Ncl-1 is Required for the Regulation of Cell Size and Ribosomal RNA Synthesis in Caenorhabditis Elegans

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1998 Apr 29

PMID 9508766

Citations 35

Authors

D J FRANK

M B Roth

Affiliations

Soon will be listed here.

Abstract

Regulation of ribosome synthesis is an essential aspect of growth control. Thus far, little is known about the factors that control and coordinate these processes. We show here that the Caenorhabditis elegans gene ncl-1 encodes a zinc finger protein and may be a repressor of RNA polymerase I and III transcription and an inhibitor of cell growth. Loss of function mutations in ncl-1, previously shown to result in enlarged nucleoli, result in increased rates of rRNA and 5S RNA transcription and enlarged cells. Furthermore, ncl-1 adult worms are larger, have more protein, and have twice as much rRNA as wild-type worms. Localization studies show that the level of NCL-1 protein is independently regulated in different cells of the embryo. In wild-type embryos, cells with the largest nucleoli have the lowest level of NCL-1 protein. Based on these results we propose that ncl-1 is a repressor of ribosome synthesis and cell growth.

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References

Cluzeaud F, Perennec J, de Amoral E, Willemin M, HATT P . Myocardial cell nucleus in cardiac overloading in the rat. Eur Heart J. 1984; 5 Suppl F:271-80. DOI: 10.1093/eurheartj/5.suppl_f.271. View

Sadoshima J, Aoki H, Izumo S . Angiotensin II and serum differentially regulate expression of cyclins, activity of cyclin-dependent kinases, and phosphorylation of retinoblastoma gene product in neonatal cardiac myocytes. Circ Res. 1997; 80(2):228-41. DOI: 10.1161/01.res.80.2.228. View

Seydoux G, Fire A . Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans. Development. 1994; 120(10):2823-34. DOI: 10.1242/dev.120.10.2823. View

Derenzini M, Trere D . Importance of interphase nucleolar organizer regions in tumor pathology. Virchows Arch B Cell Pathol Incl Mol Pathol. 1991; 61(1):1-8. DOI: 10.1007/BF02890399. View

Kurata S, Koga K, Sakaguchi B . Nucleolar size in parallel with ribosomal RNA synthesis at diapause termination in the eggs of Bombyx mori. Chromosoma. 1978; 68(4):313-7. DOI: 10.1007/BF00327166. View

McDermott P, Rothblum L, Smith S, Morgan H . Accelerated rates of ribosomal RNA synthesis during growth of contracting heart cells in culture. J Biol Chem. 1989; 264(30):18220-7. View

Moss T, Stefanovsky V . Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Prog Nucleic Acid Res Mol Biol. 1995; 50:25-66. DOI: 10.1016/s0079-6603(08)60810-7. View

Ellis R, Sulston J, Coulson A . The rDNA of C. elegans: sequence and structure. Nucleic Acids Res. 1986; 14(5):2345-64. PMC: 339662. DOI: 10.1093/nar/14.5.2345. View

Schauer I, Wood W . Early C. elegans embryos are transcriptionally active. Development. 1990; 110(4):1303-17. DOI: 10.1242/dev.110.4.1303. View

10.

Liebhaber S, Wolf S, Schlessinger D . Differences in rRNA metabolism of primary and SV40-transformed human fibroblasts. Cell. 1978; 13(1):121-7. DOI: 10.1016/0092-8674(78)90143-5. View

11.

Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg H . The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J. 1992; 11(6):2211-8. PMC: 556688. DOI: 10.1002/j.1460-2075.1992.tb05280.x. View

12.

Sulston J, Du Z, Thomas K, Wilson R, Hillier L, Staden R . The C. elegans genome sequencing project: a beginning. Nature. 1992; 356(6364):37-41. DOI: 10.1038/356037a0. View

13.

Hedgecock E, Herman R . The ncl-1 gene and genetic mosaics of Caenorhabditis elegans. Genetics. 1995; 141(3):989-1006. PMC: 1206860. DOI: 10.1093/genetics/141.3.989. View

14.

Takano H, Komuro I, Zou Y, Kudoh S, Yamazaki T, Yazaki Y . Activation of p70 S6 protein kinase is necessary for angiotensin II-induced hypertrophy in neonatal rat cardiac myocytes. FEBS Lett. 1996; 379(3):255-9. DOI: 10.1016/0014-5793(95)01523-x. View

15.

Mu Z, Chin K, Liu J, Lozano G, Chang K . PML, a growth suppressor disrupted in acute promyelocytic leukemia. Mol Cell Biol. 1994; 14(10):6858-67. PMC: 359216. DOI: 10.1128/mcb.14.10.6858-6867.1994. View

16.

Borrow J, Goddard A, Sheer D, Solomon E . Molecular analysis of acute promyelocytic leukemia breakpoint cluster region on chromosome 17. Science. 1990; 249(4976):1577-80. DOI: 10.1126/science.2218500. View

17.

Kurabayashi M, Yazaki Y . Molecular biology of heart disease. Synopsis of the pathophysiological basis of cardiac hypertrophy, familial hypertrophic cardiomyopathy, long QT syndrome and Marfan syndrome. Intern Med. 1996; 35(4):243-8. DOI: 10.2169/internalmedicine.35.243. View

18.

Dalen H, Saetersdal T, Odegarden S . Some ultrastructural features of the myocardial cells in the hypertrophied human papillary muscle. Virchows Arch A Pathol Anat Histopathol. 1987; 410(4):281-94. DOI: 10.1007/BF00711285. View

19.

Guo S, Kemphues K . par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell. 1995; 81(4):611-20. DOI: 10.1016/0092-8674(95)90082-9. View

20.

Vallett S, Brudnak M, Pellegrini M, Weber H . In vivo regulation of rRNA transcription occurs rapidly in nondividing and dividing Drosophila cells in response to a phorbol ester and serum. Mol Cell Biol. 1993; 13(2):928-33. PMC: 358976. DOI: 10.1128/mcb.13.2.928-933.1993. View