This review describes the two interrelated and interdependent processes of transcription and replication for measles virus. First, we concentrate on the ribonucleoprotein (RNP) complex, which contains the negative sense genomic template and in encapsidated in every virion. Second, we examine the viral proteins involved in these processes, placing particular emphasis on their structure, conserved sequence motifs, their interaction partners and the domains which mediate these associations. Transcription is discussed in terms of sequence motifs in the template, editing, co-transcriptional modifications of the mRNAs and the phase of the gene start sites within the genome. Likewise, replication is considered in terms of promoter strength, copy numbers and the remarkable plasticity of the system. The review emphasises what is not known or known only by analogy rather than by direct experimental evidence in the MV replication cycle and hence where additional research, using reverse genetic systems, is needed to complete our understanding of the processes involved.
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References
Afzal MA, Osterhaus AD, Cosby SL, Jin L, Beeler J, Takeuchi K, Kawashima H (2003) Comparative evaluation of measles virus-specific RT-PCR methods through an international collaborative study. J Med Virol 70:171–176
Albertini AA, Wernimont AK, Muziol T, Ravelli RB, Clapier CR, Schoehn G, Weissenhorn W, Ruigrok RW (2006) Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313:360–363
Alkhatib G, Massie B, Briedis DJ (1988) Expression of bicistronic measles virus P/C mRNA by using hybrid adenoviruses: levels of C protein synthesized in vivo are unaffected by the presence or absence of the upstream P initiator codon. J Virol 62:4059–4069
Andzhaparidze OG, Chaplygina NM, Bogomolova NN, Lotte VD, Koptyaeva IB, Boriskin Y (1987) Non-infectious morphologically altered nucleocapsids of measles virus from persistently infected cells. Arch Virol 95:17–28
Auwaerter PG, Kaneshima H, McCune JM, Wiegand G, Griffin DE (1996) Measles virus infection of thymic epithelium in the SCID-hu mouse leads to thymocyte apoptosis. J Virol 70:3734–3740
Baczko K, Liebert UG, Billeter M, Cattaneo R, Budka H, ter Meulen V (1986) Expression of defective measles virus genes in brain tissues of patients with subacute sclerosing panencepha-litis. J Virol 59:472–478
Banerjee AK (1987) Transcription and replication of rhabdoviruses 262. Microbiol Rev 51:66–87
Banerjee AK, Barik S, De BP (1991) Gene expression of nonsegmented negative strand RNA viruses. Pharmacol Ther 51:47–70
Bankamp B, Bellini WJ, Rota PA (1999) Comparison of L proteins of vaccine and wild-type measles viruses. J Gen Virol 80:1617–1625
Bankamp B, Wilson J, Bellini WJ, Rota PA (2005) Identification of naturally occurring amino acid variations that affect the ability of the measles virus C protein to regulate genome replication and transcription. Virology 336:120–129
Barr JN, Whelan SP, Wertz GW (2002) Transcriptional control of the RNA-dependent RNA polymerase of vesicular stomatitis virus. Biochim Biophys Acta 1577:337–353
Barrett T, Underwood B (1985) Comparison of messenger RNAs induced in cells infected with each member of the morbillivirus group. Virology 145:195–199
Bellini WJ, Englund G, Rozenblatt S, Arnheiter H, Richardson CD (1985) Measles virus P gene codes for two proteins. J Virol 53:908–919
Bellini WJ, Englund G, Richardson CD, Rozenblatt S, Lazzarini RA (1986) Matrix genes of measles virus and canine distemper virus: cloning, nucleotide sequences, and deduced amino acid sequences. J Virol 58:408–416
