Antagonism of RNase L is required for murine coronavirus replication in Kupffer cells and liver sinusoidal endothelial cells but not in hepatocytes

Journal of Virology

Volumn 90, Issue 21, 2016, Pages 9826-9832

  Li, Yize ^a   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; RIBONUCLEASE L; 2',5'-OLIGOADENYLATE; 2-5A-DEPENDENT RIBONUCLEASE; ADENINE NUCLEOTIDE; OLIGORIBONUCLEOTIDE; RIBONUCLEASE; VIRAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; HEPATITIS; HISTOPATHOLOGY; KUPFFER CELL; LIVER CELL; MOUSE; MURINE CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; RNA DEGRADATION; VIROGENESIS; VIRUS REPLICATION; VIRUS TITRATION; WESTERN BLOTTING; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CORONAVIRINAE; DNA REPLICATION; GENETICS; HOST PATHOGEN INTERACTION; LIVER; METABOLISM; MURINE HEPATITIS VIRUS; PHYSIOLOGY; VIROLOGY;

2',5'-OLIGOADENYLATE SYNTHETASE; ADENINE NUCLEOTIDES; ANIMALS; CELLS, CULTURED; CORONAVIRUS; DNA REPLICATION; ENDORIBONUCLEASES; ENDOTHELIAL CELLS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; KUPFFER CELLS; LIVER; MICE; MICE, INBRED C57BL; MURINE HEPATITIS VIRUS; MYELOID CELLS; OLIGORIBONUCLEOTIDES; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84994048698     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01423-16     Document Type: Article

References (29)

