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

Journal of Virology

Volumn 89, Issue 5, 2015, Pages 2710-2717

  Watanabe, Shumpei ^a   Ohno, Shinji ^a   Shirogane, Yuta ^a   Suzuki, Satoshi O ^a   Koga, Ritsuko ^a   Yanagi, Yusuke ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; GLYCOPROTEIN; NECTIN 4 PROTEIN; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; MUTANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPATHOLOGY; HUMAN; HUMAN CELL; MEASLES; MOUSE; NERVE CELL CULTURE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STABILITY; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS MUTATION; VIRUS RECOMBINANT; WILD TYPE; ANIMAL; CELL CULTURE; CYTOPATHOGENIC EFFECT; GENETICS; MEASLES VIRUS; METABOLISM; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE; VIROLOGY; VIRUS ENTRY;

CRICETINAE; MEASLES VIRUS; MUS;

ANIMALS; CELLS, CULTURED; CYTOPATHOGENIC EFFECT, VIRAL; HUMANS; MEASLES VIRUS; MICE, TRANSGENIC; MUTANT PROTEINS; NEURONS; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84922998448     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03346-14     Document Type: Article

References (61)

1. Griffin DE. 2007. Measles virus, p 1551-1585. In Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott/The Williams & Wilkins Co, Philadelphia, PA.
2. Ferreira CS, Frenzke M, Leonard VH, Welstead GG, Richardson CD, Cattaneo R. 2010. Measles virus infection of alveolar macrophages and dendritic cells precedes spread to lymphatic organs in transgenic mice expressing human signaling lymphocytic activation molecule (SLAM, CD150). J Virol 84:3033-3042. http://dx.doi.org/10.1128/JVI.01559-09.
3. Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G, Yuksel S, Ludlow M, Rennick LJ, Kuiken T, Rima BK, Geijtenbeek TB, Osterhaus AD, Duprex WP, de Swart RL. 2011. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog 7:e1001263. http://dx.doi.org/10.1371/journal.ppat.1001263.
4. Frenzke M, Sawatsky B, Wong XX, Delpeut S, Mateo M, Cattaneo R, von Messling V. 2013. Nectin-4-dependent measles virus spread to the cynomolgus monkey tracheal epithelium: role of infected immune cells infiltrating the lamina propria. J Virol 87:2526-2534. http://dx.doi.org/10.1128/JVI.03037-12.
5. Ludlow M, Lemon K, de Vries RD, McQuaid S, Millar EL, van Amerongen G, Yuksel S, Verburgh RJ, Osterhaus AD, de Swart RL, Duprex WP. 2013. Measles virus infection of epithelial cells in the macaque upper respiratory tract is mediated by subepithelial immune cells. J Virol 87: 4033-4042. http://dx.doi.org/10.1128/JVI.03258-12.
6. Muhlebach MD, Mateo M, Sinn PL, Prufer S, Uhlig KM, Leonard VH, Navaratnarajah CK, Frenzke M, Wong XX, Sawatsky B, Ramachandran S, McCray PB, Cichutek K, von Messling V, Lopez M, Cattaneo R. 2011. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480:530-533. http://dx.doi.org/10.1038/nature10639.
7. Noyce RS, Bondre DG, Ha MN, Lin LT, Sisson G, Tsao MS, Richardson CD. 2011. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog 7:e1002240. http://dx.doi.org/10.1371/journal.ppat.1002240.
8. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, Braun W, McCray PB, Jr, McChesney MB, Cattaneo R. 2008. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J Clin Invest 118: 2448-2458. http://dx.doi.org/10.1172/JCI35454.
9. Tatsuo H, Ono N, Tanaka K, Yanagi Y. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897. http://dx.doi.org/10.1038/35022579.
10. Ono N, Tatsuo H, Hidaka Y, Aoki T, Minagawa H, Yanagi Y. 2001. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75: 4399-4401. http://dx.doi.org/10.1128/JVI.75.9.4399-4401.2001.
11. Erlenhoefer C, Wurzer WJ, Loffler S, Schneider-Schaulies S, ter Meulen V, Schneider-Schaulies J. 2001. CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J Virol 75:4499-4505. http://dx.doi.org/10.1128/JVI.75.10.4499-4505.2001.
12. Hsu EC, Iorio C, Sarangi F, Khine AA, Richardson CD. 2001. CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279:9-21.
