Identification and characterization of Sindbis virus RNA-host protein interactions

Journal of Virology

Volumn 92, Issue 7, 2018, Pages

  LaPointe, Autumn T ^a   Gebhart, Natasha N ^b   Meller, Megan E ^b   Hardy, Richard W ^b   Sokoloski, Kevin J ^a  

^a University of Louisville School of Medicine   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Alphavirus; Plus strand RNA virus; Posttranscriptional RNA binding proteins; RNA binding proteins; Virus host interactions

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN GROUP M; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN I; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; SEQUENCE ANALYSIS; SINDBIS VIRUS; VIROGENESIS; VIRUS CELL INTERACTION; WILD TYPE; ALPHAVIRUS INFECTION; CELL CULTURE; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PATHOGENICITY; VIROLOGY; VIRUS ASSEMBLY; VIRUS REPLICATION;

ALPHAVIRUS INFECTIONS; CELLS, CULTURED; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; RNA, VIRAL; SINDBIS VIRUS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 85041894160     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02171-17     Document Type: Article

References (86)

1. Johansson MA, Powers AM, Pesik N, Cohen NJ, Staples JE. 2014. Nowcasting the spread of chikungunya virus in the Americas. PLoS One 9:e104915. https://doi.org/10.1371/journal.pone.0104915
2. Kendrick K, Stanek D, Blackmore C, Centers for Disease Control and Prevention. 2014. Notes from the field: transmission of chikungunya virus in the continental United States-Florida, 2014. MMWR Morb Mortal Wkly Rep 63:1137
3. Ligon BL. 2006. Reemergence of an unusual disease: the chikungunya epidemic. Semin Pediatr Infect Dis 17:99-104. https://doi.org/10.1053/j.spid.2006.04.009
4. Renault P, Balleydier E, D'Ortenzio E, Baville M, Filleul L. 2012. Epidemiology of Chikungunya infection on Reunion Island, Mayotte, and neighboring countries. Med Mal Infect 42:93-101. https://doi.org/10.1016/j.medmal.2011.12.002
5. Renault P, Solet JL, Sissoko D, Balleydier E, Larrieu S, Filleul L, Lassalle C, Thiria J, Rachou E, de Valk H, Ilef D, Ledrans M, Quatresous I, Quenel P, Pierre V. 2007. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005-2006. Am J Trop Med Hyg 77:727-731
6. Staples JE, Breiman RF, Powers AM. 2009. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clin Infect Dis 49:942-948. https://doi.org/10.1086/605496
7. Weaver SC. 2014. Arrival of chikungunya virus in the new world: prospects for spread and impact on public health. PLoS Negl Trop Dis 8:e2921. https://doi.org/10.1371/journal.pntd.0002921
8. Calisher CH. 1994. Medically important arboviruses of the United States and Canada. Clin Microbiol Rev 7:89-116. https://doi.org/10.1128/CMR.7.1.89
9. de la Monte S, Castro F, Bonilla NJ, Gaskin de Urdaneta A, Hutchins GM. 1985. The systemic pathology of Venezuelan equine encephalitis virus infection in humans. Am J Trop Med Hyg 34:194-202. https://doi.org/ 10.4269/ajtmh.1985.34.194
10. Ronca SE, Dineley KT, Paessler S. 2016. Neurological sequelae resulting from encephalitic alphavirus infection. Front Microbiol 7:959. https://doi.org/10.3389/fmicb.2016.00959
11. Kurkela S, Helve T, Vaheri A, Vapalahti O. 2008. Arthritis and arthralgia three years after Sindbis virus infection: clinical follow-up of a cohort of 49 patients. Scand J Infect Dis 40:167-173. https://doi.org/10.1080/00365540701586996
