Involvement of fish signal transducer and activator of transcription 3 (STAT3) in nodavirus infection induced cell death

Fish and Shellfish Immunology

Volumn 43, Issue 1, 2015, Pages 241-248

  Huang, Youhua ^a,b   Huang, Xiaohong ^a,b   Yang, Ying ^a,b   Wang, Wei ^a,b   Yu, Yepin ^a,b   Qin, Qiwei ^a,b  

^a SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Autophagy; Necrotic cell death; RGNNV; STAT3; Viral replication

Indexed keywords

EPINEPHELINAE; NODAVIRIDAE; REDSPOTTED GROUPER NERVOUS NECROSIS VIRUS; SINGAPORE GROUPER IRIDOVIRUS;

FISH PROTEIN; STAT3 PROTEIN;

ANIMAL; BASS; CELL CULTURE; CELL DEATH; FISH DISEASE; GENETICS; METABOLISM; NODAVIRIDAE; PATHOPHYSIOLOGY; PHYSIOLOGY; RNA VIRUS INFECTION; VETERINARY; VIROLOGY;

ANIMALS; BASS; CELL DEATH; CELLS, CULTURED; FISH DISEASES; FISH PROTEINS; NODAVIRIDAE; RNA VIRUS INFECTIONS; STAT3 TRANSCRIPTION FACTOR;

EID: 84921275330     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2014.12.031     Document Type: Article

References (59)

