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Collective fusion activity determines neurotropism of an en bloc transmitted enveloped virus

Shirogane, Yuta Harada, Hidetaka Hirai, Yuichi Takemoto, Ryuichi Suzuki, Tateki Hashiguchi, Takao Yanagi, Yusuke 京都大学 DOI:10.1126/sciadv.adf3731

2023.01

概要

Measles virus (MeV), which is usually non-neurotropic, sometimes persists in the brain and causes subacute sclerosing panencephalitis (SSPE) several years after acute infection, serving as a model for persistent viral infections. The persisting MeVs have hyperfusogenic mutant fusion (F) proteins that likely enable cell-cell fusion at synapses and "en bloc transmission" between neurons. We here show that during persistence, F protein fusogenicity is generally enhanced by cumulative mutations, yet mutations paradoxically reducing the fusogenicity may be selected alongside the wild-type (non-neurotropic) MeV genome. A mutant F protein having SSPE-derived substitutions exhibits lower fusogenicity than the hyperfusogenic F protein containing some of those substitutions, but by the wild-type F protein coexpression, the fusogenicity of the former F protein is enhanced, while that of the latter is nearly abolished. These findings advance the understanding of the long-term process of MeV neuropathogenicity and provide critical insight into the genotype-phenotype relationships of en bloc transmitted viruses.

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参考文献

1. E. Domingo, J. Sheldon, C. Perales, Viral quasispecies evolution. Microbiol. Mol. Biol. Rev. 76, 159–216 (2012).

2. R. Andino, E. Domingo, Viral quasispecies. Virology 479-480, 46–51 (2015).

3. Y. Shirogane, S. Watanabe, Y. Yanagi, Cooperation between different variants: A unique potential for virus evolution. Virus Res. 264, 68–73 (2019).

4. R. Sanjuán, Collective infectious units in viruses. Trends Microbiol. 25, 402–412 (2017).

5. N. Altan-Bonnet, C. Perales, E. Domingo, Extracellular vesicles: Vehicles of en bloc viral transmission. Virus Res. 265, 143–149 (2019).

6. S. L. Díaz-Muñoz, R. Sanjuán, S. West, Sociovirology: Conflict, cooperation, and communication among viruses. Cell Host Microbe 22, 437–441 (2017).

7. A. Leeks, S. A. West, M. Ghoul, The evolution of cheating in viruses. Nat. Commun. 12, 6928 (2021).

8. M. Coughlin, A. Beck, B. Bankamp, P. Rota, M. M. Coughlin, A. S. Beck, B. Bankamp, P. A. Rota, Perspective on global measles epidemiology and control and the role of novel vaccination strategies. Viruses 9, 11 (2017).

9. M. Mekki, B. Eley, D. Hardie, J. M. Wilmshurst, Subacute sclerosing panencephalitis: Clinical phenotype, epidemiology, and preventive interventions. Dev. Med. Child Neurol. 61, 1139–1144 (2019).

10. D. E. Griffin, Measles virus, in Fields Virology, D. M. Knipe, P. M. Howley, Eds. (Lippincott Williams & Wilkins, ed. 6, 2013), pp. 1042–1069.

11. S. Watanabe, Y. Shirogane, Y. Sato, T. Hashiguchi, Y. Yanagi, New insightsinto measles virus brain infections. Trends Microbiol. 27, 164–175 (2019).

12. Y. Shirogane, T. Hashiguchi, Y. Yanagi, Weak cis and transinteractions of the hemagglutinin with receptors trigger fusion proteins of neuropathogenic measles virus isolates. J. Virol. 94, e01727–e01719 (2020).

13. Y. Shirogane, R. Takemoto, T. Suzuki, T. Kameda, K. Nakashima, T. Hashiguchi, Y. Yanagi, CADM1 and CADM2 trigger neuropathogenic measles virus-mediated membrane fusion by acting in cis. J. Virol. 95, e00528–e00521 (2021).

14. R. Takemoto, T. Suzuki, T. Hashiguchi, Y. Yanagi, Y. Shirogane, Short-stalk isoforms of CADM1 and CADM2 trigger neuropathogenic measles virus-mediated membrane fusion by interacting with the viral hemagglutinin. J. Virol. 96, e01949–e01921 (2022).

15. Y. Iwasaki, H. Koprowski, Cell to cell transmission of virus in the central nervous system. I. Subacute sclerosing panencephalitis. Lab. Invest. 31, 187–196 (1974).