12. Kurkela S, Manni T, Myllynen J, Vaheri A, Vapalahti O. 2005. Clinical and laboratory manifestations of Sindbis virus infection: prospective study, Finland, 2002-2003. J Infect Dis 191:1820-1829. https://doi.org/10.1086/430007
13. Adouchief S, Smura T, Sane J, Vapalahti O, Kurkela S. 2016. Sindbis virus as a human pathogen-epidemiology, clinical picture and pathogenesis. Rev Med Virol 26:221-241. https://doi.org/10.1002/rmv.1876
14. Sissoko D, Malvy D, Ezzedine K, Renault P, Moscetti F, Ledrans M, Pierre V. 2009. Post-epidemic Chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Negl Trop Dis 3:e389. https://doi.org/10.1371/journal.pntd.0000389
15. Hawman DW, Stoermer KA, Montgomery SA, Pal P, Oko L, Diamond MS, Morrison TE. 2013. Chronic joint disease caused by persistent Chikungunya virus infection is controlled by the adaptive immune response. J Virol 87:13878-13888. https://doi.org/10.1128/JVI.02666-13
16. Marimoutou C, Vivier E, Oliver M, Boutin JP, Simon F. 2012. Morbidity and impaired quality of life 30 months after chikungunya infection: comparative cohort of infected and uninfected French military policemen in Reunion Island. Medicine 91:212-219. https://doi.org/10.1097/ MD.0b013e318260b604
17. Schwartz O, Albert ML. 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8:491-500. https://doi.org/10.1038/nrmicro2368
18. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491-562
19. Rupp JC, Sokoloski KJ, Gebhart NN, Hardy RW. 2015. Alphavirus RNA synthesis and non-structural protein functions. J Gen Virol 96: 2483-2500. https://doi.org/10.1099/jgv.0.000249
20. Sokoloski KJ, Nease LM, May NA, Gebhart NN, Jones CE, Morrison TE, Hardy RW. 2017. Identification of interactions between Sindbis virus capsid protein and cytoplasmic vRNA as novel virulence determinants. PLoS Pathog 13:e1006473. https://doi.org/10.1371/journal.ppat.1006473
21. Sokoloski KJ, Haist KC, Morrison TE, Mukhopadhyay S, Hardy RW. 2015. Noncapped alphavirus genomic RNAs and their role during infection. J Virol 89:6080-6092. https://doi.org/10.1128/JVI.00553-15
22. Varjak M, Saul S, Arike L, Lulla A, Peil L, Merits A. 2013. Magnetic fractionation and proteomic dissection of cellular organelles occupied by the late replication complexes of Semliki Forest virus. J Virol 87:10295-10312. https://doi.org/10.1128/JVI.01105-13
23. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM, Rout MP, Chait BT, MacDonald MR. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol 84:6720-6732. https://doi.org/10.1128/JVI.01983-09
24. Cristea IM, Carroll JW, Rout MP, Rice CM, Chait BT, MacDonald MR. 2006. Tracking and elucidating alphavirus-host protein interactions. J Biol Chem 281:30269-30278. https://doi.org/10.1074/jbc.M603980200
25. Frolova E, Gorchakov R, Garmashova N, Atasheva S, Vergara LA, Frolov I. 2006. Formation of nsP3-specific protein complexes during Sindbis virus replication. J Virol 80:4122-4134. https://doi.org/10.1128/JVI.80.8.4122-4134.2006
26. Panas MD, Ahola T, McInerney GM. 2014. The C-terminal repeat domains of nsP3 from the Old World alphaviruses bind directly to G3BP. J Virol 88:5888-5893. https://doi.org/10.1128/JVI.00439-14
27. Frolova EI, Gorchakov R, Pereboeva L, Atasheva S, Frolov I. 2010. Functional Sindbis virus replicative complexes are formed at the plasma membrane. J Virol 84:11679-11695. https://doi.org/10.1128/JVI.01441-10
