Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge

Developmental and Comparative Immunology

Volumn 41, Issue 4, 2013, Pages 569-577

  Yue, Feng ^a,b   Zhou, Zhi ^a   Wang, Lingling ^a   Ma, Zhaopeng ^a   Wang, Jingjing ^a,b   Wang, Mengqiang ^a   Zhang, Huan ^a   Song, Linsheng ^a  

^a INSTITUTE OF OCEANOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Chlamys farreri; Maternal immunity; Ontogeny; Trans generational effect

Indexed keywords

BPI PROTEIN; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; ELONGATION FACTOR 1ALPHA; GBP PROTEIN; LBP PROTEIN; LEC 3 PROTEIN; LYZ PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL IMMUNITY; BACTERICIDAL ACTIVITY; CHLAMYS FARRERI; CONTROLLED STUDY; COPPER ZINC SUPEROXIDE DISMUTASE GENE; DEVELOPMENTAL STAGE; EGG; ELONGATION FACTOR 1ALPHA GENE; EMBRYO; ESCHERICHIA COLI; FEMALE; GENE; IMMUNOCOMPETENCE; IMMUNOSTIMULATION; LARVA; LBP/BPI GENE; LECTIN 3 GENE; LGBP GENE; LISTONELLA ANGUILLARUM; LYSOZYME GENE; MORTALITY; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROGENY; PROTEIN TRANSPORT; TROCHOPHORE;

BACTERIA (MICROORGANISMS); CHLAMYS FARRERI; ESCHERICHIA COLI; FUNGI; NEGIBACTERIA; PECTINIDAE; PICHIA PASTORIS;

CHLAMYS FARRERI; MATERNAL IMMUNITY; ONTOGENY; TRANS-GENERATIONAL EFFECT;

ANIMALS; BACTERIAL INFECTIONS; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOLOGIC FACTORS; OVUM; PECTINIDAE; PICHIA; PROTEINS; RNA, MESSENGER;

EID: 84883441870     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.07.001     Document Type: Article

References (63)

