Maternal immune transfer in mollusc

Developmental and Comparative Immunology

Volumn 48, Issue 2, 2015, Pages 354-359

  Wang, Lingling ^a   Yue, Feng ^a   Song, Xiaorui ^a   Song, Linsheng ^a  

^a INSTITUTE OF OCEANOLOGY   (China)

Author keywords

Egg; Immune factors; Maternal immunity; Mollusc; Trans generational effect

Indexed keywords

ANTIBODY; BETA 1,3 GLUCAN; CATALASE; COMPLEMENT COMPONENT C1Q; HEAT SHOCK PROTEIN 70; LECTIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; LYSOZYME; MONOPHENOL MONOOXYGENASE; N ACETYLGALACTOSAMINE; PATTERN RECOGNITION RECEPTOR; SCAVENGER RECEPTOR; SUPEROXIDE DISMUTASE; VITELLOGENIN; IMMUNOLOGIC FACTOR;

ARTICLE; CROSS PRESENTATION; ENVIRONMENTAL EXPOSURE; IMMUNE RESPONSE; IMMUNITY; INNATE IMMUNITY; LARVAL DEVELOPMENT; MATERNAL NUTRITION; MOLLUSC; NONHUMAN; PASSIVE IMMUNIZATION; PREGNANCY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VERTICAL TRANSMISSION; VITELLOGENESIS; ANIMAL; FEMALE; IMMUNOLOGY; METABOLISM;

MOLLUSCA;

ANIMALS; FEMALE; IMMUNITY, MATERNALLY-ACQUIRED; IMMUNOLOGIC FACTORS; MOLLUSCA;

EID: 84918513258     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2014.05.010     Document Type: Article

References (111)

