The measles virus nucleocapsid protein tail domain is dispensable for viral polymerase recruitment and activity

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29943-29953

  Krumm, Stefanie A ^a   Takeda, Makoto ^b   Plemper, Richard K ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYL-TERMINAL; MOLECULAR RECOGNITION ELEMENT; NUCLEOCAPSID PROTEINS; POLYMERASE ACTIVITIES; POLYMERASE COMPLEX; REGULATORY EFFECTS; REPLICATION MODELS; RIBONUCLEOPROTEINS;

RESTORATION; RNA; VIRUSES;

POLYMERS;

NUCLEOCAPSID PROTEIN; RNA POLYMERASE;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; MEASLES VIRUS; MOLECULAR DOCKING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; RESIDUE ANALYSIS; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

ANIMAL VIRUSES; MICROBIOLOGY; VIRAL POLYMERASE; VIRAL REPLICATION; VIRUS;

ANIMALS; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; IMMUNOBLOTTING; MEASLES VIRUS; MODELS, MOLECULAR; MUTATION; NUCLEOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBONUCLEOPROTEINS; RNA REPLICASE; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84885648103     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.503862     Document Type: Article

References (51)

1. Ruigrok, R. W., Crépin, T., and Kolakofsky, D. (2011) Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 14, 504-510
2. Longhi, S. (2009) Nucleocapsid structure and function. Curr. Top. Microbiol. Immunol. 329, 103-128
3. Bankamp, B., Horikami, S. M., Thompson, P. D., Huber, M., Billeter, M., and Moyer, S. A. (1996) Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216, 272-277
4. Curran, J., Pelet, T., and Kolakofsky, D. (1994) An acidic activation-like domain of the Sendai virus P protein is required for RNA synthesis and encapsidation. Virology 202, 875-884
5. Buchholz, C. J., Retzler, C., Homann, H. E., and Neubert, W. J. (1994) The carboxy-terminal domain of Sendai virus nucleocapsid protein is involved in complex formation between phosphoprotein and nucleocapsid-like particles. Virology 204, 770-776
6. Kingston, R. L., Hamel, D. J., Gay, L. S., Dahlquist, F. W., and Matthews, B. W. (2004) Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc. Natl. Acad. Sci. U.S.A. 101, 8301-8306
7. Desfosses, A., Goret, G., Farias Estrozi, L., Ruigrok, R. W., and Gutsche, I. (2011) Nucleoprotein-RNA orientation in the measles virus nucleocapsid by three-dimensional electron microscopy. J. Virol. 85, 1391-1395
8. Jensen, M. R., Communie, G., Ribeiro, E. A., Jr., Martinez, N., Desfosses, A., Salmon, L., Mollica, L., Gabel, F., Jamin, M., Longhi, S., Ruigrok, R. W., and Blackledge, M. (2011) Intrinsic disorder in measles virus nucleocapsids. Proc. Natl. Acad. Sci. U.S.A. 108, 9839-9844
9. Zhang, X., Glendening, C., Linke, H., Parks, C. L., Brooks, C., Udem, S. A., and Oglesbee, M. (2002) Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J. Virol. 76, 8737-8746
10. Longhi, S., Receveur-Bréchot, V., Karlin, D., Johansson, K., Darbon, H., Bhella, D., Yeo, R., Finet, S., and Canard, B. (2003) The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278, 18638-18648
11. Schoehn, G., Mavrakis, M., Albertini, A., Wade, R., Hoenger, A., and Ruigrok, R. W. (2004) The 12 A structure of trypsin-treated measles virus N-RNA. J. Mol. Biol. 339, 301-312
12. Bhella, D., Ralph, A., and Yeo, R. P. (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
13. Tawar, R. G., Duquerroy, S., Vonrhein, C., Varela, P. F., Damier-Piolle, L., Castagné, N., MacLellan, K., Bedouelle, H., Bricogne, G., Bhella, D., Eléouët, J. F., and Rey, F. A. (2009) Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326, 1279-1283
