Comparative analysis of the activation of unfolded protein response by spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus HKU1

Cell and Bioscience

Volumn 4, Issue 1, 2014, Pages

  Siu, Kam Leung ^a   Chan, Ching Ping ^a   Kok, Kin Hang ^a   Woo, Patrick C Y ^b   Jin, Dong Yan ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

ER stress; Human coronavirus HKU1; SARS coronavirus; Spike; Unfolded protein response

Indexed keywords

EID: 84892398010     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-4-3     Document Type: Article

References (61)

1. Weiss SR, Leibowitz JL. Coronavirus pathogenesis. Adv Virus Res 2011, 81:85-164.
2. Totura AL, Baric RS. SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon. Curr Opin Virol 2012, 2:264-275. 10.1016/j.coviro.2012.04.004, 22572391.
3. Chan CP, Siu KL, Chin KT, Yuen KY, Zheng B, Jin DY. Modulation of the unfolded protein response by severe acute respiratory syndrome coronavirus spike protein. J Virol 2006, 80:9279-9287. 10.1128/JVI.00659-06, 1563899, 16940539.
4. Versteeg GA, van de Nes PS, Bredenbeek PJ, Spaan WJM. The coronavirus spike protein induces endoplasmic reticulum stress and upregulation of intracellular chemokine mRNA concentrations. J Virol 2007, 81:10981-10990. 10.1128/JVI.01033-07, 2045536, 17670839.
5. Bechill J, Chen Z, Brewer JW, Baker SC. Coronavirus infection modulates the unfolded protein response and mediates sustained translational repression. J Virol 2008, 82:4492-4501. 10.1128/JVI.00017-08, 2293058, 18305036.
6. Ye Z, Wong CK, Li P, Xie Y. A SARS-CoV protein, ORF-6, induces caspase-3 mediated, ER stress and JNK-dependent apoptosis. Biochim Biophys Acta - Gen Subj 2008, 1780:1383-1387.
7. Minakshi R, Padhan K, Rani M, Khan N, Ahmad F, Jameel S. The SARS Coronavirus 3a protein causes endoplasmic reticulum stress and induces ligand-independent downregulation of the type 1 interferon receptor. PLoS One 2009, 4:e8342. 10.1371/journal.pone.0008342, 2791231, 20020050.
8. Sung SC, Chao CY, Jeng KS, Yang JY, Lai MMC. The 8ab protein of SARS-CoV is aluminal ER membrane-associated protein and induces the activation of ATF6. Virology 2009, 387:402-413. 10.1016/j.virol.2009.02.021, 19304306.
9. DeDiego ML, Nieto-Torres JL, Jiménez-Guardeño JM, Regla-Nava JA, Alvarez E, Oliveros JC, Zhao J, Fett C, Perlman S, Enjuanes L. Severe acute respiratory syndrome coronavirus envelope protein regulates cell stress response and apoptosis. PLoS Pathog 2011, 7:e1002315. 10.1371/journal.ppat.1002315, 3197621, 22028656.
10. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B. Identification of a new human coronavirus. Nat Med 2004, 10:368-373. 10.1038/nm1024, 15034574.
11. Woo PCY, Lau SKP, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RWS, Cai JJ, Luk WK, Poon LLM, Wong SSY, Guan Y, Peiris JSM, Yuen KY. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol 2005, 79:884-895. 10.1128/JVI.79.2.884-895.2005, 538593, 15613317.
12. Jevšnik M, Uršič T, Zigon N, Lusa L, Krivec U, Petrovec M. Coronavirus infections in hospitalized pediatric patients with acute respiratory tract disease. BMC Infect Dis 2012, 12:365. 10.1186/1471-2334-12-365, 3557153, 23256846.
13. Peiris JSM, Lai ST, Poon LLM, Guan Y, Yam LYC, Lim W, Nicholls J, Yee WKS, Yan WW, Cheung MT, Cheng VCC, Chan KH, Tsang DNC, Yung RWH, Ng TK, Yuen KY. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 2003, 361:1319-1325. 10.1016/S0140-6736(03)13077-2, 12711465.
14. Cheng VCC, Lau SKP, Woo PCY, Yuen KY. Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clin Microbiol Rev 2007, 20:660-694. 10.1128/CMR.00023-07, 2176051, 17934078.
15. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012, 367:1814-1820. 10.1056/NEJMoa1211721, 23075143.
16. Chan JFW, Lau SKP, Woo PCY. The emerging novel Middle East respiratory syndrome coronavirus: The " knowns" and " unknowns" J Formos Med Assoc 2013, 112:372-381. 10.1016/j.jfma.2013.05.010, 23883791.
17. Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol 2012, 197:857-867. 10.1083/jcb.201110131, 3384412, 22733998.
18. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012, 13:89-102.
19. Lau SKP, Woo PCY, Yip CCY, Tse H, Tsoi HW, Cheng VCC, Lee P, Tang BSF, Cheung CHY, Lee RA, So LY, Lau YL, Chan KH, Yuen KY. Coronavirus HKU1 and other coronavirus infections in Hong Kong. J Clin Microbiol 2006, 44:2063-2071. 10.1128/JCM.02614-05, 1489438, 16757599.
20. Woo PCY, Lau SKP, Yip CC, Huang Y, Yuen KY. More and more coronaviruses: human coronavirus HKU1. Viruses 2009, 1:57-71. 10.3390/v1010057, 3185465, 21994538.
21. Pyrc K, Sims AC, Dijkman R, Jebbink M, Long C, Deming D, Donaldson E, Vabret A, Baric R, van der Hoek L, Pickles R. Culturing the unculturable: human coronavirus HKU1 infects, replicates, and produces progeny virions in human ciliated airway epithelial cell cultures. J Virol 2010, 84:11255-11263. 10.1128/JVI.00947-10, 2953148, 20719951.
22. Dominguez SR, Travanty EA, Qian Z, Mason RJ. Human coronavirus HKU1 infection of primary human type II alveolar epithelial cells: Cytopathic effects and innate immune response. PLoS One 2013, 8:e70129. 10.1371/journal.pone.0070129, 3722178, 23894604.
23. Dijkman R, Jebbink MF, Koekkoek SM, Deijs M, Jónsdóttir HR, Molenkamp R, Ieven M, Goossens H, Thiel V, van der Hoek L. Isolation and characterization of current human coronavirus strains in primary human epithelial cell cultures reveal differences in target cell tropism. J Virol 2013, 87:6081-6090. 10.1128/JVI.03368-12, 3648119, 23427150.
24. Du L, He Y, Zhou Y, Liu S, Zheng BJ, Jiang S. The spike protein of SARS-CoV - a target for vaccine and therapeutic development. Nat Rev Microbiol 2009, 7:226-236. 10.1038/nrmicro2090, 2750777, 19198616.
25. Xiao H, Xu LH, Yamada Y, Liu DX. Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PLoS One 2008, 3:e1494. 10.1371/journal.pone.0001494, 2204050, 18231581.
26. Haga S, Yamamoto N, Nakai-Murakami C, Osawa Y, Tokunaga K, Sata T, Yamamoto N, Sasazuki T, Ishizaka Y. Modulation of TNF-α-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-α production and facilitates viral entry. Proc Natl Acad Sci USA 2008, 105:7809-7814. 10.1073/pnas.0711241105, 2409424, 18490652.
27. Chiang SF, Lin TY, Chow KC, Chiou SH. SARS spike protein induces phenotypic conversion of human B cells to macrophage-like cells. Mol Immunol 2010, 47:2575-2586. 10.1016/j.molimm.2010.06.014, 20667598.
28. Graham RL, Baric RS. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J Virol 2010, 84:3134-3146. 10.1128/JVI.01394-09, 2838128, 19906932.
29. Du L, Kao RY, Zhou Y, He Y, Zhao G, Wong C, Jiang S, Yuen KY, Jin DY, Zheng BJ. Cleavage of spike protein of SARS coronavirus by protease factor Xa is associated with viral infectivity. Biochem Biophys Res Commun 2007, 359:174-179. 10.1016/j.bbrc.2007.05.092, 2323977, 17533109.
30. Bosch BJ, Bartelink W, Rottier PJ. Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide. J Virol 2008, 82:8887-8890. 10.1128/JVI.00415-08, 2519682, 18562523.
31. Belouzard S, Chu VC, Whittaker GR. Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci USA 2009, 106:5871-5876. 10.1073/pnas.0809524106, 2660061, 19321428.