1. Arason G.J. Lectins as defence molecules in vertebrates and invertebrates. Fish Shellfish Immunol. 1996, 6:277-289.
2. Bai G., Brown J.F., Watson C., Yoshino T.P. Isolation and characterization of phenoloxidase from egg masses of the gastropod mollusc, Biomphalaria glabrata. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1997, 118:463-469.
3. Beasley R.P., Lee C.Y., Roan C.H., Hwang L.Y., Lan C.C., Huang F.Y., Chen C.L. Prevention of perinatally transmitted hepatitis B virus infections with hepatitis B immune globulin and hepatitis B vaccine. Lancet 1983, 322:1099-1102.
4. Benkendorff K., Davis A.R., Bremner J.B. Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. J. Invertebr. Pathol. 2001, 78:109-118.
5. Canesi L., Gallo G., Gavioli M., Pruzzo C. Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc. Res. Tech. 2002, 57:469-476.
6. Chen H., Mai K.S., Zhang W.B., Liufu Z.G., Xu W., Tan B.P. Effects of dietary pyridoxine on immune responses in abalone, Haliotis discus hannai Ino. Fish Shellfish Immunol. 2005, 19:241-252.
7. Chucri T.M., Monteiro J.M., Lima A.R., Salvadori M.L.B., Junior J.R., Miglino M.A. A review of immune transfer by the placenta. J. Reprod. Immunol. 2010, 87:14-20.
8. Cong M., Song L., Wang L., Zhao J., Qiu L., Li L., Zhang H. The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151:191-196.
9. Corporeau C., Vanderplancke G., Boulais M., Suquet M., Quéré C., Boudry P., Huvet A., Madec S. Proteomic identification of quality factors for oocytes in the Pacific oyster Crassostrea gigas. J. Proteomics 2012, 75:5554-5563.
10. Curley J.P., Mashoodh R., Champagne F.A. Epigenetics and the origins of paternal effects. Horm. Behav. 2011, 59:306-314.
11. Dang V.T., Li Y., Speck P., Benkendorff K. Effects of micro and macroalgal diet supplementations on growth and immunity of greenlip abalone, Haliotis laevigata. Aquaculture 2011, 320:91-98.
12. Ding J., Li J., Bao Y., Li L., Wu F., Zhang G. Molecular characterization of a mollusk chicken-type lysozyme gene from Haliotis discus hannai Ino, and the antimicrobial activity of its recombinant protein. Fish Shellfish Immunol. 2011, 30:163-172.
13. Ding Y., Liu X., Bu L., Li H., Zhang S. Antimicrobial-immunomodulatory activities of zebrafish phosvitin-derived peptide Pt5. Peptides 2012, 37:309-313.
14. Diz A.P., Dudley E., Cogswell A., MacDonald B.W., Kenchington E.L., Zouros E., Skibinski D.O. Proteomic analysis of eggs from Mytilus edulis females differing in mitochondrial DNA transmission mode. Mol. Cell. Proteomics 2013, 12:3068-3080.
15. Dreon M., Lavarias S., Garin C., Heras H., Pollero R. Synthesis, distribution, and levels of an egg lipoprotein from the apple snail Pomacea canaliculata (Mollusca: Gastropoda). J. Exp. Zool. 2002, 292:323-330.
16. Duchemin M.B., Fournier M., Auffret M. Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg). Aquaculture 2007, 264:73-81.
17. Ehrlich P. Ueber immunität durch vererbung und säugung. Z. Hyg. Infektionskrankheiten 1892, 12:183-203.
18. Elsbach P., Weiss J. Role of the bactericidal/permeability-increasing protein in host defence. Curr. Opin. Immunol. 1998, 10:45-49.
19. Elsbach P., Weiss J., Levy O. Integration of antimicrobial host defenses: role of the bactericidal/permeability-increasing protein. Trends Microbiol. 1994, 2:324-328.
20. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
21. Fiolka M.J., Witkowski A. Lysozyme-like activity in eggs and in some tissues of land snails Helix aspersa maxima and Achatina achatina. Folia Biol. 2004, 52:3-4.
22. Garnier R., Boulinier T., Gandon S. Coevolution between maternal transfer of immunity and other resistance strategies against pathogens. Evolution 2012, 66:3067-3078.
23. Gonzalez M., Gueguen Y., Destoumieux-Garzón D., Romestand B., Fievet J., Pugnière M., Roquet F., Escoubas J.M., Vandenbulcke F., Levy O. Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. Proc. Natl. Acad. Sci. 2007, 104:17759-17764.
24. Gopalakrishnan S., Thilagam H., Huang W.B., Wang K.J. Immunomodulation in the marine gastropod Haliotis diversicolor exposed to benzo (a) pyrene. Chemosphere 2009, 75:389-397.
25. Gueguen Y., Cadoret J.P., Flament D., Barreau Roumiguière C., Girardot A.L., Garnier J., Hoareau A., Bachère E., Escoubas J.M. Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 2003, 303:139-145.
26. Hathaway J.J., Adema C.M., Stout B.A., Mobarak C.D., Loker E.S. Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca). Dev. Comp. Immunol. 2010, 34:425-435.
27. Herpin A., Favrel P., Cunningham C. Gene structure and expression of cg-ALR1, a type I activin-like receptor from the bivalve mollusc Crassostrea gigas. Gene 2002, 301:21-30.