1. Cavanagh D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol 142:629-633.
2. Weiss SR, Leibowitz JL. 2011. Coronavirus pathogenesis. Adv Virus Res 81:85-164. http://dx.doi.org/10.1016/B978-0-12-385885-6.00009-2.
3. Zhao L, Jha BK, Wu A, Elliott R, Ziebuhr J, Gorbalenya AE, Silverman RH, Weiss SR. 2012. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 11:607-616. http://dx.doi.org/10.1016/j.chom.2012.04.011.
4. Dong B, Silverman RH. 1995. 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J Biol Chem 270:4133-4137. http://dx.doi.org/10.1074/jbc.270.8.4133.
5. Han JQ, Barton DJ. 2002. Activation and evasion of the antiviral 2=-5= oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA 8:512-525. http://dx.doi.org/10.1017/S1355838202020617.
6. Washenberger CL, Han JQ, Kechris KJ, Jha BK, Silverman RH, Barton DJ. 2007. Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res 130:85-95. http://dx.doi.org/10.1016/j.virusres.2007.05.020.
7. Kakuta S, Shibata S, Iwakura Y. 2002. Genomic structure of the mouse 2=,5=-oligoadenylate synthetase gene family. J Interferon Cytokine Res 22: 981-993. http://dx.doi.org/10.1089/10799900260286696.
8. Justesen J, Hartmann R, Kjeldgaard NO. 2000. Gene structure and function of the 2=-5=-oligoadenylate synthetase family. Cell Mol Life Sci 57:1593-1612. http://dx.doi.org/10.1007/PL00000644.
9. Zhao L, Birdwell LD, Wu A, Elliott R, Rose KM, Phillips JM, Li Y, Grinspan J, Silverman RH, Weiss SR. 2013. Cell-type-specific activation of the oligoadenylate synthetase-RNase L pathway by a murine coronavirus. J Virol 87:8408-8418. http://dx.doi.org/10.1128/JVI.00769-13.
10. Birdwell LD, Zalinger ZB, Li Y, Wright PW, Elliott R, Rose KM, Silverman RH, Weiss SR. 2016. Activation of RNase L by murine coronavirus in myeloid cells is dependent on basal Oas gene expression and independent of virus-induced interferon. J Virol 90:3160-3172. http://dx.doi.org/10.1128/JVI.03036-15.
11. Racanelli V, Rehermann B. 2006. The liver as an immunological organ. Hepatology 43:S54-S62. http://dx.doi.org/10.1002/hep.21060.
12. Crispe IN. 2009. The liver as a lymphoid organ. Annu Rev Immunol 27:147-163. http://dx.doi.org/10.1146/annurev.immunol.021908.132629.
13. Reference deleted.
14. Roth-Cross JK, Stokes H, Chang G, Chua MM, Thiel V, Weiss SR, Gorbalenya AE, Siddell SG. 2009. Organ-specific attenuation of murine hepatitis virus strain A59 by replacement of catalytic residues in the putative viral cyclic phosphodiesterase ns2. J Virol 83:3743-3753. http://dx.doi.org/10.1128/JVI.02203-08.
15. Schwarz B, Routledge E, Siddell SG. 1990. Murine coronavirus nonstructural protein ns2 is not essential for virus replication in transformed cells. J Virol 64:4784-4791.
16. Kitani H, Takenouchi T, Sato M, Yoshioka M, Yamanaka N. 24 May 2011. A simple and efficient method to isolate macrophages from mixed primary cultures of adult liver. J Vis Exp http://dx.doi.org/10.3791/2757.
17. Øie CI, Appa RS, Hilden I, Petersen HH, Gruhler A, Smedsrød B, Hansen JB. 2011. Rat liver sinusoidal endothelial cells (LSECs) express functional low density lipoprotein receptor-related protein-1 (LRP-1). J Hepatol 55:1346-1352. http://dx.doi.org/10.1016/j.jhep.2011.03.013.
18. Gombold JL, Hingley ST, Weiss SR. 1993. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J Virol 67:4504-4512.
19. Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP. 2005. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 115:56-65. http://dx.doi.org/10.1172/JCI200522675.
20. Li J, Ning G, Duncan SA. 2000. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 14:464-474.
21. Klein I, Cornejo JC, Polakos NK, John B, Wuensch SA, Topham DJ, Pierce RH, Crispe IN. 2007. Kupffer cell heterogeneity: functional properties of bone marrow-derived and sessile hepatic macrophages. Blood 110:4077-4085. http://dx.doi.org/10.1182/blood-2007-02-073841.
22. Ling W, Lougheed M, Suzuki H, Buchan A, Kodama T, Steinbrecher UP. 1997. Oxidized or acetylated low density lipoproteins are rapidly cleared by the liver in mice with disruption of the scavenger receptor class A type I/II gene. J Clin Invest 100:244-252. http://dx.doi.org/10.1172/JCI119528.
23. Malhi H, Annamaneni P, Slehria S, Joseph B, Bhargava KK, Palestro CJ, Novikoff PM, Gupta S. 2002. Cyclophosphamide disrupts hepatic sinusoidal endothelium and improves transplanted cell engraftment in rat liver. Hepatology 36:112-121. http://dx.doi.org/10.1053/jhep.2002.33896.
24. van Til NP, Markusic DM, van der Rijt R, Kunne C, Hiralall JK, Vreeling H, Frederiks WM, Oude-Elferink RP, Seppen J. 2005. Kupffer cells and not liver sinusoidal endothelial cells prevent lentiviral transduction of hepatocytes. Mol Ther 11:26-34. http://dx.doi.org/10.1016/j.ymthe.2004.09.012.
25. Li YZ, Banerjee S, Wang YY, Goldstein SA, Dong BH, Gaughan C, Silverman RH, Weiss SR. 2016. Activation of RNase L is dependent on OAS3 expression during infection with diverse human viruses. Proc Natl Acad Sci U S A 113:2241-2246. http://dx.doi.org/10.1073/pnas.1519657113.
26. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336:86-90. http://dx.doi.org/10.1126/science.1219179.
27. Cervantes-Barragán L, Kalinke U, Züst R, König M, Reizis B, López-Macías C, Thiel V, Ludewig B. 2009. Type I IFN-mediated protection of macrophages and dendritic cells secures control of murine coronavirus infection. J Immunol 182:1099-1106. http://dx.doi.org/10.4049/jimmunol.182.2.1099.
28. Elvevold K, Smedsrod B, Martinez I. 2008. The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity.AmJ Physiol Gastrointest Liver Physiol 294:G391-G400.
29. Castelli JC, Hassel BA, Maran A, Paranjape J, Hewitt JA, Li XL, Hsu YT, Silverman RH, Youle RJ. 1998. The role of 2=-5= oligoadenylate-activated ribonuclease L in apoptosis. Cell Death Differ 5:313-320. http://dx.doi.org/10.1038/sj.cdd.4400352.