DOI: 10.1261/rna.5420503. The Ref/Aly proteins are dispensable for mRNA export and development in <i>Caenorhabditis elegans</i>

The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans

10.1261/rna.5420503

Crossref journal-article

Cold Spring Harbor Laboratory

RNA (246)

Abstract

The mRNA export pathway is highly conserved throughout evolution. We have used RNA interference (RNAi) to functionally characterize bona fide RNA export factors and components of the exon–exon junction complex (EJC) in Caenorhabditis elegans. RNAi of CeNXT1/p15, the binding partner of CeNXF1/TAP, caused early embryonic lethality, demonstrating an essential function of this gene during C. elegans development. Moreover, depletion of this protein resulted in nuclear accumulation of poly(A)+ RNAs, supporting a direct role of NXT1/p15 in mRNA export in C. elegans. Previously, we have shown that RNAi of CeSRm160, a protein of the EJC complex, resulted in wild-type phenotype; in the present study, we demonstrate that RNAi of CeY14, another component of this complex, results in embryonic lethality. In contrast, depletion of the EJC component CeRNPS1 results in no discernible phenotype. Proteins of the REF/Aly family act as adaptor proteins mediating the recruitment of the mRNA export factor, NXF1/TAP, to mRNAs. The C. elegans genome encodes three members of the REF/Aly family. RNAi of individual Ref genes, or codepletion of two Ref genes in different combinations, resulted in wild-type phenotype. Simultaneous suppression of all three Ref genes did not compromise viability or progression through developmental stages in the affected progeny, and only caused a minor defect in larval mobility. Furthermore, no defects in mRNA export were observed upon simultaneous depletion of all three REF proteins. These results suggest the existence of multiple adaptor proteins that mediate mRNA export in C. elegans.

Bibliography

LONGMAN, D., JOHNSTONE, I. L., & CÃCERES, J. F. (2003). The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans. RNA, 9(7), 881â891.

Authors 3

DASA LONGMAN (first)
IAIN L. JOHNSTONE (additional)
JAVIER F. CÁCERES (additional)

References 80 Referenced 80

10.1017/S1355838200991994
10.1128/MCB.19.9.6306 / Mol. Cell. Biol. (1999)
10.1101/gad.12.7.996
10.1074/jbc.M100400200
10.1073/pnas.91.4.1256
10.1128/MCB.22.19.6871-6882.2002
10.1016/S0168-9525(98)01658-8
10.1073/pnas.97.1.4
10.1128/MCB.20.12.4181-4187.2000
10.1242/jcs.00268
10.1038/nrm760
10.1002/yea.320110104
10.1038/35888
10.1101/gad.11.14.1864
10.1016/S1097-2765(01)00348-3
10.1083/jcb.200207128
10.1016/S0960-9822(01)00532-2
10.1016/S1097-2765(00)80065-9
10.1128/MCB.21.7.2545-2554.2001
10.1016/S0960-9822(01)00508-5
10.1128/MCB.20.23.8996-9008.2000
{'key': '2021112105333697000_9.7.881.22', 'first-page': '1768', 'volume': '7', 'year': '2001', 'journal-title': 'RNA'} / RNA (2001)
10.1093/genetics/123.2.301 / Genetics (1989)
10.1016/S1097-2765(01)00233-7
10.1016/S1097-2765(03)00089-3
10.1074/jbc.275.12.8361
10.1078/0171-9335-00273
10.1016/S0960-9822(01)00529-2
10.1038/nature01278
10.1101/gad.13.9.1126
10.1093/emboj/18.9.2593
10.1016/S1097-2765(00)00065-4
10.1016/S0960-9822(02)00840-0
10.1126/science.1062829
10.1093/emboj/20.20.5769
10.1093/emboj/19.24.6860
10.1093/embo-reports/kve245
10.1093/emboj/20.17.4987
10.1101/gad.10.10.1233
10.1016/S1534-5807(02)00134-X
10.1006/dbio.1999.9593
10.1101/gad.852101
10.1093/emboj/19.7.1625
10.1016/S0960-9822(01)00589-9
10.1261/rna.5260303
10.1073/pnas.96.26.14937
10.1038/35098106
10.1126/science.1062786
MacMorris, M.A., Brocker, C., and Blumenthal, T. 2003. UAP56 levels affect viability and mRNA export in C. elegans. RNA (this issue). (10.1261/rna.5480803)
10.1093/emboj/18.16.4560
10.1083/jcb.150.2.309
10.1038/nrg908
10.1091/mbc.7.12.1921
10.1083/jcb.134.6.1365
10.1242/dev.124.16.3197 / Development (1997)
10.1261/rna.5250403
10.1083/jcb.129.4.925
10.1093/emboj/16.24.7500
{'key': '2021112105333697000_9.7.881.59', 'first-page': '527', 'volume': '3', 'year': '1997', 'journal-title': 'RNA'} / RNA (1997)
10.1017/S1355838202020046
10.1016/S0092-8674(02)00627-X
10.1073/pnas.031586198
10.1016/S0960-9822(06)00288-0
10.1128/MCB.18.11.6826 / Mol. Cell Biol. (1998)
10.1093/emboj/16.11.3256
10.1093/emboj/17.9.2663
10.1093/emboj/19.3.410
10.1038/35098113
10.1101/gad.12.21.3303
10.1017/S1355838200000078
10.1126/science.282.5388.430
10.1017/S1355838200000832
10.1038/27579
10.1093/emboj/17.9.2651
10.1073/pnas.95.12.6779
10.1128/MCB.22.1.245-256.2002
{'key': '2021112105333697000_9.7.881.77', 'first-page': '1781', 'volume': '7', 'year': '2001', 'journal-title': 'RNA'} / RNA (2001)
10.1016/S0014-5793(01)02482-6
10.1006/geno.1999.6064
10.1038/35030160

Dates

Type	When
Created	22 years, 2 months ago (June 16, 2003, 3:39 p.m.)
Deposited	3 years, 9 months ago (Nov. 21, 2021, 8:34 a.m.)
Indexed	1 year, 2 months ago (June 3, 2024, 3:19 a.m.)
Issued	22 years, 1 month ago (July 1, 2003)
Published	22 years, 1 month ago (July 1, 2003)
Published Online	22 years, 1 month ago (July 1, 2003)
Published Print	22 years, 1 month ago (July 1, 2003)

Funders 0

None

BibTeX

@article{LONGMAN_2003, title={The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans}, volume={9}, ISSN={1469-9001}, url={http://dx.doi.org/10.1261/rna.5420503}, DOI={10.1261/rna.5420503}, number={7}, journal={RNA}, publisher={Cold Spring Harbor Laboratory}, author={LONGMAN, DASA and JOHNSTONE, IAIN L. and CÁCERES, JAVIER F.}, year={2003}, month=jul, pages={881–891} }

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