The Effects of Letrozole in Transfer of Maternal Immunity against Lactococcosis to Eggs and Larvae in Rainbow Trout (Oncorhynchus mykiss, Walbaum)

Abstract

This study evaluated transfer of maternal lysozyme and immunoglobulin (IgM) against Lactococcus garviea, the causative agent of lactococcosis to eggs and larvae in rainbow trout. Changes in circulating lysozyme and IgM during development of eggs and larvae were measured by a method based on the ability of lysozyme to lyse the bacterium Micrococcus lysodeikticus and enzyme-linked immunosorbent assay (ELISA) respectively. For doing this, twelve broodstocks were injected weekly with 2.5 mg·kg-1 letrozole (an endocrine disrupter component) two months before spawning season and vaccinated intraperitoneally (i.p) with a bacterin (inactivated L. garviae) one month before spawning. Twelve broodstocks for vaccination and twelve female rainbow trouts as control group were also immiunised (i.p) with the bacterin and injected (i.p) with PBS respectively. Results showed that at day 8 after hatching, lysozyme and IgM levels during pre-larval stages decreased gradually, as yolks were absorbed. Lysozyme and IgM levels were significantly higher in the letrozole injected immiunised parents 30 days after immunisation as well as their larvae compared to the control group (p < 0.05). These results showed the lysozyme and IgM detected from day 0 to day 8 derived from maternal fish while the lysozyme and IgM detected from day 10 onward are neo-synthesized lysozyme and IgM. The present study indicated the role of the injection of letrozole (two months before spawning) and parent immunisation with a bacterin (inactivated L. garviae) (one month before spawning) in maternal transfer of lysozyme and IgM levels to eggs and larvae.

Share and Cite:

Akbary, P. , Mirvaghefi, A. , Akhlaghi, M. , Amiri, B. and Fereidouni, M. (2015) The Effects of Letrozole in Transfer of Maternal Immunity against Lactococcosis to Eggs and Larvae in Rainbow Trout (Oncorhynchus mykiss, Walbaum). Food and Nutrition Sciences, 6, 254-264. doi: 10.4236/fns.2015.62026.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Vendrell, D., Balcázar, J.L., Ruiz-Zarzuela, I., Blas, I.D., Gironés, O. and Mùzquiz, J.L. (2006) Lactococcus garvieae in Fish: A Review. Comparative Immunology Microbiology and Infectious Disease, 29, 177-198.
http://dx.doi.org/10.1016/j.cimid.2006.06.003
[2] Ellis, A.E. (1988) Ontogeny of the Immune System in Teleost Fish. In: Ellis, A.E., Ed., Fish Vaccination, Academic Press, London, 20-31.
[3] Hanif, A., Bakopoulos, V. and Dimitriadis, G.J. (2004) Maternal Transfer of Humoral Specific and Non-Specific Immune Parameters to Sea Bream (Sparus auratus) Larvae. Fish Shellfish Immunology, 17, 411-435.
http://dx.doi.org/10.1016/j.fsi.2004.04.013
[4] Petrie-Hanson, L. and Ainsworth, A.J. (2001) Ontogeny of Channel Catfish Lymphoid Organs. Veterinary Immunology and Immunopathology, 81, 113-127.
http://dx.doi.org/10.1016/S0165-2427(01)00331-2
[5] Zhang, S., Wang, Z. and Wang, H. (2013) Maternal Immunity in Fish. Development and Comparative Immunology, 39, 72-78.
http://dx.doi.org/10.1016/j.dci.2012.02.009
[6] Magnadottir, B., Lange, S., Gudmundsdottir, S., Bogwald, J. and Dalmo, R.A. (2005) Ontogeny of Humoral Immune Parameters in Fish. Fish and Shellfish Immonology, 19, 429-439.
http://dx.doi.org/10.1016/j.fsi.2005.03.010
[7] 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 Part A, 84, 309-313.
http://dx.doi.org/10.1016/0300-9629(86)90620-1
[8] Suzuki, Y., Orito, M., Furukawa, K. and Aida, K. (1994) Existence of Low Molecular Weight Immunoglobulin-M in Carp Eggs. Fisheries Science, 60, 152-169.