28. Huang C., Song Y. Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev. Comp. Immunol. 1999, 23:545-552.
29. Ituarte S., Dreon M.S., Ceolin M., Heras H. Agglutinating activity and structural characterization of scalarin, the major egg protein of the snail Pomacea scalaris (d'Orbigny, 1832). PLoS One 2012, 7:e50115.
30. Izquierdo M.S., Fernandez-Palacios H., Tacon A.G.J. Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 2001, 197:25-42.
31. Janeway C.A., Medzhitov R. Innate immune recognition. Sci. Signal. 2002, 20:197-216.
32. Jimbo M., Nakanishi F., Sakai R., Muramoto K., Kamiya H. Characterization of L-amino acid oxidase and antimicrobial activity of aplysianin A, a sea hare derived antitumor-antimicrobial protein. Fish. Sci. 2003, 69:1240-1246.
33. Jiménez de Oya N., Alonso-Padilla J., Blázquez A.B., Escribano-Romero E., Escribano J.M., Saiz J.C. Maternal transfer of antibodies to the offspring after mice immunization with insect larvae-derived recombinant hepatitis E virus ORF-2 proteins. Virus Res. 2011, 158:28-32.
34. Jung Y., Nowak T.S., Zhang S.M., Hertel L.A., Loker E.S., Adema C.M. Manganese superoxide dismutase from Biomphalaria glabrata. J. Invertebr. Pathol. 2005, 90:59-63.
35. Kamiya H., Shimizu Y. A natural agglutinin inhibitable by d-galacturonic acid in the sea hare Aplysia eggs: characterization and purification. Bull. Jpn. Soc. Sci. Fish. 1981, 47:255-259.
36. Kamiya H., Muramoto K., Yamazaki M. Aplysianin-A, an antibacterial and antineoplastic glycoprotein in the albumen gland of a sea hare, Aplysia kurodai. Experientia 1986, 42:1065-1067.
37. Kawsar S.M., Matsumoto R., Fujii Y., Yasumitsu H., Dogasaki C., Hosono M., Nitta K., Hamako J., Matsui T., Kojima N. Purification and biochemical characterization of a d-galactose binding lectin from Japanese sea hare (Aplysia kurodai) eggs. Biochemistry (Moscow) 2009, 74:709-716.
38. Kawsar S.M., Mamun S.M., Rahman M.S., Yasumitsu H., Ozeki Y. Growth inhibitory effects on microorganisms by a d-galactose-binding lectin purified from the sea hare (Aplysia kurodai) eggs: an in vitro study. Nat. Sci. 2010, 8:82-89.
39. Kim Y.S., Yoo H.S., Ko J.H. Implication of aberrant glycosylation in cancer and use of lectin for cancer biomarker discovery. Protein Pept. Lett. 2009, 16:499-507.
40. Kisugi J., Kamiya H., Yamazaki M. Purification and characterization of aplysianin E, an antitumor factor from sea hare eggs. Cancer Res. 1987, 47:5649-5653.
41. Kisugi J., Ohye H., Kamiya H., Yamazaki M. Biopolymers from marine invertebrates. X. Mode of action of an antibacterial glycoprotein, aplysianin E, from eggs of a sea hare, Aplysia kurodai. Chem. Pharm. Bull. 1989, 37:3050-3053.
42. Köhler W., Prokop O. Agglutination of streptococci of the group C by an agglutinin from Helix pomatia. Z. Immunitatsforsch. Allerg. Klin. Immunol. 1967, 133:50-53.
43. Köhler W., Prokop O., Kühnemund O. Routine identification of group-C streptococci by means of an agglutinin (protectin) from the albumen gland of the edible snail, Helix pomatia. J. Med. Microbiol. 1973, 6:127-130.
44. Lacoste A., Malham S.K., Gélébart F., Cueff A., Poulet S.A. Stress-induced immune changes in the oyster Crassostrea gigas. Dev. Comp. Immunol. 2002, 26:1-9.
45. Leicht K., Jokela J., Seppälä O. An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecol. Evol. 2013, 3:4861-4871.
46. Levenson J.M., Sweatt J.D. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6:108-118.
47. 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, 24:26-34.
48. Li Z., Zhang S., Liu Q. Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity. PLoS One 2008, 3:e1940.
49. Li C., Sun H., Chen A., Ning X., Wu H., Qin S., Xue Q., Zhao J. Identification and characterization of an intracellular Cu, Zn-superoxide dismutase (icCu/Zn-SOD) gene from clam Venerupis philippinarum. Fish Shellfish Immunol. 2010, 28:499-503.
50. Lijima R., Kisugi J., Yamazaki M. Antifungal activity of Aplysianin E, A cytotoxic protein of sea hare (Aplysia kurodai) eggs. Dev. Comp. Immunol. 1995, 19:13-19.
51. Little T.J., O'Connor B., Colegrave N., Watt K., Read A.F. Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 2003, 13:489-492.
52. Lochmiller R.L., Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos 2000, 88:87-98.
53. 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.
54. Malek A., Sager R., Schneider H. Transport of proteins across the human placenta. Am. J. Reprod. Immunol. 1998, 40:347-351.
55. Mao Y., Zhou C., Zhu L., Huang Y., Yan T., Fang J., Zhu W. Identification and expression analysis on bactericidal permeability-increasing protein (BPI)/lipopolysaccharide-binding protein (LBP) of ark shell, Scapharca broughtonii. Fish Shellfish Immunol. 2013, 35:642-652.
