Influences of cyclosporin A and non-immunosuppressive derivatives on cellular cyclophilins and viral nucleocapsid protein during human coronavirus 229E replication

Antiviral Research

Volumn 173, Issue , 2020, Pages

  Ma Lauer, Yue ^a,b   Zheng, Yu ^a,b   Malešević, Miroslav ^c   von Brunn, Brigitte ^a,b   Fischer, Gunter ^d   von Brunn, Albrecht ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b German Center of Infection Research   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Broad spectrum antiviral; Coronavirus nucleocapsid; Cyclophilin A B; Cyclophilin inhibitors; HCoV 229E

Indexed keywords

CYCLOPHILIN; CYCLOPHILIN A; CYCLOPHILIN B; CYCLOSPORINE; NUCLEOCAPSID PROTEIN; NUCLEOCAPSID PROTEIN, CORONAVIRUS; PROTEIN BINDING;

CHEMISTRY; CORONAVIRUS INFECTION; DRUG EFFECT; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CORONAVIRUS 229E; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

CORONAVIRUS 229E, HUMAN; CORONAVIRUS INFECTIONS; CYCLOPHILIN A; CYCLOPHILINS; CYCLOSPORINE; HOST-PATHOGEN INTERACTIONS; HUMANS; NUCLEOCAPSID PROTEINS; PROTEIN BINDING; VIRUS REPLICATION;

EID: 85076503156     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2019.104620     Document Type: Article

References (50)

