Viral double-stranded RNA sensors induce antiviral, pro-inflammatory, and pro-apoptotic responses in human renal tubular epithelial cells

Kidney International

Volumn 82, Issue 6, 2012, Pages 664-675

  Heutinck, Kirstin M ^a   Rowshani, Ajda T ^a,b   Kassies, Jorien ^a   Claessen, Nike ^a   Van Donselaar Van Der Pant, Karlijn A M I ^a   Bemelman, Fréderike J ^a   Eldering, Eric ^a   Van Lier, René A W ^a   Florquin, Sandrine ^a   Ten Berge, Ineke J M ^a   Hamann, Jörg ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

apoptosis; BK virus; cytomegalovirus; dsRNA receptors; tubular epithelial cells

Indexed keywords

BETA INTERFERON; CYTOPLASMIC RECEPTOR; DOUBLE STRANDED RNA; FAS ANTIGEN; MELANOMA DIFFERENTIATION ASSOCIATED GENE 5 PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; BK VIRUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; EPITHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY GRAFT; KIDNEY TUBULE EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 84865803520     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.206     Document Type: Article

References (67)

1. Weikert BC, Blumberg EA. Viral infection after renal transplantation: surveillance and management. Clin J Am Soc Nephrol 2008; 3(Suppl 2): S76-S86.
2. Staras SA, Dollard SC, Radford KW et al. Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis 2006; 43: 1143-1151.
3. Egli A, Infanti L, Dumoulin A et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 2009; 199: 837-846.
4. Morris MC, Edmunds WJ, Hesketh LM et al. Sero-epidemiological patterns of Epstein-Barr and herpes simplex (HSV-1 and HSV-2) viruses in England and Wales. J Med Virol 2002; 67: 522-527.
5. Boothpur R, Brennan DC. Human polyoma viruses and disease with emphasis on clinical BK and JC. J Clin Virol 2010; 47: 306-312.
6. Becker JL, Miller F, Nuovo GJ et al. Epstein-Barr virus infection of renal proximal tubule cells: possible role in chronic interstitial nephritis. J Clin Invest 1999; 104: 1673-1681.
7. Low J, Humes HD, Szczypka M et al. BKV and SV40 infection of human kidney tubular epithelial cells in vitro. Virology 2004; 323: 182-188.
8. Bowie AG, Unterholzner L. Viral evasion and subversion of patternrecognition receptor signalling. Nat Rev Immunol 2008; 8: 911-922.
9. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140: 805-820.
10. Kawai T, Takahashi K, Sato S et al. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-988.
11. Borden EC, Sen GC, Uze G et al. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 2007; 6: 975-990.
12. Trinchieri G. Type I interferon: friend or foe? J Exp Med 2010; 207: 2053-2063.
13. Besch R, Poeck H, Hohenauer T et al. Proapoptotic signaling induced by RIG-I and MDA-5 results in type I interferon-independent apoptosis in human melanoma cells. J Clin Invest 2009; 119: 2399-2411.
14. Lallemand C, Blanchard B, Palmieri M et al. Single-stranded RNA viruses inactivate the transcriptional activity of p53 but induce NOXA-dependent apoptosis via post-translational modifications of IRF-1, IRF-3 and CREB. Oncogene 2007; 26: 328-338.
15. Chattopadhyay S, Marques JT, Yamashita M et al. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J 2010; 29: 1762-1773.
16. Paone A, Starace D, Galli R et al. Toll-like receptor 3 triggers apoptosis of human prostate cancer cells through a PKC-alpha-dependent mechanism. Carcinogenesis 2008; 29: 1334-1342.
17. Peng S, Geng J, Sun R et al. Polyinosinic-polycytidylic acid liposome induces human hepatoma cells apoptosis which correlates to the up-regulation of RIG-I like receptors. Cancer Sci 2009; 100: 529-536.
18. Weber A, Kirejczyk Z, Besch R et al. Proapoptotic signalling through Tolllike receptor-3 involves TRIF-dependent activation of caspase-8 and is under the control of inhibitor of apoptosis proteins in melanoma cells. Cell Death Differ 2010; 17: 942-951.