16. D. M. P. Lawrence, C. E. Patterson, T. L. Gales, J. L. D’Orazio, M. M. Vaughn, G. F. Rall, Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J. Virol. 74, 1908–1918 (2000).

17. M. Ayata, K. Takeuchi, M. Takeda, S. Ohgimoto, S. Kato, L. B. Sharma, M. Tanaka, M. Kuwamura, H. Ishida, H. Ogura, The F gene of the Osaka-2 strain of measles virus derived from a case of subacute sclerosing panencephalitis is a major determinant of neurovirulence. J. Virol. 84, 11189–11199 (2010).

18. S. Watanabe, Y. Shirogane, S. O. Suzuki, S. Ikegame, R. Koga, Y. Yanagi, Mutant fusion proteins with enhanced fusion activity promote measles virus spread in human neuronal cells and brains of suckling hamsters. J. Virol. 87, 2648–2659 (2013).

19. S. Watanabe, S. Ohno, Y. Shirogane, S. O. Suzuki, R. Koga, Y. Yanagi, Measles virus mutants possessing the fusion protein with enhanced fusion activity spread effectively in neuronal cells, but not in other cells, without causing strong cytopathology. J. Virol. 89, 2710–2717 (2015).

20. E. M. Jurgens, C. Mathieu, L. M. Palermo, D. Hardie, B. Horvat, A. Moscona, M. Porotto, Measles fusion machinery is dysregulated in neuropathogenic variants. mBio 6, e02528–e02514 (2015).

21. Y. Sato, S. Watanabe, Y. Fukuda, T. Hashiguchi, Y. Yanagi, S. Ohno, Cell-to-cell measles virus spread between human neurons is dependent on hemagglutinin and hyperfusogenic fusion protein. J. Virol. 92, e02166–e02117 (2018).

22. S. Ikegame, T. Hashiguchi, C.-T. Hung, K. Dobrindt, K. J. Brennand, M. Takeda, B. Lee, Fitness selection of hyperfusogenic measles virus F proteins associated with neuropathogenic phenotypes. Proc. Natl. Acad. Sci. 118, e2026027118 (2021).

23. Y. Shirogane, S. Watanabe, Y. Yanagi, Cooperation between different RNA virus genomes produces a new phenotype. Nat. Commun. 3, 1235 (2012).

24. M. Ayata, M. Tanaka, K. Kameoka, M. Kuwamura, K. Takeuchi, M. Takeda, K. Kanou, H. Ogura, Amino acid substitutions in the heptad repeat A and C regions of the F protein responsible for neurovirulence of measles virus Osaka-1 strain from a patient with subacute sclerosing panencephalitis. Virology 487, 141–149 (2016).

25. F. Angius, H. Smuts, K. Rybkina, D. Stelitano, B. Eley, J. Wilmshurst, M. Ferren, A. Lalande, C. Mathieu, A. Moscona, B. Horvat, T. Hashiguchi, M. Porotto, D. Hardie, Analysis of a subacute sclerosing panencephalitis genotype B3 virus from the 2009-2010 South African measles epidemic shows that hyperfusogenic F proteins contribute to measles virus infection in the brain. J. Virol. 93, e01700–e01718 (2018).

26. K. Baczko, U. G. Liebert, M. Billeter, R. Cattaneo, H. Budka, V. ter Meulen, Expression of defective measles virus genes in brain tissues of patients with subacute sclerosing panencephalitis. J. Virol. 59, 472–478 (1986).

27. R. Cattaneo, A. Schmid, D. Eschle, K. Baczko, V. ter Meulen, M. A. Billeter, Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55, 255–265 (1988).

28. R. Cattaneo, A. Schmid, P. Spielhofer, K. Kaelin, K. Baczko, V. ter Meulen, J. Pardowitz, S. Flanagan, B. K. Rima, S. A. Udem, M. A. Billeter, Mutated and hypermutated genes of persistent measles viruses which caused lethal human brain diseases. Virology 173, 415–425 (1989).

29. X. Ning, M. Ayata, M. Kimura, K. Komase, K. Furukawa, T. Seto, N. Ito, M. Shingai, I. Matsunaga, T. Yamano, H. Ogura, Alterations and diversity in the cytoplasmic tail of the fusion protein ofsubacute sclerosing panencephalitis virusstrainsisolated in Osaka, Japan. Virus Res. 86, 123–131 (2002).

30. N. Kondo, K. Miyauchi, F. Meng, A. Iwamoto, Z. Matsuda, Conformational changes of the HIV-1 envelope protein during membrane fusion are inhibited by the replacement of its membrane-spanning domain. J. Biol. Chem. 285, 14681–14688 (2010).