Bhella D, Ralph A, Yeo RP (2004) Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J Mol Biol 340:319–331
Blumberg BM, Crowley JC, Silverman JI, Menonna J, Cook SD, Dowling PC (1988) Measles virus L protein evidences elements of ancestral RNA polymerase. Virology 164:487–497
Bousse T, Matrosovich T, Portner A, Kato A, Nagai Y, Takimoto T (2002) The long noncoding region of the human parainfluenza virus type 1 F gene contributes to the read-through transcription at the M-F gene junction. J Virol 76:8244–8251
Brown DD, Rima BK, Allen IV, Baron MD, Banyard AC, Barrett T, Duprex WP (2005) Rational attenuation of a morbillivirus by modulating the activity of the RNA-dependent RNA polymer-ase. J Virol 79:14330–14338
Calain P, Roux L (1993) The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67:4822–4830
Campbell JJ, Cosby SL, Scott JK, Rima BK, Martin SJ, Appel M (1980) A comparison of measles and canine distemper virus polypeptides. J Gen Virol 48:149–159
Casali P, Sissons JG, Fujinami RS, Oldstone MB (1981) Purification of measles virus glycopro-teins and their integration into artificial lipid membranes. J Gen Virol 54:161–171
Castaneda SJ, Wong TC (1990) Leader sequence distinguishes between translatable and encapsi-dated measles virus RNAs. J Virol 64:222–230
Cathomen T, Buchholz CJ, Spielhofer P, Cattaneo R (1995) Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 214:628–632
Cattaneo R, Rebmann G, Schmid A, Baczko K, ter Meulen V, Billeter MA (1987) Altered transcription of a defective measles virus genome derived from a diseased human brain. EMBO J 6:681–688
Cattaneo R, Kaelin K, Baczko K, Billeter MA (1989a) Measles virus editing provides an additional cysteine-rich protein. Cell 56:759–764
Cattaneo R, Schmid A, Spielhofer P, Kaelin K, Baczko K, ter Meulen V, Pardowitz J, Flanagan S,Rima BK, Udem SA, Billeter MA (1989b) Mutated and hypermutated genes of persistent measles viruses which caused lethal human brain diseases. Virology 173:415–425
Cevik B, Smallwood S, Moyer SA (2003) The L-L oligomerization domain resides at the very N-terminus of the sendai virus L RNA polymerase protein. Virology 313:525–536
Chen M, Ogino T, Banerjee AK (2006) Mapping and functional role of the self-association domain of vesicular stomatitis virus phosphoprotein. J Virol 80:9511–9518
Chui LW, Vainionpaa R, Marusyk R, Salmi A, Norrby E (1986) Nuclear accumulation of measles virus nucleoprotein associated with a temperature-sensitive mutant. J Gen Virol 67:2153–2161
Curran J, Kolakofsky D (2008) Nonsegmented negative-strand RNA virus RNA synthesis in vivo.Virology 371:227–230
Curran JA, Richardson C, Kolakofsky D (1986) Ribosomal initiation at alternate AUGs on the Sendai virus P/C mRNA. J Virol 57:684–687
de Carvalho NC, Williamson RA, Parren PW, Lundkvist A, Burton DR, Björling E (2002)Neutralizing human Fab fragments against measles virus recovered by phage display. J Virol 76:251–258
de Swart RL, Ludlow M, de Witte L, Yanagi Y, van Amerongen G, McQuaid S, Yuksel S,Geijtenbeek TB, Duprex WP, Osterhaus AD (2007) Predominant infection of CD150 +lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog 3:e178
Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R (2007) Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72+83
Dowling PC, Blumberg BM, Menonna J, Adamus JE, Cook P, Crowley JC, Kolakofsky D, Cook SD (1986) Transcriptional map of the measles virus genome. J Gen Virol 67:198–1992
