ATP-binding cassette protein E is involved in gene transcription and translation in Caenorhabditis elegans

https://doi.org/10.1016/j.bbrc.2004.08.068Get rights and content

Abstract

ATP-binding cassette protein E (ABCE) gene has been annotated as an RNase L inhibitor in eukaryotes. All eukaryotic species show the ubiquitous presence and high degree of conservation of ABCEs, however, RNase L is present only in mammals. This indicates that ABCEs may function not only as RNase L inhibitors, but also may have other functions that have yet to be determined. As an initial investigation into the novel functions of ABCE, we characterized the gene (Y39E4B.1) in Caenorhabditis elegans by a combination of data mining and functional assays. ABCE promoters drove GFP expressions in hypoderm, pharynx, vulvae, head, and tail neurons at all developmental stages. Three genes, rpl-4, nhr-91, and C07B5.3, were previously found to interact with ABCE. Our expression data showed overlapping expression patterns of ABCE and rpl-4 and nhr-91, but not C07B5.3. RNAi against ABCE resulted in embryonic lethality and slow growth. These data suggest that ABCE protein might be involved in the control of translation and transcription, work as shuttle protein between cytoplasm and nucleus, and possibly as a nucleocytoplasmic transporter. In addition, RNAi data suggest that ABCE and NHR-91 may function in vulvae development and molting pathways in C. elegans. Furthermore, our data suggest that ABCE, along with its interacting components, functions in a well-conserved pathway.

Section snippets

Materials and methods

Strains. All strains were maintained and cultured using standard techniques. N2 (Bristol); KR3532, dpy-5(e907); GR1373 eri-1(mg366) IV; BC10798, dpy-5(e907), sEX10798[dpy-5(+) + rCesY39E4B.1-GFP + pCes361]; BC06518, dpy-5(e907), sEX1050[dpy-5(+) + rCes rpl-4::GFP + pCeh361]; BC06519, dpy-5(e907), sEX1051[dpy-5(+) + rCesC07B5.3-GFP + pCes361]; BC06495, dpy-5(e907), sEX1029[dpy-5(+) + rCes-nhr-91-RFP + pCes361]; BC12778, dpy-5(e907), sEX12778[dpy-5(+) + rCesC26C6.5-GFP + pCes361]; BC11724, dpy-5(e907),

ABCEs are well conserved across all eukaryotic species

The protein sequences of eukaryotic ABCE are well conserved. There is over 65% identity between human and worm ABCE protein sequences. They also have comparable numbers of amino acids in each protein, ranging from 594 to 610 (Table 1). Surprisingly, the ABCE subfamily has only one member in most species except for A. thaliana, which has two members (Table 1). This indicates there have been few gene duplications or that, in general, no functional redundancy, or separable noval function ABCE

Discussion

ATP-binding cassette protein E protein has been annotated as RNase L inhibitor in all sequenced eukaryotes because it has been demonstrated in vitro that this protein reversibly associates and inhibits RNase L [7]. This is probably not biologically significant for non-mammalian species because only mammals have RNase L. All eukaryotic species show a high degree of conservation of ABCEs. This indicates that ABCEs have functions other than as RNase L inhibitors.

As an initial step in investigating

Acknowledgments

We thank Dr. Ann Rose and Colin Thacker for dpy-5 rescuing plasmid and mutant worms, Dr. Andy Fire for GFP vector, SAGE data, Dr. J.A. Ahringer for RNAi bacteria, and the Caenorhabditis Genetics Center for eri-1(mg366) strain. This work depended crucially upon free access to the Caenorhabditis elegans sequence data in GenBank and WormBase. We express our gratitude to Martin Jones for help during RNAi and Christine Beauchamp for critical proofreading of the manuscripts. This project was funded

References (31)

  • A. Decottignies et al.

    Complete inventory of the yeast ABC proteins

    Nat. Genet.

    (1997)
  • J.A. Sheps et al.

    The ABC transporter gene family of C. elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes

    Genome Biol.

    (2004)
  • B.A. Hassel et al.

    A dominant negative mutant of 2–5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon

    EMBO J.

    (1993)
  • G. Floyd-Smith et al.

    Interferon action: RNA cleavage pattern of a (2′–5′) oligoadenylate-dependent endonuclease

    Science

    (1981)
  • I.M. Kerr et al.

    pppA2′p5′A2′p5′A: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells

    Proc. Natl. Acad. Sci. USA.

    (1978)

    • Cited by (0)

    View full text
    Copyright © 2004 Elsevier Inc. All rights reserved.