14. Curran, J., Homann, H., Buchholz, C., Rochat, S., Neubert, W., and Kolakofsky, D. (1993) The hypervariable C-terminal tail of the Sendai paramyxovirus nucleocapsid protein is required for template function but not for RNA encapsidation. J. Virol. 67, 4358-4364
15. Kingston, R. L., Baase, W. A., and Gay, L. S. (2004) Characterization of nucleocapsid binding by the measles virus and mumps virus phosphoproteins. J. Virol. 78, 8630-8640
16. Bourhis, J. M., Canard, B., and Longhi, S. (2006) Structural disorder within the replicative complex of measles virus. Functional implications. Virology 344, 94-110
17. Longhi, S. (2012) The measles virus N(TAIL)-XD complex. An illustrative example of fuzziness. Adv. Exp. Med. Biol. 725, 126-141
18. Communie, G., Crépin, T., Maurin, D., Jensen, M. R., Blackledge, M., and Ruigrok, R. W. (2013) Structure of the tetramerization domain of measles virus phosphoprotein. J. Virol. 87, 7166-7169
19. Houben, K., Blanchard, L., Blackledge, M., and Marion, D. (2007) Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P. Biophys. J. 93, 2830-2844
20. Curran, J. (1998) A role for the Sendai virus P protein trimer in RNA synthesis. J. Virol. 72, 4274-4280
21. Longhi, S. (2011) Structural Disorder within the Measles Virus Nucleoprotein and Phosphoprotein: Functional Implications for Transcription and Replication, in Negative Strand RNA Virus (Luo, M., ed.) pp. 95-125, World Scientific Publishing, Singapore
22. Shu, Y., Habchi, J., Costanzo, S., Padilla, A., Brunel, J., Gerlier, D., Oglesbee, M., and Longhi, S. (2012) Plasticity in structural and functional interactions between the phosphoprotein and nucleoprotein of measles virus. J. Biol. Chem. 287, 11951-11967
23. Buchholz, U. J., Finke, S., and Conzelmann, K. K. (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA. BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73, 251-259
24. Ono, N., Tatsuo, H., Hidaka, Y., Aoki, T., Minagawa, H., and 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
25. Doyle, J., Prussia, A., White, L. K., Sun, A., Liotta, D. C., Snyder, J. P., Compans, R. W., and Plemper, R. K. (2006) Two domains that control prefusion stability and transport competence of the measles virus fusion protein. J. Virol. 80, 1524-1536
26. Paal, T., Brindley, M. A., St Clair, C., Prussia, A., Gaus, D., Krumm, S. A., Snyder, J. P., and Plemper, R. K. (2009) Probing the spatial organization of measles virus fusion complexes. J. Virol. 83, 10480-10493
27. Krumm, S. A., Ndungu, J. M., Yoon, J. J., Dochow, M., Sun, A., Natchus, M., Snyder, J. P., and Plemper, R. K. (2011) Potent host-directed smallmolecule inhibitors of myxovirus RNA-dependent RNA-polymerases. PLoS One 6, e20069
28. Radecke, F., Spielhofer, P., Schneider, H., Kaelin, K., Huber, M., Dötsch, C., Christiansen, G., and Billeter, M. A. (1995) Rescue of measles viruses from cloned DNA. EMBO J. 14, 5773-5784
29. Seki, F., Yamada, K., Nakatsu, Y., Okamura, K., Yanagi, Y., Nakayama, T., Komase, K., and 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
30. Madani, F., Lind, J., Damberg, P., Adams, S. R., Tsien, R. Y., and Gräslund, A. O. (2009) Hairpin structure of a biarsenical-tetracysteine motif determined by NMR spectroscopy. J. Am. Chem. Soc. 131, 4613-4615
31. Takeda, M., Takeuchi, K., Miyajima, N., Kobune, F., Ami, Y., Nagata, N., Suzaki, Y., Nagai, Y., and Tashiro, M. (2000) Recovery of pathogenic measles virus from cloned cDNA. J. Virol. 74, 6643-6647
32. Dochow, M., Krumm, S. A., Crowe, J. E., Jr., Moore, M. L., and Plemper, R. K. (2012) Independent structural domains in the paramyxovirus polymerase protein. J. Biol. Chem. 287, 6878-6891
33. Buchholz, C. J., Spehner, D., Drillien, R., Neubert, W. J., and Homann, H. E. (1993) The conserved N-terminal region of Sendai virus nucleocapsid protein NP is required for nucleocapsid assembly. J. Virol. 67, 5803-5812