Duprex WP, McQuaid S, Hangartner L, Billeter MA, Rima BK (1999) Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J Virol 73:9568–9575
Duprex WP, McQuaid S, Rima BK (2000a) Measles virus-induced disruption of the glial-fibrillary-acidic protein cytoskeleton in an astrocytoma cell line (U-251). J Virol 74:3874–3880
Duprex WP, McQuaid S, Roscic-Mrkic B, Cattaneo R, McCallister C, Rima BK (2000b) In vitro and in vivo infection of neural cells by a recombinant measles virus expressing enhanced green fluorescent protein. J Virol 74:7972–7979
Duprex WP, Collins FM, Rima BK (2002) Modulating the function of the measles virus RNA-dependent RNA polymerase by insertion of green fluorescent protein into the open reading frame. J Virol 76:7322–7328
Enders JF, Peebles TC (1954) Propagation in tissue cultures of cytopathic agents from patients with measles. Proc Soc Exp Biol Med 86:277–286
Ferron F, Longhi S, Henrissat B, Canard B (2002) Viral RNA-polymerases — a predicted 2'-O-ribose methyltransferase domain shared by all Mononegavirales. Trends Biochem Sci 27:222–224
Follett EA, Pringle CR, Pennington TH (1976) Events following the infections of enucleate cells with measles virus. J Gen Virol 32:163–175
ellini WJ, Rota PA (2008) Regulation of interferon signaling by the C and V proteins from attenuated and wild-type strains of measles virus. Virology 374:71–81
Green TJ, Zhang X, Wertz GW, Luo M (2006) Structure of the vesicular stomatitis virus nucleo-protein-RNA complex. Science 313:357–360
Gubbay O, Curran J, Kolakofsky D (2001) Sendai virus genome synthesis and assembly are coupled: a possible mechanism to promote viral RNA polymerase processivity. J Gen Virol 82:2895–2903
Gupta KC, Kingsbury DW (1985) Polytranscripts of Sendai virus do not contain intervening polyadenylate sequences. Virology 141:102–109
Hall WW, ter Meulen V (1977) The effects of actinomycin D on RNA synthesis in measles virus-infected cells. J Gen Virol 34:391–396
Horikami SM, Moyer SA (1991) Synthesis of leader RNA and editing of the P mRNA during transcription by purified measles virus. J Virol 65:5342–5347
Huber M, Cattaneo R, Spielhofer P, Örvell C, Norrby E, Messerli M, Perriard JC, Billeter MA (1991) Measles virus phosphoprotein retains the nucleocapsid protein in the cytoplasm.Virology 185:299–308
Iizuka M, Smith MM (2003) Functional consequences of histone modifications. Curr Opin Genet Dev 13:154–160
Iseni F, Baudin F, Garcin D, Marq JB, Ruigrok RW, Kolakofsky D (2002) Chemical modification of nucleotide bases and mRNA editing depend on hexamer or nucleoprotein phase in Sendai virus nucleocapsids. RNA 8:1056–1067
Kingsbury DW (1974) The molecular biology of paramyxoviruses. Med Microbiol Immunol 160:73–83
Kozak M (1991a) A short leader sequence impairs the fidelity of initiation by eukaryotic ribos-omes. Gene Expr 1:111–115
Kozak M (1991b) Effects of long 5' leader sequences on initiation by eukaryotic ribosomes in vitro. Gene Expr 1:117–125
Lamb RA, Parks GD (2007) Paramyxoviridae : the viruses and their replication. In: Knipe DM,Howley PM (eds) Fields Virology, 5th edn. Lippincott Williams Wilkins, Philadelphia,pp 1449–1496
Lamb RA, Mahy BW, Choppin PW (1976) The synthesis of Sendai virus polypeptides in infected cells. Virology 69:116–131
Liston P Briedis DJ (1994) Measles virus V protein binds zinc. Virology 198:399–404
Liu X, Bankamp B, Xu W, Bellini WJ, Rota PA (2006) The genomic termini of wild-type and vaccine strains of measles virus. Virus Res 122:78–84