28. Atasheva S, Gorchakov R, English R, Frolov I, Frolova E. 2007. Development of Sindbis viruses encoding nsP2/GFP chimeric proteins and their application for studying nsP2 functioning. J Virol 81:5046-5057. https:// doi.org/10.1128/JVI.02746-06
29. Gorchakov R, Garmashova N, Frolova E, Frolov I. 2008. Different types of nsP3-containing protein complexes in Sindbis virus-infected cells. J Virol 82:10088-10101. https://doi.org/10.1128/JVI.01011-08
30. Bourai M, Lucas-Hourani M, Gad HH, Drosten C, Jacob Y, Tafforeau L, Cassonnet P, Jones LM, Judith D, Couderc T, Lecuit M, Andre P, Kummerer BM, Lotteau V, Despres P, Tangy F, Vidalain PO. 2012. Mapping of Chikungunya virus interactions with host proteins identified nsP2 as a highly connected viral component. J Virol 86:3121-3134. https://doi.org/ 10.1128/JVI.06390-11
31. Foy NJ, Akhrymuk M, Akhrymuk I, Atasheva S, Bopda-Waffo A, Frolov I, Frolova EI. 2013. Hypervariable domains of nsP3 proteins of New World and Old World alphaviruses mediate formation of distinct, virus-specific protein complexes. J Virol 87:1997-2010. https://doi.org/10.1128/JVI.02853-12
32. Lenarcic EM, Landry DM, Greco TM, Cristea IM, Thompson SR. 2013. Thiouracil cross-linking mass spectrometry: a cell-based method to identify host factors involved in viral amplification. J Virol 87:8697-8712. https://doi.org/10.1128/JVI.00950-13
33. Viktorovskaya OV, Greco TM, Cristea IM, Thompson SR. 2016. Identification of RNA binding proteins associated with dengue virus RNA in infected cells reveals temporally distinct host factor requirements. PLoS Negl Trop Dis 10:e0004921. https://doi.org/10.1371/journal.pntd.0004921
34. Sessions OM, Barrows NJ, Souza-Neto JA, Robinson TJ, Hershey CL, Rodgers MA, Ramirez JL, Dimopoulos G, Yang PL, Pearson JL, Garcia-Blanco MA. 2009. Discovery of insect and human dengue virus host factors. Nature 458:1047-1050. https://doi.org/10.1038/nature07967
35. Burnham AJ, Gong L, Hardy RW. 2007. Heterogeneous nuclear ribonuclear protein K interacts with Sindbis virus nonstructural proteins and viral subgenomic mRNA. Virology 367:212-221. https://doi.org/10.1016/ j.virol.2007.05.008
36. Sokoloski KJ, Dickson AM, Chaskey EL, Garneau NL, Wilusz CJ, Wilusz J. 2010. Sindbis virus usurps the cellular HuR protein to stabilize its transcripts and promote productive infections in mammalian and mosquito cells. Cell Host Microbe 8:196-207. https://doi.org/10.1016/j.chom.2010.07.003
37. Lin JY, Shih SR, Pan M, Li C, Lue CF, Stollar V, Li ML. 2009. hnRNP A1 interacts with the 5= untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol 83:6106-6114. https://doi.org/10.1128/JVI.02476-08
38. Gui H, Lu CW, Adams S, Stollar V, Li ML. 2010. hnRNP A1 interacts with the genomic and subgenomic RNA promoters of Sindbis virus and is required for the synthesis of G and SG RNA. J Biomed Sci 17:59. https:// doi.org/10.1186/1423-0127-17-59
39. Pardigon N, Strauss JH. 1996. Mosquito homolog of the La autoantigen binds to Sindbis virus RNA. J Virol 70:1173-1181
40. Pardigon N, Lenches E, Strauss JH. 1993. Multiple binding sites for cellular proteins in the 3= end of Sindbis alphavirus minus-sense RNA. J Virol 67:5003-5011
41. Bensaude O. 2011. Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription 2:103-108
42. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jr, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141:129-141. https://doi.org/10.1016/j.cell.2010.03.009
