Skip to main content

Shrimp Immune System and Immune Responses

  • Chapter
  • First Online:
Fish immune system and vaccines
  • 973 Accesses

Abstract

Shrimp, being an invertebrate, lack a vertebrate-like adaptive immune system. However, an efficient innate immune system, consisting of physical barriers and cellular and humoral components, exists in shrimp. The innate immunity is activated by the recognition of different microbial cellular components (pathogen-associated molecular patterns, PAMPs) by the host-associated pattern recognition receptors (PRRs), which triggers different signalling pathways and subsequently leads to different cellular and humoral immune responses. Cellular defence involves various processes (phagocytosis, encapsulation, nodule formation, coagulation, apoptosis etc.) directly mediated by haemocytes. However, humoral components include activation of different cascade systems and release of molecules accumulated within the haemocytes (prophenoloxidase (proPO) activating system, antioxidant system, agglutinins, protease-inhibitors, anti-microbial peptides, phosphatase, lysozyme etc.). Apart from this, RNA interference (RNAi), microRNA and complement system have been found to play crucial roles in the protective immunity in shrimp. Moreover, existence of immunological memory and adaptive immunity in shrimp has been suggested, and molecules such as Down syndrome cell adhesion molecules (Dscam), fibrinogen-related proteins (FREPs) and hemolin have been reported to be involved in this. The existence of adaptive immunity in shrimp suggests the possibility of vaccinating shrimp against specific pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Bachère E. Shrimp immunity and disease control. Aquaculture. 2000;191(1–3):3–11.

    Article  Google Scholar 

  2. Flegel TW. Detection of major penaeid shrimp viruses in Asia, a historical perspective with emphasis on Thailand. Aquaculture. 2006;258(1–4):1–33.

    Article  Google Scholar 

  3. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature. 2007;449:819–26.

    Article  CAS  PubMed  Google Scholar 

  4. Kvell K, Cooper EL, Engelmann P, Bovari J, Nemeth P. Blurring borders: innate immunity with adaptive features. Clin Dev Immunol. 2007;2007:83671. https://doi.org/10.1155/2007/83671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Söderhäll K. Invertebrate immunity. Dev Comp Immunol. 1999;23(4–5):263–6.

    PubMed  Google Scholar 

  6. Little TJ, Hultmark D, Read AF. Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol. 2005;6:651–4.

    Article  CAS  PubMed  Google Scholar 

  7. Rowley AF, Powell A. Invertebrate immune systems specific, quasi-specific, or nonspecific? J Immunol. 2007;179(11):7209–14.

    Article  CAS  PubMed  Google Scholar 

  8. Chou PH, Chang HS, Chen IT, Lin HY, Chen YM, Yang HL, Wang KHC. The putative invertebrate adaptive immune protein Litopenaeus vannamei Dscam (LvDscam) is the first reported Dscam to lack a transmembrane domain and cytoplasmic tail. Dev Comp Immunol. 2009;33:1258–67.

    Article  CAS  PubMed  Google Scholar 

  9. Chou PH, Chang HS, Chen IT, Lee CW, Hung HY, Wang KHC. Penaeus monodon Dscam (PmDscam) has a highly diverse cytoplasmic tail and is the first membrane-bound shrimp Dscam to be reported. Fish Shellfish Immunol. 2011;30:1109–23.

    Article  PubMed  Google Scholar 

  10. Chai YM, Zhu Q, Yu SS, Zhao XF, Wang JX. A novel protein with a fibrinogen-like domain involved in the innate immune response of Marsupenaeus japonicus. Fish Shellfish Immunol. 2012;32:307–15.

    Article  CAS  PubMed  Google Scholar 

  11. Chiang YA, Hung HY, Lee CW, Huang YT, Wang HC. Shrimp Dscam and its cytoplasmic tail splicing activator serine/arginine (SR)-rich protein B52 were both induced after white spot syndrome virus challenge. Fish Shellfish Immunol. 2013;34:209–19.

    Article  CAS  PubMed  Google Scholar 

  12. Ng TH, Chiang YA, Yeh YC, Wang HC. Review of Dscam-mediated immunity in shrimp and other arthropods. Dev Comp Immunol. 2014;46:129–38.

    Article  CAS  PubMed  Google Scholar 

  13. Sun JJ, Lan JF, Shi XZ, Yang MC, Yang HT, Zhao XF, Wang JX. A fibrinogen-related protein (FREP) is involved in the antibacterial immunity of Marsupenaeus japonicus. Fish Shellfish Immunol. 2014;39:296–304.

    Article  CAS  PubMed  Google Scholar 

  14. Zuo H, Li H, Wei E, Su Z, Zheng J, Li C, Chen Y, Weng S, He J, Xu X. Identification and functional analysis of a hemolin like protein from Litopenaeus vannamei. Fish Shellfish Immunol. 2015;43(1):51–9.

    Article  CAS  PubMed  Google Scholar 

  15. Coelho JDR, Barreto C, Silveira ADS, Vieira GC, Rosa RD, Perazzolo LM. 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. 2016;56:123–6.

    Article  CAS  PubMed  Google Scholar 

  16. Jiravanichpaisal P, Lee BL, Söderhäll K. Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology. 2006;211:213–36.

    Article  CAS  PubMed  Google Scholar 

  17. Tyagi A, Khushiramani R, Karunasagar I, Karunasagar I. Antivibrio activity of recombinant lysozyme expressed from black tiger shrimp, Penaeus monodon. Aquaculture. 2007;272:246–53.

    Article  CAS  Google Scholar 

  18. Maiti B, Khushiramani R, Tyagi A, Karunasagar I, Karunasagar I. Recombinant ferritin protein protects Penaeus monodon infected pathogenic Vibrio harveyi. Dis Aquat Org. 2010;88:99–105.

