The immune system and its modulation mechanism in scallop

Fish and Shellfish Immunology

Volumn 46, Issue 1, 2015, Pages 65-78

  Song, Linsheng ^a   Wang, Lingling ^b   Zhang, Huan ^b   Wang, Mengqiang ^b  

^a DALIAN OCEAN UNIVERSITY   (China)

^b INSTITUTE OF OCEANOLOGY   (China)

Author keywords

Cellular immunity; Effector synthesis; Immune recognition; Immune response; Neuroendocrine regulation; Scallop; Signal transduction

Indexed keywords

BIVALVIA; INVERTEBRATA; PECTINIDAE;

ANIMAL; IMMUNOLOGY; IMMUNOMODULATION; INNATE IMMUNITY; NEUROSECRETION; SCALLOP;

ANIMALS; IMMUNITY, INNATE; IMMUNOMODULATION; NEUROSECRETORY SYSTEMS; PECTINIDAE;

EID: 84937162209     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2015.03.013     Document Type: Review

References (181)

1. Shumway S.E. Scallops: Biology, Ecology, and Aquaculture. Developments in Aquaculture and Fisheries Science 1991, 1095. Elsevier, Amsterdam; New York.
2. Ottaviani E. The mollusc as a suitable model for mammalian immune-neuroendocrine investigations. Invertebr. Surviv. J. 2004, 1:2-4.
3. Loker E.S., Adema C.M., Zhang S.-M., Kepler T.B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol. Rev. 2004, 198:10-24.
4. Iwanaga S., Lee B.L. Recent advances in the innate immunity of invertebrate animals. J.Biochem. Mol. Biol. 2005, 38(2):128-150.
5. de Lange R.P., Moorer-van Delft C.M., de Boer P.A., van Minnen J., de Jong-Brink M. Target-dependent differentiation and development of molluscan neurons and neuroendocrine cells: use of parasitisation as a tool. Neuroscience 2001, 103(1):289-299.
6. Ottaviani E. The importance of studying invertebrate immune-neuroendocrine functions. Isj-Invertebrate Surviv. J. 2014, 11:1-3.
7. Wang L., Song L., Chang Y., Xu W., Ni D., Guo X. Apreliminary genetic map of zhikong scallop (Chlamys farreri Jones et Preston 1904). Aquac. Res. 2005, 36(7):643-653.
8. Song L., Xu W., Li C., Li H., Wu L., Xiang J., et al. Development of expressed sequence tags from the bay scallop, Argopecten irradians irradians. Mar. Biotechnol. (NY) 2006, 8(2):161-169.
9. Janeway C.A., Medzhitov R. Innate immune recognition. Annu Rev. Immunol. 2002, 20:197-216.
10. Medzhitov R., Janeway C.A. Decoding the patterns of self and nonself by the innate immune system. Science 2002, 296(5566):298-300.
11. Ni D., Song L., Wu L., Chang Y., Yu Y., Qiu L., et al. Molecular cloning and mRNA expression of peptidoglycan recognition protein (PGRP) gene in bay scallop (Argopecten irradians, Lamarck 1819). Dev. Comp. Immunol. 2007, 31(6):548-558.
12. Su J., Ni D., Song L., Zhao J., Qiu L. Molecular cloning and characterization of a short type peptidoglycan recognition protein (CfPGRP-S1) cDNA from zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 23(3):646-656.
13. Yang J., Wang W., Wei X., Qiu L., Wang L., Zhang H., et al. Peptidoglycan recognition protein of Chlamys farreri (CfPGRP-S1) mediates immune defenses against bacterial infection. Dev. Comp. Immunol. 2010, 34(12):1300-1307.
14. Wang L., Wang L., Huang M., Zhang H., Song L. The immune role of C-type lectins in molluscs 2011, 8:241-246.
15. Song X., Zhang H., Zhao J., Wang L., Qiu L., Mu C., et al. An immune responsive multidomain galectin from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2010, 28(2):326-332.
16. Song X., Zhang H., Wang L., Zhao J., Mu C., Song L., et al. Agalectin with quadruple-domain from bay scallop Argopecten irradians is involved in innate immune response. Dev. Comp. Immunol. 2011, 35(5):592-602.
17. Zhang H., Song L., Li C., Zhao J., Wang H., Gao Q., et al. Molecular cloning and characterization of a thioester-containing protein from Zhikong scallop Chlamys farreri. Mol. Immunol. 2007, 44(14):3492-3500.
18. Liu L., Yang J., Qiu L., Wang L., Zhang H., Wang M., et al. Anovel scavenger receptor-cysteine-rich (SRCR) domain containing scavenger receptor identified from mollusk mediated PAMP recognition and binding. Dev. Comp. Immunol. 2011, 35(2):227-239.
19. Qiu L., Song L., Xu W., Ni D., Yu Y. Molecular cloning and expression of a toll receptor gene homologue from Zhikong Scallop, Chlamys farreri. Fish Shellfish Immunol. 2007, 22:451-466.
20. Yang C., Wang L., Zhang H., Huang M., Sun Z., Sun Y., et al. Anew fibrinogen-related protein from Argopecten irradians (AiFREP-2) with broad recognition spectrum and bacteria agglutination activity. Fish Shellfish Immunol. 2014, 38(1):221-229.
