Immunity mechanisms in crustaceans

Innate Immunity

Volumn 15, Issue 3, 2009, Pages 179-188

  Vazquez, Lorena ^a   Alpuche, Juan ^b   Maldonado, Guadalupe ^b   Agundis, Concepción ^b   Pereyra Morales, Ali ^b   Zenteno, Edgar ^b,c  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSIDAD RICARDO PALMA   (Peru)

Author keywords

Crustaceans; Decapoda; Defense mechanisms; Immunity; Lectins

Indexed keywords

CARBOHYDRATE; CELL SURFACE PROTEIN; LECTIN; MICROORGANISM PROTEIN; MONOPHENOL MONOOXYGENASE; ANTIMICROBIAL CATIONIC PEPTIDE; CATECHOL OXIDASE; ENZYME PRECURSOR; PATTERN RECOGNITION RECEPTOR; PRO PHENOLOXIDASE; PRO-PHENOLOXIDASE;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIGEN ANTIBODY REACTION; ANTIGEN SPECIFICITY; BACTERIAL STRAIN; CARBOHYDRATE ANALYSIS; CARBOXY TERMINAL SEQUENCE; CELLULAR IMMUNITY; CRUSTACEA; ENCAPSULATION; ENZYME ACTIVITY; FUNGAL STRAIN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNITY; INNATE IMMUNITY; INVERTEBRATE; MOLECULAR EVOLUTION; NONHUMAN; PHAGOCYTOSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; VERTEBRATE; ANIMAL; IMMUNOLOGY; METABOLISM;

CRUSTACEA; DECAPODA (CRUSTACEA); FUNGI; INVERTEBRATA; NEGIBACTERIA; POSIBACTERIA;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CATECHOL OXIDASE; CRUSTACEA; ENZYME PRECURSORS; IMMUNITY, INNATE; LECTINS; PHAGOCYTOSIS; RECEPTORS, PATTERN RECOGNITION;

EID: 66149190710     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425909102876     Document Type: Review

References (101)

1. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA Phylogenetic perspectives in innate immunity. Science 1999; 284: 1313-1318.
2. Iwanaga S., Lee BL Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 2005; 38: 128-150.
3. Yeaton RW Invertebrate lectins: II Diversity of specificity, biological synthesis and function in recognition. Dev Comp Immunol 1981; 5: 535-545.
4. Vasta GR, Quesenberry M., Ahmed H., O'Leary N. C-type lectins and galectins mediate innate and adaptive immune functions: Their roles in the complement activation pathway. Dev Comp Immunol 1999; 23: 401-420.
5. Sritunyalucksana K., Söderhäll K. The proPO and clotting system in crustaceans. Aquaculture 2000; 191: 53-69.
6. Cerenius L., Liang Z., Duvic B. et al. Structure and biological activity of a 1,3-β-D-glucan-binding protein in crustacean blood. J Biol Chem 1994; 269: 29462-29467.
7. Vazquez L., Maldonado G., Agundis C. et al. Participation of a sialic acid specific serum lectin from freshwater prawn Macrobrachium rosenbergii hemocytes in the recognition of non-self cells. J Exp Zool 1997; 279: 265-272.
8. Söderhäll K. Prophenoloxidase activating system and melanization - a recognition system of arthropods? A review. Dev Comp Immunol 1982; 6: 601-611.
9. Ratcliffe NA, Rowley AF, Fitzgerald SW, Rhodes CP Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol 1985; 97: 183-350.
10. Vargas-Albores F., Yepiz-Plascencia G. Beta glucan binding protein (BGBP) and its role in immune response. Aquaculture 2000; 191: 13-21.
11. Kawabata SI, Mutua T., Iwanaga S. The clotting cascade and defense molecules found in the hemolymph of the horseshoe crab. New direction. In: Söderhäll K, Iwanaga S, Vasta GR., (eds) Invertebrate Immunology. Fair Haven, CT: SOS, 1996; 255-283.
12. Söderhäll K., Aspán A., Duvic B. The proPO system and associated proteins - role in cellular communication in arthropods. Res Immunol 1990; 141: 896-907.
13. Smith VJ, Chisholm JR Antimicrobial proteins in crustaceans. Adv Exp Med Biol 2001; 484: 95-112.
14. Padhi A., Verghese B. Detecting molecular adaptation at individual codons in the pattern recognition protein, lipopolysaccharide- and β-1,3-glucan-binding protein of decapods. Fish Shellfish Immunol 2008; 24: 638-648.
15. Medzhitov R., Janeway CAJr Innate immunity: The virtues of a nonclonal system of recognition. Cell 1997; 91: 295-307.
16. Carroll MC, Prodeus AP Linkages of innate and adaptive immunity. Curr Opin Immunol 1998; 10: 36-40.
17. Lee SY, Söderhäll K. Characterization of a pattern recognition protein, a masquerade-like protein, in the freshwater crayfish Pacifastacus leniusculus. J Immunol 2001; 166: 7319-7326.
18. Yoshida H., Ochiai M., Ashida M. β-1,3-Glucan receptor and peptidoglycan receptor are present as separate entities within insect prophenoloxidase activating system. Biochem Biophys Res Commun 1986; 141: 1177-1184.
19. Koizumi N., Imamura M., Kadotani T., Yaoi K., Iwahana H., Sato R. The lipopolysaccharide-binding protein participating in hemocyte nodule formation in the silkworm Bombyx mori is a novel member of the C-type lectin superfamily with two different tandem carbohydrate-recognition domains. FEBS Lett 1999; 443: 139-143.
20. Lee SY, Wang R., Söderhäll K. A lipopolysaccharide- and β-1,3-glucan binding protein from hemocytes of freshwater crayfish Pacifastacus leniusculus: Purification, characterization, and cDNA cloning. J Biol Chem 2000; 275: 1337-1343.
21. Koizumi N., Morozumi A., Imamura M. et al. Lipopolysaccharide-binding protein and their involvement in the bacterial clearance from the hemolymph of the silkworm Bombyx mori. Eur J Biochem 1997; 248: 217-224.
22. Cheng W., Liu CH, Tsai CH, Chen JC Molecular cloning and characterisation of a pattern recognition molecule, lipopolysaccharide- and β-1,3-glucan binding protein (LGBP) from the white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 2005; 18: 297-310.
23. Roux MM, Pain A., Klimpel KR, Dhar AK The lipopolysaccharide and β-1,3-glucan binding protein gene is upregulated in white spot virus-infected shrimp. (Penaeus stylirostris). J Virol 2002; 76: 7140-7149.
24. Kilpatrick DC Handbook of Animal Lectins. New York: John Wiley, 2000.
25. Marques MRF, Barracco MA Lectins as non-self recognition factors, in crustaceans. Aquaculture 2000; 191: 23-44.
26. Sahoo P., Pillai BR, Mohanty J., Kumari J., Mohanty S., Mishra BK Differential affinity of the natural haemagglutinin of Macrobrachium rosenbergii towards vertebrate erythrocytes: Effect of sex, size and moult stage on haemagglutination titre. Indian J Exp Biol 2007; 45: 1-5.