34. Gardner, M. J., and Altman, D. G. (1986) Confidence intervals rather than P values. Estimation rather than hypothesis testing. Br. Med. J. (Clin. Res. Ed.) 292, 746-750
35. Iwasaki, M., Takeda, M., Shirogane, Y., Nakatsu, Y., Nakamura, T., and Yanagi, Y. (2009) The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J. Virol. 83, 10374-10383
36. Couturier, M., Buccellato, M., Costanzo, S., Bourhis, J. M., Shu, Y., Nicaise, M., Desmadril, M., Flaudrops, C., Longhi, S., and Oglesbee, M. (2010) High affinity binding between Hsp70 and the C-terminal domain of the measles virus nucleoprotein requires an Hsp40 co-chaperone. J. Mol. Recognit. 23, 301-315
37. Zhang, X., Bourhis, J. M., Longhi, S., Carsillo, T., Buccellato, M., Morin, B., Canard, B., and Oglesbee, M. (2005) Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337, 162-174
38. Griffin, B. A., Adams, S. R., and Tsien, R. Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272
39. Duprex, W. P., McQuaid, S., Hangartner, L., Billeter, M. A., and Rima, B. K. (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
40. Collins, P. L., and Wertz, G. W. (1983) cDNA cloning and transcriptional mapping of nine polyadenylylated RNAs encoded by the genome of human respiratory syncytial virus. Proc. Natl. Acad. Sci. U.S.A. 80, 3208-3212
41. Houben, K., Marion, D., Tarbouriech, N., Ruigrok, R. W., and Blanchard, L. (2007) Interaction of the C-terminal domains of sendai virus N and P proteins. Comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J. Virol. 81, 6807-6816
42. Rennick, L. J., Duprex, W. P., and Rima, B. K. (2007) Measles virus minigenomes encoding two autofluorescent proteins reveal cell-to-cell variation in reporter expression dependent on viral sequences between the transcription units. J. Gen. Virol. 88, 2710-2718
43. Diallo, A., Barrett, T., Barbron, M., Meyer, G., and Lefèvre, P. C. (1994) Cloning of the nucleocapsid protein gene of peste-des-petits-ruminants virus. Relationship to other morbilliviruses. J. Gen. Virol. 75, 233-237
44. Cox, R., Green, T. J., Purushotham, S., Deivanayagam, C., Bedwell, G. J., Prevelige, P. E., and Luo, M. (2013) Structural and functional characterization of the mumps virus phosphoprotein. J. Virol. 87, 7558-7568
45. Laine, D., Trescol-Biémont, M. C., Longhi, S., Libeau, G., Marie, J. C., Vidalain, P. O., Azocar, O., Diallo, A., Canard, B., Rabourdin-Combe, C., and Valentin, H. (2003) Measles virus (MV) nucleoprotein binds to a novel cell surface receptor distinct from FcγRII via its C-terminal domain. Role in MV-induced immunosuppression. J. Virol. 77, 11332-11346
46. Laine, D., Bourhis, J. M., Longhi, S., Flacher, M., Cassard, L., Canard, B., Sautès-Fridman, C., Rabourdin-Combe, C., and Valentin, H. (2005) Measles virus nucleoprotein induces cell-proliferation arrest and apoptosis through NTAIL-NR and NCORE-FcγRIIB1 interactions, respectively. J. Gen. Virol. 86, 1771-1784
47. Cevik, B., Kaesberg, J., Smallwood, S., Feller, J. A., and Moyer, S. A. (2004) Mapping the phosphoprotein binding site on Sendai virus NP protein assembled into nucleocapsids. Virology 325, 216-224
48. Cathomen, T., Mrkic, B., Spehner, D., Drillien, R., Naef, R., Pavlovic, J., Aguzzi, A., Billeter, M. A., and 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
49. Curran, J., and Kolakofsky, D. (1999) Replication of paramyxoviruses. Adv. Virus Res. 54, 403-4222
50. Kolakofsky, D., Le Mercier, P., Iseni, F., and Garcin, D. (2004) Viral DNA polymerase scanning and the gymnastics of Sendai virus RNA synthesis. Virology 318, 463-473
51. Johansson, K., Bourhis, J. M., Campanacci, V., Cambillau, C., Canard, B., and Longhi, S. (2003) Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J. Biol. Chem. 278, 44567-44573