21. Zhang H., Wang L., Song L., Song X., Wang B., Mu C., et al. Afibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor. Fish Shellfish Immunol. 2009, 26(1):56-64.
22. Kong P., Zhang H., Wang L., Zhou Z., Yang J., Zhang Y., et al. AiC1qDC-1, a novel gC1q-domain-containing protein from bay scallop Argopecten irradians with fungi agglutinating activity. Dev. Comp. Immunol. 2010, 34(8):837-846.
23. Wang L., Kong P., Yang J., Zhang H., Wang M., Zhou Z., et al. Anovel C1qDC protein acting as pattern recognition receptor in scallop Argopecten irradians. Fish Shellfish Immunol. 2012, 33(2):427-435.
24. Wang L., Zhang H., Zhou Z., Siva V.S., Song L. AC1q domain containing protein from scallop Chlamys farreri serving as pattern recognition receptor with heat-aggregated IgG binding activity. PLoS One 2012, 7(8):e43289.
25. Zhang H., Song L., Li C., Zhao J., Wang H., Qiu L., et al. Anovel C1q-domain-containing protein from Zhikong scallop Chlamys farreri with lipopolysaccharide binding activity. Fish Shellfish Immunol. 2008, 25(3):281-289.
26. Zelensky A.N., Gready J.E. The C-type lectin-like domain superfamily. FEBS J. 2005, 272(24):6179-6217.
27. Zhang H., Wang H., Wang L., Song L., Song X., Zhao J., et al. Cflec-4, a multidomain C-type lectin involved in immune defense of Zhikong scallop Chlamys farreri. Dev. Comp. Immunol. 2009, 33(6):780-788.
28. Zhang H., Wang H., Wang L., Song X., Zhao J., Qiu L., et al. Anovel C-type lectin (Cflec-3) from Chlamys farreri with three carbohydrate-recognition domains. Fish Shellfish Immunol. 2009, 26(5):707-715.
29. Wang L., Yang J., Zhang H., Huang M., Kong P., Zhou Z., et al. Amulti-CRD C-type lectin with broad recognition spectrum and cellular adhesion from Argopecten irradians. Dev. Comp. Immunol. 2012, 36(3):591-601.
30. Huang M., Song X., Zhao J., Mu C., Wang L., Zhang H., et al. AC-type lectin (AiCTL-3) from bay scallop Argopecten irradians with mannose/galactose binding ability to bind various bacteria. Gene 2013, 531(1):31-38.
31. Yang J., Wang L., Zhang H., Qiu L., Wang H., Song L. C-Type lectin in Chlamys farreri (CfLec-1) mediating immune recognition and opsonization. Plos One 2011, 6(2):e17089.
32. Yang J., Qiu L., Wei X., Wang L., Wang L., Zhou Z., et al. An ancient C-type lectin in Chlamys farreri (CfLec-2) that mediate pathogen recognition and cellular adhesion. Dev. Comp. Immunol. 2010, 34(12):1274-1282.
33. Huang M., Wang L., Yang J., Zhang H., Wang L., Song L. Afour-CRD C-type lectin from Chlamys farreri mediating nonself-recognition with broader spectrum and opsonization. Dev. Comp. Immunol. 2013, 39(4):363-369.
34. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., et al. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298(5591):159-165.
35. Tasumi S., Vasta G.R. Agalectin of unique domain organization from haemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J.Immunol. 2007, 179(5):3086-3098.
36. Zhang D., Jiang S., Hu Y., Cui S., Guo H., Wu K., et al. Amultidomain galectin involved in innate immune response of pearl oyster Pinctada fucata. Dev. Comp. Immunol. 2011, 35(1):1-6.
37. Kim J.Y., Kim Y.M., Cho S.K., Choi K.S., Cho M. Noble tandem-repeat galectin of Manila clam Ruditapes philippinarum is induced upon infection with the protozoan parasite Perkinsus olseni. Dev. Comp. Immunol. 2008, 32(10):1131-1141.
38. Cooper D.N. Galectinomics: finding themes in complexity. Biochim. Biophys. Acta 2002, 1572(2-3):209-231.
39. Siva V.S., Yang C., Yang J., Wang L., Zhou Z., Qiu L., et al. Association between the polymorphism of CfPGRP-S1 gene and disease susceptibility/resistance of zhikong scallop (Chlamys farreri) to Listonella anguillarum challenge. Fish Shellfish Immunol. 2012, 33(4):736-742.
40. Huan P., Zhang X., Li F., Zhang Y., Zhao C., Xiang J. Chromosomal localization and molecular marker development of the lipopolysaccharide and beta-1,3-glucan binding protein gene in the Zhikong scallop Chlamys farreri (Jones et Preston) (Pectinoida, Pectinidae). Genet. Mol. Biol. 2010, 33(1):36-43.
41. Wang L., Song L., Zhao J., Qiu L., Zhang H., Xu W., et al. Expressed sequence tags from the zhikong scallop (Chlamys farreri): discovery and annotation of host-defense genes. Fish Shellfish Immunol. 2009, 26(5):744-750.
42. Yang J., Qiu L., Wang L., Wei X., Zhang H., Zhang Y., et al. CfLGBP, a pattern recognition receptor in Chlamys farreri involved in the immune response against various bacteria. Fish Shellfish Immunol. 2010, 29(5):825-831.