    Article  CAS  Google Scholar 

  19. Banerjee D, Maiti B, Girisha SK, Venugopal MN, Karunasagar I. Broad spectrum anti-bacterial activity of a recombinant phosphatase-like protein isolated from the shrimp Penaeus monodon. Isr J Aquacult Bamidgeh. 2015;67:1146.

    Google Scholar 

  20. Banerjee D, Maiti B, Kallappa GS, Venugopal MN, Karunasagar I. A crustin isoform from black tiger shrimp, Penaeus monodon exhibits broad spectrum anti-bacterial activity. Aquacult Rep. 2015;2:106–11.

    Google Scholar 

  21. Rowley AF. The immune system of crustaceans. In: Ratcliffe M, editor. Encyclopedia of immunobiology. Amsterdam: Elsevier; 2016. p. 437–9.

    Chapter  Google Scholar 

  22. Martin GG, Simcox R, Nguyen A, Chilingaryan A. Peritrophic membrane of the penaeid shrimp Sicyonia ingentis: structure, formation, and permeability. Biol Bull. 2006;211:275–85.

    Article  PubMed  Google Scholar 

  23. Amparyup P, Sutthangkul J, Charoensapsri W, Tassanakajon A. Pattern recognition protein binds to lipopolysaccharide and β-1,3-glucan and activates shrimp prophenoloxidase system. J Biol Chem. 2012;287:10060–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lin X, Söderhäll I. Crustacean hematopoiesis and the astakine cytokines. Blood. 2011;117:6417–24.

    Article  CAS  PubMed  Google Scholar 

  25. Kumar B, Deepika A, Arumugam M, Mullainadhan P, Makesh M, Tripathi G, Purushothaman CS, Rajendran KV. Microscopic and cytochemical characterization of hemocytes of mud crab, Scylla serrata (FORSKAL, 1775) (Decapoda, Portunidae). Crustaceana. 2013;86(10):1234–49.

    Article  Google Scholar 

  26. Zhang Z, Shao M, Kang KH. Classification of haematopoietic cells and haemocytes in Chinese prawn Fenneropenaeus chinensis. Fish Shellfish Immunol. 2006;21(2):159–69.

    Article  PubMed  CAS  Google Scholar 

  27. Martin GG, Graves L. Fine structure and classification of shrimp hemocytes. J Morphol. 2005;185:339–48.

    Article  Google Scholar 

  28. Kobayashi M, Johansson M, Söderhäll K. The 76 kD cell-adhesion factor from crayfish haemocytes promotes encapsulation in vitro. Cell Tissue Res. 1990;260:13–8.

    Article  CAS  Google Scholar 

  29. Johansson MW, Keyser P, Sritunyalucksana K, Soderhall K. Crustacean haemocytes and haematopoiesis. Aquaculture. 2000;191:45–52.

    Article  CAS  Google Scholar 

  30. Pollard TD, Earnshaw WC, Lippincott-Schwartz J. Cell biology. Amsterdam: Elsevier Health Sciences; 2007.

    Google Scholar 

  31. Underhill DM, Goodridge HS. Information processing during phagocytosis. Nat Rev Immunol. 2012;12:492–502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Iwanaga S, Lee BL. Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol. 2005;38:128–50.

    CAS  PubMed  Google Scholar 

  33. Li F, Xiang J. Signaling pathways regulating innate immune responses in shrimp. Fish Shellfish Immunol. 2013;34:973–80.

    Article  CAS  PubMed  Google Scholar 

  34. Liu S, Zheng SC, Li YL, Li J, Liu HP. Hemocyte-mediated phagocytosis in crustaceans. Front Immunol. 2020;3(11):268. https://doi.org/10.3389/fimmu.2020.00268.

    Article  CAS  Google Scholar 

  35. Wang XW, Wang JX. Diversity and multiple functions of lectins in shrimp immunity. Dev Comp Immunol. 2013;39:27–38.

    Article  PubMed  CAS  Google Scholar 

  36. Canton J, Neculai D, Grinstein S. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol. 2013;13:621–34.

    Article  CAS  PubMed  Google Scholar 

  37. Johansson MW. Cell adhesion molecules in invertebrate immunity. Dev Comp Immunol. 1999;23:303–15.

    Article  CAS  PubMed  Google Scholar 

  38. Vazquez L, Alpuche J, Maldonado G, Agundis C, Pereyra-Morales A, Zenteno E. Immunity mechanisms in crustaceans. Innate Immun. 2009;15(3):179–88.

    Article  CAS  PubMed  Google Scholar 

  39. Smith VJ. Immunology of invertebrates: cellular. In: Encyclopedia of life sciences. Chichester: Wiley; 2016.

    Google Scholar 

  40. Söderhäll I, Bangyeekhun E, Mayo S, Söderhäll K. Hemocyte production and maturation in an invertebrate animal; proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus. Dev Comp Immunol. 2003;27:661–72.

    Article  PubMed  CAS  Google Scholar 

  41. Sugumaran M. Role of insect cuticle in immunity. In: Soderhall K, Iwanaga S, Vastha G, editors. New directions in invertebrate immunology. Fair Haven: SOS Publications; 1996. p. 355–74.

    Google Scholar 

  42. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science. 1998;281:5381.

    Article  Google Scholar 

  43. Liu H, Söderhäll K, Jiravanichpaisal P. Antiviral immunity in crustaceans. Fish Shellfish Immunol. 2009;27:79–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Aubert M, Jerome KR. Apoptosis prevention as a mechanism of immune evasion. Int Rev Immunol. 2003;22(5–6):361–71.