1. Bartenschlager, R., Pietschmann, T., Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9739–9740.
2. Blight, K.J., McKeating, J.A., Rice, C.M., Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76 (2002), 13001–13014.
3. Cao, J., Forrest, J.C., Zhang, X., A screen of the NIH Clinical Collection small molecule library identifies potential anti-coronavirus drugs. Antivir. Res. 114 (2015), 1–10.
4. Carbajo-Lozoya, J., Ma-Lauer, Y., Malesevic, M., Theuerkorn, M., Kahlert, V., Prell, E., von Brunn, B., Muth, D., Baumert, T.F., Drosten, C., Fischer, G., von Brunn, A., Human coronavirus NL63 replication is cyclophilin A-dependent and inhibited by non-immunosuppressive cyclosporine A-derivatives including Alisporivir. Virus Res. 184 (2014), 44–53.
5. Carbajo-Lozoya, J., Muller, M.A., Kallies, S., Thiel, V., Drosten, C., von Brunn, A., Replication of human coronaviruses SARS-CoV, HCoV-NL63 and HCoV-229E is inhibited by the drug FK506. Virus Res. 165 (2012), 112–117.
6. Cervantes-Barragan, L., Zust, R., Maier, R., Sierro, S., Janda, J., Levy, F., Speiser, D., Romero, P., Rohrlich, P.S., Ludewig, B., Thiel, V., Dendritic cell-specific antigen delivery by coronavirus vaccine vectors induces long-lasting protective antiviral and antitumor immunity. mBio, 1, 2010.
7. Chang, C.-k., Hou, M.-H., Chang, C.-F., Hsiao, C.-D., Huang, T.-h., The SARS coronavirus nucleocapsid protein – forms and functions. Antivir. Res. 103 (2014), 39–50.
8. Corman, V.M., Muth, D., Niemeyer, D., Drosten, C., Hosts and sources of endemic human coronaviruses. Adv. Virus Res. 100 (2018), 163–188.
9. Cui, J., Li, F., Shi, Z.-L., Origin and evolution of pathogenic coronaviruses. Nat. Rev. Microbiol. 17 (2019), 181–192.
10. de Paulis, A., Ciccarelli, A., de Crescenzo, G., Cirillo, R., Patella, V., Marone, G., Cyclosporin H is a potent and selective competitive antagonist of human basophil activation by N-formyl-methionyl-leucyl-phenylalanine. J. Allergy Clin. Immunol. 98 (1996), 152–164.
11. de Wilde, A.H., Jochmans, D., Posthuma, C.C., Zevenhoven-Dobbe, J.C., van Nieuwkoop, S., Bestebroer, T.M., van den Hoogen, B.G., Neyts, J., Snijder, E.J., Screening of an FDA-approved compound library identifies four small-molecule inhibitors of Middle East respiratory syndrome coronavirus replication in cell culture. Antimicrob. Agents Chemother. 58 (2014), 4875–4884.
12. de Wilde, A.H., Li, Y., van der Meer, Y., Vuagniaux, G., Lysek, R., Fang, Y., Snijder, E.J., van Hemert, M.J., Cyclophilin inhibitors block Arterivirus replication by interfering with viral RNA synthesis. J. Virol. 87 (2013), 1454–1464.
13. de Wilde, A.H., Raj, V.S., Oudshoorn, D., Bestebroer, T.M., van Nieuwkoop, S., Limpens, R.W., Posthuma, C.C., van der Meer, Y., Barcena, M., Haagmans, B.L., Snijder, E.J., van den Hoogen, B.G., MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J. Gen. Virol. 94 (2013), 1749–1760.
14. de Wilde, A.H., Zevenhoven-Dobbe, J.C., Beugeling, C., Chatterji, U., de Jong, D., Gallay, P., Szuhai, K., Posthuma, C.C., Snijder, E.J., Coronaviruses and arteriviruses display striking differences in their cyclophilin A-dependence during replication in cell culture. Virology 517 (2018), 148–156.
15. de Wilde, A.H., Zevenhoven-Dobbe, J.C., van der Meer, Y., Thiel, V., Narayanan, K., Makino, S., Snijder, E.J., van Hemert, M.J., Cyclosporin A inhibits the replication of diverse coronaviruses. J. Gen. Virol. 92 (2011), 2542–2548.
16. Dyall, J., Coleman, C.M., Hart, B.J., Venkataraman, T., Holbrook, M.R., Kindrachuk, J., Johnson, R.F., Olinger, G.G., Jahrling, P.B., Laidlaw, M., Johansen, L.M., Lear-Rooney, C.M., Glass, P.J., Hensley, L.E., Frieman, M.B., Repurposing of clinically developed drugs for treatment of Middle East respiratory syndrome coronavirus infection. Antimicrob. Agents Chemother. 58 (2014), 4885–4893.
17. Feigelstock, D.A., Mihalik, K.B., Kaplan, G., Feinstone, S.M., Increased susceptibility of Huh7 cells to HCV replication does not require mutations in RIG-I. Virol. J., 7, 2010, 44.
18. Fischer, G., Aumuller, T., Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. Rev. Physiol. Biochem. Pharmacol. 148 (2003), 105–150.
19. Friebe, P., Boudet, J., Simorre, J.P., Bartenschlager, R., Kissing-loop interaction in the 3' end of the hepatitis C virus genome essential for RNA replication. J. Virol. 79 (2005), 380–392.
20. Gallay, P.A., Lin, K., Profile of alisporivir and its potential in the treatment of hepatitis C. Drug Des. Dev. Ther. 7 (2013), 105–115.
21. Hopkins, S., Gallay, P.A., The role of immunophilins in viral infection. Biochim. Biophys. Acta 1850 (2015), 2103–2110.
22. Hopkins, S., Scorneaux, B., Huang, Z., Murray, M.G., Wring, S., Smitley, C., Harris, R., Erdmann, F., Fischer, G., Ribeill, Y., SCY-635, a novel nonimmunosuppressive analog of cyclosporine that exhibits potent inhibition of hepatitis C virus RNA replication in vitro. Antimicrob. Agents Chemother. 54 (2010), 660–672.
23. Huang, S., Bjornsti, M.A., Houghton, P.J., Rapamycins: mechanism of action and cellular resistance. Cancer Biol. Ther. 2 (2003), 222–232.
24. Koutsoudakis, G., Herrmann, E., Kallis, S., Bartenschlager, R., Pietschmann, T., The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J. Virol. 81 (2007), 588–598.
25. LaFemina, R.L., Alternative screening approaches for discovery of Middle East respiratory syndrome coronavirus inhibitors. Antimicrob. Agents Chemother. 58 (2014), 4251–4252.