Ludlow M, McQuaid S, Cosby SL, Cattaneo R, Rima BK, Duprex WP (2005) Measles virus superinfection immunity and receptor redistribution in persistently infected NT2 cells. J Gen Virol 86:2291–2303
Ludlow M, Duprex WP, Cosby SL, Allen IV, McQuaid S (2008) Advantages of using recombinant measles viruses expressing a fluorescent reporter gene with vibratome slice technology in experimental measles neuropathogenesis. Neuropathol Appl Neurobiol 34:424–434
Lund GA, Tyrrell DL, Bradley RD, Scraba DG (1984) The molecular length of measles virus RNA and the structural organization of measles nucleocapsids. J Gen Virol 65:1535–1542
Luo M, Green TJ, Zhang X, Tsao J, Qiu S (2007) Structural comparisons of the nucleoprotein from three negative strand RNA virus families. Virol J 4:72
Lyles DS, Rupprecht CE (2007) Rhabdoviridae. In: Knipe DM, Howley PM (eds) Fields Virology,5th edn. Lippincott Williams Wilkins, Philadelphia, pp 1363–1408
McIlhatton MA, Curran MD, Rima BK (1997) Nucleotide sequence analysis of the large (L) genes of phocine distemper virus and canine distemper virus (corrected sequence) J Gen Virol 78:571–576
Nishie T, Nagata K, Takeuchi K (2007) The C protein of wild-type measles virus has the ability to shuttle between the nucleus and the cytoplasm. Microbes Infect 9:344–354
Ogura H, Baczko K, Rima BK, ter Meulen V (1987) Selective inhibition of translation of the mRNA coding for measles virus membrane protein at elevated temperatures. J Virol 61:472–479
Ogura H, Rima BK, Tas P, Baczko K, ter Meulen V (1988) Restricted synthesis of the fusion protein of measles virus at elevated temperatures. J Gen Virol 69:925–929
Pain VM (1996) Initiation of protein synthesis in eukaryotic cells. Eur J Biochem 236:747–771
Parks CL, Witko SE, Kotash C, Lin SL, Sidhu MS, Udem SA (2006) Role of V protein RNA binding in inhibition of measles virus minigenome replication. Virology 348:96–106
Paterson RG, Harris TJ, Lamb RA (1984) Analysis and gene assignment of mRNAs of a para-myxovirus, simian virus 5. Virology 138:310–323
Plumet S, Duprex WP, Gerlier D (2005) Dynamics of viral RNA synthesis during measles virus infection. J Virol 79:6900–6908
Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, Gerlier D (2007) Cytosolic 5'-triphos-phate ended viral leader transcript of measles virus as activator of the RIG I-mediated inter-feron response. PLoS ONE 2:e279
Poch O, Blumberg BM, Bougueleret L, Tordo N (1990) Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 71:1153–1162
Portner A, Murti KG, Morgan EM, Kingsbury DW (1988) Antibodies against Sendai virus L protein: distribution of the protein in nucleocapsids revealed by immunoelectron microscopy.Virology 163:236–239
Qanungo KR, Shaji D, Mathur M, Banerjee AK (2004) Two RNA polymerase complexes from vesicular stomatitis virus-infected cells that carry out transcription and replication of genome RNA. Proc Natl Acad Sci U S A 101:5952–5957
Radecke F, Billeter MA (1995) Appendix: measles virus antigenome and protein consensus sequences. Curr Top Microbiol Immunol 191:181–192
Radecke F, Billeter (1996) The nonstructural C protein is not essential for multiplication of Edmonston B strain measles virus in cultured cells. Virology 217:418–421
Rager M, Vongpunsawad S, Duprex WP, Cattaneo R (2002) Polyploid measles virus with hexam-eric genome length. EMBO J 21:2364–2372
Rahaman A, Srinivasan N, Shamala N, Shaila MS (2004) Phosphoprotein of the rinderpest virus forms a tetramer through a coiled coil region important for biological function. A structural insight. J Biol Chem 279:23606–23614
