Analysis of host- and strain-dependent cell death responses during infectious salmon anemia virus infection in vitro

Virology Journal

Volumn 6, Issue , 2009, Pages

  Schiøtz, Berit L ^a   Bækkevold, Espen S ^a   Poulsen, Lene C ^a   Mjaaland, Siri ^b   Gjøen, Tor ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; INTERFERON; PHOSPHATIDYLSERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATLANTIC SALMON; CELL DEATH; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; FISH DISEASE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INFECTIOUS SALMON ANEMIA; INFECTIOUS SALMON ANEMIA VIRUS; MITOCHONDRION; MORPHOLOGY; MORTALITY; NONHUMAN; ORTHOMYXOVIRUS; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS STRAIN; ANIMAL; CELL LINE; CELL MEMBRANE; CELL SURVIVAL; CHEMISTRY; METABOLISM; PATHOGENICITY; PHYSIOLOGY;

INFECTIOUS SALMON ANEMIA VIRUS; ORTHOMYXOVIRIDAE; SALMO SALAR;

ANIMALS; CASPASE 3; CASPASE 7; CELL DEATH; CELL LINE; CELL MEMBRANE; CELL SURVIVAL; ISAVIRUS; MITOCHONDRIA; PHOSPHATIDYLSERINES; SALMO SALAR;

EID: 68349124973     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-6-91     Document Type: Article

References (59)