27. Vazquez L., Perez A., Millan D. et al. Morphological analysis of hemocytes from the freshwater prawn Macrobrachium rosenbergii. J Morphol 1997; 234: 147-153.
28. Sierra C., Guevara J., Lascurain R. et al. Sialylation is modulated through maturation in hemocytes from Macrobrachium rosenbergii. Comp Biochem Physiol C 2001; 130: 179-189.
29. Soria F., Sierra C., Bouquelet S. et al. The effect of sugars and free amino acids from the freshwater prawn Macrobrachium rosenbergii hemolymph on lectin activity and on oxidative burst. Comp. Biochem Physiol C 2006; 142: 212-219.
30. Alpuche J., Pereyra A., Agundis C. et al. Purification and characterization of a lectin from the white shrimp Litopenaeus setiferus (Crustacea decapoda) hemolymph. Biochim Biophys Acta 2005; 1724: 86-93.
31. Vasta GR, Ahmed H., Tasumi S., Odom E., Saito K. Biological roles of lectins in innate immunity: Molecular and structural basis for diversity in self/non-self recognition. Adv Exp Med Biol 2007; 598: 389-406.
32. Fragkiadakis GA, Stratakis EK Characterization of hemolymph lectins in the prawn Parapenaeus longirostris. J Invert Pathol 1995; 65: 111-117.
33. Suetake T., Tsuda S., Kawabata S. et al. Chitin-binding proteins in invertebrates and plants comprise a common chitin-binding structural motif. J Biol Chem 2000; 275: 17929-17932.
34. Vazquez L., Lanz H., Montaño LF, Vasquez L., Zenteno E. Biological activity of the lectin from Macrobrachium rosenbergii. Lectins 1994; 10: 261-265.
35. Vazquez L., Jaramillo L., Lascurain R., Cooper EL, Rosas P., Zenteno E. Bacterial agglutination by the sialic acid specific serum lectin from Macrobrachium rosenbergii. Comp Biochem Physiol B 1996; 113: 355-359.
36. Dorai DT, Mohan S., Primal S., Bachhanwat BK On the multi-specificity of carcinoscorpin, the sialic acid binding lectin from the horseshoe crab Carcinoscorpius rotunda cauda. FEBS Lett 1982; 148: 98-102.
37. Liu Y., Li FH, Dong B., Wang B. Molecular cloning, characterization and expression analysis of a putative C-type lectin (Fclectin) gene in Chinese shrimp Fenneropenaeus chinensis. Mol Immunol 2007; 44: 598-607.
38. Kong HJ, Park EM, Nam BH et al. A C-type lectin like-domain (CTLD)-containing protein (PtLP) from the swimming crab Portunus trituberculatus. Fish Shellfish Immunol 2008; 25: 311-314.
39. Ma TH, Tiu SH, He JG, Chan SM Molecular cloning of a C-type lectin (LvLT) from the shrimp Litopenaeus vannamei: Early gene down-regulation after white spot syndrome virus (WSSV) infection. Fish Shellfish Immunol 2007; 23: 430-437.
40. Gross PS, Bartlett TC, Browdy CL, Chapman RW, Warr GW Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the Pacific white shrimp, Litopenaeus vannamei, and the Atlantic white shrimp, L. setiferus. Dev Comp Immunol 2001; 25: 565-577.
41. Leu JH, Chang CC, Wu JL et al. Comparative analysis of differentially expressed genes in normal and white spot syndrome virus infected Penaeus monodon. BMC Genomics 2007; 8: 120.
42. Söderhäll K., Cerenius L., Johansson MW The prophenoloxidase activating system and its role in invertebrate defense. Ann NY Acad Sci 1994; 712: 155-161.
43. Vargas-Albores F., Jimenez-Vega F., Söderhäll K. A plasma protein isolated from brown shrimp (Penaeus californiensis) which enhances the activation of prophenoloxidase system by β-1,3-glucan. Dev Comp Immunol 1996; 5: 299-306.
44. Adachi K., Hirata T., Nishioka T., Sakaguchi M. Hemocyte components in crustaceans convert hemocyanin into a phenoloxidase-like enzyme. Comp Biochem Physiol B 2002; 134: 135-141.
45. Smith VJ, Söderhäll K. β-1,3 Glucan activation of crustacean hemocytes in vitro and in vivo. Biol Bull 1983; 164: 299-314.
46. Aspán A., Söderhäll K. Purification of prophenoloxidase from crayfish blood cells and its activation by an endogenous serine proteinase. Insect Biochem 1991; 21: 363-373.
47. Söderhäll K., Vey A., Rented M. Haemocytes lysate enhancement of fungal spore encapsulation by crayfish hemocytes. Dev Comp Immunol 1984; 8: 23-29.
48. Cerenius L., Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol Rev 2004; 198: 116-126.
49. Mudlarz L., Jones LE, Harvell CD Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 2006; 37: 251-288.
50. Bayne CJ Phagocytosis and recognition invertebrates. Bioscience 1990; 40: 723-731.
51. McKay D., Jenkin CR Immunity in the invertebrates. Aust J Exp Biol Med Sci 1970; 48: 139-150.