13. Manchester M, Liszewski MK, Atkinson JP, Oldstone MB. 1994. Multiple isoforms of CD46 (membrane cofactor protein) serve as receptors for measles virus. Proc Natl Acad Sci USA 91:2161-2165. http://dx.doi.org/10.1073/pnas.91.6.2161.
14. Naniche D, Varior-Krishnan G, Cervoni F, Wild TF, Rossi B, Rabourdin-Combe C, Gerlier D. 1993. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67:6025-6032.
15. Dorig RE, Marcil A, Chopra A, Richardson CD. 1993. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295-305. http://dx.doi.org/10.1016/0092-8674(93)80071-L.
16. Masse N, Barrett T, Muller CP, Wild TF, Buckland R. 2002. Identification of a second major site for CD46 binding in the hemagglutinin protein from a laboratory strain of measles virus (MV): potential consequences for wild-type MV infection. J Virol 76:13034-13038. http://dx.doi.org/10.1128/JVI.76.24.13034-13038.2002.
17. Tahara M, Takeda M, Seki F, Hashiguchi T, Yanagi Y. 2007. Multiple amino acid substitutions in hemagglutinin are necessary for wild-type measles virus to acquire the ability to use receptor CD46 efficiently. J Virol 81:2564-2572. http://dx.doi.org/10.1128/JVI.02449-06.
18. Rima BK, Duprex WP. 2006. Morbilliviruses and human disease. J Pathol 208:199-214. http://dx.doi.org/10.1002/path.1873.
19. Bellini WJ, Rota JS, Lowe LE, Katz RS, Dyken PR, Zaki SR, Shieh WJ, Rota PA. 2005. Subacute sclerosing panencephalitis: more cases of this fatal disease are prevented by measles immunization than was previously recognized. J Infect Dis 192:1686-1693. http://dx.doi.org/10.1086/497169.
20. Gutierrez J, Issacson RS, Koppel BS. 2010. Subacute sclerosing panencephalitis: an update. Dev Med Child Neurol 52:901-907. http://dx.doi.org/10.1111/j.1469-8749.2010.03717.x.
21. Brancati F, Fortugno P, Bottillo I, Lopez M, Josselin E, Boudghene-Stambouli O, Agolini E, Bernardini L, Bellacchio E, Iannicelli M, Rossi A, Dib-Lachachi A, Stuppia L, Palka G, Mundlos S, Stricker S, Kornak U, Zambruno G, Dallapiccola B. 2010. Mutations in PVRL4, encoding cell adhesion molecule nectin-4, cause ectodermal dysplasia-syndactyly syndrome.AmJHumGenet 87:265-273. http://dx.doi.org/10.1016/j.ajhg.2010.07.003.
22. McQuaid S, Cosby SL. 2002. An immunohistochemical study of the distribution of the measles virus receptors, CD46 and SLAM, in normal human tissues and subacute sclerosing panencephalitis. Lab Invest 82: 403-409. http://dx.doi.org/10.1038/labinvest.3780434.
23. Reymond N, Fabre S, Lecocq E, Adelaide J, Dubreuil P, Lopez M. 2001. Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectin1/PRR1 through V domain interaction. J Biol Chem 276:43205-43215. http://dx.doi.org/10.1074/jbc.M103810200.
24. Prussia AJ, Plemper RK, Snyder JP. 2008. Measles virus entry inhibitors: a structural proposal for mechanism of action and the development of resistance. Biochemistry 47:13573-13583. http://dx.doi.org/10.1021/bi801513p.
25. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38-44. http://dx.doi.org/10.1038/nature04322.
26. Plemper RK, Brindley MA, Iorio RM. 2011. Structural and mechanistic studies of measles virus illuminate paramyxovirus entry. PLoS Pathog 7:e1002058. http://dx.doi.org/10.1371/journal.ppat.1002058.
27. Rota JS, Hummel KB, Rota PA, Bellini WJ. 1992. Genetic variability of the glycoprotein genes of current wild-type measles isolates. Virology 188: 135-142. http://dx.doi.org/10.1016/0042-6822(92)90742-8.
28. Rota JS, Wang ZD, Rota PA, Bellini WJ. 1994. Comparison of sequences of the H, F, and N coding genes of measles virus vaccine strains. Virus Res 31:317-330. http://dx.doi.org/10.1016/0168-1702(94)90025-6.
29. Watanabe S, Shirogane Y, Suzuki SO, Ikegame S, Koga R, Yanagi Y. 2013. Mutant fusion proteins with enhanced fusion activity promote mea-sles virus spread in human neuronal cells and brains of suckling hamsters. J Virol 87:2648-2659. http://dx.doi.org/10.1128/JVI.02632-12.