[9] 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 Immonology, 7, 29-43.
http://dx.doi.org/10.1006/fsim.1996.0061
[10] Picchietti, S., Taddei, A.R., Scapigliati, G., Buonocore, F., Fausto, A.M., Romano, N., et al. (2004) Immunoglobulin Protein and Gene Transcripts in Ovarian Follicles throughout Oogenesis in the Teleost Dicentrarchus labrax. Cell Tissue Research, 315, 259-270.
http://dx.doi.org/10.1007/s00441-003-0819-9
[11] Olsen, Y.A. and Press, C.M. (1997) Degradation Kinetics of Immunoglobulin in the Egg, Alevin and Fry of Atlantic Salmon, Salmo salar L., and the Localisation of Immunoglobulin in the Egg. Fish & Shellfish Immunology, 7, 81-91.
http://dx.doi.org/10.1006/fsim.1996.0064
[12] Magnadottir, B., Lange, S., Steinarsson, A. and Gudmundsdottir, S. (2004) The Ontogenic Development of Innate Immune Parameters of Cod (Gadus morhua L.). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 139, 217-224.
http://dx.doi.org/10.1016/j.cbpc.2004.07.009
[13] Yousif, A.N., Albright, L. and Evelyn, T.P.T. (1991) Occurrence of Lysozyme in the Eggs of Coho Salmon Oncorhynchus kisutch. Diseases of Aquatic Organisms, 10, 45-49.
http://dx.doi.org/10.3354/dao010045
[14] 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.
http://dx.doi.org/10.3354/dao019015
[15] Swain, P. and Nayak, S.K. (2009) Role of Maternally Derived Immunity in Fish. Fish & Shellfish Immunology, 27, 89-99.
http://dx.doi.org/10.1016/j.fsi.2009.04.008
[16] Harris, J. and Bird, D.J. (2000) Modulation of the Fish Immune System by Hormones. Veterinary Immunology and Immunopathology, 77, 163-176.
http://dx.doi.org/10.1016/S0165-2427(00)00235-X
[17] Milla, S., Depiereus, S. and Kestemont, P. (2011) The Effects of Estrogenic and Androgenic Endocrine Disruptors on the Immune System of Fish: A Review. Ectoxicology, 20, 305-319.
http://dx.doi.org/10.1007/s10646-010-0588-7
[18] Hou, Y.Y. (1998) Endocrinological Aspects of Reduced Immunocompetence with Gonadal Maturation in Rainbow trout. Ph.D. Thesis, The University of Tokyo, Tokyo.
[19] Slater, C.H. and Schreck, C.B. (1993) Testosterone Alters the Immune Response of Chinook Salmon, Oncorhynchus tshawytscha. General and Comparative Endocrinology, 89, 291-298.
http://dx.doi.org/10.1006/gcen.1993.1035
[20] Suzuki, Y., Otaka, T., Sato, S., Hou, Y.Y. and Aida, K. (1997) Reproduction Related Immunoglobulin Changes in Rainbow Trout. Fish Physiology and Biochemistry, 17, 415-421.
http://dx.doi.org/10.1023/A:1007795827112
[21] Thilagam, H., Gopalakrishnan, S., Bo, J. and Wang, K.J. (2009) Effect of 17β-Estradiol on the Immunocompetence of Japanese Sea Bass (Lateolabrax japonicus). Environmental Toxicology and Chemistry, 28, 1722-1731.
http://dx.doi.org/10.1897/08-642.1
[22] Smith, L.E. (1999) Aromatase Inhibitors: A Dose-Response Effect? Endocrine-Related Cancer, 6, 245-249.
http://dx.doi.org/10.1677/erc.0.0060245
[23] Akbary, P., Mirvaghefi, A.R., Akhlaghi, M. and Majazi Amiri, B. (2015) Effect of Letrozole, Aromatase Inhibitor, on Serum Sex Steroid Levels, Egg Diameter, Gonado-Somatic Index (GSI) in Rainbow Trout (Oncorhynchus mykiss). Iranian Journal of Fisheries Science, in press.
[24] Shilling, A.D., Carlson, B. and Williams, D.E. (1999) Rainbow Trout, Oncorhynchus mykiss, as a Model for Aromatase Inhibition. The Journal of Steroid Biochemistry and Molecular Biology, 70, 89-95.
http://dx.doi.org/10.1016/S0960-0760(99)00090-4
[25] Sharifiyazdi, H., Akhlaghi, M., Tabatabaei, M. and Mostafavi Zadeh, S.M. (2010) Isolation and Characterization of Lactococcus garvieae from Diseased Rainbow Trout (Oncorhynchus mykiss, Walbaum) Cultured in Iran. Iranian Journal of Veterinary Researches, 11, 342-350.
