Differentiating size-dependent responses of juvenile pink salmon (Oncorhynchus gorbuscha) to sea lice (Lepeophtheirus salmonis) infections

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 6, Issue 2, 2011, Pages 213-223

  Sutherland, Ben J G ^a   Jantzen, Stuart G ^a   Sanderson, Dan S ^a   Koop, Ben F ^a   Jones, Simon R M ^b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b PACIFIC BIOLOGICAL STATION   (Canada)

Author keywords

Cell proliferation; Conservation; Development; Immune system; Inflammation; Pink salmon; Sea lice; Transcriptomics

Indexed keywords

COMPLEMENTARY DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; COPEPOD; DNA MICROARRAY; DOWN REGULATION; GLUCOSE ABSORPTION; GROWTH RATE; IMMUNE RESPONSE; INFLAMMATION; LABORATORY TEST; LEPEOPHTHEIRUS SALMONIS; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCORHYNCHUS; ONCORHYNCHUS GORBUSCHA; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA LOUSE INFESTATION; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; UPREGULATION;

COPEPODA; LEPEOPHTHEIRUS SALMONIS; ONCORHYNCHUS; ONCORHYNCHUS GORBUSCHA; PHTHIRAPTERA;

EID: 79956357677     PISSN: 1744117X     EISSN: 18780407     Source Type: Journal    
DOI: 10.1016/j.cbd.2011.04.001     Document Type: Article

References (65)