43. Niranjanakumari S, Lasda E, Brazas R, Garcia-Blanco MA. 2002. Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26:182-190. https://doi.org/10.1016/S1046-2023(02)00021-X
44. Huang Da W, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1-13. https://doi.org/10.1093/nar/gkn923
45. Huang Da W, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. https://doi.org/10.1038/nprot.2008.211
46. Akhrymuk I, Kulemzin SV, Frolova EI. 2012. Evasion of the innate immune response: the Old World alphavirus nsP2 protein induces rapid degradation of Rpb1, a catalytic subunit of RNA polymerase II. J Virol 86: 7180-7191. https://doi.org/10.1128/JVI.00541-12
47. Amaya M, Keck F, Lindquist M, Voss K, Scavone L, Kehn-Hall K, Roberts B, Bailey C, Schmaljohn C, Narayanan A. 2015. The ubiquitin proteasome system plays a role in Venezuelan equine encephalitis virus infection. PLoS One 10:e0124792. https://doi.org/10.1371/journal.pone.0124792
48. Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C. 2017. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res 45:D362-D368. https://doi.org/10.1093/nar/gkw937
49. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C. 2015. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447-D452. https:// doi.org/10.1093/nar/gku1003
50. Ascano M, Hafner M, Cekan P, Gerstberger S, Tuschl T. 2012. Identification of RNA-protein interaction networks using PAR-CLIP. Wiley Interdiscip Rev RNA 3:159-177. https://doi.org/10.1002/wrna.1103
51. Spitzer J, Hafner M, Landthaler M, Ascano M, Farazi T, Wardle G, Nusbaum J, Khorshid M, Burger L, Zavolan M, Tuschl T. 2014. PAR-CLIP (photoactivatable ribonucleoside-enhanced crosslinking and immunoprecipitation): a step-by-step protocol to the transcriptome-wide identification of binding sites of RNA-binding proteins. Methods Enzymol 539:113-161. https://doi.org/10.1016/B978-0-12-420120-0.00008-6
52. Chaudhury A, Chander P, Howe PH. 2010. Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: focus on hnRNP E1's multifunctional regulatory roles. RNA 16:1449-1462. https://doi.org/10.1261/rna.2254110
53. Geuens T, Bouhy D, Timmerman V. 2016. The hnRNP family: insights into their role in health and disease. Hum Genet 135:851-867. https://doi.org/10.1007/s00439-016-1683-5
54. Habelhah H, Shah K, Huang L, Ostareck-Lederer A, Burlingame AL, Shokat KM, Hentze MW, Ronai Z. 2001. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat Cell Biol 3:325-330. https://doi.org/10.1038/35060131
55. Gorchakov R, Frolova E, Frolov I. 2005. Inhibition of transcription and translation in Sindbis virus-infected cells. J Virol 79:9397-9409. https:// doi.org/10.1128/JVI.79.15.9397-9409.2005
56. Patel RK, Burnham AJ, Gebhart NN, Sokoloski KJ, Hardy RW. 2013. Role for subgenomic mRNA in host translation inhibition during Sindbis virus infection of mammalian cells. Virology 441:171-181. https://doi.org/10.1016/j.virol.2013.03.022
57. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, Laishram RS, Qiao M, Lipshitz HD, Piano F, Corbett AH, Carstens RP, Frey BJ, Anderson RA, Lynch KW, Penalva LO, Lei EP, Fraser AG, Blencowe BJ, Morris QD, Hughes TR. 2013. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499:172-177. https://doi.org/10.1038/nature12311
58. Paziewska A, Wyrwicz LS, Bujnicki JM, Bomsztyk K, Ostrowski J. 2004. Cooperative binding of the hnRNP K three KH domains to mRNA targets. FEBS Lett 577:134-140. https://doi.org/10.1016/j.febslet.2004.08.086