[26] Toranzo, A.E., Devesa, S., Romalde, J.L., Lamas, J., Riaza, A., Leiro, J. and Barja, J.L.M. (1995) Efficacy of Intraperitoneal and Immersion Vaccination against Enterococcus sp. Infection in Turbot. Aquaculture, 134, 17-27.
http://dx.doi.org/10.1016/0044-8486(95)00038-4
[27] Romalde, J.L., Alvarez, A.L., Ravelo, C., Toranzo, A.E. and Mendez, J.B. (2004) Oral Immunisation Using Alginate Microparticles as a Useful Strategy for Booster Vaccination against Fish Lactoccocosis. Aquaculture, 236, 119-129.
http://dx.doi.org/10.1016/j.aquaculture.2004.02.028
[28] Ellis, A.E. (1990) Lysozyme Assays. In: Stolen, J.S., Fletcher, T.C., Anderson, D.P., Roberson, B.S. and Van Muiswinkel, W.B., Eds., Techniques in Fish Immunology Fair Haven, SOS Publications, Fair Haven, 101-103.
[29] Swain, P., Nayak, S., Sahu, A., Mahapatra, B.C. and Meher, P.K. (2002) Bath Immunisation of Spawn, Fry and Fingerlings of Indian Major Carps Using a Particulate Antigen. Fish & Shellfish Immunology, 13, 133-140.
http://dx.doi.org/10.1006/fsim.2001.0388
[30] Sugita, H., Okano, R., Suzuki, Y., Iwai, D., Mizukami, M., Akiyama, N., et al. (2002) Antibacterial Abilities of Intestinal Bacteria from Larvae and Juvenile Japanese Flounder against Fish Pathogens. Fisheries Science, 68, 1004-1011.
http://dx.doi.org/10.1046/j.1444-2906.2002.00525.x
[31] 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(Han). Fish & Shellfish Immunology, 20, 519-527.
http://dx.doi.org/10.1016/j.fsi.2005.06.011
[32] Hosseini, M.H., Akhlaghi, M. and Moazzeni Jula, G. (2011) Experimental Vaccine against Lactococcosis in Cultured Rainbow Trout (Oncorhynchus mykiss). Archives of Razi Institute, 66, 51-57.
[33] Kim, J.H., Go, J., Cho, C.R., Kim, J.I., Lee, M.S. and Parka, S.C. (2013) First Report of Human Acute Acalculous Cholecystitis Caused by the Fish Pathogen Lactococcus garvieae. Journal of Clinical Microbiolgy, 51, 712-714.
http://dx.doi.org/10.1128/JCM.02369-12
[34] Hou, Y., Suzuki, Y.Y. and Aida, K. (1999) Effects of Steroid Hormones on Immunoglobulin M (IgM) in Rainbow Trout, Oncorhynchus mykiss. Fish Physiology and Biochemistry, 20, 155-162.
http://dx.doi.org/10.1023/A:1007799617597
[35] Cuasco, B., Gucco, M., Malacarne, G., Ottonelli, R. and Tanvez, A. (2008) Yolk Testosterone Levels and Dietary Carotenoids Influence Growth and Immunity of Grey Partridge Chicks. General and Comparative Endocrinology, 156, 418-425.
http://dx.doi.org/10.1016/j.ygcen.2007.12.010
[36] ángeles Esteban, M., Cuesta, A., Chaves-Pozo, E. and Meseguer, J. (2013) Influence of Melatonin on the Immune System of Fish: A Review. International Journal of Molecular Science, 14, 7979-7999.
http://dx.doi.org/10.3390/ijms14047979
[37] Lei, L., Zhang, S., Tongo, Z. and Liu, J. (2010) In Vivo Effect of 17-β-Estradiol on Plasma Immunoglobulin Levels and Leukocyte Density in Zebrafish Danio rerio. Chinese Journal of Oceanology and Limnology, 28, 527-532.
http://dx.doi.org/10.1007/s00343-009-9048-8
[38] Williams, T.D., Amer, M.D., George, S.G., Sabine, V. and Chipman, J.K. (2007) Gene Expression Responses of European Flounder (Platichtys flesus) to 17-β Estradiol. Toxicology Letters, 168, 236-248.
http://dx.doi.org/10.1016/j.toxlet.2006.10.020
[39] Wang, K.J., Cai, J.J., Qu, H.D., Yang, M. and Zhan, M. (2009) Cloning and Expression of a Hepcidin Gene from a Marine Fish (Pseudosciaena crocea) and the Antimicrobial Activity of Its Synthetic Peptide. Peptides, 30, 638-646.