43. Siva V.S., Yang C., Yang J., Wang L., Zhou Z., Qiu L., et al. Association of CfLGBP gene polymorphism with disease susceptibility/resistance of Zhikong scallop (Chlamys farreri) to Listonella anguillarum. Fish Shellfish Immunol. 2012, 32(6):1117-1123.
44. Kishore U., Ghai R., Greenhough T.J., Shrive A.K., Bonifati D.M., Gadjeva M.G., et al. Structural and functional anatomy of the globular domain of complement protein C1q. Immunol. Lett. 2004, 95(2):113-128.
45. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490(7418):49-54.
46. Gerdol M., Manfrin C., De Moro G., Figueras A., Novoa B., Venier P., et al. The C1q domain containing proteins of the Mediterranean mussel Mytilus galloprovincialis: a widespread and diverse family of immune-related molecules. Dev. Comp. Immunol. 2011, 35(6):635-643.
47. Borregaard N., Elsbach P., Ganz T., Garred P., Svejgaard A. Innate immunity: from plants to humans. Immunol. Today 2000, 21(2):68-70.
48. Wang B., Zhao J., Song L., Zhang H., Wang L., Li C., et al. Molecular cloning and expression of a novel Kazal-type serine proteinase inhibitor gene from Zhikong scallop Chlamys farreri, and the inhibitory activity of its recombinant domain. Fish Shellfish Immunol. 2008, 24(5):629-637.
49. Zhu L., Song L., Chang Y., Xu W., Wu L. Molecular cloning, characterization and expression of a novel serine proteinase inhibitor gene in bay scallops (Argopecten irradians, Lamarck 1819). Fish Shellfish Immunol. 2006, 20(3):320-331.
50. Zhu L., Song L., Mao Y., Zhao J., Li C., Xu W. Anovel serine protease with clip domain from scallop Chlamys farreri. Mol. Biol. Rep. 2008, 35(2):257-264.
51. Zhu L., Song L., Zhao J., Xu W., Chang Y. Molecular cloning, characterization and expression of a serine protease with clip-domain homologue from scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 22(5):556-566.
52. Pauletto M., Milan M., Moreira R., Novoa B., Figueras A., Babbucci M., et al. Deep transcriptome sequencing of Pecten maximus haemocytes: a genomic resource for bivalve immunology. Fish Shellfish Immunol. 2014, 37(1):154-165.
53. Wang M., Yang J., Zhou Z., Qiu L., Wang L., Zhang H., et al. Aprimitive toll-like receptor signaling pathway in mollusk Zhikong scallop Chlamys farreri. Dev. Comp. Immunol. 2011, 35(4):511-520.
54. Qiu L., Song L., Yu Y., Zhao J., Wang L., Zhang Q. Identification and expression of TRAF6 (TNF receptor-associated factor 6) gene in Zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2009, 26(3):359-367.
55. He C.B., Wang Y., Liu W.D., Gao X.G., Chen P.H., Li Y.F., et al. Cloning, promoter analysis and expression of the tumor necrosis factor receptor-associated factor 6 (TRAF6) in Japanese scallop (Mizuhopecten yessoensis). Mol. Biol. Rep. 2013, 40(8):4769-4779.
56. Mu C., Yu Y., Zhao J., Wang L., Song X., Zhang H., et al. An inhibitor kappa B homologue from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2010, 28(4):687-694.
57. Zhou Z., Jiang Q., Wang M., Yue F., Wang L., Wang L., et al. Modulation of haemocyte phagocytic and antibacterial activity by alpha-adrenergic receptor in scallop Chlamys farreri. Fish Shellfish Immunol. 2013, 35(3):825-832.
58. Chen G., Goeddel D.V. TNF-R1 signaling: a beautiful pathway. Science 2002, 296(5573):1634-1635.
59. Li L., Qiu L., Song L., Song X., Zhao J., Wang L., et al. First molluscan TNFR homologue in Zhikong scallop: molecular characterization and expression analysis. Fish Shellfish Immunol. 2009, 27(5):625-632.
60. Su J., Qiu L., Li L., Liu L., Wang L., Siva V.S., et al. cDNA cloning and characterization of a new member of the tumor necrosis factor receptor family gene from scallop, Chlamys farreri. Mol. Biol. Rep. 2011, 38(7):4483-4490.
61. Yu Y., Qiu L., Song L., Zhao J., Ni D., Zhang Y., et al. Molecular cloning and characterization of a putative lipopolysaccharide-induced TNF-[alpha] factor (LITAF) gene homologue from Zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 23(2):419-429.
62. Hao C., Zhu B., Liu W., Bao X., Li Y., Shan Z., et al. Cloning and expression analysis of lipopolysaccharide-induced TNF-α(LITAF) of Japanese scallop (Mizuhopecten yessoensis). Hereditas 2012, (06):736-741.
63. Tang X., Marciano D.L., Leeman S.E., Amar S. LPS induces the interaction of a transcription factor, LPS-induced TNF-alpha factor, and STAT6(B) with effects on multiple cytokines. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(14):5132-5137.
