DOI: 10.1083/jcb.200706048. Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains

Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains

10.1083/jcb.200706048

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

In myotonic dystrophy type 1 (DM1), triplet repeat expansion in the 3′ untranslated region of dystrophia myotonica protein kinase (DMPK) causes the nuclear retention of mutant messenger RNA (mRNA). Although the DMPK gene locus positions precisely at the outer edge of a factor-rich SC-35 domain, the normal mRNA consistently accumulates within the domain, and this RNA is depleted upon transcriptional inhibition. In DM1, mutant transcripts detach from the gene but accumulate in granules that abut but do not enter SC-35 domains, suggesting that RNA entry into the domain is blocked. Despite their exclusion from these compartments, mutant transcripts are spliced. MBNL1 (muscleblind-like protein 1) is an alternative splicing factor that becomes highly concentrated with mutant RNA foci. Small interfering RNA–mediated knockdown of MBNL1 promotes the accumulation or entry of newly synthesized mutant transcripts in the SC-35 domain. Collectively, these data suggest that an initial step in the intranuclear path of some mRNAs is passage from the gene into an SC-35 domain and implicate these structures in postsplicing steps before export.

Bibliography

Smith, K. P., Byron, M., Johnson, C., Xing, Y., & Lawrence, J. B. (2007). Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains. The Journal of Cell Biology, 178(6), 951â964.

Authors 5

Kelly P. Smith (first)
Meg Byron (additional)
Carol Johnson (additional)
Yigong Xing (additional)
Jeanne B. Lawrence (additional)

References 71 Referenced 51

10.1038/355548a0 / Nature. (1992)
10.1083/jcb.127.3.593 / J. Cell Biol. (1994)
10.1101/gad.12.7.996 / Genes Dev. (1998)
10.1016/j.bbadis.2005.11.004 / Biochim. Biophys. Acta. (2006)
{'key': '2023072223070092400_BIB5', 'first-page': '385', 'volume': '69', 'year': '1992', 'journal-title': 'Cell.'} / Cell. (1992)
10.1083/jcb.115.5.1191 / J. Cell Biol. (1991)
10.1126/science.8446902 / Science. (1993)
10.1101/SQB.1996.061.01.061 / Cold Spring Harb. Symp. Quant. Biol. (1996)
10.1101/gad.380906 / Genes Dev. (2006)
10.1126/science.1108625 / Science. (2005)
10.1073/pnas.0601069103 / Proc. Natl. Acad. Sci. USA. (2006)
10.1074/jbc.M410781200 / J. Biol. Chem. (2005)
10.1073/pnas.94.14.7388 / Proc. Natl. Acad. Sci. USA. (1997)
10.1016/j.nmd.2004.09.012 / Neuromuscul. Disord. (2005)
10.1212/01.WNL.0000054481.84978.F9 / Neurology. (2003)
10.1126/science.1088679 / Science. (2004)
10.1016/0962-8924(94)90180-5 / Trends Cell Biol. (1994)
10.1016/0014-4827(71)90628-8 / Exp. Cell Res. (1971)
10.1093/nar/29.13.2766 / Nucleic Acids Res. (2001)
10.1016/S0960-9822(01)00632-7 / Curr. Biol. (2002)