http://dx.doi.org/10.1016/j.peptides.2008.12.014
[40] Sin, Y.M., Ling, K.H. and Lam, T.J. (1994) Passive Transfer of Protective Immunity against Ichthophthiriasis from Vaccinated Mother to Fry in Tilapias, Oreochromis aureus. Aquaculture, 120, 229-237.
http://dx.doi.org/10.1016/0044-8486(94)90081-7
[41] Chantanachookhin, C., Seikai, T. and Tanaka, M. (1991) Comparative Study of the Ontogeny of the Lymphoid Organs in Three Species of Marine Fish. Aquaculture, 99, 143-155.
http://dx.doi.org/10.1016/0044-8486(91)90294-H
[42] Mor, A. and Avtalion, R.R. (1988) Evidence of Transfer of Immunity From Mother to Eggs in Tilapias. The Israeli Journal of Aquaculture, 40, 22-28.
[43] Mor, A. and Avtalion, R.R. (1990) Transfer of Antibody Activity from Immunized Mother to Embryo in Tilapias. Journal of Fish Biology, 37, 249-255.
http://dx.doi.org/10.1111/j.1095-8649.1990.tb05856.x
[44] Takemura, A. and Takano, K. (1997) Transfer of Maternally-Derived Immunoglobulin (IgM) to Larvae in Tilapia, Oreochromis mossambicus. Fish & Shellfish Immunology, 7, 355-363.
http://dx.doi.org/10.1006/fsim.1997.0090
[45] Kanlis, G., Suzuki, Y., Tauchi, M., Numata, T., Shirojo, Y. and Kawano, K. (1995) Immunoglobulin Concentration and Specific Antibody Activity in Oocytes and Eggs of Immunized Red Sea Bream. Fisheries Science, 61, 791-795.
http://www.affrc.go.jp/en/
[46] Hanif, A., Bakopoulos, V., Leonardos, I. and Dimitriadis, G.J. (2005) The Effect of Sea Bream (Sparus aurata) Broodstock and Larval Vaccination on the Susceptibility by Photobacterium damsela subsp. piscicida and on the Humoral Immune Parameters. Fish & Shellfish Immunology, 19, 345-361.
http://dx.doi.org/10.1016/j.fsi.2004.12.009
[47] Picchietti, S., Scapigliati, G., Fanelli, M. and Barbato, F., Canese, S., Mastrolia, L, et al. (2001) Sex-Related Variations of Serum Immunoglobulins during Reproduction in Gilthead Sea Bream and Evidence for a Transfer from the FEMALE to the Eggs. Journal of Fish Biology, 59, 1503-1511.
http://dx.doi.org/10.1111/j.1095-8649.2001.tb00215.x
[48] Lillehaug, A., Sevatdal, G. and Endal, T. (1996) Passive Transfer of Specific Maternal Immunity Does Not Protect Atlantic Salmon (Salmo salarL.) Fry against Yersiniosis. Fish & Shellfish Immunology, 6, 521-535.
http://dx.doi.org/10.1006/fsim.1996.0049
[49] Scapigliati, G., Romano, N. and Abelli, L. (1999) Monoclonal Antibodies in Fish Immunology: Identification, Ontogeny and Activity of Tand B-lymphocytes. Aquaculture, 172, 3-28.
http://dx.doi.org/10.1016/S0044-8486(98)00440-2
[50] Pepin, J.F., Brueil, G., Rigobert, P. and Romestand, B. (1997) Detection and Characterization of Immunoglobulins in the Eggs of the Sea Bass (Dicentrarchus labrax). Ichtyophysiolgy Acta, 20, 77-85.
[51] Takemura, A. (1993) Changes in an Immunoglobulin M (IgM)-Like Protein during Larval Stages in Tilapia, Oreochromis mossambicus. Aquaculture, 115, 233-241.
http://dx.doi.org/10.1016/0044-8486(93)90139-P
[52] Campbell, B., Dickey, J.T. and Swanson, P. (2003) Endocrine Changes during Onset of Puberty in Male Spring Chinook Salmon, Oncorhynchus tshawytscha. Biology of Reproduction, 69, 2109-2117.
http://dx.doi.org/10.1095/biolreprod.103.020560
[53] Nagae, M., Fuda, H., Hara, A., Kawamura, H. and Yamauchi, K. (1993) Changes in Serum Immunoglobulin M (IgM) Concentrations during Early Development of Chum Salmon (Oncorhynchus keta) as Determined by Sensitive ELISA Technique. Comparative Biochemistry and Physiology Part A: Physiology, 106, 69-74.
http://dx.doi.org/10.1016/0300-9629(93)90041-2

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.