30. Ohno S, Ono N, Seki F, Takeda M, Kura S, Tsuzuki T, Yanagi Y. 2007. Measles virus infection of SLAM (CD150) knock-in mice reproduces tropism and immunosuppression in human infection. J Virol 81:1650-1659. http://dx.doi.org/10.1128/JVI.02134-06.
31. Takeda M, Ohno S, Seki F, Nakatsu Y, Tahara M, Yanagi Y. 2005. Long untranslated regions of the measles virus M and F genes control virus replication and cytopathogenicity. J Virol 79:14346-14354. http://dx.doi.org/10.1128/JVI.79.22.14346-14354.2005.
32. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199. http://dx.doi.org/10.1016/0378-1119(91)90434-D.
33. Seki F, Yamada K, Nakatsu Y, Okamura K, Yanagi Y, Nakayama T, Komase K, Takeda M. 2011. 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. http://dx.doi.org/10.1128/JVI.05067-11.
34. Hashimoto K, Ono N, Tatsuo H, Minagawa H, Takeda M, Takeuchi K, Yanagi Y. 2002. SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol 76:6743-6749. http://dx.doi.org/10.1128/JVI.76.13.6743-6749.2002.
35. Harrison SC. 2008. Viral membrane fusion. Nat Struct Mol Biol 15:690-698. http://dx.doi.org/10.1038/nsmb.1456.
36. Higuchi H, Bronk SF, Bateman A, Harrington K, Vile RG, Gores GJ. 2000. Viral fusogenic membrane glycoprotein expression causes syncytia formation with bioenergetic cell death: implications for gene therapy. Cancer Res 60:6396-6402.
37. Koga R, Ohno S, Ikegame S, Yanagi Y. 2010. Measles virus-induced immunosuppression in SLAM knock-in mice. J Virol 84:5360-5367. http://dx.doi.org/10.1128/JVI.02525-09.
38. Takeda M, Ohno S, Tahara M, Takeuchi H, Shirogane Y, Ohmura H, Nakamura T, Yanagi Y. 2008. Measles viruses possessing the polymerase protein genes of the Edmonton vaccine strain exhibit attenuated gene expression and growth in cultured cells and SLAM knock-in mice. J Virol 82:11979-11984. http://dx.doi.org/10.1128/JVI.00867-08.
39. Heidmeier S, Hanauer JR, Friedrich K, Prufer S, Schneider IC, Buchholz CJ, Cichutek K, Muhlebach MD. 2014. A single amino acid substitution in the measles virus F(2) protein reciprocally modulates membrane fusion activity in pathogenic and oncolytic strains. Virus Res 180:43-48. http://dx.doi.org/10.1016/j.virusres.2013.12.016.
40. Altomonte J, Marozin S, Schmid RM, Ebert O. 2010. Engineered Newcastle disease virus as an improved oncolytic agent against hepatocellular carcinoma. Mol Ther 18:275-284. http://dx.doi.org/10.1038/mt.2009.231.
41. Gainey MD, Manuse MJ, Parks GD. 2008. A hyperfusogenic F protein enhances the oncolytic potency of a paramyxovirus simian virus 5 P/V mutant without compromising sensitivity to type I interferon. J Virol 82:9369-9380. http://dx.doi.org/10.1128/JVI.01054-08.
42. Rima BK, Duprex WP. 2005. Molecular mechanisms of measles virus persistence. Virus Res 111:132-147. http://dx.doi.org/10.1016/j.virusres.2005.04.005.
43. Schneider-Schaulies J, Meulen V, Schneider-Schaulies S. 2003. Measles infection of the central nervous system. J Neurovirol 9:247-252. http://dx.doi.org/10.1080/13550280390193993,http://dx.doi.org/10.1080/713831489.
44. Allen IV, McQuaid S, McMahon J, Kirk J, McConnell R. 1996. The significance of measles virus antigen and genome distribution in the CNS in SSPE for mechanisms of viral spread and demyelination. J Neuropathol Exp Neurol 55:471-480. http://dx.doi.org/10.1097/00005072-199604000-00010.
45. Kirk J, Zhou AL, McQuaid S, Cosby SL, Allen IV. 1991. Cerebral endothelial cell infection by measles virus in subacute sclerosing panencephalitis: ultrastructural and in situ hybridization evidence. Neuropathol Appl Neurobiol 17:289-297. http://dx.doi.org/10.1111/j.1365-2990.1991.tb00726.x.
46. Avila M, Alves L, Khosravi M, Ader-Ebert N, Origgi F, Schneider-Schaulies J, Zurbriggen A, Plemper RK, Plattet P. 2014. Molecular determinants defining the triggering range of prefusion F complexes of canine distemper virus. J Virol 88:2951-2966. http://dx.doi.org/10.1128/JVI.03123-13.