10.1038/343437a0 / Nature. (1990)
10.1126/science.1546326 / Science. (1992)
10.1016/j.ceb.2006.03.002 / Curr. Opin. Cell Biol. (2006)
10.1093/hmg/11.25.3157 / Hum. Mol. Genet. (2002)
{'key': '2023072223070092400_BIB25', 'first-page': '664', 'volume': '288', 'year': '2006', 'journal-title': 'Anat. Rec. A Discov. Mol. Cell. Evol. Biol.'} / Anat. Rec. A Discov. Mol. Cell. Evol. Biol. (2006)
10.1073/pnas.94.14.7394 / Proc. Natl. Acad. Sci. USA. (1997)
10.1083/jcb.126.4.877 / J. Cell Biol. (1994)
10.1186/1471-2164-8-39 / BMC Genomics. (2007)
10.1093/hmg/ddh327 / Hum. Mol. Genet. (2004)
10.1016/S0091-679X(08)60569-5 / Methods Cell Biol. (1991)
10.1083/jcb.150.3.417 / J. Cell Biol. (2000)
10.1016/j.tig.2004.12.009 / Trends Genet. (2005)
10.1083/jcb.145.6.1133 / J. Cell Biol. (1999)
10.1126/science.1088583 / Science. (2003)
10.1093/nar/gki698 / Nucleic Acids Res. (2005)
10.1101/SQB.1993.058.01.088 / Cold Spring Harb. Symp. Quant. Biol. (1993)
10.1093/hmg/ddl132 / Hum. Mol. Genet. (2006)
10.1126/science.1062125 / Science. (2001)
10.1126/science.1546325 / Science. (1992)
10.1093/hmg/10.19.2165 / Hum. Mol. Genet. (2001)
10.1093/hmg/ddl103 / Hum. Mol. Genet. (2006)
10.1101/gad.1302205 / Genes Dev. (2005)
10.1093/emboj/19.17.4439 / EMBO J. (2000)
10.1093/hmg/4.suppl_1.1779 / Hum. Mol. Genet. (1995)
10.1091/mbc.e03-06-0388 / Mol. Biol. Cell. (2004)
10.1083/jcb.200310139 / J. Cell Biol. (2004)
10.1083/jcb.102.1.137 / J. Cell Biol. (1986)
{'key': '2023072223070092400_BIB48', 'first-page': 'R162', 'volume': '2', 'year': '2006', 'journal-title': 'Hum. Mol. Genet.'} / Hum. Mol. Genet. (2006)
10.1111/j.1432-0436.2006.00060.x / Differentiation. (2006)
10.1038/sj.emboj.7601296 / EMBO J. (2006)
10.1126/science.280.5364.737 / Science. (1998)
10.1091/mbc.e03-06-0395 / Mol. Biol. Cell. (2003)
{'key': '2023072223070092400_BIB53', 'first-page': '179', 'volume': '1', 'year': '1981', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. (1981)
10.1083/jcb.200503061 / J. Cell Biol. (2006)
10.1016/S1047-8477(02)00507-5 / J. Struct. Biol. (2002)
10.1083/jcb.200303131 / J. Cell Biol. (2003)
10.1083/jcb.144.4.617 / J. Cell Biol. (1999)
10.1146/annurev.cb.09.110193.001405 / Annu. Rev. Cell Biol. (1993)
10.1002/j.1460-2075.1991.tb04911.x / EMBO J. (1991)
{'key': '2023072223070092400_BIB60', 'year': '2002'} (2002)
10.1083/jcb.128.6.995 / J. Cell Biol. (1995)
10.1017/S1355838200991544 / RNA. (2000)
10.1093/nar/24.22.4407 / Nucleic Acids Res. (1996)
10.1073/pnas.92.12.5366 / Proc. Natl. Acad. Sci. USA. (1995)
10.1074/jbc.M005960200 / J. Biol. Chem. (2001)
10.1111/j.1365-2443.2006.00936.x / Genes Cells. (2006)
10.1016/0014-4827(88)90159-0 / Exp. Cell Res. (1988)
10.1083/jcb.146.3.543 / J. Cell Biol. (1999)
10.1126/science.8446901 / Science. (1993)
10.1083/jcb.131.6.1635 / J. Cell Biol. (1995)
10.1038/35030160 / Nature. (2000)