    Article  CAS  PubMed  Google Scholar 

  45. Wang L, Zhi B, Wu W, Zhang X. Requirement for shrimp caspase in apoptosis against virus infection. Dev Comp Immunol. 2008;32:706–15.

    Article  CAS  PubMed  Google Scholar 

  46. Leu JH, Chen YC, Chen LL, Chen KY, Huang HT, Ho JM, Lo CF. Litopenaeus vannamei inhibitor of apoptosis protein 1 (LvIAP1) is essential for shrimp survival. Dev Comp Immunol. 2012;38(1):78–87.

    Article  CAS  PubMed  Google Scholar 

  47. Wang PH, Wan DH, Chen YG, Weng SP, Yu XQ, He JG. Characterization of four novel caspases from Litopenaeus vannamei (Lvcaspase2-5) and their role in WSSV infection through dsRNA-mediated gene silencing. PLoS One. 2013;8(12):e80418. https://doi.org/10.1371/journal.pone.0080418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hu WY, Yao CL. Molecular and immune response characterizations of a novel AIF and cytochrome c in Litopenaeus vannamei defending against WSSV infection. Fish Shellfish Immunol. 2016;56:84–95.

    Article  CAS  PubMed  Google Scholar 

  49. Hasson KW, Lightner DV, Mohney LL, Redman RM, White BM. Role of lymphoid organ spheroids in chronic Taura syndrome virus (TSV) infections in Penaeus vannamei. Dis Aquat Org. 1999;38:93–105.

    Article  Google Scholar 

  50. Wang W, Zhang X. Comparison of antiviral efficiency of immune responses in shrimp. Fish Shellfish Immunol. 2008;25:522–7.

    Article  CAS  PubMed  Google Scholar 

  51. Rijiravanich A, Browdy CL, Withyachumnarnkul B. Knocking down caspase-3 by RNAi reduces mortality in Pacific white shrimp Penaeus (Litopenaeus) vannamei challenged with a low dose of white-spot syndrome virus. Fish Shellfish Immunol. 2008;24:308–13.

    Article  CAS  PubMed  Google Scholar 

  52. Leu JH, Chen LL, Lin YR, Kou GH, Lo CF. Molecular mechanism of the interactions between white spot syndrome virus anti-apoptosis protein AAP-1 (WSSV449) and shrimp effector caspase. Dev Comp Immunol. 2010;34:1068–74.

    Article  CAS  PubMed  Google Scholar 

  53. Lertwimol T, Sangsuriya P, Phiwsaiya K, Senapin S, Phongdara A, Boonchird C, Flegel TW. Two new anti-apoptotic proteins of white spot syndrome virus that bind to an effector caspase (PmCasp) of the giant tiger shrimp Penaeus (Penaeus) monodon. Fish Shellfish Immunol. 2014;38:1–6.

    Article  CAS  PubMed  Google Scholar 

  54. Iwanaga S. The molecular basis of innate immunity in the horseshoe crab. Curr Opin Immunol. 2002;14:87–95.

    Article  CAS  PubMed  Google Scholar 

  55. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O. The coagulation of insect hemolymph. Cell Mol Life Sci. 2002;59:363–72.

    Article  CAS  PubMed  Google Scholar 

  56. Maningas MBB, Kondo H, Hirono I. Molecular mechanisms of the shrimp clotting system. Fish Shellfish Immunol. 2013;34(4):968–72.

    Article  CAS  PubMed  Google Scholar 

  57. Tait J. Types of crustacean blood coagulation. J Mar Biol Assoc U K. 1911;9:191–8.

    Article  Google Scholar 

  58. Ghidalia W, Vendrely R, Montmory C, Coirault Y, Brouard MO. Coagulation in decapod crustacea. J Comp Physiol. 1981;142(4):473–8.

    Article  CAS  Google Scholar 

  59. Hose JE, Martin GG, Gerard AS. A decapod hemocyte classification scheme integrating morphology, cytochemistry, and function. Biol Bull. 1990;178:33–45.

    Article  CAS  PubMed  Google Scholar 

  60. Hall M, Wang R, van Antwerpen R, Sottrup-Jensen L, Söderhäll K. The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc Natl Acad Sci U S A. 1999;96:1965–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lorand L, Conrad SM. Transglutaminases. Mol Cell Biochem. 1984;58(1–2):9–35.

    Article  CAS  PubMed  Google Scholar 

  62. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol. 2003;4(2):140–56.

    Article  CAS  PubMed  Google Scholar 

  63. Perdomo-Morales R, Montero-Alejo V, Perera E. The clotting system in decapod crustaceans: history, current knowledge and what we need to know beyond the models. Fish Shellfish Immunol. 2019;84:204–12.

    Article  CAS  PubMed  Google Scholar 

  64. Cerenius L, Söderhäll K. Coagulation in invertebrates. J Innate Immun. 2011;3(1):3–8.

    Article  PubMed  Google Scholar 

  65. Gupta AP. Immunology of invertebrates: humoral. In: Encyclopedia of life sciences. Chichester: Wiley; 2010.

    Google Scholar 

  66. Gillespie P, Kanost MR. Biological mediators of insect immunity. Annu Rev Entomol. 1997;42:611–43.

    Article  CAS  PubMed  Google Scholar 

  67. Sritunyalucksana K, Söderhäll K. The proPO and clotting system in crustaceans. Aquaculture. 2000;191:53–69.

    Article  CAS  Google Scholar 

  68. Sugumaran M, Kanost M. Regulation of insect hemolymph phenoloxidases. In: Beckage NE, Thompson SM, Federici BA, editors. Parasites and pathogens of insects. San Diego: Academic Press; 1993. p. 317–42.

    Chapter  Google Scholar 

  69. Aspan A, Soderhall K. Purification of prophenoloxidase from crayfish blood cells, and its activation by an endogeneous serine proteinase. Insect Biochem. 1991;21:363–73.

