The alternative splicing factor hnRNP A1 is up-regulated during virus-infected epithelial cell differentiation and binds the human papillomavirus type 16 late regulatory element

Virus Research

Volumn 131, Issue 2, 2008, Pages 189-198

  Cheunim, Thanaporn ^a   Zhang, Jingxin ^a   Milligan, Steven G ^a   McPhillips, Maria G ^a   Graham, Sheila V ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Alternative splicing; hnRNP A1; HPV16; RNA processing

Indexed keywords

GLUTATHIONE TRANSFERASE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOHISTOCHEMISTRY; LIFE CYCLE; MONOLAYER CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REGULATORY SEQUENCE; RNA PROCESSING; UTERINE CERVIX CANCER; VIRUS INFECTION; WESTERN BLOTTING;

CELL LINE; DNA, VIRAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPITHELIAL CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMAN PAPILLOMAVIRUS 16; HUMANS; ORGAN CULTURE TECHNIQUES; PROTEIN BINDING; REGULATORY ELEMENTS, TRANSCRIPTIONAL; UP-REGULATION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 38849199244     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.09.006     Document Type: Article

References (46)

1. Black D.J., Chan R., Min H., Wang J., and Bell L. The electrophoretic mobility shift assay for RNA binding proteins. In: Smith C.W.J. (Ed). RNA:Protein Interactions: A Practical Approach (1998), Oxford University Press, Oxford, UK 109-136
2. Blanchette M., and Chabot B. Modulation of exon skipping by high affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J. 18 (1999) 1939-1952
3. Bonnal S., Pileur F., Orsini C., Parker F., Pujol F., Prats A.-C., and Vagner S. Heterogeneous nuclear ribonucleoprotein A1 is a novel internal ribosome entry site trans-acting factor that modulates alternative initiation of translation of the fibroblast growth factor 2 mRNA. J. Biol. Chem. 280 (2005) 4144-4153
4. Boukamp P., Petrussevska R.T., Breitkreutz R., Horhung J., Markham A., and Fusenig N.E. Normal keratinization in a spontaneously immortalised aneuploid human keratinocyte cell line. J. Cell Biol. 106 (1988) 761-771
5. Burd C., and Dreyfuss G. RNA binding specificities of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 13 (1994) 1197-1204
6. Caceres J.F., Stamm S., Helfman D., and Krainer A.R. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265 (1994) 1706-1709
7. Collier B., Goobar-Larsson L., Sokolowski M., and Schwartz S. Translational inhibition in vitro of human papillomavirus type 16 L2 mRNA mediated through interaction with heterogenous ribonucleoprotein K and poly(rC)-binding proteins 1 and 2. J. Biol. Chem. 273 (1998) 22648-22656
8. Collier B., Oberg D., Zhao X., and Schwartz S. Specific inactivation of inhibitory sequences in the 5' end of the human papillomavirus type 16 L1 open reading frame results in production of high levels of L1 protein in human epithelial cells. J. Virol. 76 (2002) 2739-2752
9. Cumming S.A., McPhillips M.G., Veerapraditsin T., Milligan S.G., and Graham S.V. Activity of the human papillomavirus type 16 late negative regulatory element is partly due to four weak consensus 5′ splice sites that bind a U1 snRNP-like complex. J. Virol. 77 (2003) 5167-5177
10. Damgaard C.R., Tange T.Ø., and Kjems J. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA 8 (2002) 1401-1415
11. Dietrich-Goetz W., Kennedy I.M., Levins B., Stanley M.A., and Clements J.B. A cellular 65 kDa protein recognizes the negative regulatory element of human papillomavirus late mRNA. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 163-168
12. Dignam J.D., Lebovitz R.M., and Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11 (1983) 1475-1489
13. Eperon I.C., Makarova O.V., Mayeda A., Munroe S.H., Caceres J.F., Hayward D.G., and Krainer A.R. Selection of alternative 5′ splice sites: role of U1 snRNP and models for the antagonistic effects of SF2/ASF and hnRNP A1. Mol. Cell. Biol. 20 (2000) 8303-8318
14. Fuchs E. Epidermal differentiation: the bare essentials. J. Cell Biol. 111 (1990) 2807-2814
15. Furth P.A., and Baker C.C. An element in the bovine papillomavirus late 3′ untranslated region reduces polyadenylated cytoplasmic RNA levels. J. Virol. 65 (1991) 5806-5812
16. Furth P.A., Choe W.-T., Rex J.H., Byrne J.C., and Baker C.C. Sequences homologous to 5′ splice sites are required for the inhibitory activity of papillomavirus late 3′ untranslated regions. Mol. Cell. Biol. 14 (1994) 5278-5289
17. Graham S.V. Late events in the life cycle of human papillomaviruses. In: Campo M.S. (Ed). Papillomavirus Research: from Natural History to Vaccines and Beyond (2006), Caister Academic Press, Wymondham, Norfolk 193-212
18. Gunderson S.I., Polycarpou-Schwarz M., and Mattaj I.W. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70 K and poly(A) polymerase. Mol. Cell 1 (1998) 255-264