Dates

Type	When
Created	17 years, 11 months ago (Sept. 10, 2007, 2:38 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 7:07 p.m.)
Indexed	1 year, 2 months ago (June 18, 2024, 9:34 p.m.)
Issued	17 years, 11 months ago (Sept. 10, 2007)
Published	17 years, 11 months ago (Sept. 10, 2007)
Published Online	17 years, 11 months ago (Sept. 10, 2007)
Published Print	17 years, 11 months ago (Sept. 10, 2007)

Funders 0

None

BibTeX

@article{Smith_2007, title={Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains}, volume={178}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200706048}, DOI={10.1083/jcb.200706048}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Smith, Kelly P. and Byron, Meg and Johnson, Carol and Xing, Yigong and Lawrence, Jeanne B.}, year={2007}, month=sep, pages={951–964} }

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      "year": "1992",
      "journal-title": "Nature."
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    {
      "key": "2023072223070092400_BIB2",
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      "first-page": "593",
      "DOI": "10.1083/jcb.127.3.593",
      "volume": "127",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "996",
      "DOI": "10.1101/gad.12.7.996",
      "volume": "12",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072223070092400_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/j.bbadis.2005.11.004",
      "volume": "1762",
      "year": "2006",
      "journal-title": "Biochim. Biophys. Acta."
    },
    {
      "key": "2023072223070092400_BIB5",
      "first-page": "385",
      "volume": "69",
      "year": "1992",
      "journal-title": "Cell."
    },
    {
      "key": "2023072223070092400_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "1191",
      "DOI": "10.1083/jcb.115.5.1191",
      "volume": "115",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "1330",
      "DOI": "10.1126/science.8446902",
      "volume": "259",
      "year": "1993",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "607",
      "DOI": "10.1101/SQB.1996.061.01.061",
      "volume": "61",
      "year": "1996",
      "journal-title": "Cold Spring Harb. Symp. Quant. Biol."
    },
    {
      "key": "2023072223070092400_BIB9",
      "doi-asserted-by": "crossref",
      "first-page": "2223",
      "DOI": "10.1101/gad.380906",
      "volume": "20",
      "year": "2006",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072223070092400_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "1149",
      "DOI": "10.1126/science.1108625",
      "volume": "308",
      "year": "2005",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "7688",
      "DOI": "10.1073/pnas.0601069103",
      "volume": "103",
      "year": "2006",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072223070092400_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "5773",
      "DOI": "10.1074/jbc.M410781200",
      "volume": "280",
      "year": "2005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072223070092400_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "7388",
      "DOI": "10.1073/pnas.94.14.7388",
      "volume": "94",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072223070092400_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1016/j.nmd.2004.09.012",
      "volume": "15",
      "year": "2005",
      "journal-title": "Neuromuscul. Disord."
    },
    {
      "key": "2023072223070092400_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "657",
      "DOI": "10.1212/01.WNL.0000054481.84978.F9",
      "volume": "60",
      "year": "2003",
      "journal-title": "Neurology."
    },
    {
      "key": "2023072223070092400_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "383",
      "DOI": "10.1126/science.1088679",
      "volume": "303",
      "year": "2004",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "86",
      "DOI": "10.1016/0962-8924(94)90180-5",
      "volume": "4",
      "year": "1994",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1016/0014-4827(71)90628-8",
      "volume": "67",
      "year": "1971",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072223070092400_BIB19",
      "doi-asserted-by": "crossref",
      "first-page": "2766",
      "DOI": "10.1093/nar/29.13.2766",
      "volume": "29",
      "year": "2001",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072223070092400_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1016/S0960-9822(01)00632-7",
      "volume": "12",
      "year": "2002",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072223070092400_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1038/343437a0",
      "volume": "343",
      "year": "1990",
      "journal-title": "Nature."
    },
    {
      "key": "2023072223070092400_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "1256",
      "DOI": "10.1126/science.1546326",
      "volume": "255",
      "year": "1992",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "284",
      "DOI": "10.1016/j.ceb.2006.03.002",
      "volume": "18",
      "year": "2006",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "3157",
      "DOI": "10.1093/hmg/11.25.3157",
      "volume": "11",
      "year": "2002",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072223070092400_BIB25",
      "first-page": "664",
      "volume": "288",
      "year": "2006",
      "journal-title": "Anat. Rec. A Discov. Mol. Cell. Evol. Biol."
    },
    {
      "key": "2023072223070092400_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "7394",
      "DOI": "10.1073/pnas.94.14.7394",
      "volume": "94",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072223070092400_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "877",
      "DOI": "10.1083/jcb.126.4.877",
      "volume": "126",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "39",
      "DOI": "10.1186/1471-2164-8-39",
      "volume": "8",
      "year": "2007",
      "journal-title": "BMC Genomics."
    },
    {
      "key": "2023072223070092400_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "3079",
      "DOI": "10.1093/hmg/ddh327",
      "volume": "13",
      "year": "2004",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072223070092400_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1016/S0091-679X(08)60569-5",
      "volume": "35",
      "year": "1991",
      "journal-title": "Methods Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "417",
      "DOI": "10.1083/jcb.150.3.417",
      "volume": "150",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "93",
      "DOI": "10.1016/j.tig.2004.12.009",
      "volume": "21",
      "year": "2005",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072223070092400_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "1133",
      "DOI": "10.1083/jcb.145.6.1133",
      "volume": "145",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "1978",
      "DOI": "10.1126/science.1088583",
      "volume": "302",
      "year": "2003",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "3866",
      "DOI": "10.1093/nar/gki698",
      "volume": "33",
      "year": "2005",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072223070092400_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "807",
      "DOI": "10.1101/SQB.1993.058.01.088",
      "volume": "58",
      "year": "1993",
      "journal-title": "Cold Spring Harb. Symp. Quant. Biol."
    },
    {