64. Yang J., Qiu L., Wang L., Huang M., Zhang H., Song L. ATRAF and TNF receptor-associated protein (TTRAP) in mollusk with endonuclease activity. Dev. Comp. Immunol. 2011, 35(8):827-834.
65. Wang L., Wang L., Kong P., Yang J., Zhang H., Wang M., et al. Anovel C1qDC protein acting as pattern recognition receptor in scallop Argopecten irradians. Fish Shellfish Immunol. 2012, 33(2):427-435.
66. Wang H., Song L., Li C., Zhao J., Zhang H., Ni D., et al. Cloning and characterization of a novel C-type lectin from Zhikong scallop Chlamys farreri. Mol. Immunol. 2007, 44(5):722-731.
67. Zheng P., Wang H., Zhao J., Song L., Qiu L., Dong C., et al. Alectin (CfLec-2) aggregating Staphylococcus haemolyticus from scallop Chlamys farreri. Fish Shellfish Immunol. 2008, 24(3):286-293.
68. Zhu L., Song L., Xu W., Qian P.-Y. Molecular cloning and immune responsive expression of a novel C-type lectin gene from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2008, 25(3):231-238.
69. Zhu L., Song L., Xu W., Qian P.-Y. Identification of a C-type lectin from the bay scallop Argopecten irradians. Mol. Biol. Rep. 2009, 36(5):1167-1173.
70. Kong P., Wang L., Zhang H., Song X., Zhou Z., Yang J., et al. Anovel C-type lectin from bay scallop Argopecten irradians (AiCTL-7) agglutinating fungi with mannose specificity. Fish Shellfish Immunol. 2011, 30(3):836-844.
71. Zhang H., Song X., Wang L., Kong P., Yang J., Liu L., et al. AiCTL-6, a novel C-type lectin from bay scallop Argopecten irradians with a long C-type lectin-like domain. Fish Shellfish Immunol. 2011, 30(1):17-26.
72. Mu C., Song X., Zhao J., Wang L., Qiu L., Zhang H., et al. Ascallop C-type lectin from Argopecten irradians (AiCTL5) with activities of lipopolysaccharide binding and Gram-negative bacteria agglutination. Fish Shellfish Immunol. 2012, 32(5):716-723.
73. Bulet P., Stocklin R., Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004, 198:169-184.
74. Li C., Zhao J., Song L. Areview of advances in research on marine molluscan antimicrobial peptides and their potential application in aquaculture. Molluscan Res. 2009, 29(1):17-26.
75. Zhao J., Song L., Li C., Ni D., Wu L., Zhu L., et al. Molecular cloning, expression of a big defensin gene from bay scallop Argopecten irradians and the antimicrobial activity of its recombinant protein. Mol. Immunol. 2007, 44(4):360-368.
76. Li C., Song L., Zhao J., Zhu L., Zou H., Zhang H., et al. Preliminary study on a potential antibacterial peptide derived from histone H2A in haemocytes of scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 22(6):663-672.
77. Prager E.M., Jolles P. Animal lysozymes c and g: an overview. EXS 1996, 75:9-31.
78. Bachali S., Jager M., Hassanin A., Schoentgen F., Jolles P., Fiala-Medioni A., et al. Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function. J.Mol. Evol. 2002, 54(5):652-664.
79. Zhao J., Song L., Li C., Zou H., Ni D., Wang W., et al. Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol. Immunol. 2007, 44(6):1198-1208.
80. Li L., Zhao J., Wang L., Qiu L., Song L. Genomic organization, polymorphisms and molecular evolution of the goose-type lysozyme gene from Zhikong scallop Chlamys farreri. Gene 2013, 513(1):40-52.
81. Li L., Zhao J., Wang L., Qiu L., Zhang H., Dong C., et al. The polymorphism of lysozyme gene in Zhikong scallop (Chlamys farreri) and its association with susceptibility/resistance to Listonella anguillarum. Fish Shellfish Immunol. 2009, 27(2):136-142.
82. Aguirre J., M M., Hewitt D., Hansberg W. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 2005, 13:111-118.
83. Winston G.W. Oxidants and antioxidants in aquatic animals. Comp. Biochem. Physiol. C 1991, 100(1-2):173-176.
84. Bao Y., Li L., Zhang G. Polymorphism of the superoxide dismutase gene family in the bay scallop (Argopecten irradians) and its association with resistance/susceptibility to Vibrio anguillarum. Dev. Comp. Immunol. 2010, 34(5):553-561.
85. Jiang B., Bao X., Zhang M., Gao X., Li Y., Liu W. Cu/Zn superoxide dismutase and its transcription expression analysis in Mizuhopecten yessoensis. Biotechnol. Bull. 2011, (12):150-156.
86. Ni D., Song L., Gao Q., Wu L., Yu Y., Zhao J., et al. The cDNA cloning and mRNA expression of cytoplasmic Cu, Zn superoxide dismutase (SOD) gene in scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 23(5):1032-1042.
87. Cong M., Song L., Wang L., Zhao J., Qiu L., Li L., et al. The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151(2):191-196.
88. Mu C., Ni D., Zhao J., Wang L., Song L., Li L., et al. cDNA cloning and mRNA expression of a selenium-dependent glutathione peroxidase from Zhikong scallop Chlamys farreri. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 157(2):182-188.
