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Response of gene expression to LPS challenge manifests the ontogeny and maturation of the complement system in zebrafish larvae

Published online by Cambridge University Press:  22 July 2013

Zhiping Wang  and
Yanjun Han
Zhiping Wang*
Affiliation:
Department of Life Science, Shaanxi Normal University, Xi'an, 710062, PR China Key Laboratory for Eco-environment of Multi-River Wetlands in Shaanxi Province, Weinan 714099, PR China
Yanjun Han
Affiliation:
Key Laboratory for Eco-environment of Multi-River Wetlands in Shaanxi Province, Weinan 714099, PR China
*
Correspondence should be addressed to: Z. Wang, Department of Life Science, Shaanxi Normal University, Xi'an, 710062, PR China email: wzhp1978@126.com
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Abstract

Information on the ontogeny of complement system might help us better understand the anti-infection mechanism in the early fish life. The ontogenic expression of the representative complement genes and their response to lipopolysaccharides (LPS) challenge in zebrafish larvae are reported here. The expression of C1r/s, C3, C4, C6 and MBL steadily increased before 21 days post-fertilization (dpf) and a decrease was detected thereafter. MASP expression elevated and peaked on 14 dpf and a decline followed. Bf expression fluctuated during the experimental period. Moreover, Bf (involved in alternative pathway, AP) expressed at higher levels than C1r/s (involved in classical pathway, CP), MASP (involved in lectin pathway, LP) and C4 (involved in both CP and LP) in the normal adult fish and larvae, suggesting the more significance of AP than CP and LP during the development of zebrafish. LPS challenge induced up-regulation of all the genes at 12 h in the adult fish. For the larvae, Bf, C3 (key complement component) and C6 (involved in lytic pathway) responded to LPS challenge at earlier stages than the other complement genes, with the up-regulation detected since 14, 14 and 7 dpf, respectively. In the larvae at 28 dpf, all the above three genes responded to LPS challenge by up-regulating their expression in a fashion similar to that of the adult fish, hinting that complement operating via AP develops earlier and plays a key role in protecting the larvae; it showed effective responses to LPS challenge from 14 dpf and might mature before 28 dpf.