Rennick LJ, Duprex WP, Rima BK (2007) Measles virus minigenomes encoding two autofluores-cent proteins reveal cell-to-cell variation in reporter expression dependent on viral sequences between the transcription units. J Gen Virol 88:2710–2718
Richardson C, Hull D, Greer P, Hasel K, Berkovich A, Englund G, Bellini W, Rima B, Lazzarini R (1986) The nucleotide sequence of the mRNA encoding the fusion protein of measles virus(Edmonston strain): a comparison of fusion proteins from several different paramyxoviruses.Virology 155:508–523
Richardson CD, Berkovich A, Rozenblatt S, Bellini WJ (1985) Use of antibodies directed against synthetic peptides for identifying cDNA clones, establishing reading frames, and deducing the gene order of measles virus. J Virol 54:186–193 Riddell MA, Rota JS, Rota PA (2005) Review of the temporal and geographical distribution of measles virus genotypes in the prevaccine and postvaccine eras. Virol J 2:87
Rima BK, Martin SJ (1979) Effect of undiluted passage on the polypeptides of measles virus. J Gen Virol 44:135–144
Rima BK, McFerran NV (1997) Dinucleotide and stop codon frequencies in single-stranded RNA viruses. J Gen Virol 78:2859–2870
Rima BK, Davidson WB, Martin SJ (1977) The role of defective interfering particles in persistent infection of Vero cells by measles virus. J Gen Virol 35:89–97
Rima BK, Baczko K, Clarke DK, Curran MD, Martin SJ, Billeter MA, ter Meulen V (1986) Characterization of clones for the sixth (L) gene and a transcriptional map for morbilliviruses.J Gen Virol 67:1971–1978
Rima BK, Earle JA, Yeo RP, Herlihy L, Baczko K, ter Meulen V, Carabana J, Caballero M, Celma ML, Fernandez-Munoz R (1995) Temporal and geographical distribution of measles virus genotypes. J Gen Virol 76:1173–1180
Rima BK, Earle JA, Baczko K, ter Meulen V, Liebert UG, Carstens C, Carabana J, Caballero M,Celma ML, Fernandez-Munoz R (1997) Sequence divergence of measles virus haemagglutinin during natural evolution and adaptation to cell culture. J Gen Virol 78:97–106
Rima BK, Collin AM, Earle JA (2005) Completion of the sequence of a cetacean morbillivirus and comparative analysis of the complete genome sequences of four morbilliviruses. Virus Genes 30:113–119
Rozenblatt S, Koch T, Pinhasi O, Bratosin S (1979) Infective substructures of measles virus from acutely and persistently infected cells. J Virol 32:329–333
Rudolph MG, Kraus I, Dickmanns A, Eickmann M, Garten W, Ficner R (2003) Crystal structure of the Borna disease virus nucleoprotein. Structure 11:1219–1226
Schneider-Schaulies S, Liebert UG, Baczko K, Cattaneo R, Billeter M, ter Meulen V (1989) Restriction of measles virus gene expression in acute and subacute encephalitis of Lewis rats.Virology 171:525–534
Schneider-Schaulies S, Kreth HW, Hofmann G, Billeter M, ter Meulen V (1991) Expression of measles virus RNA in peripheral blood mononuclear cells of patients with measles SSPE, and autoimmune diseases. Virology 182:703–711
Schneider-Schaulies S, Schneider-Schaulies J, Dunster LM, ter Meulen V (1995) Measles virus gene expression in neural cells. Curr Top Microbiol Immunol 191:101–116
Schneider H, Kaelin K, Billeter MA (1997) Recombinant measles viruses defective for RNA editing and V protein synthesis are viable in cultured cells. Virology 227:314–322
Schnorr JJ, Schneider-Schaulies S, Simon-Jodicke A, Pavlovic J, Horisberger MA, ter Meulen V (1993) MxA-dependent inhibition of measles virus glycoprotein synthesis in a stably trans-fected human monocytic cell line. J Virol 67:4760–4768