89. Bao Y., Li L., Zhang G. The manganese superoxide dismutase gene in bay scallop Argopecten irradians: cloning, 3D modelling and mRNA expression. Fish Shellfish Immunol. 2008, 25(4):425-432.
90. Wang L., Qiu L., Zhou Z., Song L. Research progress on the mollusc immunity in China. Dev. Comp. Immunol. 2013, 39(1-2):2-10.
91. Xing J., Lin T., Zhan W. Variations of enzyme activities in the haemocytes of scallop Chlamys farreri after infection with the acute virus necrobiotic virus (AVNV). Fish Shellfish Immunol. 2008, 25(6):847-852.
92. Wang L., Yang C., Song L. The molluscan HSP70s and their expression in haemocytes. Invertebr. Surviv. J. 2013, 10:77-83.
93. Ivanina A.V., Taylor C., Sokolova I.M. Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters Crassostrea virginica (Gmelin). Aquat. Toxicol. 2009, 91(3):245-254.
94. Pantzartzi C.N., Kourtidis A., Drosopoulou E., Yiangou M., Scouras Z.G. Isolation and characterization of two cytoplasmic hsp90s from Mytilus galloprovincialis (Mollusca: Bivalvia) that contain a complex promoter with a p53 binding site. Gene 2009, 431(1-2):47-54.
95. Yang C., Zhang L., Wang L., Zhang H., Qiu L., Siva V.S., et al. The Gln32Lys polymorphism in HSP22 of Zhikong scallop Chlamys farreri is associated with heat tolerance. PLoS One 2011, 6(12):e28564.
96. Yang C., Wang L., Liu C., Zhou Z., Zhao X., Song L. The polymorphisms in the promoter of HSP90 gene and their association with heat tolerance of bay scallop. Cell. Stress Chaperones 2015, 20(2):297-308.
97. Yang C., Wang L., Wang J., Jiang Q., Qiu L., Zhang H., et al. The polymorphism in the promoter of HSP70 gene is associated with heat tolerance of two congener endemic bay scallops (Argopecten irradians irradians and A.i. concentricus). PLoS One 2014, 9(7):e102332.
98. Vasak M., Meloni G. Chemistry and biology of mammalian metallothioneins. J.Biol. Inorg. Chem. 2011, 16(7):1067-1078.
99. Wang L., Song L., Ni D., Zhang H., Liu W. Alteration of metallothionein mRNA in bay scallop Argopecten irradians under cadmium exposure and bacteria challenge. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2009, 149(1):50-57.
100. Pan K., Wang W.X. The subcellular fate of cadmium and zinc in the scallop Chlamys nobilis during waterborne and dietary metal exposure. Aquat. Toxicol. 2008, 90(4):253-260.
101. Metian M., Warnau M., Cosson R.P., Oberhansli F., Bustamante P. Bioaccumulation and detoxification processes of Hg in the king scallop Pecten maximus: field and laboratory investigations. Aquat. Toxicol. 2008, 90(3):204-213.
102. Quinn B., Gagne F., Weber J.P., Blaise C. Ecotoxicological effects of a semi-submerged municipal dump (Castle harbour, Bermuda) on the Calico scallop Argopecten gibbus. Mar. Pollut. Bull. 2005, 51(5-7):534-544.
103. Yang C., Wang L., Jiang Q., Wang J., Yue F., Zhang H., et al. The polymorphism in the promoter region of metallothionein 1 is associated with heat tolerance of scallop Argopecten irradians. Gene 2013, 526(2):429-436.
104. Wang M., Wang L., Guo Y., Zhou Z., Yi Q., Zhang D., et al. Ahigh mobility group box 1 (HMGB1) gene from Chlamys farreri and the DNA-binding ability and pro-inflammatory activity of its recombinant protein. Fish Shellfish Immunol. 2014, 36(2):393-400.
105. Pauletto M., Milan M., Babbucci M., Figueras A., Novoa B., Balseiro P., et al. Transcriptome analysis of Pecten maximus haemocytes. Fish Shellfish Immunol. 2013, 34(6):1671.
106. Meng X.L., Tian X., Liu M., Nie G.X., Jiang K.Y., Wang B.J., et al. The transcriptomic response to copper exposure by the gill tissue of Japanese scallops (Mizuhopecten yessoensis) using deep-sequencing technology. Fish Shellfish Immunol. 2014, 38(2):287-293.
107. Sun Z., Yang C., Wang L., Wang X., Wang J., Yue F., et al. The protein expression profile in hepatopancreas of scallop Chlamys farreri under heat stress and Vibrio anguillarum challenge. Fish Shellfish Immunol. 2014, 36(1):252-260.
108. Xing J., Zhan W.B., Zhou L. Endoenzymes associated with haemocyte types in the scallop (Chlamys farreri). Fish Shellfish Immunol. 2002, 13(4):271-278.
109. Wang X., Wang L., Zhang H., Ji Q., Song L., Qiu L., et al. Immune response and energy metabolism of Chlamys farreri under Vibrio anguillarum challenge and high temperature exposure. Fish Shellfish Immunol. 2012, 33(4):1016-1026.
110. Liu R., Qiu L., Yu Z., Zi J., Yue F., Wang L., et al. Identification and characterisation of pathogenic Vibrio splendidus from Yesso scallop (Patinopecten yessoensis) cultured in a low temperature environment. J.Invertebr. Pathol. 2013, 114(2):144-150.