    Article  CAS  Google Scholar 

  70. Aspan A, Huang TS, Cerenius L, Soderhall K. cDNA cloning of prophenoloxidase from the freshwater crayfish Pacifastacus leniusculus and its activation. Proc Natl Acad Sci U S A. 1995;92:939–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Sritunyalucksana K, Cerenius L, Soderhall K. Molecular cloning and characterization of prophenoloxidase in the black tiger shrimp, Penaeus monodon. Dev Comp Immunol. 1999;23:179–86.

    Article  CAS  PubMed  Google Scholar 

  72. Amparyup P, Charoensapsri W, Tassanakajon A. Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish Shellfish Immunol. 2013;34(4):990–1001.

    Article  CAS  PubMed  Google Scholar 

  73. Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A. 2000;97:8841–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Nordberg J, Arnér ESJ. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med. 2001;31(11):1287–312.

    Article  CAS  PubMed  Google Scholar 

  75. Tassanakajon A, Somboonwiwat K, Supungul P, Tang S. Discovery of immune molecules and their crucial functions in shrimp immunity. Fish Shellfish Immunol. 2013;34(4):954–67.

    Article  CAS  PubMed  Google Scholar 

  76. Mai HN, Nguyen HTN, Koiwai K, Kondo H, Hirono I. Characterization of a Kunitz-type protease inhibitor (MjKuPI) reveals the involvement of MjKuPI positive hemocytes in the immune responses of kuruma shrimp Marsupenaeus japonicus. Dev Comp Immunol. 2016;63:121–7.

    Article  CAS  PubMed  Google Scholar 

  77. Söderhäll I, Kim YA, Jiravanichpaisal P, Lee SY, Söderhäll K. An ancient role for a prokineticin domain in invertebrate hematopoiesis. J Immunol. 2005;174(10):6153–60.

    Article  PubMed  Google Scholar 

  78. Hsiao CY, Song YL. A long form of shrimp astakine transcript: molecular cloning, characterization and functional elucidation in promoting hematopoiesis. Fish Shellfish Immunol. 2010;28:77–86.

    Article  CAS  PubMed  Google Scholar 

  79. Liang GF, Liang Y, Xue Q, Lu JF, Cheng JJ, Huang J. Astakine LvAST binds to the β-subunit of F1-ATP synthase and likely plays a role in white shrimp Litopeneaus vannamei defense against white spot syndrome virus. Fish Shellfish Immunol. 2015;43(1):75–81.

    Article  CAS  PubMed  Google Scholar 

  80. Lin X, Söderhäll K, Söderhäll I. Transglutaminase activity in the hematopoietic tissue of a crustacean, Pacifastacus leniusculus, importance in hemocyte homeostasis. BMC Immunol. 2008;9:58. https://doi.org/10.1186/1471-2172-9-58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Bachère E. Anti-infectious immune effectors in marine invertebrates: potential tools for disease control in larviculture. Aquaculture. 2003;227:427–38.

    Article  Google Scholar 

  82. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002;21:2568–79.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Cuthbertson BJ, Shepard EF, Chapman RW, Gross PS. Diversity of the penaeidin antimicrobial peptides in two shrimp species. Immunogenetics. 2002;54:442–5.

    Article  CAS  PubMed  Google Scholar 

  84. Li H, Yin B, Wang S, Fu Q, Xiao B, LÇš K, He J, Li C. RNAi screening identifies a new Toll from shrimp Litopenaeus vannamei that restricts WSSV infection through activating Dorsal to induce antimicrobial peptides. PLoS Pathog. 2018;14(9):e1007109. https://doi.org/10.1371/journal.ppat.1007109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Smith VJ, Fernandes JM, Kemp GD, Hauton C. Crustins: enigmatic WAP domain-containing antibacterial proteins from crustaceans. Dev Comp Immunol. 2008;32(7):758–72.

    Article  CAS  PubMed  Google Scholar 

  86. Barreto C, Coelho JDR, Yuan J, Xiang J, Perazzolo LM, Rosa RD. Specific molecular signatures for type II crustins in Penaeid shrimp uncovered by the identification of crustin-like antimicrobial peptides in Litopenaeus vannamei. Mar Drugs. 2018;16:31. https://doi.org/10.3390/md16010031.

    Article  CAS  PubMed Central  Google Scholar 

  87. Chen D, He N, Xu J, Mj DWD. A double WAP domain-containing protein with antiviral relevance in Marsupenaeus japonicus. Fish Shellfish Immunol. 2008;25(6):775–81.

    Article  CAS  PubMed  Google Scholar 

  88. Du ZQ, Ren Q, Zhao XF, Wang JX. A double WAP domain (DWD)-containing protein with proteinase inhibitory activity in Chinese white shrimp, Fenneropenaeus chinensis. Comp Biochem Physiol B Biochem Mol Biol. 2009;154(2):203–10.

    Article  PubMed  CAS  Google Scholar 

  89. Tassanakajon A, Amparyup P, Somboonwiwat K, Supungul P. Cationic antimicrobial peptides in penaeid shrimp. Mar Biotechnol. 2011;13(4):639–57.

    Article  CAS  Google Scholar 

  90. Matos GM, Schmitt P, Barreto C, Farias ND, Toledo-Silva G, Guzmán F, Destoumieux-Garzón D, Perazzolo LM, Rosa RD. Massive gene expansion and sequence diversification is associated with diverse tissue distribution, regulation and antimicrobial properties of anti-lipopolysaccharide factors in shrimp. Mar Drugs. 2018;16:381. https://doi.org/10.3390/md16100381.

