2014) Identification and characterization of a QM protein as a possible peptidoglycan recognition protein (PGRP) from the giant tiger shrimp Penaeus monodon. Dev Comp Immunol 46:146–154CrossRefGoogle Scholar
  58. Unestam T, Söderhäll K (1977) Soluble fragments from fungal cell walls elicit defence reactions in crayfish. Nature 267:45–46CrossRefGoogle Scholar
  59. Wang XW, Wang JX (2013) Pattern recognition receptors acting in innate immune system of shrimp against pathogen infections. Fish Shellfish Immunol 34:981–989CrossRefGoogle Scholar
  60. Wang S, Chen AJ, Shi LJ et al (2012) TRBP and eIF6 homologue in Marsupenaeus japonicus play crucial roles in antiviral response. PLoS One:e30057. https://doi.org/10.1371/journal.pone.0030057 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wang XW, Zhao XF, Wang JX (2014a) C-type lectin binds to beta-integrin to promote hemocytic phagocytosis in an invertebrate. J Biol Chem 289:2405–2414CrossRefPubMedGoogle Scholar
  62. Wang XW, Xu JD, Zhao XF et al (2014b) A shrimp C-type lectin inhibits proliferation of the hemolymph microbiota by maintaining the expression of antimicrobial peptides. J Biol Chem 289:11779–11790CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang M, Wang L, Huang M et al (2016) A galectin from Eriocheir sinensis functions as pattern recognition receptor enhancing microbe agglutination and haemocytes encapsulation. Fish Shellfish Immunol 55:10–20CrossRefPubMedGoogle Scholar
  64. Wu C, Söderhäll K, Söderhäll I (2011) Two novel ficolin-like proteins act as pattern recognition receptors for invading pathogens in the freshwater crayfish Pacifastacus leniusculus. Proteomics 11:2249–2264CrossRefPubMedGoogle Scholar
  65. Wu C, Noonin C, Söderhäll I et al (2012) An insect TEP in a crustacean is specific for cuticular tissues and involved in intestinal defense. Insect Biochem Mol Biol 42:71–80CrossRefPubMedGoogle Scholar
  66. Xu S, Wang L, Wang XW et al (2014) L-type lectin from the kuruma shrimp Marsupenaeus japonicus promotes hemocyte phagocytosis. Dev Comp Immunol 44:397–405CrossRefPubMedGoogle Scholar
  67. Yang MC, Shi XZ, Yang HT et al (2016) Scavenger receptor C mediates phagocytosis of white spot syndrome virus and restricts virus proliferation in shrimp. Plos Pathog:e1006127. https://doi.org/10.1371/journal.ppat.1006127 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yepiz-Plascencia G, Vargas-Albores F, Jimenez-Vega F et al (1998) Shrimp plasma HDL and β-glucan binding protein (BGBP): comparison of biochemical characteristics. Comp Biochem Biophys B 121:309–314CrossRefGoogle Scholar
  69. Yu XQ, Jiang H, Wang Y et al (2003) Nonproteolytic serine proteinase homologs involved in phenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 33:197–208CrossRefGoogle Scholar
  70. Zhang XW, Wang XW, Sun C et al (2011) C-type lectin from red swamp crayfish Procambarus clarkii participates in cellular immune response. Arch Insect Biochem Physiol 76:168–184CrossRefGoogle Scholar
  71. Zhang QX, Liu HP, Chen RY et al (2013a) Identification of a serine proteinase homolog (Sp-SPH) involved in immune defense in the mud crab Scylla paramamosain. PLoS One:e63787. https://doi.org/10.1371/journal.pone.0063787
  72. Zhang XW, Liu YY, Mu Y et al (2013b) Overexpression of a C-type lectin enhances bacterial resistance in red swamp crayfish Procambarus clarkii. Fish Shellfish Immunol 34:1112–1118CrossRefGoogle Scholar
  73. Zhang Q, Wang XQ, Jiang HS et al (2014a) Calnexin functions in antibacterial immunity of Marsupenaeus japonicas. Dev Comp Immunol 46:356–363CrossRefGoogle Scholar
  74. Zhang XW, Wang XW, Huang Y et al (2014b) Cloning and characterization of two different ficolins from the giant prawn Macrobrachium rosenbergii. Dev Comp Immunol 44:359–369CrossRefGoogle Scholar
  75. Zhang XW, Wang Y, Wang XW et al (2016) A C-type lectin with an immunoglobulin-like domain promotes phagocytosis of hemocytes in crayfish Procambarus clarkii. Sci Rep 6:2994. https://doi.org/10.1038/srep2994 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Organismal BiologyUppsala UniversityUppsalaSweden

Personalised recommendations