19. Galluzzi L, Brenner C, Morselli E et al. Viral control of mitochondrial apoptosis. PLoS Pathog 2008; 4: e1000018.
20. Chavez-Galan L, renas-Del Angel MC, Zenteno E et al. Cell deathmechanisms induced by cytotoxic lymphocytes. Cell Mol Immunol 2009; 6: 15-25.
21. Heutinck KM, ten Berge IJM, Hack CE et al. Serine proteases of the human immune system in health and disease. Mol Immunol 2010; 47: 1943-1955.
22. Wilson NS, Dixit V, Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 2009; 10: 348-355.
23. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163.
24. Heutinck KM, Kassies K, Florquin S et al. SerpinB9 expression in human renal tubular epithelial cells is induced by triggering of the viral dsRNA sensors TLR3, MDA5 and RIG-I. Nephrol Dial Transplant; e-pub ahead of print 13 December 2011.
25. Imaizumi T, Tanaka H, Matsumiya T et al. Retinoic acid-inducible gene-I is induced by double-stranded RNA and regulates the expression of CC chemokine ligand (CCL) 5 in human mesangial cells. Nephrol Dial Transplant 2010; 25: 3534-3539.
26. Kariko K, Ni H, Capodici J et al. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004; 279: 12542-12550.
27. Tormo D, Checinska A, onso-Curbelo D et al. Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 2009; 16: 103-114.
28. Le Goffic R, Pothlichet J, Vitour D et al. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 2007; 178: 3368-3372.
29. Iwai A, Shiozaki T, Kawai T et al. Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator J Biol Chem 2010; 285: 32064-32074.
30. Ehrhardt C, Seyer R, Hrincius ER et al. Interplay between influenza A virus and the innate immune signaling. Microbes Infect 2010; 12: 81-87.
31. Boonstra JG, van der Woude FJ, Wever PC et al. Expression and function of Fas (CD95) on human renal tubular epithelial cells. J Am Soc Nephrol 1997; 8: 1517-1524.
32. Khan S, Koepke A, Jarad G et al. Apoptosis and JNK activation are differentially regulated by Fas expression level in renal tubular epithelial cells. Kidney Int 2001; 60: 65-76.
33. Sun Y, Leaman DW. Involvement of Noxa in cellular apoptotic responses to interferon, double-stranded RNA, and virus infection. J Biol Chem 2005; 280: 15561-15568.
34. Salaun B, Lebecque S, Matikainen S et al. Toll-like receptor 3 expressed by melanoma cells as a target for therapy? Clin Cancer Res 2007; 13(15 Pt 1): 4565-4574.
35. Eldering E, Spek CA, Aberson HL et al. Expression profiling via novel multiplex assay allows rapid assessment of gene regulation in defined signalling pathways. Nucleic Acids Res 2003; 31: e153.
36. Srinivasula SM, Ashwell JD. IAPs: what's in a name? Mol Cell 2008; 30: 123-135.
37. Vince JE, Wong WW, Khan N et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007; 131: 682-693.
38. Yew KH, Carsten B, Harrison C. Scavenger receptor A1 is required for sensing HCMV by endosomal TLR-3/-9 in monocytic THP-1 cells. Mol Immunol 2010; 47: 883-893.
39. Mezger M, Bonin M, Kessler T et al. Toll-like receptor 3 has no critical role during early immune response of human monocyte-derived dendritic cells after infection with the human cytomegalovirus strain TB40E. Viral Immunol 2009; 22: 343-351.
40. Iwakiri D, Zhou L, Samanta M et al. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from tolllike receptor 3. J Exp Med 2009; 206: 2091-2099.
41. Samanta M, Iwakiri D, Kanda T et al. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 2006; 25: 4207-4214.
42. Tanner J, Weis J, Fearon D et al. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 1987; 50: 203-213.
43. Revello MG, Gerna G. Human cytomegalovirus tropism for endothelial/epithelial cells: scientific background and clinical implications. Rev Med Virol 2010; 20: 136-155.
44. Sinclair J. Human cytomegalovirus: latency and reactivation in the myeloid lineage. J Clin Virol 2008; 41: 180-185.