1. Orthomyxoviridae. Y Kawaoka NJ Cox O Haller S Hongo N Kaverin H-D Klenk RA Lamb J McCauley P Palese E Rimstad RG Webster, Virus Taxonomy, Classification and Nomenclature of Viruses, Eight report of the International Committee on the Taxonomy of Viruses New York: Elsevier Academic Press, Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, 2005 681 693
2. Mortality patterns in infectious salmon anaemia virus outbreaks in New Brunswick, Canada. KL Hammell IR Dohoo, J Fish Dis 2005 28 639 650 10.1111/j.1365-2761.2005.00667.x 16303026
3. Epidemiological investigation of infectious salmon anaemia (ISA) outbreaks in Norway 20032005. TM Lyngstad PA Jansen H Sindre CM Jonassen MJ Hjortaas S Johnsen E Brun, Prev Vet Med 2008 84 213 227 10.1016/j.prevetmed. 2007.12.008 18243376
4. Isolation of infectious salmon anemia virus (ISAV) from Atlantic salmon in New Brunswick, Canada. D Bouchard W Keleher HM Opitz S Blake KC Edwards BL Nicholson, Dis Aquat Organ 1999 35 131 137 10.3354/dao035131 10092976
5. First identification of infectious salmon anaemia virus in North America with haemorrhagic kidney syndrome. JE Lovely BH Dannevig K Falk L Hutchin AM MacKinnon KJ Melville E Rimstad SG Griffiths, Dis Aquat Organ 1999 35 145 148 10.3354/dao035145 10092978
6. Susceptibility and immune responses following experimental infection of MHC compatible Atlantic salmon (Salmo salar L.) with different infectious salmon anaemia virus isolates. S Mjaaland T Markussen H Sindre S Kjoglum BH Dannevig S Larsen U Grimholt, Arch Virol 2005 150 2195 2216 10.1007/s00705-005-0588-8 16012784 (Pubitemid 41456021)
7. Comparative virulence of Infectious salmon anaemia virus isolates in Atlantic salmon, Salmo salar L. RJ Ritchie JT McDonald B Glebe W Young-Lai E Johnsen N Gagne, J Fish Dis 2009 32 157 171 10.1111/j.1365-2761.2008.00973.x 19261043
8. Virulence and pathogenicity of infectious salmon anemia virus isolated from farmed salmon in Atlantic Canada. SRM Jones AM MacKinnon DB Groman, Journal of Aquatic Animal Health 1999 11 400 405 10.1577/1548-8667(1999)011<0400: VAPOIS2.0.CO;2
9. Cohabitation transmission of infectious salmon anemia virus among freshwater-reared Atlantic salmon. SRM Jones DB Groman, Journal of Aquatic Animal Health 2001 13 340 346 10.1577/1548-8667(2001)013<0340:CTOISA2.0.CO;2
10. Experimental infection models and susceptibility of Atlantic salmon Salmo salar to a Scottish isolate of infectious salmon anaemia virus. RS Raynard M Snow DW Bruno, Dis Aquat Organ 2001 47 169 174 10.3354/dao047169 11804415
11. Relative resistance of Pacific salmon to infectious salmon anaemia virus. JB Rolland JR Winton, J Fish Dis. 2003 26 9 511 520 10.1046/j.1365-2761.2003. 00473.x 14575369 (Pubitemid 37261409)
12. Infectious anemia in Atlantic salmon (Salmo salar L.). KE Thorud HO Djupvik, Bull Eur Assoc Fish Pathol 1988 8 109 111
13. Mechanism of cell death during infectious salmon anemia virus infection is cell type-specific. T Joseph A Cepica L Brown BO Ikede FS Kibenge, J Gen Virol 2004 85 3027 3036 10.1099/vir.0.80091-0 15448366 (Pubitemid 39360047)
14. Apoptosis: an innate immune response to virus infection. H Everett G McFadden, Trends Microbiol 1999 7 160 165 10.1016/S0966-842X(99)01487-0 10217831 (Pubitemid 29229902)
15. Role of apoptosis and cytokines in influenza virus morbidity. EW Brydon SJ Morris C Sweet, FEMS Microbiol Rev 2005 29 837 850 10.1016/j.femsre.2004.12. 003 16102605 (Pubitemid 41139183)
16. Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. H Fesq M Bacher M Nain D Gemsa, Immunobiology 1994 190 175 182 8082884
17. Apoptosis: a mechanism of cell killing by influenza A and B viruses. VS Hinshaw CW Olsen N Dybdahl-Sissoko D Evans, J Virol 1994 68 3667 3673 8189504
18. Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells. T Takizawa S Matsukawa Y Higuchi S Nakamura Y Nakanishi R Fukuda, J Gen Virol 1993 74 Pt 11 2347 2355 10.1099/0022-1317-74- 11-2347 7504071
19. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. JF Kerr AH Wyllie AR Currie, Br J Cancer 1972 26 239 257 4561027
20. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. VA Fadok DR Voelker PA Campbell JJ Cohen DL Bratton PM Henson, J Immunol 1992 148 2207 2216 1545126
21. To kill or be killed: viral evasion of apoptosis. CA Benedict PS Norris CF Ware, Nat Immunol 2002 3 1013 1018 10.1038/ni1102-1013 12407409 (Pubitemid 35363651)
22. A time to kill: viral manipulation of the cell death program. S Hay G Kannourakis, J Gen Virol 2002 83 1547 1564 12075073
23. Genes with homology to mammalian apoptosis regulators identified in zebrafish. N Inohara G Nunez, Cell Death Differ 2000 7 509 510 10.1038/sj.cdd.4400679 10917738
24. Caspases and apoptosis in fish. H Takle O Andersen, 2007 71 326 349 18262834
25. Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos. H Takle A McLeod O Andersen, Comp Biochem Physiol B Biochem Mol Biol 2006 144 188 198 10.1016/j.cbpb.2006.02.006 16574452
26. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. J Bereiter-Hahn M Voth, Microsc Res Tech 1994 27 198 219 10.1002/jemt.1070270303 8204911
27. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. S Frank B Gaume ES Bergmann-Leitner WW Leitner EG Robert F Catez CL Smith RJ Youle, Dev Cell 2001 1 515 525 10.1016/S1534-5807(01)00055-7 11703942 (Pubitemid 33586103)
28. Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. K Morimoto DC Hooper S Spitsin H Koprowski B Dietzschold, J Virol 1999 73 510 518 9847357
29. Induction of apoptosis by paramyxovirus simian virus 5 lacking a small hydrophobic gene. Y Lin AC Bright TA Rothermel B He, J Virol 2003 77 3371 3383 12610112 10.1128/JVI.77.6.3371-3383.2003 (Pubitemid 36297256)
30. Increased induction of apoptosis by a Sendai virus mutant is associated with attenuation of mouse pathogenicity. M Itoh H Hotta M Homma, J Virol 1998 72 2927 2934 9525613
31. Transcriptomic analysis of responses to infectious salmon anemia virus infection in macrophage-like cells. BL Schiotz SM Jorgensen C Rexroad T Gjoen A Krasnov, Virus Res 2008 136 65 74 10.1016/j.virusres.2008.04.019 18534703
32. Induction of a common pathway of apoptosis by staurosporine. R Bertrand E Solary P O'Connor KW Kohn Y Pommier, Exp Cell Res 1994 211 314 321 10.1006/excr.1994.1093 8143779 (Pubitemid 24174963)
33. Constitutive expression of the machinery for programmed cell death. M Weil MD Jacobson HS Coles TJ Davies RL Gardner KD Raff MC Raff, J Cell Biol 1996 133 1053 1059 8655578 10.1083/jcb.133.5.1053 (Pubitemid 26172510)
34. Caspases: the executioners of apoptosis. GM Cohen, Biochem J 1997 326 Pt 1 1 16 9337844
35. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. S Van Cruchten W Van Den Broeck, Anat Histol Embryol 2002 31 214 223 10.1046/j.1439-0264.2002.00398.x 12196263
36. YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. T Idziorek J Estaquier F De Bels JC Ameisen, J Immunol Methods 1995 185 249 258 10.1016/0022-1759(95)00172- 7 7561136
37. Expression of MHC class I pathway genes in response to infectious salmon anaemia virus in Atlantic salmon (Salmo salar L.) cells. SM Jorgensen BL Syvertsen M Lukacs U Grimholt T Gjoen, Fish Shellfish Immunol 2006 21 548 560 10.1016/j.fsi.2006.03.004 16772112 (Pubitemid 44499022)
38. Isolation of a FIP2-like gene from Atlantic salmon (Salmo salar L.), found upregulated following infection with the monogenean parasite Gyrodactylus salaris Malmberg, 1957. CM Collins K Olstad E Sterud CS Jones LR Noble TA Mo CO Cunningham, Fish Shellfish Immunol 2007 22 282 288 10.1016/j.fsi.2006.06.006 16928451 (Pubitemid 44828539)
39. Gene expression profiles of some immune relevant genes from skin of susceptible and responding Atlantic salmon (Salmo salar L.) infected with Gyrodactylus salaris (Monogenea) revealed by suppressive subtractive hybridisation. I Matejusova B Felix T Sorsa-Leslie J Gilbey LR Noble CS Jones CO Cunningham, Int J Parasitol 2006 36 1175 1183 10.1016/j.ijpara.2006.04.009 16806223 (Pubitemid 44240431)
40. Cloning and expression of TNF-alpha, IL-1beta and COX-2 in an anadromous and landlocked strain of Atlantic salmon (Salmo salar L.) during the smolting period. HC Ingerslev C Cunningham HI Wergeland, Fish Shellfish Immunol 2006 20 450 461 10.1016/j.fsi.2005.06.002 16246585 (Pubitemid 41571243)