32. Matsuyama S, Nagata N, Shirato K, Kawase M, Takeda M, Taguchi F. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J Virol 2010, 84:12658-12664. 10.1128/JVI.01542-10, 3004351, 20926566.
33. Shulla A, Heald-Sargent T, Subramanya G, Zhao J, Perlman S, Gallagher T. A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol 2011, 85:873-882. 10.1128/JVI.02062-10, 3020023, 21068237.
34. Bertram S, Glowacka I, Müller MA, Lavender H, Gnirss K, Nehlmeier I, Niemeyer D, He Y, Simmons G, Drosten C, Soilleux EJ, Jahn O, Steffen I, Pöhlmann S. Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease. J Virol 2011, 85:13363-13372. 10.1128/JVI.05300-11, 3233180, 21994442.
35. Bertram S, Dijkman R, Habjan M, Heurich A, Gierer S, Glowacka I, Welsch K, Winkler M, Schneider H, Hofmann-Winkler H, Thiel V, Pöhlmann S. TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J Virol 2013, 87:6150-6160. 10.1128/JVI.03372-12, 3648130, 23536651.
36. Gierer S, Bertram S, Kaup F, Wrensch F, Heurich A, Krämer-Kühl A, Welsch K, Winkler M, Meyer B, Drosten C, Dittmer U, von Hahn T, Simmons G, Hofmann H, Pöhlmann S. The spike protein of the emerging betacoronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2, and is targeted by neutralizing antibodies. J Virol 2013, 87:5502-5511. 10.1128/JVI.00128-13, 3648152, 23468491.
37. Bertram S, Glowacka I, Blazejewska P, Soilleux E, Allen P, Danisch S, Steffen I, Choi SY, Park Y, Schneider H, Schughart K, Pöhlmann S. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J Virol 2010, 84:10016-10025. 10.1128/JVI.00239-10, 2937781, 20631123.
38. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011, 13:184-190. 10.1038/ncb0311-184, 3107571, 21364565.
39. Lai WL, Wong NS. ROS mediates 4HPR-induced posttranscriptional expression of the Gadd153 gene. Free Rad Biol Med 2005, 38:1585-1593. 10.1016/j.freeradbiomed.2005.02.024, 15917187.
40. Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem 2004, 136:343-350. 10.1093/jb/mvh122, 15598891.
41. Chin KT, Zhou HJ, Wong CM, Lee JMF, Chan CP, Qiang BQ, Yuan JG, Ng IOL, Jin DY. The liver-enriched transcription factor CREB-H is a growth suppressor protein underexpressed in hepatocellular carcinoma. Nucl Acids Res 2005, 33:1859-1873. 10.1093/nar/gki332, 1072803, 15800215.
42. Chan CP, Mak TY, Chin KT, Ng IOL, Jin DY. N-linked glycosylation is required for optimal proteolytic activation of membrane-bound transcription factor CREB-H. J Cell Sci 2010, 123:1438-1448. 10.1242/jcs.067819, 20356926.
43. Chan CP, Kok KH, Jin DY. CREB3 subfamily transcription factors are not created equal: Recent insights from global analyses and animal models. Cell Biosci 2011, 1:6. 10.1186/2045-3701-1-6, 3116243, 21711675.
44. Takayanagi S, Fukuda R, Takeuchi Y, Tsukada S, Yoshida K. Gene regulatory network of unfolded protein response genes in endoplasmic reticulum stress. Cell Stress Chaperones 2013, 18:11-23. 10.1007/s12192-012-0351-5, 3508129, 22802018.
45. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003, 23:7448-7459. 10.1128/MCB.23.21.7448-7459.2003, 207643, 14559994.
46. Baumeister P, Luo S, Skarnes WC, Sui G, Seto E, Shi Y, Lee AS. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol Cell Biol 2005, 25:4529-4540. 10.1128/MCB.25.11.4529-4540.2005, 1140640, 15899857.
47. Chan CP, Kok KH, Tang HMV, Wong CM, Jin DY. Internal ribosome entry site-mediated translational regulation of ATF4 splice variant in mammalian unfolded protein response. Biochim Biophys Acta - Mol Cell Res 2013, 1833:2165-2175.