56. Martins E., Queiroz A., Santos R.S., Bettencourt R. Finding immune gene expression differences induced by marine bacterial pathogens in the Deep-sea hydrothermal vent mussel Bathymodiolus azoricus. Biogeosciences 2013, 10:7279-7291.
57. Matés J. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 2000, 153:83-104.
58. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., Bouchut A., Coustau C. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev. Comp. Immunol. 2005, 29:393-407.
59. Moreau J., Martinaud G., Troussard J.P., Zanchi C., Moret Y. Trans-generational immune priming is constrained by the maternal immune response in an insect. Oikos 2012, 121:1828-1832.
60. Morgan H.D., Sutherland H.G., Martin D.I., Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 1999, 23:314-318.
61. Mousseau T.A., Fox C.W. The adaptive significance of maternal effects. Trends Ecol. Evol. 1998, 13:403-407.
62. Osada M., Takamura T., Sato H., Mori K. Vitellogenin synthesis in the ovary of scallop, Patinopecten yessoensis: control by estradiol-17β and the central nervous system. J. Exp. Zoolog. A Comp. Exp. Biol. 2003, 299:172-179.
63. Ottaviani E., Accorsi A., Rigillo G., Malagoli D., Blom J.M., Tascedda F. Epigenetic modification in neurons of the mollusc Pomacea canaliculata after immune challenge. Brain Res. 2013, 1537:18-26.
64. Oubella R., Paillard C., Maes P., Auffret M. Changes in hemolymph parameters in the manila Clam Ruditapes philippinarum (Mollusca, Bivalvia) following bacterial challenge. J. Invertebr. Pathol. 1994, 64:33-38.
65. Patchett R., Kelly A.F., Kroll R. The adsorption of bacteria to immobilized lectins. J. Appl. Microbiol. 1991, 71:277-284.
66. Pipe R.K., Coles J.A. Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol. 1995, 5:581-595.
67. Poorten T.J., Kuhn R.E. Maternal transfer of antibodies to eggs in Xenopus laevis. Dev. Comp. Immunol. 2009, 33:171-175.
68. Portela J., Duval D., Rognon A., Galinier R., Boissier J., Coustau C., Mitta G., Théron A., Gourbal B. Evidence for specific genotype-dependent immune priming in the lophotrochozoan Biomphalaria glabrata snail. J. Innate Immun. 2013, 5:261-276.
69. Poulin R., Thomas F. Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations. Oikos 2008, 117:331-335.
70. Prokop O., Köhler W. Agglutination reactions of micro-organisms with Helix pomatia protein gland extract. (Anti-Ahel-agglutination). Z. Immunitätsforsch. Allerg. klin. Immunol. 1967, 133:176.
71. Prokop O., Uhlenbruck G., Köhler W. A new source of antibody-like substances having anti-blood group specificity: a discussion on the specificity of Helix agglutinins. Vox Sang. 1968, 14:321-333.
72. Ramirez Llodra E. Fecundity and life-history strategies in marine invertebrates. Adv. Mar. Biol. 2002, 43:87-170.
73. Rodrigues J., Brayner F.A., Alves L.C., Dixit R., Barillas-Mury C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010, 329:1353-1355.
74. Roth O., Joop G., Eggert H., Hilbert J., Daniel J., Schmid-Hempel P., Kurtz J. Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 2010, 79:403-413.
75. Rowley A.F., Powell A. Invertebrate immune systems-specific, quasi-specific, or nonspecific?. J. Immunol. 2007, 179:7209-7214.
76. Sadd B.M., Schmid-Hempel P. Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Curr. Biol. 2007, 17:R1046-R1047.
77. Sadd B.M., Kleinlogel Y., Schmid-Hempel R., Schmid-Hempel P. Trans-generational immune priming in a social insect. Biol. Lett. 2005, 1:386-388.
78. Sanchez J.F., Lescar J., Chazalet V., Audfray A., Gagnon J., Alvarez R., Breton C., Imberty A., Mitchell E.P. Biochemical and structural analysis of Helix pomatia agglutinin a hexameric lectic with a novel fold. J. Biol. Chem. 2006, 281:20171-20180.
79. Seppälä O., Jokela J. Maintenance of genetic variation in immune defense of a freshwater snail: role of environmental heterogeneity. Evolution 2010, 64:2397-2407.
80. Sheldon B.C., Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 1996, 11:317-321.
81. Shi X., Zhang S., Pang Q. Vitellogenin is a novel player in defense reactions. Fish Shellfish Immunol. 2006, 20:769-772.
82. Shlichta J.G., Smilanich A.M. Immune responses and their potential role in insect outbreaks. Insect Outbreaks Revisited 2012, 47-70.
83. Shumway S.E., Parsons J.G. Scallops: Biology, Ecology and Aquaculture 2011, Elsevier.
84. Slifkin M., Cumbie R. Rapid detection of herpes simplex virus with fluorescein-labeled Helix pomatia lectin. J. Clin. Microbiol. 1989, 27:1036-1039.
85. Song L., Wang L., Qiu L., Zhang H. Bivalve Immunity, Invertebrate Immunity 2010, Springer, pp. 44-65.