1. Arnott, S.A., Barber, I., Huntingford, F.A., 2000. Parasite-associated growth enhancement in a fish-cestode system. Proc. Biol. Sci. 267, 657-663.
2. Arunachalam, B., Phan, U.T., Geuze, H.J., Cresswell, P., 2000. Enzymatic reduction of disulfide bonds in lysosomes: characterization of a gamma-interferon-inducible lysosomal thiol reductase (GILT). Proc. Natl. Acad. Sci. U.S.A. 97, 745-750.
3. Ballabeni, P., 1994. Experimental differences in mortality patterns between European minnows, Phoxinus phoxinus, infected with sympatric or allopatric trematodes, Diplostomum phoxini. J. Fish Biol. 45, 257-267. (Pubitemid 2117871)
4. Bandara, L.R., Buck, V.M., Zamanian, M., Johnston, L.H., La Thangue, N.B., 1993. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 12, 4317-4324. (Pubitemid 23302046)
5. Barton, B.A., Schreck, C.B., Barton, L.D., 1987. Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis. Aquat. Org. 2, 173-185.
6. Baudoin, M., 1975. Host castration as a parasitic strategy. Evolution 29, 335-352.
7. Bowers, J.M.,Mustafa, A., Speare, D.J., Conboy, G.A., Brimacombe,M., Sims, D.E., Burka, J.F., 2000. The physiological response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice, Lepeophtheirus salmonis. J. Fish Dis. 23, 165-172.
8. Bron, J.E., Sommerville, C., Rae, G.H., 1993. The functional morphology of the alimentary canal of larval stages of the parasitic copepod Lepeophtheirus salmonis. J. Zool. 230, 207-220.
9. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., Turner, C., 1988. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Dev. Biol. 4, 487-525.
10. Chadzinska, M., Baginski, P., Kolaczkowska, E., Savelkoul, H.F.J., Verburg-van Kemenade, B.M.L., 2008. Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation. Immunology 125, 601-610.
11. Costello, M.J., 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol. 22, 475-483. (Pubitemid 44333288)
12. DeBenedetti, F., Alonzi, T., Moretta, A., Lazzaro, D., Costa, P., Poli, V., Martini, A., Ciliberto, G., Fattori, E., 1997. Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I - a model for stunted growth in children with chronic inflammation. J. Clin. Invest. 99, 643-650.
13. Easy, R.H., Ross, N.W., 2009. Changes in Atlantic salmon (Salmo salar) epidermal mucus protein composition profiles following infection with sea lice (Lepeophtheirus salmonis). Comp. Biochem. Physiol. Part D Genomics Proteomics 4, 159-167.
14. Fast, M.D., Ross, N.W., Mustafa, A., Sims, D.E., Johnson, S.C., Conboy, G.A., Speare, D.J., Johnson, G., Burka, J.F., 2002. Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Dis. Aquat. Org. 52, 57-68.
15. Fast, M.D., Burka, J.F., Johnson, S.C., Ross, N.W., 2003. Enzymes released from Lepeophtheirus salmonis in response to mucus from different salmonids. J. Parasitol. 89, 7-13. (Pubitemid 36278641)
16. Fast, M.D., Ross, N.W., Craft, C.A., Locke, S.J., MacKinnon, S.L., Johnson, S.C., 2004. Lepeophtheirus salmonis: characterization of prostaglandin E-2 in secretory products of the salmon louse by RP-HPLC and mass spectrometry. Exp. Parasitol. 107, 5-13.
17. Fast, M.D., Ross, N.W., Johnson, S.C., 2005. Prostaglandin E-2 modulation of gene expression in an Atlantic salmon (Salmo salar) macrophage-like cell line (SHK-1). Dev. Comp. Immunol. 29, 951-963.
18. Fast, M.D., Johnson, S.C., Eddy, T.D., Pinto, D., Ross, N.W., 2007. Lepeophtheirus salmonis secretory/excretory products and their effects on Atlantic salmon immune gene regulation. Parasite Immunol. 29, 179-189. (Pubitemid 46434884)
19. Fernandez, J., Esch, G.W., 1991. Effect of parasitism on the growth rate of the pulmonate snail Helisoma anceps. J. Parasitol. 77, 937-944. (Pubitemid 23397447)
20. Finstad, B., Bjørn, P.A., Grimnes, A., Hvidsten, N.A., 2000. Laboratory and field investigations of salmon lice Lepeophtheirus salmonis (Krøyer) infestation on Atlantic salmon (Salmo salar L.) post-smolts. Aquacult. Res. 31, 795-803.
21. Firth, K.J., Johnson, S.C., Ross, N.W., 2000. Characterization of proteases in the skin mucus of Atlantic salmon (Salmo salar) infected with the salmon louse (Lepeophtheirus salmonis) and in whole-body louse homogenate. J. Parasitol. 86, 1199-1205. (Pubitemid 32047187)