45. Nickeleit V, Mihatsch MJ. Polyomavirus nephropathy in native kidneys and renal allografts: an update on an escalating threat. Transpl Int 2006; 19: 960-973.
46. Tsai JD, Lee HC, Lin CC et al. Epstein-Barr virus-associated acute renal failure: diagnosis, treatment, and follow-up. Pediatr Nephrol 2003; 18: 667-674.
47. Hägele H, Allam R, Pawar RD et al. Double-stranded RNA activates type I interferon secretion in glomerular endothelial cells via retinoic acidinducible gene (RIG)-1. Nephrol Dial Transplant 2009; 24: 3312-3318.
48. Imaizumi T, Hatakeyama M, Yamashita K et al. Interferon-gamma induces retinoic acid-inducible gene-I in endothelial cells. Endothelium 2004; 11: 169-173.
49. Imaizumi T, Hatakeyama M, Yamashita K et al. Double-stranded RNA induces the synthesis of retinoic acid-inducible gene-I in vascular endothelial cells. Endothelium 2005; 12: 133-137.
50. van de Berg PJ, Heutinck KM, Raabe R et al. Human cytomegalovirus induces systemic immune activation characterized by a type 1 cytokine signature. J Infect Dis 2010; 202: 690-699.
51. Ribeiro A, Wornle M, Motamedi N et al. Activation of innate immune defense mechanisms contributes to polyomavirus BK-associated nephropathy. Kidney Int 2011; 81: 100-111.
52. Mannon RB, Hoffmann SC, Kampen RL et al. Molecular evaluation of BK polyomavirus nephropathy. Am J Transplant 2005; 5: 2883-2893.
53. Dessing MC, Bemelman FJ, Claessen N et al. Intragraft Toll-like receptor profiling in acute renal allograft rejection. Nephrol Dial Transplant 2010; 25: 4087-4092.
54. Abend JR, Low JA, Imperiale MJ. Global effects of BKV infection on gene expression in human primary kidney epithelial cells. Virology 2010; 397: 73-79.
55. Grinde B, Gayorfar M, Rinaldo CH. Impact of a polyomavirus (BKV) infection on mRNA expression in human endothelial cells. Virus Res 2007; 123: 86-94.
56. Goubau D, Romieu-Mourez R, Solis M et al. Transcriptional reprogramming of primary macrophages reveals distinct apoptotic and anti-tumoral functions of IRF-3 and IRF-7. Eur J Immunol 2009; 39: 527-540.
57. Flur K, Allam R, Zecher D et al. Viral RNA induces type I interferondependent cytokine release and cell death in mesangial cells via melanoma-differentiation-associated gene-5: implications for viral infection-associated glomerulonephritis. Am J Pathol 2009; 175: 2014-2022.
58. Chiron D, Pellat-Deceunynck C, Amiot M et al. TLR3 ligand induces NF-\{kappa\}B activation and various fates of multiple myeloma cells depending on IFN-\{alpha\} production. J Immunol 2009; 182: 4471-4478.
59. Brenner D, Mak TW. Mitochondrial cell death effectors. Curr Opin Cell Biol 2009; 21: 871-877.
60. Lopez H, Zhang L, George NM et al. Perturbation of the Bcl-2 network and an induced Noxa/Bcl-xL interaction trigger mitochondrial dysfunction after DNA damage. J Biol Chem 2010; 285: 15016-15026.
61. Hagenbuchner J, Ausserlechner MJ, Porto V et al. The anti-apoptotic protein BCL2L1/Bcl-xL is neutralized by pro-apoptotic PMAIP1/Noxa in neuroblastoma, thereby determining bortezomib sensitivity independent of prosurvival MCL1 expression. J Biol Chem 2010; 285: 6904-6912.
62. Schutze S, Tchikov V, Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 2008; 9: 655-662.
63. Jost PJ, Grabow S, Gray D et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009; 460: 1035-1039.
64. Du C, Jiang J, Guan Q et al. Renal tubular epithelial cell self-injury through Fas/Fas ligand interaction promotes renal allograft injury. Am J Transplant 2004; 4: 1583-1594.
65. Lorz C, Ortiz A, Justo P et al. Proapoptotic Fas ligand is expressed by normal kidney tubular epithelium and injured glomeruli. J Am Soc Nephrol 2000; 11: 1266-1277.
66. Lorz C, ito-Martin A, Boucherot A et al. The death ligand TRAIL in diabetic nephropathy. J Am Soc Nephrol 2008; 19: 904-914.
67. van Kooten C, Lam S, Daha MR. Isolation, culture, characterization and use of human renal tubular epithelial cells. J Nephrol 2001; 14: 204-210.