1. 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(2):109-118.
2. Bly J.E., Grimm A., Morris I. Transfer of passive immunity from mother to young in a teleost fish: Haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L. Comp. Biochem. Physiol. A Physiol. 1986, 84(2):309-313.
3. Boots M., Roberts K.E. Maternal effects in disease resistance: poor maternal environment increases offspring resistance to an insect virus. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2012, 279(1744):4009-4014.
4. Chucri T.M., Monteiro J., Lima A., Salvadori M., Junior J., Miglino M.A. A review of immune transfer by the placenta. J. Reprod. Immunol. 2010, 87(1):14-20.
5. Ciacci C., Citterio B., Betti M., Canonico B., Roch P., Canesi L. Functional differential immune responses of Mytilus galloprovincialis to bacterial challenge. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2009, 153(4):365-371.
6. 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(2):191-196.
7. Curley J.P., Mashoodh R., Champagne F.A. Epigenetics and the origins of paternal effects. Horm. Behav. 2011, 59(3):306-314.
8. Elsbach P., Weiss J. The bactericidal/permeability-increasing protein (BPI), a potent element in host-defense against gram-negative bacteria and lipopolysaccharide. Immunobiology 1993, 187(3):417-429.
9. Esteves E., Fogaça A., Maldonado R., Silva F., Manso P., Pelajo-Machado M., Valle D., Daffre S. Antimicrobial activity in the tick Rhipicephalus (Boophilus) microplus eggs: cellular localization and temporal expression of microplusin during oogenesis and embryogenesis. Dev. Comp. Immunol. 2009, 33(8):913-919.
10. Fernandez-Sousa J.M., Gavilanes J.G., Municio A.M., Perez-Aranda A., Roderiguez R. Lysozyme from the insect Ceratitis capitata eggs. Eur. J. Biochem. 2008, 72(1):25-33.
11. 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. USA 2007, 104(45):17759-17764.
12. Grindstaff J.L., Brodie E.D., Ketterson E.D. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2003, 270(1531):2309-2319.
13. Groothuis T.G.G., Müller W., von Engelhardt N., Carere C., Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 2005, 29(2):329-352.
14. Hamal K., Burgess S., Pevzner I., Erf G. Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poult. Sci. 2006, 85(8):1364-1372.
15. Hanif A. Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish Shellfish Immunol. 2004, 17(5):411-435.
16. Hasan I., Kabir S.R., Haque M.A., Absar N. Biochemical analysis and physico chemical stability of a partially purified lectin from hilsha eggs. J. Bio-Sci. 2009, 17:35-40.
17. Hathaway J.J.M., 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(4):425-435.
18. Huang C., Song Y. Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev. Comp. Immunol. 1999, 23(7-8):545-552.
19. Huttenhuis H., Grou C., Tavernethiele A., Taverne N., Rombout J. Carp (Cyprinus carpio L.) innate immune factors are present before hatching. Fish Shellfish Immunol. 2006, 20(4):586-596.
20. Kamiya H., Muramoto K., Ogata K. Antibacterial activity in the egg mass of a sea hare. Cell. Mol. Life Sci. 1984, 40(9):947-949.
21. 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.
22. 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(6):489-492.
23. -δδCT method. Methods 2001, 25(4):402-408.
24. Løvoll M., Kilvik T., Boshra H., Bøgwald J., Sunyer J.O., Dalmo R.A. Maternal transfer of complement components C3-1, C3-3, C3-4, C4, C5, C7, Bf, and Df to offspring in rainbow trout (Oncorhynchus mykiss). Immunogenetics 2006, 58(2):168-179.
25. Magnadottir B., Lange S., Gudmundsdottir S., Bogwald J., Dalmo R. Ontogeny of humoral immune parameters in fish. Fish Shellfish Immunol. 2005, 19(5):429-439.
26. Malek A., Sager R., Schneider H. Transport of proteins across the human placenta. Am. J. Reprod. Immunol. 2011, 40(5):347-351.
27. Marchini D., Marri L., Rosetto M., Manetti A.G.O., Dallai R. Presence of antibacterial peptides on the laid egg chorion of the medfly Ceratitis capitata. Biochem. Biophys. Res. Commun. 1997, 240(3):657-663.
28. Marlow F.L. Maternal control of development in vertebrates. Colloquium Series on Developmental Biology 2010, 1-196. Morgan & Claypool Life Sciences.
29. Ni D., Song L., Gao Q., Wu L., Yu Y., Zhao J., Qiu L., Zhang H., Shi F. 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.
30. Paik E.J., Zon L.I. Hematopoietic development in the zebrafish. Int. J. Dev. Biol. 2010, 54(6-7):1127-1137.
31. Picchietti S., Abelli L., Buonocore F., Randelli E., Fausto A.M., Scapigliati G., Mazzini M. Immunoglobulin protein and gene transcripts in sea bream (Sparus aurata L.) oocytes. Fish Shellfish Immunol. 2006, 20(3):398-404.
32. Pölkki M., Kangassalo K., Rantala M.J. Transgenerational effects of heavy metal pollution on immune defense of the blow fly Protophormia terraenovae. PLoS ONE 2012, 7(6):e38832.