22. Grimnes, A., Jakobsen, P.J., 1996. The physiological effects of salmon lice infection on post-smolt of Atlantic salmon. J. Fish Biol. 48, 1179-1194. (Pubitemid 26310447)
23. Heard, W.R., 1991. Life history of pink salmon (Oncorhynchus gorbuscha), In: Groot, C., Margolis, L. (Eds.), Pacific Salmon Life Histories, 1st ed. UBC Press, Vancouver, pp. 177-181.
24. Hoegy, S.E., Oh, H.R., Corcoran, M.L., Stetler-Stevenson, W.G., 2001. Tissue inhibitor of metalloproteinases-2 (TIMP-2) suppresses TKR-growth factor signaling independent of metalloproteinase inhibition. J. Biol. Chem. 276, 3203-3214.
25. Hou, Y.Q., Qin, H.M., Follit, J.A., Pazour, G.J., Rosenbaum, J.L., Witman, G.B., 2007. Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J. Cell Biol. 176, 653-665. (Pubitemid 46333980)
26. Hunter, T., Poon, R.Y.C., 1997. Cdc37: a protein kinase chaperone? Trends Cell Biol. 7, 251-251.
27. Hynes, R.O., 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
28. Johnson, S.C., Albright, L.J., 1991. The developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae). Can. J. Zool. 69, 929-950.
29. Johnson, S.C., Albright, L.J., 1992. Comparative susceptibility and histopathology of the response of naive Atlantic, chinook and coho salmon to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae). Dis. Aquat. Org. 14, 179-193.
30. Johnson, K.A., Flynn, J.K., Amend, D.F., 1982. Onset of immunity in salmonid fry vaccinated by direct immersion in Vibrio anguillarum and Yersinia ruckeri bacterins. J. Fish Dis. 5, 197-205.
31. Jones, S.R.M., 2009. Controlling salmon lice on farmed salmon and implications for wild salmon. CAB Rev. 4, 1-13.
32. Jones, S.R.M., Fast, M.D., Johnson, S.C., Groman, D.B., 2007. Differential rejection of salmon lice by pink and chum salmon: disease consequences and expression of proinflammatory genes. Dis. Aquat. Org. 75, 229-238.
33. Jones, S., Kim, E., Bennett, W., 2008. Early development of resistance to the salmon louse, Lepeophtheirus salmonis (Krøyer), in juvenile pink salmon, Oncorhynchus gorbuscha (Walbaum). J. Fish Dis. 31, 591-600. (Pubitemid 351951910)
34. Keas, B.E., Esch, G.W., 1997. The effect of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). J. Parasitol. 83, 96-104.
35. Koop, B.F., von Schalburg, K.R., Leong, J., Walker, N., Lieph, R., Cooper, G.A., Robb, A., Beetz-Sargent, M., Holt, R.A., Moore, R., Brahmbhatt, S., Rosner, J., Rexroad, C.E., McGowan, C.R., Davidson, W.S., 2008. A salmonid EST genomic study: genes, duplications, phylogeny and microarrays. BMC Genomics 9.
36. Kudo, N., Khochbin, S., Nishi, K., Kitano, K., Yanagida, M., Yoshida, M., Horinouchi, S., 1997. Molecular cloning and cell cycle-dependent expression of mammalian CRM1, a protein involved in nuclear export of proteins. J. Biol. Chem. 272, 29742-29751.
37. Labeit, S., Kolmerer, B., 1995. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270, 293-296.
38. Li, C.F., MacDonald, J.R., Wei, R.Y., Ray, J., Lau, K., Kandel, C., Koffman, R., Bell, S., Scherer, S.W., Alman, B.A., 2007. Human sterile alpha motif domain 9, a novel gene identified as down-regulated in aggressive fibromatosis, is absent in the mouse. BMC Genomics 8.
39. Losos, C.J.C., Reynolds, J.D., Dill, L.M., 2010. Sex-selective predation by threespine sticklebacks on sea lice: a novel cleaning behaviour. Ethology 116, 981-989.
40. Mackinnon, B.M., 1993. Host response of Atlantic salmon (Salmo salar) to infection by sea lice (Caligus elongatus). Can. J. Fish. Aquat. Sci. 50, 789-792.
41. Maekawa, M., Nishida, E., Tanoue, T., 2002. Identification of the anti-proliferative protein Tob as a MAPK substrate. J. Biol. Chem. 277, 37783-37787.
42. Nagasawa, K., Ishida, Y., Ogura, M., Tadokoro, K., Hiramatsu, K., 1993. The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on six species of Pacific salmon in offshore waters of the North Pacific Ocean and Bering Sea, In: Boxshall, G., Defaye, D. (Eds.), Pathogens of Wild and Farmed Fish: sea lice, 1st ed. CRC Press, pp. 166-178.