59. Datar KV, Dreyfuss G, Swanson MS. 1993. The human hnRNP M proteins: identification of a methionine/arginine-rich repeat motif in ribonucleoproteins. Nucleic Acids Res 21:439-446. https://doi.org/10.1093/nar/21.3.439
60. Swanson MS, Dreyfuss G. 1988. Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol Cell Biol 8:2237-2241. https://doi.org/10.1128/MCB.8.5.2237
61. Garcia-Blanco MA, Jamison SF, Sharp PA. 1989. Identification and purification of a 62, 000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev 3:1874-1886. https://doi.org/10.1101/gad.3.12a.1874
62. Sanz MA, Garcia-Moreno M, Carrasco L. 2015. Inhibition of host protein synthesis by Sindbis virus: correlation with viral RNA replication and release of nuclear proteins to the cytoplasm. Cell Microbiol 17:520-541. https://doi.org/10.1111/cmi.12381
63. Barnes M, van Rensburg G, Li WM, Mehmood K, Mackedenski S, Chan CM, King DT, Miller AL, Lee CH. 2015. Molecular insights into the coding region determinant-binding protein-RNA interaction through sitedirected mutagenesis in the heterogeneous nuclear ribonucleoprotein-K-homology domains. J Biol Chem 290:625-639. https://doi.org/10.1074/jbc.M114.614735
64. Doyle GA, Betz NA, Leeds PF, Fleisig AJ, Prokipcak RD, Ross J. 1998. The c-myc coding region determinant-binding protein: a member of a family of KH domain RNA-binding proteins. Nucleic Acids Res 26:5036-5044. https://doi.org/10.1093/nar/26.22.5036
65. Prokipcak RD, Herrick DJ, Ross J. 1994. Purification and properties of a protein that binds to the C-terminal coding region of human c-myc mRNA. J Biol Chem 269:9261-9269
66. Liu TY, Chen YC, Jong YJ, Tsai HJ, Lee CC, Chang YS, Chang JG, Chang YF. 2017. Muscle developmental defects in heterogeneous nuclear ribonucleoprotein A1 knockout mice. Open Biol 7:160303. https://doi.org/10.1098/rsob.160303
67. Ye J, Beetz N, O'Keeffe S, Tapia JC, Macpherson L, Chen WV, Bassel-Duby R, Olson EN, Maniatis T. 2015. hnRNP U protein is required for normal pre-mRNA splicing and postnatal heart development and function. Proc Natl Acad Sci U S A 112:E3020-E3029. https://doi.org/10.1073/pnas.1508461112
68. Jin Z, Liang F, Yang J, Mei W. 2017. hnRNP I regulates neonatal immune adaptation and prevents colitis and colorectal cancer. PLoS Genet 13: e1006672. https://doi.org/10.1371/journal.pgen.1006672
69. Ghanem LR, Kromer A, Silverman IM, Chatterji P, Traxler E, Penzo-Mendez A, Weiss MJ, Stanger BZ, Liebhaber SA. 2015. The poly(C) binding protein Pcbp2 and its retrotransposed derivative Pcbp1 are independently essential to mouse development. Mol Cell Biol 36: 304-319. https://doi.org/10.1128/MCB.00936-15
70. Gaudreau MC, Grapton D, Helness A, Vadnais C, Fraszczak J, Shooshtarizadeh P, Wilhelm B, Robert F, Heyd F, Moroy T. 2016. Heterogeneous nuclear ribonucleoprotein L is required for the survival and functional integrity of murine hematopoietic stem cells. Sci Rep 6:27379. https:// doi.org/10.1038/srep27379
71. Krecic AM, Swanson MS. 1999. hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 11:363-371. https://doi.org/10.1016/S0955-0674(99)80051-9
72. Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T, Chabot B. 2007. hnRNP proteins and splicing control. Adv Exp Med Biol 623: 123-147
73. Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, Yan BY, Donohue JP, Shiue L, Hoon S, Brenner S, Ares M, Jr, Yeo GW. 2012. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 1:167-178. https://doi.org/10.1016/ j.celrep.2012.02.001