    Article  CAS  PubMed Central  Google Scholar 

  91. Suraprasit S, Methatham T, Jaree P, Phiwsaiya K, Senapin S, Hirono I, Lo CF, Tassanakajon A, Somboonwiwat K. Anti-lipopolysaccharide factor isoform 3 from Penaeus monodon (ALFPm3) exhibits antiviral activity by interacting with WSSV structural proteins. Antivir Res. 2014;110:142–50.

    Article  CAS  PubMed  Google Scholar 

  92. Methatham T, Boonchuen P, Jaree P, Tassanakajon A, Somboonwiwat K. Antiviral action of the antimicrobial peptide ALFPm3 from Penaeus monodon against white spot syndrome virus. Dev Comp Immunol. 2017;69:23–32.

    Article  CAS  PubMed  Google Scholar 

  93. Rolland JL, Abdelouahab M, Dupont J, Lefevre F, Bachère E, Romestand B. Stylicins, a new family of antimicrobial peptides from the Pacific blue shrimp Litopenaeus stylirostris. Mol Immunol. 2010;47(6):1269–77.

    Article  CAS  PubMed  Google Scholar 

  94. Liu HT, Wang J, Mao Y, Liu M, Niu SF, Qiao Y, Su YQ, Wang CZ, Zheng ZP. Identification and expression analysis of a novel stylicin antimicrobial peptide from Kuruma shrimp (Marsupenaeus japonicus). Fish Shellfish Immunol. 2015;47(2):817–23.

    Article  CAS  PubMed  Google Scholar 

  95. Farias ND, Falchetti M, Matos GM, Schmitt P, Barreto C, Argenta N, Rolland JL, Bachère E, Perazzolo LM, Rosa RD. Litopenaeus vannamei stylicins are constitutively produced by hemocytes and intestinal cells and are differentially modulated upon infections. Fish Shellfish Immunol. 2019;86:82–92.

    Article  CAS  PubMed  Google Scholar 

  96. Marques MRF, Barracco MA. Lectins, as non-self-recognition factors, in crustaceans. Aquaculture. 2000;191:23–44.

    Article  CAS  Google Scholar 

  97. Söderhäll K, Cerenius L. Crustacean immunity. Annu Rev Fish Dis. 1992;2:3–23.

    Article  Google Scholar 

  98. An MY, Gao J, Zhao XF, Wang JX. A new subfamily of penaeidin with an additional serine-rich region from kuruma shrimp (Marsupenaeus japonicus) contributes to antimicrobial and phagocytic activities. Dev Comp Immunol. 2016;59:86–98.

    Article  CAS  Google Scholar 

  99. Sun B, Wang Z, Zhu F. The crustin-like peptide plays opposite role in shrimp immune response to Vibrio alginolyticus and white spot syndrome virus (WSSV) infection. Fish Shellfish Immunol. 2017;66:487–96.

    Article  CAS  PubMed  Google Scholar 

  100. Fagutao FF, Maningas MBB, Kondo H, Aoki T, Hirono I. Transglutaminase regulates immune-related genes in shrimp. Fish Shellfish Immunol. 2012;32(5):711–5.

    Article  CAS  PubMed  Google Scholar 

  101. Maningas MBB, Kondo H, Hirono I, Saito-Taki T, Aoki T. Essential function of transglutaminase and clotting protein in shrimp immunity. Fish Shellfish Immunol. 2008;45(5):1269–75.

    CAS  Google Scholar 

  102. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol. 2006;80:5059–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Su J, Oanh DTH, Lyons RE, Leeton L, van Hulten MCW, Tan SH, Song L, Rajendran KV, Walker PJ. A key gene of RNA interference pathway in the black tiger shrimp, Peaneus monodon: identification and functional characterization of Dicer-1. Fish Shellfish Immunol. 2008;24:223–33.

    Article  PubMed  CAS  Google Scholar 

  104. Labreuche Y, Warr GW. Insights into the antiviral functions of the RNAi machinery in penaeid shrimp. Fish Shellfish Immunol. 2013;34:1002–10.

    Article  CAS  PubMed  Google Scholar 

  105. Xu J, Han F, Zhang X. Silencing shrimp white spot syndrome virus (WSSV) genes by siRNA. Antivir Res. 2007;73:126–31.

    Article  CAS  PubMed  Google Scholar 

  106. Yodmuang S, Tirasophon W, Roshorm Y, Chinnirunvong W, Panyim S. YHV-protease dsRNA inhibits YHV replication in Penaeus monodon and prevents mortality. Biochem Biophys Res Commun. 2006;341:351–6.

    Article  CAS  PubMed  Google Scholar 

  107. Robalino J, Bartlett T, Shepard E, Prior S, Jaramillo G, Scura E, Chapman RW, Gross PS, Browdy CL, Warr GW. Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: convergence of RNA interference and innate immunity in the invertebrate antiviral response? J Virol. 2005;79:13561–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Robalino J, Bartlett TC, Chapman RW, Gross PS, Browdy CL, Warr GW. Double-stranded RNA and antiviral immunity in marine shrimp: inducible host mechanisms and evidence for the evolution of viral counter-responses. Dev Comp Immunol. 2007;31:539–47.

    Article  CAS  PubMed  Google Scholar 

  109. Kim CS, Kosuke Z, Nam YK, Kim SK, Kim KH. Protection of shrimp (Penaeus chinensis) against white spot syndrome virus (WSSV) challenge by double-stranded RNA. Fish Shellfish Immunol. 2007;23:242–6.

    Article  CAS  PubMed  Google Scholar 

  110. Paria P, Greeshma SS, Chaudhari A, Makesh M, Purushothaman CS, Rajendran KV. Non-specific effect of double-stranded (ds) RNA on prophenoloxidase (proPO) expression in Penaeus monodon. Appl Biochem Biotechnol. 2013;169:281–9.