47. Cattaneo R, Schmid A, Eschle D, Baczko K, ter Meulen V, Billeter MA. 1988. Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55:255-265. http://dx.doi.org/10.1016/0092-8674(88)90048-7.
48. Billeter MA, Cattaneo R, Spielhofer P, Kaelin K, Huber M, Schmid A, Baczko K, ter Meulen V. 1994. Generation and properties of measles virus mutations typically associated with subacute sclerosing panencephalitis. Ann N Y Acad Sci 724:367-377. http://dx.doi.org/10.1111/j.1749-6632.1994.tb38934.x.
49. Ning X, Ayata M, Kimura M, Komase K, Furukawa K, Seto T, Ito N, Shingai M, Matsunaga I, Yamano T, Ogura H. 2002. Alterations and diversity in the cytoplasmic tail of the fusion protein of subacute sclerosing panencephalitis virus strains isolated in Osaka, Japan. Virus Res 86:123-131. http://dx.doi.org/10.1016/S0168-1702(02)00042-4.
50. Schmid A, Spielhofer P, Cattaneo R, Baczko K, ter Meulen V, Billeter MA. 1992. Subacute sclerosing panencephalitis is typically characterized by alterations in the fusion protein cytoplasmic domain of the persisting measles virus. Virology 188:910-915. http://dx.doi.org/10.1016/0042-6822(92)90552-Z.
51. Ayata M, Komase K, Shingai M, Matsunaga I, Katayama Y, Ogura H. 2002. Mutations affecting transcriptional termination in the p gene end of subacute sclerosing panencephalitis viruses. J Virol 76:13062-13068. http://dx.doi.org/10.1128/JVI.76.24.13062-13068.2002.
52. Cattaneo R, Schmid A, Rebmann G, Baczko K, Ter Meulen V, Bellini WJ, Rozenblatt S, Billeter MA. 1986. Accumulated measles virus mutations in a case of subacute sclerosing panencephalitis: interrupted matrix protein reading frame and transcription alteration. Virology 154:97-107. http://dx.doi.org/10.1016/0042-6822(86)90433-2.
53. Cathomen T, Mrkic B, Spehner D, Drillien R, Naef R, Pavlovic J, Aguzzi A, Billeter MA, Cattaneo R. 1998. A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J 17:3899-3908. http://dx.doi.org/10.1093/emboj/17.14.3899.
54. Cathomen T, Naim HY, Cattaneo R. 1998. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72:1224-1234.
55. Tahara M, Takeda M, Yanagi Y. 2007. Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion. J Virol 81: 6827-6836. http://dx.doi.org/10.1128/JVI.00248-07.
56. Makino S, Sasaki K, Nakagawa M, Saito M, Shinohara Y. 1977. Isolation and biological characterization of a measles virus-like agent from the brain of an autopsied case of subacute sclerosing panencephalitis (SSPE). Microbiol Immunol 21:193-205. http://dx.doi.org/10.1111/j.1348-0421.1977.tb00281.x.
57. Moulin E, Beal V, Jeantet D, Horvat B, Wild TF, Waku-Kouomou D. 2011. Molecular characterization of measles virus strains causing subacute sclerosing panencephalitis in France in 1977 and 2007. J Med Virol 83: 1614-1623. http://dx.doi.org/10.1002/jmv.22152.
58. Baricevic M, Forcic D, Santak M, Mazuran R. 2007. A comparison of complete untranslated regions of measles virus genomes derived from wild-type viruses and SSPE brain tissues. Virus Genes 35:17-27. http://dx.doi.org/10.1007/s11262-006-0035-2.
59. Hotta H, Nihei K, Abe Y, Kato S, Jiang DP, Nagano-Fujii M, Sada K. 2006. Full-length sequence analysis of subacute sclerosing panencephalitis (SSPE) virus, a mutant of measles virus, isolated from brain tissues of a patient shortly after onset of SSPE. Microbiol Immunol 50:525-534. http://dx.doi.org/10.1111/j.1348-0421.2006.tb03822.x.
60. Homma M, Tashiro M, Konno H, Ohara Y, Hino M, Takase S. 1982. Isolation and characterization of subacute sclerosing panencephalitis virus (Yamagata-1 strain) from a brain autopsy. Microbiol Immunol 26: 1195-1202. http://dx.doi.org/10.1111/j.1348-0421.1982.tb00270.x.
61. Plemper RK, Compans RW. 2003. Mutations in the putative HR-C region of the measles virus F2 glycoprotein modulate syncytium formation. J Virol 77:4181-4190. http://dx.doi.org/10.1128/JVI.77.7.4181-4190.2003.