      "key": "2023072223070092400_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "2087",
      "DOI": "10.1093/hmg/ddl132",
      "volume": "15",
      "year": "2006",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072223070092400_BIB38",
      "doi-asserted-by": "crossref",
      "first-page": "864",
      "DOI": "10.1126/science.1062125",
      "volume": "293",
      "year": "2001",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB39",
      "doi-asserted-by": "crossref",
      "first-page": "1253",
      "DOI": "10.1126/science.1546325",
      "volume": "255",
      "year": "1992",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB40",
      "doi-asserted-by": "crossref",
      "first-page": "2165",
      "DOI": "10.1093/hmg/10.19.2165",
      "volume": "10",
      "year": "2001",
      "journal-title": "Hum. Mol. Genet."
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    {
      "key": "2023072223070092400_BIB41",
      "doi-asserted-by": "crossref",
      "first-page": "1808",
      "DOI": "10.1093/hmg/ddl103",
      "volume": "15",
      "year": "2006",
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    },
    {
      "key": "2023072223070092400_BIB42",
      "doi-asserted-by": "crossref",
      "first-page": "1512",
      "DOI": "10.1101/gad.1302205",
      "volume": "19",
      "year": "2005",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072223070092400_BIB43",
      "doi-asserted-by": "crossref",
      "first-page": "4439",
      "DOI": "10.1093/emboj/19.17.4439",
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      "year": "2000",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072223070092400_BIB44",
      "doi-asserted-by": "crossref",
      "first-page": "1779",
      "DOI": "10.1093/hmg/4.suppl_1.1779",
      "volume": "4",
      "year": "1995",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072223070092400_BIB45",
      "doi-asserted-by": "crossref",
      "first-page": "197",
      "DOI": "10.1091/mbc.e03-06-0388",
      "volume": "15",
      "year": "2004",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072223070092400_BIB46",
      "doi-asserted-by": "crossref",
      "first-page": "191",
      "DOI": "10.1083/jcb.200310139",
      "volume": "165",
      "year": "2004",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB47",
      "doi-asserted-by": "crossref",
      "first-page": "137",
      "DOI": "10.1083/jcb.102.1.137",
      "volume": "102",
      "year": "1986",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB48",
      "first-page": "R162",
      "volume": "2",
      "year": "2006",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072223070092400_BIB49",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1111/j.1432-0436.2006.00060.x",
      "volume": "74",
      "year": "2006",
      "journal-title": "Differentiation."
    },
    {
      "key": "2023072223070092400_BIB50",
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      "first-page": "4271",
      "DOI": "10.1038/sj.emboj.7601296",
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      "year": "2006",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072223070092400_BIB51",
      "doi-asserted-by": "crossref",
      "first-page": "737",
      "DOI": "10.1126/science.280.5364.737",
      "volume": "280",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072223070092400_BIB52",
      "doi-asserted-by": "crossref",
      "first-page": "4805",
      "DOI": "10.1091/mbc.e03-06-0395",
      "volume": "14",
      "year": "2003",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072223070092400_BIB53",
      "first-page": "179",
      "volume": "1",
      "year": "1981",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072223070092400_BIB54",
      "doi-asserted-by": "crossref",
      "first-page": "373",
      "DOI": "10.1083/jcb.200503061",
      "volume": "172",
      "year": "2006",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB55",
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      "first-page": "131",
      "DOI": "10.1016/S1047-8477(02)00507-5",
      "volume": "140",
      "year": "2002",
      "journal-title": "J. Struct. Biol."
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    {
      "key": "2023072223070092400_BIB56",
      "doi-asserted-by": "crossref",
      "first-page": "981",
      "DOI": "10.1083/jcb.200303131",
      "volume": "162",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB57",
      "doi-asserted-by": "crossref",
      "first-page": "617",
      "DOI": "10.1083/jcb.144.4.617",
      "volume": "144",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB58",
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      "first-page": "265",
      "DOI": "10.1146/annurev.cb.09.110193.001405",
      "volume": "9",
      "year": "1993",
      "journal-title": "Annu. Rev. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB59",
      "doi-asserted-by": "crossref",
      "first-page": "3467",
      "DOI": "10.1002/j.1460-2075.1991.tb04911.x",
      "volume": "10",
      "year": "1991",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072223070092400_BIB60",
      "year": "2002"
    },
    {
      "key": "2023072223070092400_BIB61",
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      "first-page": "995",
      "DOI": "10.1083/jcb.128.6.995",
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      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072223070092400_BIB62",
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      "first-page": "79",
      "DOI": "10.1017/S1355838200991544",
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      "journal-title": "RNA."
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      "key": "2023072223070092400_BIB63",
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      "first-page": "4407",
      "DOI": "10.1093/nar/24.22.4407",
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      "journal-title": "Nucleic Acids Res."
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    {
      "key": "2023072223070092400_BIB64",
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      "first-page": "5366",
      "DOI": "10.1073/pnas.92.12.5366",
      "volume": "92",
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      "journal-title": "Proc. Natl. Acad. Sci. USA."
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    {
      "key": "2023072223070092400_BIB65",
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      "first-page": "7820",
      "DOI": "10.1074/jbc.M005960200",
      "volume": "276",
      "year": "2001",
      "journal-title": "J. Biol. Chem."
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    {
      "key": "2023072223070092400_BIB66",
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      "first-page": "305",
      "DOI": "10.1111/j.1365-2443.2006.00936.x",
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      "first-page": "252",
      "DOI": "10.1016/0014-4827(88)90159-0",
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      "journal-title": "Exp. Cell Res."
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      "first-page": "543",
      "DOI": "10.1083/jcb.146.3.543",
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      "first-page": "1635",
      "DOI": "10.1083/jcb.131.6.1635",
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      "first-page": "401",
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