1. Ray J.P., Marshall H.D., Laidlaw B.J., Staron M.M., Kaech S.M., Craft J. Transcription factor STAT3 and type I interferons are corepressive insulators for differentiation of follicular helper and T helper 1 cells. Immunity 2014, 40:367-377.
2. Stark G.R., Darnell J.E. The JAK-STAT pathway at twenty. Immunity 2012, 36:503-514.
3. Koganti S., Hui-Yuen J., McAllister S., Gardner B., Grasser F., Palendira U., et al. STAT3 interrupts ATR-Chk1 signaling to allow oncovirus-mediated cell proliferation. Proc Natl Acad Sci U S A 2014, 111:4946-4951.
4. King C.A. Kaposi's sarcoma-associated herpesvirus kaposin B induces unique monophosphorylation of STAT3 at serine 727 and MK2-mediated inactivation of the STAT3 transcriptional repressor TRIM28. JVirol 2013, 87:8779-8791.
5. Timofeeva O.A., Tarasova N.I., Zhang X., Chasovskikh S., Cheema A.K., Wang H., et al. STAT3 suppresses transcription of proapoptotic genes in cancer cells with the involvement of its N-terminal domain. Proc Natl Acad Sci U S A 2013, 110:1267-1272.
6. Choi S.M., McAleer J.P., Zheng M., Pociask D.A., Kaplan M.H., Qin S., et al. Innate Stat3-mediated induction of the antimicrobial protein Reg3γ is required for host defense against MRSA pneumonia. JExp Med 2013, 210:551-561.
7. Lin L., Liu A., Peng Z., Lin H.J., Li P.K., Li C., et al. STAT3 is necessary for proliferation and survival in colon cancer-initiating cells. Cancer Res 2011, 71:7226-7237.
8. Punjabi A.S., Carroll P.A., Chen L., Lagunoff M. Persistent activation of STAT3 by latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells. JVirol 2007, 81:2449-2458.
9. El Kasmi K.C., Holst J., Coffre M., Mielke L., de Pauw A., Lhocine N., et al. General nature of the STAT3-activated anti-inflammatory response. JImmunol 2006, 177:7880-7888.
10. Huang X., Huang Y., Yang Y., Wei S., Qin Q. Involvement of fish signal transducer and activator of transcription 3 (STAT3) in SGIV replication and virus induced paraptosis. Fish Shellfish Immunol 2014, 41:308-316.
11. Okemoto K., Wagner B., Meisen H., Haseley A., Kaur B., Chiocca E.A. STAT3 activation promotes oncolytic HSV1 replication in glioma cells. PLoS One 2013, 8:e71932.
12. McCartney E.M., Helbig K.J., Narayana S.K., Eyre N.S., Aloia A.L., Beard M.R. Signal transducer and activator of transcription 3 is a proviral host factor for hepatitis C virus. Hepatology 2013, 58:1558-1568.
13. Sen N., Che X., Rajamani J., Zerboni L., Sung P., Ptacek J., et al. Signal transducer and activator of transcription 3 (STAT3) and survivin induction by varicella-zoster virus promote replication and skin pathogenesis. Proc Natl Acad Sci U S A 2012, 109:600-605.
14. Wang W.B., Levy D.E., Lee C.K. STAT3 negatively regulates type I IFN-mediated antiviral response. JImmunol 2011, 187:2578-2585.
15. Sargeant T.J., Lloyd-Lewis B., Resemann H.K., Ramos-Montoya A., Skepper J., Watson C.J. Stat3 controls cell death during mammary gland involution by regulating uptake of milk fat globules and lysosomal membrane permeabilization. Nat Cell Biol 2014, 16:1057-1068.
16. Shulga N., Pastorino J.G. GRIM-19-mediated translocation of STAT3 to mitochondria is necessary for TNF-induced necroptosis. JCell Sci 2012, 125:2995-3003.
17. Shen S., Niso-Santano M., Adjemian S., Takehara T., Malik S.A., Minoux H., et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell 2012, 48:667-680.
18. Thyrell L., Arulampalam V., Hjortsberg L., Farnebo M., Grandér D., Pokrovskaja Tamm K. Interferon alpha induces cell death through interference with interleukin 6 signaling and inhibition of STAT3 activity. Exp Cell Res 2007, 313:4015-4024.
19. Keawcharoen J., Techangamsuwan S., Ponpornpisit A., Lombardini E.D., Patchimasiri T., Pirarat N. Genetic characterization of a betanodavirus isolated from a clinical disease outbreak in farm-raised tilapia Oreochromis niloticus (L.) in Thailand. JFish Dis 2013, 10.1111/jfd.12200.
20. Liu H., Teng Y., Zheng X., Wu Y., Xie X., He J., et al. Complete sequence of a viral nervous necrosis virus (NNV) isolated from red-spotted grouper (Epinephelus akaara) in China. Arch Virol 2012, 157:777-782.
21. Gomez D.K., Matsuoka S., Mori K., Okinaka Y., Park S.C., Nakai T. Genetic analysis and pathogenicity of betanodavirus isolated from wild redspotted grouper Epinephelus akaara with clinical signs. Arch Virol 2009, 154:343-346.
22. Furusawa R., Okinaka Y., Nakai T. Betanodavirus infection in the freshwater model fish medaka (Oryzias latipes). JGen Virol 2006, 87:2333-2339.
23. Johansen R., Sommerset I., Tørud B., Korsnes K., Hjortaas M.J., Nilsen F., et al. Characterization of nodavirus and viral encephalopathy and retinopathy in farmed turbot, Scophthalmus maximus (L.). JFish Dis 2004, 27:591-601.
24. Tan C., Huang B., Chang S.F., Ngoh G.H., Munday B., Chen S.C., et al. Determination of the complete nucleotide sequences of RNA1 and RNA2 from greasy grouper (Epinephelus tauvina) nervous necrosis virus, Singapore strain. JGen Virol 2001, 82:647-653.
25. Kara H.M., Chaoui L., Derbal F., Zaidi R., de Boisséson C., Baud M., et al. Betanodavirus-associated mortalities of adult wild groupers Epinephelus marginatus (Lowe) and Epinephelus costae (Steindachner) in Algeria. JFish Dis 2014, 37:273-278.
26. Roongkamnertwongsa S., Kanchanakhan S., Danayadol Y. Isolation and characteristics of nodavirus from giant grouper (Epinephelus ianceolatus). JFish Technol Res 2008, 2:146-158.
27. Liu W., Hsu C.H., Hong Y.R., Wu S.C., Wang C.H., Wu Y.M., et al. Early endocytosis pathways in SSN-1 cells infected by dragon grouper nervous necrosis virus. JGen Virol 2005, 86:2553-2561.