19. Hamilton B.J., Burns C.M., Nichols R.C., and Rigby W.F.C. Modulation of AUUUA response element binding by heterogeneous nuclear ribonucleoprotein A1 in human T lymphocytes. J. Biol. Chem. 272 (1997) 28732-28741
20. Hanamura A., Càceres J.F., Mayeda A., Franza B.R., and Krainer A.R. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4 (1998) 430-444
21. Howley P.M. Papillomavirinae: the viruses and their replication. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields Virology (1996), Lippincott-Raven Publishers, Philadelphia, PA 2045-2076
22. Izaurralde E., Jarnolowski A., Beisel C., Mattaj I.W., Dreyfuss G., and Fischer V. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137 (1997) 27-35
23. Jeon S., Allen-Hoffman B.L., and Lambert P.F. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J. Virol. 69 (1995) 2989-2997
24. Kamma H., Portman D.S., and Dreyfuss G. Cell type-specific expression of hnRNP proteins. Exp. Cell Res. 221 (1995) 187-196
25. Kennedy I.M., Haddow J.K., and Clements J.B. Analysis of human papillomavirus type 16 late mRNA 3′ processing signals in vitro and in vivo. J. Virol. 64 (1990) 1825-1829
26. Koffa M.D., Graham S.V., Takagaki Y., Manley J.L., and Clements J.B. The human papillomavirus type 16 negative regulatory element interacts with three proteins that act at different posttranscriptional levels. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4677-4682
27. Krecic A.M., and Swanson M.S. hnRNP A1 complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11 (1999) 363-371
28. Marchand V., Méreau A., Jacquenet S., Thomas D., Mougin A., Gattoni R., Stévenin J., and Branlant C.A. Janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding. J. Mol. Biol. 323 (2002) 629-652
29. McPhillips M.G., Veerapraditsin T., Cumming S.A., Karali D., Milligan S.G., Boner W., Morgan I.M., and Graham S.V. SF2/ASF binds the human papillomavirus type 16 late RNA control element and is regulated during epithelial differentiation. J. Virol. 78 (2004) 10598-10605
30. Meyers C., Frattini M.G., Hudson J.B., and Laimins L.A. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science 257 (1992) 971-973
31. Meyers C., and Laimins L.A. In vitro systems for the study and propagation of human papillomaviruses. Curr. Top. Microbiol. Immunol. 186 (1994) 199-215
32. Mili S., Shu H.J., Zhao Y., and Pinol-Roma S. Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol. Cell. Biol. 21 (2001) 7307-7319
33. Milligan S.G., Veerapraditsin T., Ahamat B., Mole S., and Graham S.V. Analysis of novel human papillomavirus type 16 late mRNAs in differentiated W12 cervical epithelial cells. Virology 360 (2007) 172-181
34. Pinol-Roma S. HnRNP proteins and the nuclear export of mRNA. Semin. Cell Dev. Biol. 8 (1997) 57-63
35. Reed R. Mechanisms of fidelity in pre-mRNA splicing. Curr. Opin. Cell Biol. 12 (2000) 340-345
36. Rush M., Zhao X., and Schwartz S.A. A splicing enhancer in the E4 coding region of human papillomavirus type 16 is required for early mRNA splicing and polyadenylation as well as inhibition of premature late gene expression. J. Virol. 79 (2005) 12002-12015
37. Sanford J.R., Ellis J., and Caceres J.F. Multiple roles of arginine/serine-rich splicing factors in RNA processing. Biochem. Soc Trans. 33 (2005) 443-446
38. Schoop V.M., Mirancea N., and Fusenig N.E. Epidermal organization and differentiation of HaCaT keratinocytes in organotypic coculture with human dermal fibroblasts. J. Invest. Dermatol. 112 (1999) 343-353
39. Stanley M.A., Browne H.M., Appelby M., and Minson A.C. Properties of a non-tumourigenic human cervical keratinocyte cell line. Int. J. Cancer 43 (1989) 672-676
40. Steele B.K., Meyers C., and Ozbun M.A. Variable expression of some "housekeeping" genes during human keratinocyte differentiation. Anal. Biochem. 307 (2002) 341-347
41. Stoler M.H., Wolinsky S.M., Whitbeck A., Broker T.R., and Chow L.T. Differentiation-linked human papillomavirus types 6 and 11 transcription in genital condylomata revealed by in situ hybridisation with message-specific RNA probes. Virology 172 (1989) 331-340
42. Stubenrauch F., and Laimins L.A. Human papillomavirus life cycle: active and latent phases. Semin. Cancer Biol. 9 (1999) 379-386
43. Zhao X., Rush M., and Schwartz S. Identification of an hnRNP A1-dependent splicing silencer in the human papillomavirus type 16 L1 coding region that prevents premature expression of the late L1 gene. J. Virol. 78 (2004) 10888-10905
44. Zheng Z.-M., Tao M., Yamanegi K., Bodaghi S., and Xiao W. Splicing of a cap-proximal human papillomavirus 16 E6E7 intron promotes E7 expression, but can be restrained by distance of the intron from its RNA 5′ cap. J. Mol. Biol. 337 (2004) 1091-1108
45. Zhu J., Mayeda A., and Krainer A.R. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8 (2001) 1351-1361
46. zur Hausen H. Papillomavirus infections-a major cause of human cancers. Biochem. Biophys. Acta 1288 (1996) F55-F78