31. H. Ishikawa, F. Meng, N. Kondo, A. Iwamoto, Z. Matsuda, Generation of a dual-functional split-reporter protein for monitoring membrane fusion using self-associating split GFP. Protein Eng. Des. Sel. 25, 813–820 (2012).

32. H. Wang, X. Li, S. Nakane, S. Liu, H. Ishikawa, A. Iwamoto, Z. Matsuda, Co-expression of foreign proteins tethered to HIV-1 envelope glycoprotein on the cell surface by introducing an intervening second membrane-spanning domain. PLOS ONE 9, e96790 (2014).

33. T. Hashiguchi, Y. Fukuda, R. Matsuoka, D. Kuroda, M. Kubota, Y. Shirogane, S. Watanabe, K. Tsumoto, D. Kohda, R. K. Plemper, Y. Yanagi, Structures of the prefusion form of measles virus fusion protein in complex with inhibitors. Proc. Natl. Acad. Sci. U.S.A. 115, 2496–2501 (2018).

34. M. Rager, S. Vongpunsawad, W. P. Duprex, R. Cattaneo, Polyploid measles virus with hexameric genome length. EMBO J. 21, 2364–2372 (2002).

35. L. J. González Aparicio, C. B. López, S. A. Felt, A virus is a community: Diversity within negative-sense RNA virus populations. Microbiol. Mol. Biol. Rev. 86, e0008621 (2022).

36. J. E. Jones, V. le Sage, S. S. Lakdawala, Viral and host heterogeneity and their effects on the viral life cycle. Nat. Rev. Microbiol. 19, 272–282 (2021).

37. Y. Shirogane, S. Watanabe, Y. Yanagi, Cooperation: Another mechanism of viral evolution. Trends Microbiol. 21, 320–324 (2013).

38. D. Luque, G. Rivas, C. Alfonso, J. L. Carrascosa, J. F. Rodríguez, J. R. Castón, Infectious bursal disease virus is an icosahedral polyploid dsRNA virus. Proc. Natl. Acad. Sci. U.S.A. 106, 2148–2152 (2009).

39. D. R. Beniac, P. L. Melito, S. L. Devarennes, S. L. Hiebert, M. J. Rabb, L. L. Lamboo, S. M. Jones, T. F. Booth, The organisation of Ebola virus reveals a capacity for extensive, modular polyploidy. PLOS ONE 7, e29608 (2012).

40. M. Combe, R. Garijo, R. Geller, J. M. Cuevas, R. Sanjuán, Single-cell analysis of RNA virus infection identifies multiple genetically diverse viral genomes within single infectious units. Cell Host Microbe 18, 424–432 (2015).

41. J. M. Cuevas, M. Durán-Moreno, R. Sanjuán, Multi-virion infectious units arise from free viral particles in an enveloped virus. Nat. Microbiol. 2, 17078 (2017).

42. J. Slack, B. M. Arif, The baculoviruses occlusion-derived virus: Virion structure and function. Adv Virus Res. 69, 99–165 (2007).

43. Y.-H. Chen, W. Du, M. C. Hagemeijer, P. M. Takvorian, C. Pau, A. Cali, C. A. Brantner, E. S. Stempinski, P. S. Connelly, H.-C. Ma, P. Jiang, E. Wimmer, G. Altan-Bonnet, N. AltanBonnet, Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160, 619–630 (2015).

44. Z. Feng, L. Hensley, K. L. McKnight, F. Hu, V. Madden, L. Ping, S.-H. Jeong, C. Walker, R. E. Lanford, S. M. Lemon, A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496, 367–371 (2013).

45. S. Nagashima, S. Jirintai, M. Takahashi, T. Kobayashi, Tanggis, T. Nishizawa, T. Kouki, T. Yashiro, H. Okamoto, Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J. Gen. Virol. 95, 2166–2175 (2014).

46. R. J. Owens, C. Limn, P. Roy, Role of an arbovirus nonstructural protein in cellular pathogenesis and virus release. J. Virol. 78, 6649–6656 (2004).

47. S. M. Robinson, G. Tsueng, J. Sin, V. Mangale, S. Rahawi, L. L. McIntyre, W. Williams, N. Kha, C. Cruz, B. M. Hancock, D. P. Nguyen, M. R. Sayen, B. J. Hilton, K. S. Doran, A. M. Segall, R. Wolkowicz, C. T. Cornell, J. L. Whitton, R. A. Gottlieb, R. Feuer, Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog. 10, e1004045 (2014).