Keywords

zebrafishcomplement systemontogenymaturation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 7 , November 2013 , pp. 1965 - 1971
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Bildfell, R.J., Markham, R.J. and Johnson, G.R. (1992) Purification and partial characterization of a rainbow trout egg lectin. Journal of Aquatic Animal Health 4, 97–105.2.3.CO;2>CrossRefGoogle Scholar
Bly, J.E., Grimm, A.S. and Morris, I.G. (1986) Transfer of passive immunity from mother to young in a teleost fish: haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L. Comparative Biochemistry and Physiology 84A, 309–313.CrossRefGoogle Scholar
Breuil, G., Vassiloglou, B., Pepin, J.F. and Romestand, B. (1997) Ontogeny of IgM-bearing cells and changes in the immunoglobulin M-like protein level (IgM) during larval stages in sea bass (Dicentrarchus labrax). Fish and Shellfish Immunology 7, 29–43.CrossRefGoogle Scholar
Brown, J.S., Hussell, T., Gilliland, S.M., Holden, D.W., Paton, J.C., Ehrenstein, M.R., Walport, M.J. and Botto, M. (2002) The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proceedings of the National Academy of Sciences of the United States of America 99, 16969–16974.CrossRefGoogle ScholarPubMed
Brown, L.L., Cox, W.T. and Levine, R.P. (1997) Evidence that the causal agent of bacterial coldwater disease Flavobacterium psychrophilum is transmitted within salmonid eggs. Diseases of Aquatic Organisms 29, 213–218.CrossRefGoogle Scholar
Castillo, A., Sanchez, C., Dominguez, J., Kvaattari, S.L. and Villena, A.J. (1993) Ontogeny of IgM and IgM-bearing cells in rainbow trout. Developmental and Comparative Immunology 17, 419–424.CrossRefGoogle ScholarPubMed
Cecchini, S., Terova, G., Caricato, G. and Saroglia, M. (2000) Lysosome activity in embryos and larvae of sea bass (Dicentrarchus labrax L.), spawned by broodstocks fed with vitamin C enriched diets. Bulletin of the European Association of Fish Pathologists 20, 120–124.Google Scholar
Chen, J.Y., Chen, J.C. and Wu, J.I. (2003) Molecular cloning and functional analysis of high density lipoprotein binding protein. Comparative Biochemistry and Physiology— 36B, 117–130.CrossRefGoogle Scholar
Choi, J.H., Park, P.J. and Kim, S.K. (2002) Purification and characterization of a trypsin inhibitor from the egg of skipjack tuna Katsuwonus pelamis. Fisheries Science 68, 1367–1373.CrossRefGoogle Scholar
Ellingsen, T., Strand, C., Monsen, E., Bøgwald, J. and Dalmo, R.A. (2005) The ontogeny of complement component C3 in the spotted wolfish (Anarhichas minor Olafsen). Fish and Shellfish Immunology 18, 351–358.CrossRefGoogle Scholar
Fujita, T. (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nature Reviews Immunology 2, 346–353.CrossRefGoogle ScholarPubMed
Hanif, A., Bakopoulos, V. and Dimitriadis, G.J. (2004) Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish and Shellfish Immunology 17, 411–435.CrossRefGoogle ScholarPubMed
Holland, M.C. and Lambris, J.D. (2002) The complement system in teleost. Fish and Shellfish Immunology 12, 399–420.CrossRefGoogle Scholar
Huttenhuis, H.B.T., Grou, C.P.O., Taverne-Thiele, A.J., Taverne, N. and Rombout, J.H.W.M. (2006) Carp (Cyprinus carpio L.) innate immune factors are present before hatching. Fish and Shellfish Immunology 20, 586–596.CrossRefGoogle ScholarPubMed
Jung, W.K., Park, P.J. and Kim, S.K. (2003) Purification and characterization of a new lectin from the hard roe of skipjack tuna, Katsuwonus pelamis. International Journal of Biochemistry & Cell Biology 35, 255–265.CrossRefGoogle ScholarPubMed
Keegan, B.R., Feldman, J.L., Lee, D.H., Koos, D.S., Ho, R.K., Stainier, D.Y. and Yelon, D. (2002) The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo. Development 129, 1623–1632.CrossRefGoogle ScholarPubMed
Kishore, U. and Reid, K.B. (2000) C1q: structure, function and receptors. Immunopharmacology 49, 159–170.CrossRefGoogle ScholarPubMed
Kudo, S. (1991) Further investigation on enzyme activities and antifungal action of fertilization envelope extract from fish eggs. Zoological Science 8, 1079.Google Scholar
Kudo, S. (1992) Enzymatic basis for protection of fish embryos by the fertilization envelope. Experientia 48, 277–281.CrossRefGoogle ScholarPubMed
Lange, S., Bambir, S.H., Dodds, A.W., Bowden, T., Bricknell, I., Espelid, S. and Magnadóttir, B. (2006) Complement component C3 transcription in Atlantic halibut (Hippoglossus hippoglossus L.) larvae. Fish and Shellfish Immunology 20, 285–294.CrossRefGoogle ScholarPubMed
Lange, S., Dodds, A.W., Gudmundsdóttir, S., Bambir, S.H. and Magnadóttir, B. (2005) The ontogenic transcription of complement component C3 and Apolipoprotein A-I tRNA in Atlantic cod (Gadus morhua L.)—a role in development and homeostasis? Developmental and Comparative Immunology 29, 1065–1077.CrossRefGoogle ScholarPubMed
Li, F.L., Zhang, S.C., Wang, Z.P. and Li, H.Y. (2011) Genes of the adaptive immune system are expressed early in zebrafish larval development following lipopolysaccharide stimulaton. Chinese Journal of Oceanology and Limnology 29, 326–333.CrossRefGoogle Scholar