52. Mori K., Stewart JE Immunogen-dependent quantitative and qualitative differences in phagocytic responses of the circulating hemocytes of the lobster Homarus americanus. Dis Aquat Organ 2006; 69: 197-203.
53. Cassels FJ, Marchalonis JJ, Vasta GR Heterogeneous humoral and hemocyte-associated lectins with N-acylamino sugar specificities from the blue crab Callinectes sapidus Rathbun. Comp Biochem Physiol B 1986; 85: 23-30.
54. Tyson CJ, Jenkin C. Phagocytosis of bacteria in vitro by haemocytes from the crayfish (Parachaeraps bicaritus). Aust J Exp Biol Med Sci 1974; 52: 341-348.
55. Kondo MH, Matsuyama H., Yano T. The opsonic effect of lectin on the phagocytosis by hemocytes of kuruma prawn, Penaeus japonicus. Fish Pathol 1992; 27: 217-222.
56. Bechteler C., Holler D. Preliminary studies of the immunization of shrimp (Penaeus monodon) against Vibrio infections. Berl Münch Tierärztl Wochenschr 1995; 108: 462-465.
57. Lee YK, Soh BS, Wu JH Quantitative assessment of phagocytic activity of hemocytes in the prawn, Penaeus merguiensis, by flow cytometric analysis. Cytometry 2001; 43: 82-85.
58. Song YL, Hsieh YT Immunostimulation of tiger (Penaeus monodon) hemocytes for generation of microbicidal substances: Analysis of reactive oxygen species. Dev Comp Immunol 1994; 18: 201-209.
59. Muñoz M., Cedeño R., Rodriguez J., van der Knaap WPW, Mialhe E., Bachere E. Measurement of reactive oxygen intermediate production in hemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture 2000; 191: 89-107.
60. Jiang G., Yu R., Zhou M. Studies on nitric oxide synthase activity in haemocytes of shrimp Fenneropenaeus chinensis and Marsupenaeus japonicus after white spot syndrome virus infection. Nitric oxide 2006; 14: 217-227.
61. Durliat M. Clotting processes in crustacea decapoda. Biol Rev 1985; 60: 473-498.
62. Persson M., Vey A., Söderhäll K. Encapsulation of foreign particles in vitro by separated blood cells from crayfish, Astacus leptodactylus. Cell Tissue Res 1987; 247: 409-415.
63. Rather S., Vinson SB Phagocytosis and encapsulation: Cellular immunity in arthropoda. Am Zool 1983; 23: 185-194.
64. 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 USA 1999; 96: 1965-1970.
65. Kawabata S., Magayama R., Hirata M. et al. Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J Biochem 1996; 120: 1253-1260.
66. Ariki S., Koori K., Osaki T., Motoyama K., Inamori K., Kawabata S. A serine protease zymogen functions as a pattern-recognition receptor for lipopolysaccharides. Proc Natl Acad Sci USA 2004; 101: 953-958.
67. Tamura H., Tanaka S., Oda T., Uemura Y., Aketagawa J., Hashimoto Y. Purification and characterization of a (1→3)-β-D-glucan-binding protein from horseshoe crab (Tachypleus tridentatus) amoebocytes. Carbohydr Res 1996; 295: 103-116.
68. Destoumieux D., Muñoz M., Cosseau C. et al. Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. J Cell Sci 2000; 113: 461-469.
69. Relf JM, Chisholm JR, Kemp GD, Smith VJ Purification and characterization of a cysteine-rich 11.5 kDa antibacterial protein from the granular haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 1999; 264: 350-357.
70. Muñoz M., Vandenbulcke F., Garnier J. et al. Involvement of penaeidins in defense reactions of the shrimp Litopenaeus stylirostris to a pathogenic Vibrio. Cell Mol Life Sci 2004; 61: 961-972.
71. Rojtinnakorn J., Hirono I., Itami T., Takahashi Y., Aoki T. Gene expression in haemocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shellfish Immunol 2002; 13: 69-83.
72. Kang CJ, Wang JX, Zhao XF, Yang XM, Shao HL, Xiang JH Molecular cloning and expression analysis of Ch-penaeidin, and antimicrobial peptide from Chinese shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol 2004; 16: 513-525.
73. Chiou TT, Wu JL, Chen TT, Lu JK Molecular cloning and characterization of cDNA of penaeidin-like antimicrobial peptide from tiger shrimp (Penaeus monodon). Marine Biotechnol 2005; 7: 119-127.
74. Supungul P., Klinbunga S., Pichyangkura R., Hirono I., Aoki T., Tassanakajon A. Antimicrobial peptides discovered in the black shrimp Penaeus monodon using the EST approach. Dis Aquat Organ 2004; 61: 123-135.
75. Bartlett TC, Guillanume J. Nutrition of Litopenaeus vannamei and Litopenaeus setiferus. Marine Biotechnol 2004; 4: 278-293.
76. Destoumieux D., Bulet P., Loew D., Van Dorsselaer A., Rodriguez J., Bachère E. Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J Biol Chem 1997; 272: 28398-28406.