26. Lang, K., Schmid, F.X., Fischer, G., Catalysis of protein folding by prolyl isomerase. Nature 329 (1987), 268–270.
27. LeGrue, S., Turner, R., Weisbrodt, N., Dedman, Does the binding of cyclosporine to calmodulin result in immunosuppression?. Science 234 (1986), 68–71.
28. Lei, J., Kusov, Y., Hilgenfeld, R., Nsp3 of coronaviruses: structures and functions of a large multi-domain protein. Antivir. Res. 149 (2018), 58–74.
29. Lin, K., Gallay, P., Curing a viral infection by targeting the host: the example of cyclophilin inhibitors. Antivir. Res. 99 (2013), 68–77.
30. Luo, C., Luo, H., Zheng, S., Gui, C., Yue, L., Yu, C., Sun, T., He, P., Chen, J., Shen, J., Luo, X., Li, Y., Liu, H., Bai, D., Yang, Y., Li, F., Zuo, J., Hilgenfeld, R., Pei, G., Chen, K., Shen, X., Jiang, H., Nucleocapsid protein of SARS coronavirus tightly binds to human cyclophilin A. Biochem. Biophys. Res. Commun. 321 (2004), 557–565.
31. Ma-Lauer, Y., Carbajo-Lozoya, J., Hein, M.Y., Müller, M.A., Deng, W., Lei, J., Meyer, B., Kusov, Y., von Brunn, B., Bairad, D.R., Hünten, S., Drosten, C., Hermeking, H., Leonhardt, H., Mann, M., Hilgenfeld, R., von Brunn, A., p53 down-regulates SARS coronavirus replication and is targeted by the SARS-unique domain and PLpro via E3 ubiquitin ligase RCHY1. Proc. Natl. Acad. Sci. 113 (2016), E5192–E5201.
32. Malešević, M., Gutknecht, D., Prell, E., Klein, C., Schumann, M., Nowak, R.A., Simon, J.C., Schiene-Fischer, C., Saalbach, A., Anti-inflammatory effects of extracellular cyclosporins are exclusively mediated by CD147. J. Med. Chem. 56 (2013), 7302–7311.
33. McBride, R., van Zyl, M., Fielding, B.C., The coronavirus nucleocapsid is a multifunctional protein. Viruses 6 (2014), 2991–3018.
34. Membreno, F.E., Espinales, J.C., Lawitz, E.J., Cyclophilin inhibitors for hepatitis C therapy. Clin. Liver Dis. 17 (2013), 129–139.
35. Naoumov, N.V., Cyclophilin inhibition as potential therapy for liver diseases. J. Hepatol. 61 (2014), 1166–1174.
36. Neuman, B.W., Joseph, J.S., Saikatendu, K.S., Serrano, P., Chatterjee, A., Johnson, M.A., Liao, L., Klaus, J.P., Yates, J.R. III, Wuthrich, K., Stevens, R.C., Buchmeier, M.J., Kuhn, P., Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3 2. J. Virol. 82 (2008), 5279–5294.
37. Nigro, P., Pompilio, G., Capogrossi, M.C., Cyclophilin A: a key player for human disease. Cell Death Dis., 4, 2013, e888.
38. Perlman, S., Netland, J., Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7 (2009), 439–450.
39. Pfefferle, S., Schopf, J., Kogl, M., Friedel, C.C., Muller, M.A., Carbajo-Lozoya, J., Stellberger, T., von Dall'Armi, E., Herzog, P., Kallies, S., Niemeyer, D., Ditt, V., Kuri, T., Zust, R., Pumpor, K., Hilgenfeld, R., Schwarz, F., Zimmer, R., Steffen, I., Weber, F., Thiel, V., Herrler, G., Thiel, H.J., Schwegmann-Wessels, C., Pohlmann, S., Haas, J., Drosten, C., von Brunn, A., The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog., 7, 2011, e1002331.
40. Prell, E., Kahlert, V., Rucknagel, K.P., Malešević, M., Fischer, G., Fine tuning the inhibition profile of cyclosporine A by derivatization of the MeBmt residue. Chembiochem 14 (2013), 63–65.
41. Price, E.R., Jin, M., Lim, D., Pati, S., Walsh, C.T., McKeon, F.D., Cyclophilin B trafficking through the secretory pathway is altered by binding of cyclosporin A. Proc. Natl. Acad. Sci. U.S.A. 91 (1994), 3931–3935.
42. Raj, V.S., Mou, H., Smits, S.L., Dekkers, D.H., Muller, M.A., Dijkman, R., Muth, D., Demmers, J.A., Zaki, A., Fouchier, R.A., Thiel, V., Drosten, C., Rottier, P.J., Osterhaus, A.D., Bosch, B.J., Haagmans, B.L., Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495 (2013), 251–254.
43. Sanglier, J.J., Quesniaux, V., Fehr, T., Hofmann, H., Mahnke, M., Memmert, K., Schuler, W., Zenke, G., Gschwind, L., Maurer, C., Schilling, W., Sanglifehrins A, B, C and D, novel cyclophilin-binding compounds isolated from Streptomyces sp. A92-308110. I. Taxonomy, fermentation, isolation and biological activity. J. Antibiot. (Tokyo) 52 (1999), 466–473.
44. Saphire, A.C., Bobardt, M.D., Gallay, P.A., Human immunodeficiency virus type 1 hijacks host cyclophilin A for its attachment to target cells. Immunol. Res. 21 (2000), 211–217.
45. Sastre, P., Dijkman, R., Camuñas, A., Ruiz, T., Jebbink, M.F., van der Hoek, L., Vela, C., Rueda, P., Differentiation between human coronaviruses NL63 and 229E using a novel double-antibody sandwich enzyme-linked immunosorbent assay based on specific monoclonal antibodies. Clin. Vaccine Immunol. 18 (2011), 113–118.
46. Tanaka, Y., Sato, Y., Sasaki, T., Feline coronavirus replication is affected by both cyclophilin A and cyclophilin B. J. Gen. Virol. 98 (2017), 190–200.
47. von Brunn, A., Ciesek, S., von Brunn, B., Carbajo-Lozoya, J., Genetic deficiency and polymorphisms of cyclophilin A reveal its essential role for Human Coronavirus 229E replication. Curr. Opin. Virol. 14 (2015), 56–61.
48. von Hahn, T., Schiene-Fischer, C., Van, N.D., Pfaender, S., Karavul, B., Steinmann, E., Potthoff, A., Strassburg, C., Hamdi, N., Abdelaziz, A.I., Sarrazin, C., Muller, T., Berg, T., Trepo, E., Wedemeyer, H., Manns, M.P., Pietschmann, T., Ciesek, S., Hepatocytes that express variants of cyclophilin A are resistant to HCV infection and replication. Gastroenterology 143 (2012), 439–447 e431.
49. Whitaker, C., Caspe, S., Synthesis of Cyclosporin H. US20120253007 A1. 2011.
50. Zhou, D., Mei, Q., Li, J., He, H., Cyclophilin A and viral infections. Biochem. Biophys. Res. Commun. 424 (2012), 647–650.