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(–ΔΔCt) method. Methods 25, 402–408.CrossRefGoogle Scholar
Løvoll, M., Johnsen, H., Boshra, H., Bøgwald, J., Sunyer, J.O. and Dalmo, R.A. (2007) The ontogeny and extrahepatic expression of complement factor C3 in Atlantic salmon (Salmo salar). Fish and Shellfish Immunology 23, 542–552.CrossRefGoogle ScholarPubMed
Løvoll, M., Kilvik, T., Boshra, H., Bogwald, J., Sunyer, J.O. and Dalmo, R.A. (2006) 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 58, 168–179.CrossRefGoogle Scholar
Mor, A. and Avtalion, R.R. (1990) Transfer of antibody activity from immunised mother to embryos in tilapias. Journal of Fish Biology 37, 249–255.CrossRefGoogle Scholar
Ober, E.A., Field, H.A. and Stainier, D.Y. (2003) From endoderm formation to liver and pancreas development in zebrafish. Mechanisms of Development 120, 5–18.CrossRefGoogle ScholarPubMed
Olsen, Y.A. (1997) Press CMcL degradation kinetics of immunoglobulin in the egg, alevin and fry of Atlantic salmon, Salmo salar L., and the localization of immunoglobulin in the egg. Fish and Shellfish Immunology 7, 81–91.CrossRefGoogle Scholar
Picchietti, S., Abelli, L., Buonocore, F., Randelli, E., Fausto, A.M., Scapigliati, G. and Mazzini, M. (2006) Immunoglobulin protein and gene transcripts in sea bream (Sparus aurata L.) oocytes. Fish and Shellfish Immunology 20, 398–404.CrossRefGoogle ScholarPubMed
Picchietti, S., Taddei, A.R., Scapigliati, G., Buonocore, F., Fausto, A.M. and Romano, N. (2004) Immunoglobulin protein and gene transcripts in ovarian follicles throughout oogenesis in the teleost Dicentrachus labrax. Cell and Tissue Research 315, 259–270.CrossRefGoogle Scholar
Swain, P., Dash, S., Bal, J., Routray, P., Sahoo, P.K., Sahoo, S.K., Saurabh, S., Gupta, S.D. and Meher, P.K. (2006) Passive transfer of maternal antibodies and their existence in eggs, larvae and fry of Indian major carp, Labeo rohita (Ham.). Fish and Shellfish Immunology 20, 519–527.CrossRefGoogle ScholarPubMed
Takemura, A. (1996) Immunohistochemical localization of lysozyme in the prelarvae of tilapia, Oreochromis mossambicus. Fish and Shellfish Immunology 6, 75–77.CrossRefGoogle Scholar
Takemura, A. and Takano, K. (1995) Lysozyme in the ovary of tilapia (Oreochromis mossambicus): its purification and some biological properties. Fish Physiology and Biochemistry 14, 415–421.CrossRefGoogle ScholarPubMed
Tang, R., Dodd, A.W., Lai, D., McNabb, W.C. and Love, D.R. (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochimica et Biophysica Sinica (Shanghai) 39, 384–390.CrossRefGoogle ScholarPubMed
Tateno, H., Yamaguchi, T., Ogawa, T., Muramoto, K., Watanabe, T., Kamiya, H. and Saneyoshi, M. (2002) Immunohistochemical localization of rhamnose-binding lectins in the steelhead trout (Oncorhynchus mykiss). Developmental and Comparative Immunology 26, 543–550.CrossRefGoogle ScholarPubMed
Thielens, N.M., Tacnet-Delorme, P. and Arlaud, G.J. (2002) Interaction of C1q and mannan-binding lectin with viruses. Immunobiology 205, 563–574.CrossRefGoogle ScholarPubMed
Trede, N.S., Langenau, D.M., Trave, D., Look, A.T. and Zon, L.I. (2004) The use of zebrafish to understand immunity. Immunity 20, 367–379.CrossRefGoogle ScholarPubMed
Van Loon, J.J.A., van Osterom, R. and van Muiswinkel, W.B. (1981) Development of the immune system in carp (Cyprinus carpio). Aspects of Developmental and Comparative Immunology 1, 469–470.CrossRefGoogle Scholar
Wang, Z.P. and Zhang, S.C. (2010) The role of lysozyme and complement in the antibacterial activity of zebrafish (Danio rerio) egg cytosol. Fish and Shellfish Immunology 29, 773–777.CrossRefGoogle ScholarPubMed
Wang, Z.P., Zhang, S.C. and Wang, G.F. (2008a) Response of complement expression to challenge with lipopolysaccharide in embryos/larvae of zebrafish Danio rerio: maturation of complement immunocompetence. Fish and Shellfish Immunology 25, 264–270.CrossRefGoogle Scholar
Wang, Z.P., Zhang, S.C., Wang, G.F. and An, Y. (2008b) Complement activity in the egg cytosol of zebrafish Danio rerio: evidence for the defense role of maternal complement components. PLOS ONE 3, e1463.Google ScholarPubMed
Wang, Z.P., Zhang, S.C., Li, L., Tong, Z. and Wang, G.F. (2009) Maternal transfer of complement and protective role of the alternative complement components in zebrafish, Danio rerio. PLOS ONE 4, e4498.Google ScholarPubMed
Yamashita, M. and Konagaya, S. (1996) A novel cysteine protease inhibitor of the egg of chum salmon, containing a cysteine-rich thyroglobulin-like motif. Journal of Biological Chemistry 271, 1282–1284.CrossRefGoogle ScholarPubMed
Yousif, A.N., Albright, L.J. and Evelyn, T.P.T. (1991) Occurrence of lysozyme in the eggs of coho salmon Oncorhynchus kisutch. Diseases of Aquatic Organisms 10, 45–49.CrossRefGoogle Scholar
Yousif, A.N., Albright, L.J. and Evelyn, T.P.T. (1994) In vitro evidence for the antibacterial role of lysozyme in salmonid eggs. Diseases of Aquatic Organisms 19, 15–19.CrossRefGoogle Scholar
Zapata, A., Diez, B., Cejalvo, T., Frías, C.G. and Cortés, A. (2006) Ontogeny of the immune system of fish. Fish and Shellfish Immunology 20, 126–136.CrossRefGoogle ScholarPubMed