Schrag SJ, Rota PA, Bellini WJ (1999) Spontaneous mutation rate of measles virus: direct estimation based on mutations conferring monoclonal antibody resistance. J Virol 73:51–54
Sidhu MS, Chan J, Kaelin K, Spielhofer P, Radecke F, Schneider H, Masurekar M, Dowling PC,Billeter MA, Udem SA (1995) Rescue of synthetic measles virus minireplicons: measles genomic termini direct efficient expression and propagation of a reporter gene. Virology 208:800–807
Stallcup KC, Wechsler SL, Fields BN (1979) Purification of measles virus and characterization of subviral components. J Virol 30:166–176
Sugiyama T, Gursel M, Takeshita F, Coban C, Conover J, Kaisho T, Akira S, Klinman DM, Ishii KJ (2005) CpG RNA: identification of novel single-stranded RNA that stimulates human CD14 +CD11c+ monocytes. J Immunol 174:2273–2279
Suryanarayana K, Baczko K, ter Meulen V, Wagner RR (1994) Transcription inhibition and other properties of matrix proteins expressed by M genes cloned from measles viruses and diseased human brain tissue. J Virol 68:1532–1543
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
Takeda M, Nakatsu Y, Ohno S, Seki F, Tahara M, Hashiguchi T, Yanagi Y (2006) Generation of measles virus with a segmented RNA genome. J Virol 80:4242–4248
Thorne HV, Dermott E (1977) Y-forms as possible intermediates in the replication of measles virus nucleocapsids. Nature 268:345–347
Udem SA, Cook KA (1984) Isolation and characterization of measles virus intracellular nucleo-capsid RNA. J Virol 49:57–65
Valsamakis A, Schneider H, Auwaerter PG, Kaneshima H, Billeter MA, Griffin DE (1998) Recombinant measles viruses with mutations in the C, V, or F gene have altered growth phe-notypes in vivo. J Virol 72:7754–7761
von Messling V, Cattaneo R (2002) Amino-terminal precursor sequence modulates canine distemper virus fusion protein function. J Virol 76:4172–4180
Walpita P (2004) An internal element of the measles virus antigenome promoter modulates replication efficiency. Virus Res 100:199–211
Washenberger CL, Han JQ, Kechris KJ, Jha BK, Silverman RH, Barton DJ (2007) Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res 130:85–95
Waterson A (1962) Two kinds of myxovirus. Nature 193:1163–1164
Whelan SP, Barr JN, Wertz GW (2004) Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283:61–119
Wileman T (2007) Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu Rev Microbiol 61:149–167
Williams BR (1999) PKR: a sentinel kinase for cellular stress. Oncogene 18:6112–6120
Witko SE, Kotash C, Sidhu MS, Udem SA, Parks CL (2006) Inhibition of measles virus minireplicon-encoded reporter gene expression by V protein. Virology 348:107–119
Yoshikawa Y, Tsuruoka H, Matsumoto M, Haga T, Shioda T, Shibuta H, Sato TA, Yamanouchi K (1990) Molecular analysis of structural protein genes of the Yamagata-1 strain of defective subacute sclerosing panencephalitis virus. II. Nucleotide sequence of a cDNA corresponding to the P plus M dicistronic mRNA Virus Genes 4:151–161
Zuniga A, Wang Z, Liniger M, Hangartner L, Caballero M, Pavlovic J, Wild P, Viret JF, Glueck R, Billeter MA, Naim HY (2007) Attenuated measles virus as a vaccine vector. Vaccine 25:2974–2983
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Rima, B.K., Duprex, W.P. (2009). The Measles Virus Replication Cycle. In: Griffin, D.E., Oldstone, M.B.A. (eds) Measles. Current Topics in Microbiology and Immunology, vol 329. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-70523-9_5
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