28. Lai Y.S., Murali S., Chiu H.C., Ju H.Y., Lin Y.S., Chen S.C., et al. Propagation of yellow grouper nervous necrosis virus (YGNNV) in a new nodavirus-susceptible cell line from yellow grouper, Epinephelus awoara (Temminck & Schlegel), brain tissue. JFish Dis 2001, 24:299-309.
29. Huang Y.H., Huang X.H., Ouyang Z.L., Wei S.N., Guo C.Y., Qin Q.W. Development of a new cell line from the snout of giant grouper, Epinephelus lanceolatus (Bloch), and its application in iridovirus and nodavirus pathogenesis. Aquaculture 2014, 432:265-272.
30. Chang J.S., Chi S.C. Grouper heat-shock cognate protein 70 (GHSC70) is involved in the cellular entry of nervous necrosis virus (NNV). JVirol 2014, pii: JVI.02523-14.
31. Su Y.C., Wu J.L., Hong J.R. Betanodavirus up-regulates chaperone GRP78 via ER stress: roles of GRP78 in viral replication and host mitochondria-mediated cell death. Apoptosis 2011, 16:272-287.
32. Hong J.R. Betanodavirus: mitochondrial disruption and necrotic cell death. World J Virol 2013, 2:1-5.
33. Chen S.P., Yang H.L., Her G.M., Lin H.Y., Jeng M.F., Wu J.L., et al. Betanodavirus induces phosphatidylserine exposure and loss of mitochondrial membrane potential in secondary necrotic cells, both of which are blocked by bongkrekic acid. Virology 2006, 347:379-391.
34. Wu H.C., Chiu C.S., Wu J.L., Gong H.Y., Chen M.C., Lu M.W., et al. Zebrafish anti-apoptotic protein zfBcl-xL can block betanodavirus protein alpha-induced mitochondria-mediated secondary necrosis cell death. Fish Shellfish Immunol 2008, 24:436-449.
35. Chen S.P., Wu J.L., Su Y.C., Hong J.R. Anti-Bcl-2 family members, zfBcl-x(L) and zfMcl-1a, prevent cytochrome c release from cells undergoing betanodavirus-induced secondary necrotic cell death. Apoptosis 2007, 12:1043-1060.
36. Huang X.H., Huang Y.H., Ouyang Z.L., Qin Q.W. Establishment of a cell line from the brain of grouper (Epinephelus akaara) for cytotoxicity testing and virus pathogenesis. Aquaculture 2011, 311:65-73.
37. Guo M., Wei J., Huang X., Huang Y., Qin Q. Antiviral effects of β-defensin derived from orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol 2012, 32:828-838.
38. Chan F.K., Moriwaki K., De Rosa M.J. Detection of necrosis by release of lactate dehydrogenase activity. Methods Mol Biol 2013, 979:65-70.
39. Yang J., Chatterjee-Kishore M., Staugaitis S.M., Nguyen H., Schlessinger K., Levy D.E., et al. Novel roles of unphosphorylated STAT3 in oncogenesis and transcriptional regulation. Cancer Res 2005, 65:939-947.
40. Zhao J., Brault J.J., Schild A., Goldberg A.L. Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 2008, 4:378-380.
41. Kroemer G., Mariño G., Levine B. Autophagy and the integrated stress response. Mol Cell 2010, 40:280-293.
42. Jamart C., Benoit N., Raymackers J.M., Kim H.J., Kim C.K., Francaux M. Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise. Eur J Appl Physiol 2012, 112:3173-3177.
43. Zhirnov O.P., Klenk H.D. Influenza A virus proteins NS1 and hemagglutinin along with M2 are involved in stimulation of autophagy in infected cells. JVirol 2013, 87:13107-13114.
44. Cha H.H., Hwang J.R., Kim H.Y., Choi S.J., Oh S.Y., Roh C.R. Autophagy induced by tumor necrosis factor α mediates intrinsic apoptosis in trophoblastic cells. Reprod Sci 2014, 21:612-622.
45. Peral de Castro C., Jones S.A., Ní Cheallaigh C., Hearnden C.A., Williams L., Winter J., et al. Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion. JImmunol 2012, 189:4144-4153.
46. Kleinnijenhuis J., Oosting M., Plantinga T.S., van der Meer J.W., Joosten L.A., Crevel R.V., et al. Autophagy modulates the Mycobacterium tuberculosis-induced cytokine response. Immunology 2011, 134:341-348.
47. Harris J. Autophagy and IL-1 family cytokines. Front Immunol 2013, 4:83.
48. Park H.J., Lee S.J., Kim S.H., Han J., Bae J., Kim S.J., et al. IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 2011, 48:720-727.
49. Yoshida T., Hanada T., Tokuhisa T., Kosai K., Sata M., Kohara M., et al. Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation. JExp Med 2002, 196:641-653.
50. Reitsma J.M., Sato H., Nevels M., Terhune S.S., Paulus C. Human cytomegalovirus IE1 protein disrupts interleukin-6 signaling by sequestering STAT3 in the nucleus. JVirol 2013, 87:10763-10776.
51. Granato M., Santarelli R., Farina A., Gonnella R., Lotti L.V., Faggioni A., et al. Epstein-Barr virus blocks the autophagic flux and appropriates the autophagic machinery to enhance viral replication. JVirol 2014, 88:12715-12726.
52. Hung C.H., Chen L.W., Wang W.H., Chang P.J., Chiu Y.F., Hung C.C., et al. Regulation of autophagic activation by Rta of Epstein-Barr virus via the extracellular signal-regulated kinase pathway. JVirol 2014, 88:12133-12145.
53. Sun Y., Yu S., Ding N., Meng C., Meng S., Zhang S., et al. Autophagy benefits the replication of Newcastle disease virus in chicken cells and tissues. JVirol 2014, 88:525-537.
54. Kim C., Bergelson J.M. Echovirus 7 entry into polarized caco-2 intestinal epithelial cells involves core components of the autophagy machinery. JVirol 2014, 88:434-443.
55. Wirawan E., Vanden Berghe T., Lippens S., Agostinis P., Vandenabeele P. Autophagy: for better or for worse. Cell Res 2012, 22:43-61.
56. Gammoh N., Lam D., Puente C., Ganley I., Marks P.A., Jiang X. Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci U S A 2012, 109:6561-6565.
57. McLean J.E., Wudzinska A., Datan E., Quaglino D., Zakeri Z. Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. JBiol Chem 2011, 286:22147-22159.
58. Kim J.S., Nitta T., Mohuczy D., O'Malley K.A., Moldawer L.L., Dunn W.A., et al. Impaired autophagy: a mechanism of mitochondrial dysfunction in anoxic rat hepatocytes. Hepatology 2008, 47:1725-1736.
59. Nishida Y., Arakawa S., Fujitani K., Yamaguchi H., Mizuta T., Kanaseki T., et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009, 461:654-658.