33. Poorten T.J., Kuhn R.E. Maternal transfer of antibodies to eggs in Xenopus laevis. Dev. Comp. Immunol. 2009, 33(2):171-175.
34. 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. 2009, 79(2):403-413.
35. Sadd B.M., Schmid-Hempel P. Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Curr. Biol. 2007, 17(24):R1046-R1047.
36. Sadd B.M., Kleinlogel Y., Schmid-Hempel R., Schmid-Hempel P. Trans-generational immune priming in a social insect. Biol. Lett. 2005, 1(4):386-388.
37. Schumacher I.M., Rostal D.C., Yates R.A., Brown D.R., Jacobson E.R., Klein P.A. Persistence of maternal antibodies against Mycoplasma agassizii in desert tortoise hatchlings. Am. J. Vet. Res. 1999, 60(7):826-831.
38. Seppola M., Johnsen H., Mennen S., Myrnes B., Tveiten H. Maternal transfer and transcriptional onset of immune genes during ontogenesis in Atlantic cod. Dev. Comp. Immunol. 2009, 33(11):1205-1211.
39. Shiina N., Tateno H., Ogawa T., Muramoto K., Saneyoshi M., Kamiya H. Isolation and characterization of l-rhamnose-binding lectins from chum salmon (Oncorhynchus keta) eggs. Fish. Sci. 2008, 68(6):1352-1366.
40. Shlichta J.G., Smilanich A.M. Immune responses and their potential role in insect outbreaks. Insect Outbreaks Revisited 2012, 47-70. Blackwell Publishing Ltd.
41. Song L., Wang L., Qiu L., Zhang H. Bivalve Immunity. Invertebr. Immun. 2010, 44-65.
42. Su J., Song L., Xu W., Wu L., Li H., Xiang J. CDNA cloning and mRNA expression of the lipopolysaccharide-and beta-1, 3-glucan-binding protein gene from scallop Chlamys farreri. Aquaculture 2004, 239(1):69-80.
43. 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.
44. Swain P., Nayak S. Role of maternally derived immunity in fish. Fish Shellfish Immunol. 2009, 27(2):89-99.
45. Tateno H., Ogawa T., Muramoto K., Kamiya H., Saneyoshi M. Rhamnose-binding lectins from steelhead trout (Oncorhynchus mykiss) eggs recognize bacterial lipopolysaccharides and lipoteichoic acid. Biosci., Biotechnol., Biochem. 2002, 66(3):604-612.
46. 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(9):859-873.
47. Valtonen T.M., Kangassalo K., Pölkki M., Rantala M.J. Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS ONE 2012, 7(2):e31611.
48. Vijendravarma R.K., Narasimha S., Kawecki T.J. Effects of parental larval diet on egg size and offspring traits in Drosophila. Biol. Lett. 2010, 6(2):238-241.
49. Wang Z., Zhang S. The role of lysozyme and complement in the antibacterial activity of zebrafish (Danio rerio) egg cytosol. Fish Shellfish Immunol. 2010, 29(5):773-777.
50. Wang Z., Zhang S., Wang G., An Y. Complement activity in the egg cytosol of zebrafish Danio rerio: evidence for the defense role of maternal complement components. PLoS ONE 2008, 3(1):e1463.
51. Wang Z., Zhang S., Tong Z., Li L., Wang G. Maternal transfer and protective role of the alternative complement components in zebrafish Danio rerio. PLoS ONE 2009, 4(2):e4498.
52. Weaver D.M., Tyler J.W., VanMetre D.C., Hostetler D.E., Barrington G.M. Passive transfer of colostral immunoglobulins in calves. J. Vet. Intern. Med. 2008, 14(6):569-577.
53. Yang J., Qiu L., Wang L., Wei X., Zhang H., Zhang Y., Liu L., Song L. CfLGBP, a pattern recognition receptor in Chlamys farreri involved in the immune response against various bacteria. Fish Shellfish Immunol. 2010, 29(5):825-831.
54. Yang J., Wang W., Wei X., Qiu L., Wang L., Zhang H., Song L. Peptidoglycan recognition protein of Chlamys farreri (CfPGRP-S1) mediates immune defenses against bacterial infection. Dev. Comp. Immunol. 2010, 34(12):1300-1307.
55. 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.
56. Yousif A., Albright L., Evelyn T. Occurrence of lysozyme in the eggs of coho salmon Oncorhynchus kisutch. Dis. Aquat. Org. 1991, 10(1):45-49.
57. Yousif A., Albright L., Evelyn T. Purification and characterization of a galactose-specific lectin from the eggs of coho salmon Oncorhynchus kisutch and its interaction with bacterial fish pathogens. Dis. Aquat. Org. 1994, 20(2):127-136.
58. Yu X.Q., Gan H., Kanost R. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem. Mol. Biol. 1999, 29(7):585-597.
59. 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(3):855-864.
60. Zanchi C., Troussard J.P., Moreau J., Moret Y. Relationship between maternal transfer of immunity and mother fecundity in an insect. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2012, 279(1741):3223-3230.
61. Zhang H., Wang H., Wang L., Song X., Zhao J., Qiu L., Li L., Cong M., Song L. A novel C-type lectin (Cflec-3) from Chlamys farreri with three carbohydrate-recognition domains. Fish Shellfish Immunol. 2009, 26(5):707-715.
62. Zhang S., Wang Z., Wang H. Maternal immunity in fish. Dev. Comp. Immunol. 2013, 39(1-2):72-78.
63. 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(6):1198-1208.