111. Hannam M.L., Bamber S.D., Moody J.A., Galloway T.S., Jones M.B. Immune function in the Arctic Scallop, Chlamys islandica, following dispersed oil exposure. Aquat. Toxicol. 2009, 92(3):187-194.
112. Hannam M.L., Bamber S.D., Moody A.J., Galloway T.S., Jones M.B. Immunotoxicity and oxidative stress in the Arctic scallop Chlamys islandica: effects of acute oil exposure. Ecotoxicol. Environ. Saf. 2010, 73(6):1440-1448.
113. Zapata M., Tanguy A., David E., Moraga D., Riquelme C. Transcriptomic response of Argopecten purpuratus post-larvae to copper exposure under experimental conditions. Gene 2009, 442(1-2):37-46.
114. Zhang H., Zhou Z., Yue F., Wang L., Yang C., Wang M., et al. The modulation of catecholamines on immune response of scallop Chlamys farreri under heat stress. Gen. Comp. Endocrinol. 2014, 195:116-124.
115. Liu J., Pan L.Q., Zhang L., Miao J., Wang J. Immune responses, ROS generation and the haemocyte damage of scallop Chlamys farreri exposed to Aroclor 1254. Fish Shellfish Immunol. 2009, 26(3):422-428.
116. Hannam M.L., Bamber S.D., Galloway T.S., John Moody A., Jones M.B. Effects of the model PAH phenanthrene on immune function and oxidative stress in the haemolymph of the temperate scallop Pecten maximus. Chemosphere 2010, 78(7):779-784.
117. Zhou Z., Wang L., Shi X., Zhang H., Gao Y., Wang M., et al. The modulation of catecholamines to the immune response against bacteria Vibrio anguillarum challenge in scallop Chlamys farreri. Fish Shellfish Immunol. 2011, 31(6):1065-1071.
118. Rosales C. Phagocytosis, a cellular immune response in insects. Invertebr. Surviv. J. 2011, 8:109-131.
119. Mortensen S.H., Glette J. Phagocytic activity of scallop (Pecten maximus) haemocytes maintained invitro. Fish Shellfish Immunol. 1996, 6(2):111-121.
120. Wang L., Gao Q., Shi F., Yang C., Qiu L., Zhang H., et al. The comparative study of immunity between two scallop species Chlamys farreri and Argopecten irradians. Invertebr. Surviv. J. 2013, 10(141-150).
121. Jiang Q., Zhou Z., Wang L., Shi X., Wang J., Yue F., et al. The immunomodulation of inducible nitric oxide in scallop Chlamys farreri. Fish Shellfish Immunol. 2013, 34(1):100-108.
122. Estrada N., Ascencio F., Shoshani L., Contreras R.G. Apoptosis of haemocytes from lions-paw scallop Nodipecten subnodosus induced with paralyzing shellfish poison from Gymnodinium catenatum. Immunobiology 2014, 219(12):964-974.
123. Zhou Z., Yang J., Wang L., Zhang H., Gao Y., Shi X., et al. Adopa decarboxylase modulating the immune response of scallop Chlamys farreri. Plos One 2011, 6(4):e18596.
124. Turvey S.E., Broide D.H. Innate immunity. J.Allergy Clin. Immunol. 2010, 125:S24-S32.
125. Sadd B.M., Schmid-Hempel P. Insect immunity shows specificity in Protection upon secondary pathogen exposure. Curr. Biol. 2006, 16:1206-1210.
126. Cong M., Song L., Qiu L., Li C., Wang B., Zhang H., et al. The expression of peptidoglycan recognition protein-S1 gene in the scallop Chlamys farreri was enhanced after a second challenge by Listonella anguillarum. J.Invertebr. Pathol. 2009, 100(2):120-122.
127. Wang J., Wang L., Yang C., Jiang Q., Zhang H., Yue F., et al. The response of mRNA expression upon secondary challenge with Vibrio anguillarum suggests the involvement of C-lectins in the immune priming of scallop Chlamys farreri. Dev. Comp. Immunol. 2013, 40(2):142-147.
128. Pham L.N., Dionne M.S., Shirasu-Hiza M., Schneider D.S. Aspecific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 2007, 3(3):e26.
129. Zhang T., Qiu L., Sun Z., Wang L., Zhou Z., Liu R., et al. The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev. Comp. Immunol. 2014, 45(1):141-150.
130. Hanington P.C., Forys M.A., Dragoo J.W., Zhang S.M., Adema C.M., Loker E.S. Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(49):21087-21092.
131. Hartenstein V. The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J.Endocrinol. 2006, 190(3):555-570.
132. Ottaviani E., Malagoli D., Franchini A. Invertebrate humoral factors: cytokines as mediators of cell survival. Prog. Mol. Subcell. Biol. 2004, 34:1-25.
133. Zhou Z., Wang L., Shi X., Yue F., Wang M., Zhang H., et al. The expression of dopa decarboxylase and dopamine beta hydroxylase and their responding to bacterial challenge during the ontogenesis of scallop Chlamys farreri. Fish Shellfish Immunol. 2012, 33(1):67-74.