    Article  CAS  PubMed  Google Scholar 

  111. Taju G, Madan N, Majeed SA, Kumar TR, Thamizvanan S, Otta SK, Hameed ASH. Immune responses of white leg shrimp, Litopenaeus vannamei (Boone, 1931) to bacterially expressed dsRNA specific to VP28 gene of white spot syndrome virus. J Fish Dis. 2015;38:451–65.

    Article  CAS  PubMed  Google Scholar 

  112. Huang T, Xu D, Zhang X. Characterization of host microRNAs that respond to DNA virus infection in a crustacean. BMC Genomics. 2012;13:159. https://doi.org/10.1186/1471-2164-13-159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Shu L, Li C, Zhang X. The role of shrimp miR-965 in virus infection. Fish Shellfish Immunol. 2016;54:427–34.

    Article  CAS  PubMed  Google Scholar 

  114. Shu L, Zhang X. Shrimp miR-12 suppresses white spot syndrome virus infection by synchronously triggering antiviral phagocytosis and apoptosis pathways. Front Immunol. 2017;8:855. https://doi.org/10.3389/fimmu.2017.00855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Cui Y, Yang X, Zhang X. Shrimp miR-34 from shrimp stress response to virus infection suppresses tumorigenesis of breast cancer. Mol Ther Nucleic Acids. 2017;9:387–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Gong Y, Ju C, Zhang X. Shrimp miR-1000 functions in antiviral immunity by simultaneously triggering the degradation of two viral mRNAs. Front Immunol. 2018;9:2999. https://doi.org/10.3389/fimmu.2018.02999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Gong Y, Ju C, Zhang X. The miR-1000-p53 pathway regulates apoptosis and virus infection in shrimp. Fish Shellfish Immunol. 2015;46:516–22.

    Article  CAS  PubMed  Google Scholar 

  118. Ren Q, Huang X, Cui Y, Sun J, Wang W, Zhang X. Two white spot syndrome virus microRNAs target the Dorsal gene to promote virus infection in Marsupenaeus japonicus shrimp. J Virol. 2017;91(8):e02261–16. https://doi.org/10.1128/JVI.02261-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Ren Q, Huang Y, He Y, Wang W, Zhang X. A white spot syndrome virus microRNA promotes the virus infection by targeting the host STAT. Sci Rep. 2015;5:18384. https://doi.org/10.1038/srep18384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Cui Y, Huang T, Zhang X. RNA editing of microRNA prevents RNA-induced silencing complex recognition of target mRNA. Open Biol. 2015;5:150126. https://doi.org/10.1098/rsob.150126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Dunkelberger JR, Song WC. Complement and its role in innate and adaptive immune responses. Cell Res. 2010;20:34–50.

    Article  CAS  PubMed  Google Scholar 

  122. Janeway CA, Travers P, Walport M, Shlomchik M. Immunobiology: the immune system in health and disease. 6th ed. New York: Garland Publishing; 2005.

    Google Scholar 

  123. Liu Y, Song Q, Li D, Zou R, Zhang Y, Hao S, Geng X, Sun J. A novel complement C3 like gene (Lv-C3L) from Litopenaeus vannamei with bacteriolytic and hemolytic activities and its role in antiviral immune response. Fish Shellfish Immunol. 2019;91:376–87.

    Article  CAS  PubMed  Google Scholar 

  124. Medzhitov R, Janeway CJ. Innate immunity. N Engl J Med. 2000;343:338–44.

    Article  CAS  PubMed  Google Scholar 

  125. Wilkins C, Gale M Jr. Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol. 2010;22:41–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Wang XW, Wang JX. Pattern recognition receptors acting in innate immune system of shrimp against pathogen infections. Fish Shellfish Immunol. 2013;34:981–9.

    Article  PubMed  CAS  Google Scholar 

  127. Deepika A, Sreedharan K, Paria A, Makesh M, Rajendran KV. Toll-pathway in tiger shrimp (Penaeus monodon) responds to white spot syndrome virus infection: evidence through molecular characterisation and expression profiles of MyD88, TRAF6 and TLR genes. Fish Shellfish Immunol. 2014;41:441–54.

    Article  CAS  PubMed  Google Scholar 

  128. Dechamma MM, Moger R, Maiti B, Mani MK, Karunasagar I. Expression of toll-like receptors (TLR), in lymphoid organ of black tiger shrimp (Penaeus monodon) in response to Vibrio harveyi infection. Aquacult Rep. 2015;1:1–4.

    Google Scholar 

  129. Sreedharan K, Deepika A, Paria A, Badekar MK, Makesh M, Rajendran KV. Ontogenetic and expression of different genes involved in the Toll pathway of black tiger shrimp (Penaeus monodon) following immersion challenge with Vibrio harveyi and white spot syndrome virus (WSSV) Agri. Gene. 2018;8:63–71.

    Google Scholar 

  130. Borregaard N, Elsbach P, Ganz T, Garred P, Svejgaard A. Innate immunity: from plants to humans. Immunol Today. 2000;21:68–70.

    Article  CAS  PubMed  Google Scholar 

  131. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007;25:697–743.

    Article  CAS  PubMed  Google Scholar 

  132. Li C, Wang S, He J. The two NF-κB pathways regulating bacterial and WSSV infection of shrimp. Front Immunol. 2019;10:1785. https://doi.org/10.3389/fimmu.2019.01785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Li F, Yan H, Wang D, Priya TAG, Li S, Wang B, Zhang J, Xiang J. Identification of a novel relish homolog in Chinese shrimp Fenneropenaeus chinensis and its function in regulating the transcription of antimicrobial peptides. Dev Comp Immunol. 2009;33:1093–101.