77. Destoumieux D., Bulet P., Strub JM, Van Dorsselaer A., Bachere E. Recombinant expression and range of activity of penaeidins, antimicrobial peptides from penaeid shrimp. Eur J Biochem 1999; 266: 335-346.
78. Destoumieux D., Muñoz P., Bulet P., Bachere E. Penaeidins, a family of antimicrobial peptides from penaeid shrimp (Crustacea, Decapoda). Cell Mol Life Sci 2000; 57: 1260-1271.
79. Bachère E., Destoumieux D., Bulet P. Penaeidins, antimicrobial molecules of shrimp: A comparison with other effectors of innate immunity. Aquaculture 2000; 191: 71-88.
80. Muñoz M., Vandenbulcke F., Saulnier D., Bachère E. Expression and distribution of penaeidin antimicrobial peptides are regulated by haemocyte reactions in microbial challenged shrimp. Eur J Biochem 2002; 269: 2678-2689.
81. Nappi AJ, Ottaviani E. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 2000; 22: 469-480.
82. Cooper EL, Kauschke E., Cossarizza A. Digging for innate immunity since Darwin and Metchnikoff. Bioessays 2002; 24: 319-333.
83. Overstreet RM, Lightner DV, Hasson KW, Mcllwain S., Lotz JM Susceptibility to taura syndrome virus of some penaeid shrimp species native to the Gulf of Mexico and the southeastern United States. J Invert Pathol 1997; 69: 165-176.
84. Siripavee S., Jeong JK, Suriyan T., Söderhäll K. Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish. Dev Comp Immunol 2005; 29: 1017-1031.
85. Muramoto K., Jin DH, Niino Y. et al. Comparison of the amino acid sequences of acorn barnacle lectins showing different inhibitory activities toward the crystal growth of calcium carbonate. Fish Sci 2001; 67: 703-709.
86. Ravindranath MH, Higa HH, Cooper EL, Paulson JC Purification and characterization of an O-acetyl sialic acid specific lectin from a marine crab Cancer antennarius. J Biol Chem 1985; 260: 8850-8856.
87. Hall JL, Rowlands DT Heterogeneity of lobster agglutinins. I. Purification and physicochemical characterization. Biochemistry 1974; 13: 821-827.
88. Imai T., Toshiki-Goto R., Rina A. et al. Lectins in the rock lobster Jasus novaehollandiae hemolymph. Crustaceana 1994; 67: 121-130.
89. Frankiadakis GA, Stratakis EK The lectin from the crustacean Liocarcinus depurator recognizes O-acetylsialic acids. Comp Biochem Physiol B 1997; 117: 545-552.
90. Cominetti MR, Marques MRF, Lorenzini DM, Lofgren SE, Daffre S., Barracco MA Characterization and partial purification of a lectin from the hemolymph of the white shrimp Litopenaeus schimitti. Dev Comp Immunol 2002; 26: 715-721.
91. Sun J., Lei W., Baojie W. et al. Purification and characterization of a natural lectin from the serum of the shrimp Litopenaeus vannamei. Fish Shellfish Immunol 2007; 23: 292-299.
92. Zenteno R., Vazquez L., Sierra C. et al. Chemical characterization of the freshwater prawn Macrobrachium rosenbergii (De Man) by Maldi-Tof. Comp Biochem Physiol 2000; 127: 243-250.
93. Muramoto K., Ogata K., Kamiya H. Comparison of the multiple agglutinins of the acorn barnacle, Megabalanus rosa. Agric Biol Chem 1985; 49: 85-93.
94. Matsubara H., Nakamura-Tsuruta S., Hirabayashi J. et al. Diverse sugar-binding specificities of marine invertebrate C-type lectins. Biosci Biotechnol Biochem 2007; 71: 513-519.
95. Vargas-Albores F., Guzman M., Ochoa JL A lipopolysaccharide-binding agglutinin isolated from brown shrimp (Penaeus californiensis Holmes) haemolymph. Comp Biochem Physiol A 1993; 104: 407-413.
96. Mashewari R., Mullainadhan P., Arumagam M. Characterization of a natural haemagglutinin with affinity for acetylated amino sugars in the serum of the marine prawn, Penaeus indicus. Fish Shellfish Immunol 1997; 7: 17-28.
97. Kondo M., Itami T., Takahashi Y. Preliminary characterization of lectin in the hemolymph of kuruma prawn. Fish Pathol 1998; 33: 429-435.
98. Ratanapo S., Chulavatnatol M. Monodin a new sialic acid-specific lectin from black tiger prawn (Penaeus monodon). Comp Biochem Physiol B 1990; 97: 515-520.
99. Luo T., Yang H., Li F., Zhang X., Xu X. Purification, characterization and cDNA cloning of a novel lipopolysaccharide-binding lectin from the shrimp Penaeus monodon. Dev Comp Immunol 2006; 30: 607-617.
100. Maghil D., Palatty PDM, Bai NR, Suriya J. Purification and characterization of a sialic acid specific lectin from the hemolymph of the freshwater crab Paratelphusa jacquemontii. Eur J Biochem 2003; 270: 4348-4355.
101. Fragkiadakis GA Isolation of lectins from hemolymph of decapod crustaceans by adsorption on formalinized erythrocytes. J Biochem Biophys Methods 2000; 44: 109-114.