134. Zhou Z., Wang L., Wang M., Zhang H., Wu T., Qiu L., et al. Scallop phenylalanine hydroxylase implicates in immune response and can be induced by human TNF-α. Fish Shellfish Immunol. 2011, 31(6):856-863.
135. Zhou Z., Wang L., Yang J., Zhang H., Kong P., Wang M., et al. Adopamine beta hydroxylase from Chlamys farreri and its induced mRNA expression in the haemocytes after LPS stimulation. Fish Shellfish Immunol. 2011, 30(1):154-162.
136. Zhou Z., Wang L., Gao Y., Wang M., Zhang H., Qiu L., et al. Amonoamine oxidase from scallop Chlamys farreri serving as an immunomodulator in response against bacterial challenge. Dev. Comp. Immunol. 2011, 35(7):799-807.
137. Tracey K.J. The inflammatory reflex. Nature 2002, 420(6917):853-859.
138. Rand J.B. Acetylcholine. WormBook 2007, 1-21.
139. Burbring E., Burn J.H., Shelley H.J. Acetylcholine and ciliary movement in the gill plates of Mytilus edulis. Proc. R. Soc. Lond. B Biol. Sci. 1953, 141(905):445-466.
140. Sattelle D.B. Invertebrate nicotinic acetylcholine receptors-targets for chemicals and drugs important in agriculture, veterinary medicine and human health. J.Pesticide Sci. 2009, 34(4):233-240.
141. Shi X., Zhou Z., Wang L., Yue F., Wang M., Yang C., et al. The immunomodulation of acetylcholinesterase in zhikong scallop Chlamys farreri. PLoS One 2012, 7(1):e30828.
142. Shi X., Wang L., Zhou Z., Liu R., Li Y., Song L. Acetylcholine modulates the immune response in Zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2014, 38(1):204-210.
143. Jiang Q., Zhou Z., Wang L., Wang L., Yue F., Wang J., et al. Ascallop nitric oxide synthase (NOS) with structure similar to neuronal NOS and its involvement in the immune defense. PLoS One 2013, 8(7):e69158.
144. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2001, 2(10):907-916.
145. Koutsogiannaki S., Kaloyianni M. Signaling molecules involved in immune responses in mussels. Isj-Invertebrate Surviv. J. 2010, 7(1):11-21.
146. Villamil L., Gomez-Leon J., Gomez-Chiarri M. Role of nitric oxide in the defenses of Crassostrea virginica to experimental infection with the protozoan parasite Perkinsus marinus. Dev. Comp. Immunol. 2007, 31(10):968-977.
147. Jeffroy F., Paillard C. Involvement of nitric oxide in the invitro interaction between Manila clam, Ruditapes philippinarum, haemocytes and the bacterium Vibrio tapetis. Fish Shellfish Immunol. 2011, 31(6):1137-1141.
148. Sun Z., Jiang Q., Wang L., Zhou Z., Wang M., Yi Q., et al. The comparative proteomics analysis revealed the modulation of inducible nitric oxide on the immune response of scallop Chlamys farreri. Fish Shellfish Immunol. 2014, 40(2):584-594.
149. Wright B., Lacchini A.H., Davies A.J., Walker A.J. Regulation of nitric oxide production in snail (Lymnaea stagnalis) defence cells: a role for PKC and ERK signalling pathways. Biol. Cell. 2006, 98(5):265-278.
150. Barcia R., Ramos-Martinez J. Effects of interleukin-2 on nitric oxide production in molluscan innate immunity. INV Surv. J. 2008, 5:43-49.
151. de Barros C.M., Mello Ade A., Allodi S. Norepinephrine depresses the nitric oxide production in the ascidian haemocytes. J.Invertebr. Pathol. 2012, 111(2):182-185.
152. Jiang Q., Zhou Z., Wang L., Yang C., Wang J., Wu T., et al. Mutual modulation between norepinephrine and nitric oxide in haemocytes during the mollusc immune response. Sci. Rep. 2014, 4:6963.
153. Isayama T., Mclaughlin P.J., Zagon I.S. Endogenous opioids regulate cell-proliferation in the retina of developing rat. Brain Res. 1991, 544(1):79-85.
154. Murgo A.J. Inhibition of B16-Bl6 Melanoma growth in mice by methionine-enkephalin. J.Natl. Cancer Inst. 1985, 75(2):341-344.
155. Stefano G.B., Leung M.K., Bilfinger T.V., Scharrer B. Effect of prolonged exposure to morphine on responsiveness of human and invertebrate immunocytes to stimulatory molecules. J.Neuroimmunol. 1995, 63(2):175-181.
156. van Rijn R.M., Defriel J.N., Whistler J.L. Pharmacological traits of delta opioid receptors: pitfalls or opportunities?. Psychopharmacol. Berl. 2013, 228(1):1-18.
157. Guo Y., Wang L., Zhou Z., Wang M., Liu R., Wang L., et al. An opioid growth factor receptor (OGFR) for [Met5]-enkephalin in Chlamys farreri. Fish Shellfish Immunol. 2013, 34(5):1228-1235.
158. Song X., Wang L., Song L., Zhao J., Zhang H., Zheng P., et al. Acyclophilin A inducible expressed in gonad of zhikong scallop Chlamys farreri. Mol. Biol. Rep. 2009, 36(6):1637-1645.