86. Song X., Zhang H., Wang L., Zhao J., Mu C., Song L., Qiu L., Liu X. A galectin with quadruple-domain from bay scallop Argopecten irradians is involved in innate immune response. Dev. Comp. Immunol. 2011, 35:592-602.
87. Sun J., Zhang H., Wang H., Heras H., Dreon M.S., Ituarte S., Ravasi T., Qian P.-Y., Qiu J.-W. First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition. J. Proteome Res. 2012, 11:4240-4248.
88. Swain P., Nayak S. Role of maternally derived immunity in fish. Fish Shellfish Immunol. 2009, 27:89-99.
89. Swain P., Dash S., Bal J., Routray P., Sahoo P., Sahoo S., Saurabh S., Gupta S., Meher P. Passive transfer of maternal antibodies and their existence in eggs, larvae and fry of Indian major carp, Labeo rohita (Ham.). Fish Shellfish Immunol. 2006, 20:519-527.
90. Thomas-Guyon H., Gagnaire B., Bado-Nilles A., Bouilly K., Lapègue S., Renault T. Detection of phenoloxidase activity in early stages of the Pacific oyster Crassostrea gigas (Thunberg). Dev. Comp. Immunol. 2009, 33:653-659.
91. Tirapé A., Bacque C., Brizard R., Vandenbulcke F., Boulo V. Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev. Comp. Immunol. 2007, 31:859-873.
92. Tobias P.S., Soldau K., Iovine N.M., Elsbach P., Weiss J. Lipopolysaccharide (LPS)-binding proteins BPI and LBP form different types of complexes with LPS. J. Biol. Chem. 1997, 272:18682-18685.
93. Triggs A.M., Knell R.J. Parental diet has strong transgenerational effects on offspring immunity. Funct. Ecol. 2012, 26:1409-1417.
94. Uhlenbruck G., Steinhausen G., Cheesman D.F. An incomplete anti-B agglutinin in the eggs of the prosobranch snailPila ovata. Experientia 1973, 29:1139-1140.
95. Wallace R.A. Vitellogenesis and oocyte growth in nonmammalian vertebrates, Oogenesis 1985, Springer, pp. 127-177.
96. Wang L., Song L., Zhao J., Qiu L., Zhang H., Xu W., Li H., Li C., Wu L., Guo X. Expressed sequence tags from the zhikong scallop (Chlamys farreri): discovery and annotation of host-defense genes. Fish Shellfish Immunol. 2009, 26:744-750.
97. Wang W., Mai K., Zhang W., Ai Q., Yao C., Li H., Liufu Z. Effects of dietary copper on survival, growth and immune response of juvenile abalone, Haliotis discus hannai Ino. Aquaculture 2009, 297:122-127.
98. Wang S., Wang Y., Ma J., Ding Y., Zhang S. Phosvitin plays a critical role in the immunity of zebrafish embryos via acting as a pattern recognition receptor and an antimicrobial effector. J. Biol. Chem. 2011, 286:22653-22664.
99. Wang L., Qiu L., Zhou Z., Song L. Research progress on the mollusc immunity in China. Dev. Comp. Immunol. 2012, 39:2-10.
100. Waterland R.A., Jirtle R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 2003, 23:5293-5300.
101. Whyte J., Bourne N., Ginther N. Biochemical and energy changes during embryogenesis in the rock scallop Crassadoma gigantea. Mar. Biol. 1990, 106:239-244.
102. Xu Q., Guo L., Xie J., Zhao C. Relationship between quality of pearl cultured in the triangle mussel Hyriopsis cumingii of different ages and its immune mechanism. Aquaculture 2011, 315:196-200.
103. Xue Q., Schey K.L., Volety A.K., Chu F.L.E., La Peyre J.F. Purification and characterization of lysozyme from plasma of the eastern oyster (Crassostrea virginica). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2004, 139:11-25.
104. 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:e17089.
105. Yue F., Shi X., Zhou Z., Wang L., Wang M., Yang J., Qiu L., Song L. The expression of immune-related genes during the ontogenesis of scallop Chlamys farreri and their response to bacterial challenge. Fish Shellfish Immunol. 2013, 34:855-864.
106. Yue F., Zhou Z., Wang L., Ma Z., Wang J., Wang M., Zhang H., Song L. Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge. Dev. Comp. Immunol. 2013, 41:569-577.
107. Zanchi C., Troussard J.P., Moreau J., Moret Y. Relationship between maternal transfer of immunity and mother fecundity in an insect. Proc. R. Soc. B Biol. Sci. 2012, 279:3223-3230.
108. Zhang S., Long L., Zhou Y., Yin H., Xiao Z., Chen Y. Effects of glycopeptides on development, growth and non-specific immunity of pearl oyster Pinctada fucata (Gould). Aquac. Nutr. 2010, 16:520-527.
109. Zhang S., Wang Z., Wang H. Maternal immunity in fish. Dev. Comp. Immunol. 2013, 39:72-78.
110. Zhao J., Song L., Li C., Zou H., Ni D., Wang W., Xu W. Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol. Immunol. 2007, 44:1198-1208.
111. Zhao J., Qiu L., Ning X., Chen A., Wu H., Li C. Cloning and characterization of an invertebrate type lysozyme from Venerupis philippinarum. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 156:56-60.