48. C. M. Robinson, P. R. Jesudhasan, J. K. Pfeiffer, Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15, 36–46 (2014).

49. L. M. Agosto, P. D. Uchil, W. Mothes, HIV cell-to-cell transmission: Effects on pathogenesis and antiretroviral therapy. Trends Microbiol. 23, 289–295 (2015).

50. C. Jolly, K. Kashefi, M. Hollinshead, Q. J. Sattentau, HIV-1 cell to cell transfer across an Envinduced, actin-dependent synapse. J Exp Med. 199, 283–293 (2004).

51. N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, W. Mothes, Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9, 310–315 (2007).

52. N. Cifuentes-Muñoz, R. E. Dutch, R. Cattaneo, Direct cell-to-cell transmission of respiratory viruses: The fast lanes. PLOS Pathog. 14, e1007015 (2018).

53. F. el Najjar, N. Cifuentes-Muñoz, J. Chen, H. Zhu, U. J. Buchholz, C. L. Moncman, R. E. Dutch, Human metapneumovirus induces reorganization of the actin cytoskeleton for direct cellto-cell spread. PLOS Pathog. 12, e1005922 (2016).

54. M. Mateo, A. Generous, P. L. Sinn, R. Cattaneo, Connections matter—How viruses use cell– cell adhesion components. J. Cell Sci. 128, 431–439 (2015).

55. M. Mehedi, T. McCarty, S. E. Martin, C. le Nouën, E. Buehler, Y.-C. Chen, M. Smelkinson, S. Ganesan, E. R. Fischer, L. G. Brock, B. Liang, S. Munir, P. L. Collins, U. J. Buchholz, Actinrelated protein 2 (ARP2) and virus-induced filopodia facilitate human respiratory syncytial virus spread. PLOS Pathog. 12, e1006062 (2016).

56. K. L. Roberts, B. Manicassamy, R. A. Lamb, Influenza a virus usesintercellular connectionsto spread to neighboring cells. J. Virol. 89, 1537–1549 (2015).

57. R. Cattaneo, R. C. Donohue, A. R. Generous, C. K. Navaratnarajah, C. K. Pfaller, Stronger together: Multi-genome transmission of measles virus. Virus Res. 265, 74–79 (2019).

58. K. Baczko, J. Lampe, U. G. Liebert, U. Brinckmann, V. ter Meulen, I. Pardowitz, H. Budka, S. L. Cosby, S. Isserte, B. K. Rima, Clonal expansion of hypermutated measles virus in a SSPE brain. Virology 197, 188–195 (1993).

59. A. Schmid, P. Spielhofer, R. Cattaneo, K. Baczko, V. ter Meulen, M. A. Billeter, Subacute sclerosing panencephalitis is typically characterized by alterations in the fusion protein cytoplasmic domain of the persisting measles virus. Virology 188, 910–915 (1992).

60. M. Ayata, T. Kimoto, K. Hayashi, T. Seto, R. Murata, H. Ogura, Nucleotide sequences of the matrix protein gene of subacute sclerosing panencephalitis viruses compared with local contemporary isolates from patients with acute measles. Virus Res. 54, 107–115 (1998).

61. H. Nakashima, K. Tsujimura, K. Irie, M. Ishizu, M. Pan, T. Kameda, K. Nakashima, Canonical TGF-β signaling negatively regulates neuronal morphogenesis through TGIF/Smad complex-mediated CRMP2 suppression. J. Neurosci. 38, 4791–4810 (2018).

62. M. Takeda, S. Ohno, F. Seki, Y. Nakatsu, M. Tahara, Y. Yanagi, Long untranslated regions of the measles virus M and F genes control virus replication and cytopathogenicity. J. Virol. 79, 14346–14354 (2005).

63. H. Niwa, K. Yamamura, J. Miyazaki, Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193–199 (1991).

64. M. Tahara, M. Takeda, Y. Shirogane, T. Hashiguchi, S. Ohno, Y. Yanagi, Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J. Virol. 82, 4630–4637 (2008).

65. F. Seki, K. Yamada, Y. Nakatsu, K. Okamura, Y. Yanagi, T. Nakayama, K. Komase, M. Takeda, The SI strain of measles virus derived from a patient with subacute sclerosing panencephalitis possesses typical genome alterations and unique amino acid changes that modulate receptor specificity and reduce membrane fusion activity. J. Virol. 85, 11871–11882 (2011).

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