48. Ma K, Vattem KM, Wek RC. Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J Biol Chem 2002, 277:18728-18735. 10.1074/jbc.M200903200, 11907036.
49. Vigerust DJ, Shepherd VL. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 2007, 15:211-218. 10.1016/j.tim.2007.03.003, 17398101.
50. Han DP, Lohani M, Cho MW. Specific asparagine-linked glycosylation sites are critical for DC-SIGN- and L-SIGN-mediated severe acute respiratory syndrome coronavirus entry. J Virol 2007, 81:12029-12039. 10.1128/JVI.00315-07, 2168787, 17715238.
51. Zhou Y, Lu K, Pfefferle S, Bertram S, Glowacka I, Drosten C, Pöhlmann S, Simmons G. A single asparagine-linked glycosylation site of the severe acute respiratory syndrome coronavirus spike glycoprotein facilitates inhibition by mannose-binding lectin through multiple mechanisms. J Virol 2010, 84:8753-8764. 10.1128/JVI.00554-10, 2919028, 20573835.
52. Fukushi M, Yoshinaka Y, Matsuoka Y, Hatakeyama S, Ishizaka Y, Kirikae T, Sasazuki T, Miyoshi-Akiyama T. Monitoring of S protein maturation in the endoplasmic reticulum by calnexin is important for the infectivity of severe acute respiratory syndrome coronavirus. J Virol 2012, 86:11745-11753. 10.1128/JVI.01250-12, 3486308, 22915798.
53. Favreau DJ, Desforges M, St-Jean JR, Talbot PJ. A human coronavirus OC43 variant harboring persistence-associated mutations in the S glycoproteindifferentially induces the unfolded protein response in human neurons as compared to wild-type virus. Virology 2009, 395:255-267. 10.1016/j.virol.2009.09.026, 19846189.
54. Fribley AM, Cruz PG, Miller JR, Callaghan MU, Cai P, Narula N, Neubig RR, Showalter HD, Larsen SD, Kirchhoff PD, Larsen MJ, Burr DA, Schultz PJ, Jacobs RR, Tamayo-Castillo G, Ron D, Sherman DH, Kaufman RJ. Complementary cell-based high-throughput screens identify novel modulators of the unfolded protein response. J Biomol Screen 2011, 16:825-835. 10.1177/1087057111414893, 3374590, 21844328.
55. Atkins C, Liu Q, Minthorn E, Zhang SY, Figueroa DJ, Moss K, Stanley TB, Sanders B, Goetz A, Gaul N, Choudhry AE, Alsaid H, Jucker BM, Axten JM, Kumar R. Characterization of a novel PERK kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res 2013, 73:1993-2002. 10.1158/0008-5472.CAN-12-3109, 23333938.
56. Yu Y, Pierciey FJ, Maguire TG, Alwine JC. PKR-like endoplasmic reticulum kinase is necessary for lipogenic activation during HCMV infection. PLoS Pathog 2013, 9:e1003266. 10.1371/journal.ppat.1003266, 3617203, 23592989.
57. Perry JW, Ahmed M, Chang KO, Donato NJ, Showalter HD, Wobus CE. Antiviral activity of a small molecule deubiquitinase inhibitor occurs via induction of the unfolded protein response. PLoS Pathog 2012, 8:e1002783. 10.1371/journal.ppat.1002783, 3390402, 22792064.
58. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins: involvement of basic leucine zipper transcription factors. J Biol Chem 1998, 273:33741-33749. 10.1074/jbc.273.50.33741, 9837962.
59. Tang HMV, Gao WW, Chan CP, Siu YT, Wong CM, Kok KH, Ching YP, Takemori H, Jin DY. LKB1 tumor suppressor and salt-inducible kinases negatively regulate human T-cell leukemia virus type 1 transcription. Retrovirology 2013, 10:40. 10.1186/1742-4690-10-40, 3640950, 23577667.
60. Ching YP, Chan SF, Jeang KT, Jin DY. Retroviral oncoprotein Tax targets coiled-coil centrosomal protein TAX1BP2 to induce centrosome overduplication. Nat Cell Biol 2006, 8:719-724.
61. Siu KL, Kok KH, Ng MHJ, Poon VKM, Yuen KY, Zheng BJ, Jin DY. Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3·TANK·TBK1/IKKε{lunate} complex. J Biol Chem 2009, 284:16202-16209. 10.1074/jbc.M109.008227, 2713514, 19380580.