159. Zhang L., Wang L., Zhao J., Qiu L., Song L., Dong C., et al. The responsive expression of heat shock protein 22 gene in zhikong scallop Chlamys farreri against a bacterial challenge. Aquac. Res. 2010, 41(2):257-266.
160. Zhang H., Kong P., Wang L., Zhou Z., Yang J., Zhang Y., et al. Cflec-5, a pattern recognition receptor in scallop Chlamys farreri agglutinating yeast Pichia pastoris. Fish Shellfish Immunol. 2010, 29(1):149-156.
161. Wang J., Zhang H., Wang L., Qiu L., Yue F., Yang C., et al. Molecular cloning and transcriptional regulation of an allograft inflammatory factor-1 (AIF-1) in Zhikong scallop Chlamys farreri. Gene 2013, 530(2):178-184.
162. Bao Y., Li L., Xu F., Zhang G. Intracellular copper/zinc superoxide dismutase from bay scallop Argopecten irradians: Its gene structure, mRNA expression and recombinant protein. Fish shellfish Immunol. 2009, 27(2):210-220.
163. Bao Y., Li L., Wu Q., Zhang G. Cloning, characterization, and expression analysis of extracellular copper/zinc superoxide dismutase gene from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2009, 27(1):17-25.
164. Li F., Huang S., Wang L., Yang J., Zhang H., Qiu L., et al. Amacrophage migration inhibitory factor like gene from scallop Chlamys farreri: Involvement in immune response and wound healing. Dev. Comp. Immunol. 2011, 35(1):62-71.
165. He X., Zhang Y., Wu X., Xiao S., Yu Z. Cloning and characterization of two ferritin subunit genes from bay scallop, Argopecten irradians (Lamarck 1819). Mol. Biol. Reports 2011, 38(3):2125-2132.
166. Li J., Li L., Zhang S., Zhang G. Cloning, genomic structure, and expression analysis of peroxiredoxin V from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2011, 30(1):309-316.
167. Li J., Li L., Zhang S., Li J., Zhang G. Three ferritin subunits involved in immune defense from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2012, 32(2):368-372.
168. Wu T., Shi X., Zhou Z., Wang L., Wang M., Wang L., et al. An iodothyronine deiodinase from Chlamys farreri and its induced mRNA expression after LPS stimulation. Fish Shellfish Immunol. 2012, 33(2):286-293.
169. Yue F., Zhou Z., Wang L., Sun R., Jiang Q., Yi Q., et al. The essential roles of core binding factors CfRunt and CfCBFβ in haemocyte production of scallop Chlamys farreri. Dev. Comp. Immunol. 2014, 44(2):291-302.
170. Liu R., Wang L., Sun Y., Wang L., Zhang H., Song L. Alow-density lipoprotein receptor-related protein (LRP)-like molecule identified from Chlamys farreri participated in immune response against bacterial infection. Fish Shellfish Immunol. 2014, 36(2):336-343.
171. Bao Y., Li L., Xu F., Zhang G. Intracellular copper/zinc superoxide dismutase from bay scallop Argopecten irradians: its gene structure, mRNA expression and recombinant protein. Fish Shellfish Immunol. 2009, 27(2):210-220.
172. Cong M., Ni D., Song L., Wang L., Zhao J., Qiu L., et al. Molecular cloning, characterization and mRNA expression of peroxiredoxin in Zhikong scallop Chlamys farreri. Mol. Biol. Rep. 2009, 36(6):1451-1459.
173. Li C., Ni D., Song L., Zhao J., Zhang H., Li L. Molecular cloning and characterization of a catalase gene from Zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2008, 24(1):26-34.
174. Zhou Z., Ni D., Wang M., Wang L., Shi X., Yue F., et al. The phenoloxidase activity and antibacterial function of a tyrosinase from scallop Chlamys farreri. Fish Shellfish Immunol. 2012, 33(2):375-381.
175. Wu L., Song L., Xu W., Qiu L., Li H., Su J., et al. The cloning and characterization of heat shork protein 70 in zhikong scallop Chlamys farreri. High. Technol. Lett. 2003, 11:75-79.
176. Gao Q., Song L., Ni D., Wu L., Zhang H., Chang Y. cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 147(4):704-715.
177. Zhang L., Wang L., Song L., Zhao J., Qiu L., Dong C., et al. The involvement of HSP22 from bay scallop Argopecten irradians in response to heavy metal stress. Mol. Biol. Rep. 2010, 37(4):1763-1771.
178. Song L., Wu L., Ni D., Chang Y., Xu W., Xing K. The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish Shellfish Immunol. 2006, 21(4):335-345.
179. Gao Q., Zhao J., Song L., Qiu L., Yu Y., Zhang H., et al. Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish Shellfish Immunol. 2008, 24(4):379-385.
180. Song L., Zou H., Chang Y., Xu W., Wu L. The cDNA cloning and mRNA expression of a potential selenium-binding protein gene in the scallop Chlamys farreri. Dev. Comp. Immunol. 2006, 30(3):265-273.
181. Yang C., Wang L., Siva V.S., Shi X., Jiang Q., Wang J., et al. Anovel cold-regulated cold shock domain containing protein from scallop Chlamys farreri with nucleic acid-binding activity. PLoS One 2012, 7(2):e32012.