43. Parker, C.M., Cepek, K.L., Russell, G.J., Shaw, S.K., Posnett, D.N., Schwarting, R., Brenner, M.B., 1992. A family of beta-7 integrins on human mucosal lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 89, 1924-1928.
44. Pérez, R., Tupac-Yupanqui, I., Dunner, S., 2008. Evaluation of suitable reference genes for gene expression studies in bovine muscular tissue. BMC Mol. Biol. 9.
45. Pfaffl, M.W., Horgan, G.W., Dempfle, L., 2002. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30.
46. Phares, K., 1996. An unusual host-parasite relationship: the growth hormone-like factor from plerocercoids of spirometrid tapeworms. Int. J. Parasitol. 26, 575-588.
47. Pulkkinen, K., Valtonen, E.T., 1999. Accumulation of plerocercoids of Triaenophorus crassus in the second intermediate host Coregonus lavaretus and their effect on growth of the host. J. Fish Biol. 55, 115-126. (Pubitemid 29311390)
48. Reynisdóttir, I., Polyak, K., Iavarone, A., Massagué, J., 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev. 9, 1831-1845.
49. Rouault, J.P., Rimokh, R., Tessa, C., Paranhos, G., Ffrench, M., Duret, L., Garoccio, M., Germain, D., Samarut, J., Magaud, J.P., 1992. BTG1, a member of a new family of antiproliferative genes. EMBO J. 11, 1663-1670.
50. Rozen, S., Skaletsky, H., 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
51. Saito, J., Toriumi, S., Awano, K., Ichijo, H., Sasaki, K., Kobayashi, T., Tamura, S., 2007. Regulation of apoptosis signal-regulating kinase 1 by protein phosphatase 2C epsilon. Biochem. J. 405, 591-596. (Pubitemid 47172057)
52. Sangfelt, O., Erickson, S., Castro, J., Heiden, T., Gustafsson, A., Einhorn, S., Grandér, D., 1999. Molecular mechanisms underlying interferon-alpha-induced G0/G1 arrest: CKI-mediated regulation of G1 Cdk-complexes and activation of pocket proteins. Oncogene 18, 2798-2810. (Pubitemid 29250869)
53. Skugor, S., Glover, K.A., Nilsen, F., Krasonov, A., 2008. Local and systemic gene expression responses of Atlantic salmon (Salmo salar L.) to infection with the salmon louse (Lepeophtheirus salmonis). BMC Genomics 9, 1-18.
54. Tian, Q.S., Streuli, M., Saito, H., Schlossman, S.F., Anderson, P., 1991. A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell 67, 629-639. (Pubitemid 121001476)
55. Tzachanis, D., Freeman, G.J., Hirano, N., van Puijenbroek, A., Delfs, M.W., Berezovskaya, A., Nadler, L.M., Boussiotis, V.A., 2001. Tob is a negative regulator of activation that is expressed in anergic and quiescent T cells. Nat. Immunol. 2, 1174-1182.
56. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3.
57. Velasco-Miguel, S.,Buckbinder,L., Jean,P.,Gelbert, L.,Talbott,R., Laidlaw, J.,Seizinger, B.,Kley, N., 1999. PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes. Oncogene 18, 127-137.
58. Vogel, B.E., Hedgecock, E.M., 2001. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128, 883-894. (Pubitemid 32288199)
59. von Schalburg, K.R., Rise, M.L., Cooper, G.A., Brown, G.D., Gibbs, A.R., Nelson, C.C., Davidson, W.S., Koop, B.F., 2005. Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 6.
60. Wagner, G.N., McKinley, R.S., Bjørn, P.A., Finstad, B., 2003. Physiological impact of sea lice on swimming performance of Atlantic salmon. J. Fish Biol. 62, 1000-1009. (Pubitemid 38592300)
61. Wagner, G.N., Fast, M.D., Johnson, S.C., 2008. Physiology and immunology of Lepeophtheirus salmonis infections of salmonids. Trends Parasitol. 24, 176-183.
62. Wang, G., Jones, S.J.M., Marra, M.A., Sadar, M.D., 2006. Identification of genes targeted by the androgen and PKA signaling pathways in prostate cancer cells. Oncogene 25, 7311-7323. (Pubitemid 44809097)
63. Wright, E.M., Turk, E., 2004. The sodium/glucose cotransport family SLC5. Pflugers Arch. 447, 510-518. (Pubitemid 38241437)
64. Yen, J.H., Khayrullina, T., Ganea, D., 2008. PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood 111, 260-270.
65. Yu, W., Imoto, I., Inoue, J., Onda, M., Emi, M., Inazawa, J., 2007. A novel amplification target, DUSP26, promotes anaplastic thyroid cancer cell growth by inhibiting p38 MAPK activity. Oncogene 26, 1178-1187.