74. Garmashova N, Gorchakov R, Volkova E, Paessler S, Frolova E, Frolov I. 2007. The Old World and New World alphaviruses use different virusspecific proteins for induction of transcriptional shutoff. J Virol 81: 2472-2484. https://doi.org/10.1128/JVI.02073-06
75. Gorchakov R, Frolova E, Williams BR, Rice CM, Frolov I. 2004. PKRdependent and-independent mechanisms are involved in translational shutoff during Sindbis virus infection. J Virol 78:8455-8467. https://doi.org/10.1128/JVI.78.16.8455-8467.2004
76. Sokoloski KJ, Hayes CA, Dunn MP, Balke JL, Hardy RW, Mukhopadhyay S. 2012. Sindbis virus infectivity improves during the course of infection in both mammalian and mosquito cells. Virus Res 167:26-33. https://doi.org/10.1016/j.virusres.2012.03.015
77. Sokoloski KJ, Snyder AJ, Liu NH, Hayes CA, Mukhopadhyay S, Hardy RW. 2013. Encapsidation of host-derived factors correlates with enhanced infectivity of Sindbis virus. J Virol 87:12216-12226. https://doi.org/10.1128/JVI.02437-13
78. Hwang CK, Wagley Y, Law PY, Wei LN, Loh HH. 2017. Phosphorylation of poly(rC) binding protein 1 (PCBP1) contributes to stabilization of mu opioid receptor (MOR) mRNA by interaction with AU-rich element RNAbinding protein 1 (AUF1) and poly A binding protein (PABP). Gene 598:113-130. https://doi.org/10.1016/j.gene.2016.11.003
79. Lee PT, Chao PK, Ou LC, Chuang JY, Lin YC, Chen SC, Chang HF, Law PY, Loh HH, Chao YS, Su TP, Yeh SH. 2014. Morphine drives internal ribosome entry site-mediated hnRNP K translation in neurons through opioid receptor-dependent signaling. Nucleic Acids Res 42:13012-13025. https:// doi.org/10.1093/nar/gku1016
80. Calabretta S, Bielli P, Passacantilli I, Pilozzi E, Fendrich V, Capurso G, Fave GD, Sette C. 2016. Modulation of PKM alternative splicing by PTBP1 promotes gemcitabine resistance in pancreatic cancer cells. Oncogene 35:2031-2039. https://doi.org/10.1038/onc.2015.270
81. Bielli P, Bordi M, Di Biasio V, Sette C. 2014. Regulation of BCL-X splicing reveals a role for the polypyrimidine tract binding protein (PTBP1/ hnRNP I) in alternative 5= splice site selection. Nucleic Acids Res 42:12070-12081. https://doi.org/10.1093/nar/gku922
82. Motallebipour M, Rada-Iglesias A, Westin G, Wadelius C. 2010. Two polypyrimidine tracts in the nitric oxide synthase 2 gene: similar regulatory sequences with different properties. Mol Biol Rep 37:2021-2030. https://doi.org/10.1007/s11033-009-9653-9
83. Marko M, Leichter M, Patrinou-Georgoula M, Guialis A. 2010. hnRNP M interacts with PSF and p54(nrb) and co-localizes within defined nuclear structures. Exp Cell Res 316:390-400. https://doi.org/10.1016/j.yexcr.2009.10.021
84. Marko M, Leichter M, Patrinou-Georgoula M, Guialis A. 2014. Selective interactions of hnRNP M isoforms with the TET proteins TAF15 and TLS/FUS. Mol Biol Rep 41:2687-2695. https://doi.org/10.1007/s11033-014-3128-3
85. Jagdeo JM, Dufour A, Fung G, Luo H, Kleifeld O, Overall CM, Jan E. 2015. Heterogeneous nuclear ribonucleoprotein M facilitates enterovirus infection. J Virol 89:7064-7078. https://doi.org/10.1128/JVI.02977-14
86. Garneau NL, Sokoloski KJ, Opyrchal M, Neff CP, Wilusz CJ, Wilusz J. 2008. The 3= untranslated region of Sindbis virus represses deadenylation of viral transcripts in mosquito and mammalian cells. J Virol 82:880-892. https://doi.org/10.1128/JVI.01205-07