    Article  CAS  PubMed  Google Scholar 

  134. Huang XD, Yin ZX, Liao JX, Wang PH, Yang LS, Ai HS, Gu ZH, Jia XT, Weng SP, Yu XQ, He JG. Identification and functional study of a shrimp Relish homologue. Fish Shellfish Immunol. 2009;27:230–8.

    Article  CAS  PubMed  Google Scholar 

  135. Wang PH, Gu ZH, Huang XD, Liu BD, Deng XX, Ai HS, Wang J, Yin ZX, Weng SP, Yu XQ, He JG. An immune deficiency homolog from the white shrimp, Litopenaeus vannamei, activates antimicrobial peptide genes. Mol Immunol. 2009;46:1897–904.

    Article  CAS  PubMed  Google Scholar 

  136. Wang PH, Gu ZH, Wan DH, Liu BD, Huang XD, Weng SP, Yu XQ, He JG. The shrimp IKK–NF-κB signaling pathway regulates antimicrobial peptide expression and may be subverted by white spot syndrome virus to facilitate viral gene expression. Cell Mol Immunol. 2013;10(5):423–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Feng N, Wang D, Wen R, Li F. Functional analysis on immune deficiency (IMD) homolog gene in Chinese shrimp Fenneropenaeus chinensis. Mol Biol Rep. 2014;41:1437–44.

    Article  CAS  PubMed  Google Scholar 

  138. Visetnan S, Supungul P, Hirono I, Tassanakajon A, Rimphanitchayakit V. Activation of PmRelish from Penaeus monodon by yellow head virus. Fish Shellfish Immunol. 2015;42:335–44.

    Article  CAS  PubMed  Google Scholar 

  139. Visetnan S, Supungul P, Tang S, Hirono I, Tassanakajon A, Rimphanitchayakit V. YHV-responsive gene expression under the influence of PmRelish regulation. Fish Shellfish Immunol. 2015;47(1):572–81.

    Article  CAS  PubMed  Google Scholar 

  140. Wang D, Li S, Li F. Screening of genes regulated by relish in Chinese shrimp Fenneropenaeus chinensis. Dev Comp Immunol. 2013;41:209–16.

    Article  CAS  PubMed  Google Scholar 

  141. Agaisse H, Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev. 2004;198:72–82.

    Article  CAS  PubMed  Google Scholar 

  142. Chen WY, Ho KC, Leu JH, Liu KF, Wang HC, Kou GH, Lo CF. WSSV infection activates STAT in shrimp. Dev Comp Immunol. 2008;32(10):1142–50.

    Article  CAS  PubMed  Google Scholar 

  143. Sun C, Shao HL, Zhang XW, Zhao XF, Wang JX. Molecular cloning and expression analysis of signal transducer and activator of transcription (STAT) from the Chinese white shrimp Fenneropenaeus chinensis. Mol Biol Rep. 2011;38:5313–9.

    Article  CAS  PubMed  Google Scholar 

  144. Okugawa S, Mekata T, Inada M, Kihara K, Shiki A, Kannabiran K, Kono T, Sakai M, Yoshida T, Itami T, Sudhakaran R. The SOCS and STAT from JAK/STAT signaling pathway of kuruma shrimp Marsupenaeus japonicus: molecular cloning, characterization and expression analysis. Mol Cell Probes. 2013;27(1):6–14.

    Article  CAS  PubMed  Google Scholar 

  145. Song X, Zhang Z, Wang S, Li H, Zuo H, Xu X, Weng S, He J, Li C. A Janus Kinase in the JAK/STAT signaling pathway from Litopenaeus vannamei is involved in antiviral immune response. Fish Shellfish Immunol. 2015;44(2):662–73.

    Article  CAS  PubMed  Google Scholar 

  146. Yan M, Li C, Su Z, Liang Q, Li H, Liang S, Weng S, He J, Xu X. Identification of a JAK/STAT pathway receptor domeless from Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol. 2015;44(1):26–32.

    Article  PubMed  CAS  Google Scholar 

  147. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev. 2001;81(2):807–69.

    Article  CAS  PubMed  Google Scholar 

  148. Shi H, Yan X, Xu X, Ruan L. Molecular cloning and characterization of a cDNA encoding extracellular signal-regulated kinase from Litopenaeus vannamei. Fish Shellfish Immunol. 2012;33(4):813–20.

    Article  CAS  PubMed  Google Scholar 

  149. Shi H, Yan X, Ruan L, Xu X. A novel JNK from Litopenaeus vannamei involved in white spot syndrome virus infection. Dev Comp Immunol. 2012;37(3–4):421–8.

    Article  CAS  PubMed  Google Scholar 

  150. Li X, Meng X, Kong J, Luo K, Luan S, Cao B, Liu N, Pang J, Shi X. Identification, cloning and characterization of an extracellular signal-regulated kinase (ERK) from Chinese shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol. 2013;35(6):1882–90.

    Article  PubMed  CAS  Google Scholar 

  151. Yao D, Ruan L, Xu X, Shi H. Identification of a c-Jun homolog from Litopenaeus vannamei as a downstream substrate of JNK in response to WSSV infection. Dev Comp Immunol. 2015;49(2):282–9.

    Article  CAS  PubMed  Google Scholar 

  152. He Y, Yao W, Liu P, Li J, Wang Q. Expression profiles of the p38 MAPK signaling pathway from Chinese shrimp Fenneropenaeus chinensis in response to viral and bacterial infections. Gene. 2018;642:381–8.