41. Viral Subversion of Apoptotic Enzymes: Escape from Death Row. SM Best, 2008 62 18729734
42. Morphological changes contribute to apoptotic cell death and are affected by caspase-3 and caspase-6 inhibitors during red sea bream iridovirus permissive replication. M Imajoh H Sugiura S Oshima, Virology 2004 322 220 230 10.1016/j.virol.2004.02.006 15110520 (Pubitemid 38521137)
43. Induction of apoptotic death in cells via Bad gene expression by infectious pancreatic necrosis virus infection. JR Hong JL Wu, Cell Death Differ 2002 9 113 124 10.1038/sj.cdd.4400933 11840162
44. Iridovirus Bcl-2 protein inhibits apoptosis in the early stage of viral infection. PW Lin YJ Huang JA John YN Chang CH Yuan WY Chen CH Yeh ST Shen FP Lin WH Tsui CY Chang, Apoptosis 2008 13 165 176 10.1007/s10495-007-0152-y 17955372
45. A novel influenza A virus mitochondrial protein that induces cell death. W Chen PA Calvo D Malide J Gibbs U Schubert I Bacik S Basta R O'Neill J Schickli P Palese, Nat Med 2001 7 1306 1312 10.1038/nm1201-1306 11726970 (Pubitemid 34007934)
46. Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. AL McCormick VL Smith D Chow ES Mocarski, J Virol 2003 77 631 641 12477866 10.1128/JVI.77.1.631-641.2003 (Pubitemid 36005000)
47. Mitochondrial distribution and function in herpes simplex virus-infected cells. T Murata F Goshima T Daikoku K Inagaki-Ohara H Takakuwa K Kato Y Nishiyama, J Gen Virol 2000 81 401 406 10644838
48. Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells. YH Huang XH Huang JF Gui QY Zhang, Apoptosis 2007 12 1569 1577 10.1007/s10495-007-0089-1 17551838
49. Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. I Kruman Q Guo MP Mattson, J Neurosci Res 1998 51 293 308 10.1002/(SICI)1097-4547(19980201)51: 3<293::AID-JNR33.0.CO;2-B 9486765
50. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. JT Cribbs S Strack, EMBO Rep 2007 8 939 944 17721437 10.1038/sj.embor.7401062 (Pubitemid 47500477)
51. Real-time imaging of mitochondria in transgenic zebrafish expressing mitochondrially targeted GFP. MJ Kim KH Kang CH Kim SY Choi, Biotechniques 2008 45 331 334 10.2144/000112909 18778258
52. Caspase 3 activation is essential for efficient influenza virus propagation. WJ Wurzer O Planz C Ehrhardt M Giner T Silberzahn S Pleschka S Ludwig, Embo J 2003 22 2717 2728 12773387 10.1093/emboj/cdg279 (Pubitemid 36712368)
53. Detection of Apoptotic DNA Ladder in Pig Leukocytes and its Precision Using LM-PCR (Ligation Mediated Polymerase Chain Reaction). ESA Matalova, ACTA VETERINARIA BRNO 2002 71 163 168
54. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. SJ Martin CP Reutelingsperger AJ McGahon JA Rader RC van Schie DM LaFace DR Green, J Exp Med 1995 182 1545 1556 7595224 10.1084/jem.182.5.1545
55. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. JC Kash TM Tumpey SC Proll V Carter O Perwitasari MJ Thomas CF Basler P Palese JK Taubenberger A Garcia-Sastre, Nature 2006 443 578 581 17006449
56. Transcriptional response of a common permissive cell type to infection by two diverse alphaherpesviruses. N Ray LW Enquist, J Virol 2004 78 3489 3501 15016872 10.1128/JVI.78.7.3489-3501.2004 (Pubitemid 38568291)
57. Host-cell interaction of attenuated and wild-type strains of yellow fever virus can be differentiated at early stages of hepatocyte infection. A Lefeuvre H Contamin T Decelle C Fournier J Lang V Deubel P Marianneau, Microbes Infect 2006 8 1530 1538 10.1016/j.micinf.2006.01.013 16697681 (Pubitemid 44192355)
58. Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. T Markussen CM Jonassen S Numanovic S Braaen M Hjortaas H Nilsen S Mjaaland, Virology 2008 374 515 527 10.1016/j.virol.2008.01.019 18280528
59. Validation of reference genes for real-time polymerase chain reaction studies in Atlantic salmon. SM Jorgensen EJ Kleveland U Grimholt T Gjoen, Mar Biotechnol (NY) 2006 8 398 408 10.1007/s10126-005-5164-4 16676145 (Pubitemid 44221549)