    Article  CAS  PubMed  Google Scholar 

  153. Li C, Li H, Chen Y, Chen Y, Wang S, Weng SP, Xu X, He J. Activation of Vago by interferon regulatory factor (IRF) suggests an interferon system-like antiviral mechanism in shrimp. Sci Rep. 2015;5:15078. https://doi.org/10.1038/srep15078.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Li H, Wang S, Lǚ K, Yin B, Xiao B, Li S, He J, Li C. An invertebrate STING from shrimp activates an innate immune defense against bacterial infection. FEBS Lett. 2017;591(7):1010–7.

    Article  CAS  PubMed  Google Scholar 

  155. Guanzon DAV, Maningas MBB. Functional elucidation of LvToll 3 receptor from P. vannamei through RNA interference and its potential role in the shrimp antiviral response. Dev Comp Immunol. 2018;84:172–80.

    Article  CAS  PubMed  Google Scholar 

  156. Paterson WD, Stewart JE. Rate and duration of phagocytic increase in lobsters induced by Pseudomonas perolens endotoxin. Dev Comp Immunol. 1979;3(2):353–7.

    Article  CAS  PubMed  Google Scholar 

  157. Huang CC, Song YL. Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev Comp Immunol. 1999;23:545–52.

    Article  CAS  PubMed  Google Scholar 

  158. Vilcinskas A. The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. Zoology. 2016;119:273–80.

    Article  PubMed  Google Scholar 

  159. Williams AF, Barclay AN. The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405.

    Article  CAS  PubMed  Google Scholar 

  160. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell. 2000;101:671–84.

    Article  CAS  PubMed  Google Scholar 

  161. 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. https://doi.org/10.1371/journal.pbio.0040229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Jin XK, Li WW, Wu MH, Guo XN, Li S, Yu AQ, Zhu YT, He L, Wang Q. Immunoglobulin superfamily protein Dscam exhibited molecular diversity by alternative splicing in hemocytes of crustacean, Eriocheir sinensis. Fish Shellfish Immunol. 2013;35:900–9.

    Article  CAS  PubMed  Google Scholar 

  163. Hung HY, Ng TH, Lin JH, Chiang YA, Chuang YC, Wang HC. Properties of Litopenaeus vannamei Dscam (LvDscam) isoforms related to specific pathogen recognition. Fish Shellfish Immunol. 2013;35:1272–81.

    Article  CAS  PubMed  Google Scholar 

  164. Hanington PC, Zhang SM. The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J Innate Immun. 2011;3:17–27.

    Article  CAS  PubMed  Google Scholar 

  165. Lu J, Le Y. Ficolins and the fibrinogen-like domain. Immunobiology. 1998;199(2):190–9.

    Article  CAS  PubMed  Google Scholar 

  166. Cerenius L, Soderhall K. Variable immune molecules in invertebrates. J Exp Biol. 2013;216:4313–9.

    Article  CAS  PubMed  Google Scholar 

  167. Gordy MA, Pila EA, Hanington PC. The role of fibrinogen-related proteins in the gastropod immune response. Fish Shellfish Immunol. 2015;46:39–49.

    Article  CAS  PubMed  Google Scholar 

  168. Söderhäll I, Wu C, Novotny M, Lee BL, Söderhäll K. A novel protein acts as a negative regulator of prophenoloxidase activation and melanization in the freshwater crayfish Pacifastacus leniusculus. J Biol Chem. 2009;284:6301–10.

    Article  PubMed  CAS  Google Scholar 

  169. Angthong P, Watthanasurorot A, Klinbunga S, Ruangdej U, Söderhäll I, Jiravanichpaisal P. Cloning and characterization of a melanization inhibition protein (PmMIP) of the black tiger shrimp, Penaeus monodon. Fish Shellfish Immunol. 2010;29:464–8.

    Article  CAS  PubMed  Google Scholar 

  170. Wu C, Söderhäll K, Söderhäll I. Two novel ficolin-like proteins act as pattern recognition receptors for invading pathogens in the freshwater crayfish Pacifastacus leniusculus. Proteomics. 2011;11:2249–64.

    Article  CAS  PubMed  Google Scholar 

  171. Zhang XW, Wang XW, Huang Y, Hui KM, Shi YR, Wang W, Ren Q. Cloning and characterization of two different ficolins from the giant freshwater prawn Macrobrachium rosenbergii. Dev Comp Immunol. 2014;44:359–69.

    Article  CAS  PubMed  Google Scholar 

  172. Hou F, Gao T, Liu T, Jia Z, Liu Y, Sun C, Liu X. Identification of 10 transcripts of FREP in penaeid shrimp Litopenaeus vannamei. Fish Shellfish Immunol. 2016;58:436–41.

    Article  CAS  PubMed  Google Scholar 

  173. Angthong P, Roytrakul S, Jarayabhand P, Jiravanichpaisal P. Characterization and function of a tachylectin 5-like immune molecule in Penaeus monodon. Dev Comp Immunol. 2017;76:120–31.

    Article  CAS  PubMed  Google Scholar 

  174. Angthong P, Roytrakul S, Jarayabhand P, Jiravanichpaisal P. Involvement of a tachylectin-like gene and its protein in pathogenesis of acute hepatopancreatic necrosis disease (AHPND) in the shrimp, Penaeus monodon. Dev Comp Immunol. 2017;76:229–37.

    Article  CAS  PubMed  Google Scholar 

  175. Su XD, Gastinel LN, Vaughn DE, Faye I, Poon P, Bjorkman PJ. Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science (New York, NY). 1998;281(5379):991–5.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rajendran K. V. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

K. V., R., K., S., Deepika, A., Kulkarni, A. (2022). Shrimp Immune System and Immune Responses. In: M., M., K.V., R. (eds) Fish immune system and vaccines. Springer, Singapore. https://doi.org/10.1007/978-981-19-1268-9_2

Download citation

Publish with us

Policies and ethics