Posttranscriptional regulation of gene expression in liver regeneration: Role of mRNA stability

FASEB Journal

Volumn 10, Issue 5, 1996, Pages 559-573

  Kren, Betsy T ^a   Steer, Clifford J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

cell cycle; partial hepatectomy; posttranscriptional regulation

Indexed keywords

RNA BINDING PROTEIN;

ARTICLE; CELL DIVISION; GENE EXPRESSION REGULATION; LIVER CELL; LIVER REGENERATION; MESSENGER RNA SYNTHESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

EID: 0029985380     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.10.5.8621056     Document Type: Article

References (93)

1. Fausto, N., and Webber, E. M. (1994) Liver regeneration. In The Liver: Biology and Pathobiology (Arias, I. M., Boyer, J. L., Fausto, N., Jakoby, W. B., Schachter, D. A., and Shafritz, D. A., eds) pp. 1059-1084, Raven Press, New York
2. Haber, B. A., Mohn, K. L., Diamond, R. H., and Taub, R. (1993) Induction patterns of 70 genes during nine days after hepatectomy define the temporal course of liver regeneration. J. Clin. Invest. 91, 1319-1326
3. Ross, J. (1995) mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-150
4. Hargrove, J. L. (1993) Microcomputer-assisted kinetic modeling of mammalian gene expression. FASEB J. 7, 1163-1170
5. Harford, J. B. (1994) mRNA metabolism in higher eukaryotes. In The Liver: Biology and Pathobiology (Arias, I. M., Boyer, J. L., Fausto, N., Jakoby, W. B., Schachter, D. A., and Shafritz, D. A., eds) pp. 69-84, Raven Press, New York
6. Beelman, C. A., and Parker, R. (1995) Degradation of mRNA in eukaryotes. Cell 81, 179-183
7. Urlaub, G., Mitchell, P. J., Ciudad, C. J., and Chasin, L. A. (1989) Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol. Cell. Biol. 9, 2868-2880
8. Goumaz, M. O., Schwartz, H., Oppenheimer, J. H., and Mariash, C. N. (1994) Kinetic modeling of the response of precursor and mature rat hepatic mRNA-S14 to thyroid hormone. Am. J. Physiol. 266, E1001-E1011
9. Baki, L., and Alexis, M. N. (1994) The efficiency of nuclear processing of the tyrosine aminotransferase mRNA transcript increases after partial hepatectomy. Eur. J. Biochem. 225, 797-803
10. Proudfoot, N. J. (1994) Chasing your own poly(A) tail. Curr. Biol. 4, 359-361
11. Jarmolowski, A., Boelens, W. C., Izaurralde, E., and Mattaj, I. W. (1994) Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol. 124, 627-635
12. Morello, D., Lavenu, A., and Babinet, C. (1990) Differential regulation and expression of jun, c-fos and c-myc proto-oncogenes during mouse liver regeneration and after inhibition of protein synthesis. Oncogene 5, 1511-1519
13. Noguchi, S., Ohba, Y., and Oka, T. (1992) The role of transcription and messenger RNA stability in the regulation of epidermal growth factor receptor gene expression m regenerating mouse liver. Hepatology 15, 88-96
14. Albrecht, J. H., Hoffman, J. S., Kren, B. T., and Steer, C. J. (1993) Cyclin and cyclin-dependent kinase 1 mRNA expression in models of regenerating liver and human liver diseases. Am. J. Physiol. 265, G857-C864
15. Kren, B. T., Kumar, N. M., Wang, S.-q., Gilula, N. B., and Steer, C. J. (1993) Differential regulation of multiple gap junction transcripts and proteins during rat liver regeneration. J. Cell Biol. 123, 707-718
16. Albrecht, J. H., Muller-Eberhard, U., Kren, B. T., and Steer, C. J. (1994) Influence of transcriptional regulation and mRNA stability on hemopexin gene expression in regenerating liver. Arch. Biochem. Biophys. 314, 229-233
17. Trembley, J. H., Kren, B. T., and Steer, C. J. (1994) Posttranscriptional regulation of cyclin B messenger RNA expression in the regenerating rat liver. Cell Growth & Differ. 5, 99-108
18. Kren, B. T., Trembley, J. H., and Steer, C. J. (1996) Alterations in mRNA stability during rat liver regeneration. Am. J. Physiol. 270, G763-G777
19. Bernstein, P., and Ross, J. (1989) Poly(A), poly(A)-binding protein and the regulation of mRNA stability. Trends Biochem. Sci. 14, 373-377
20. Shyu, A.-B., Belasco, J. G., and Greenberg, M. E. (1991) Two distinct destabilizing elements in the c-fos messenger trigger deadenylation as a first step in rapid mRNA decay. Genes & Dev. 5, 221-234
21. Wilson, T., and Treisman, R. (1988) Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3′ AU-rich sequences. Nature (London) 336, 396-399
22. Chen, C.-Y. A., and Shyu, A.-B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470
23. Görlach, M., Burd, C. G., and Dreyfuss, G. (1994) The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211, 400-407
24. Sheiness, D., and Darnell, J. E. (1973) Polyadenylic acid segment in mRNA becomes shorter with age. Nature (London) 241, 265-268
25. Åström, J., Åström, A., and Virtanen, A. (1992) Properties of a HeLa cell 3′ exonuclease specific for degrading poly(A) tails of mammalian mRNA. J. Biol. Chem. 267, 18154-18159
26. Caruccio, N., and Ross, J. (1994) Purification of a human polyribosome-associated 3′ to 5′ exoribonuclease. J. Biol. Chem. 269, 31814-31821
27. Scheper, W., Meinsma, D., Holthuizen, P. E., and Sussenbach, J. S. (1995) Long-range RNA interaction of two sequence elements required for endonucleolytic cleavage of human insulin-like growth factor II mRNAs. Mol. Cell. Biol. 15, 235-245
28. Bernstein, P. L., Herrick, D. J., Prokipack, R. D., and Ross, J. (1992) Control of c-myc mRNA half-life in vitro by a protein capable of binding to a coding region stability determinant. Genes & Dev. 6, 642-654
29. Tharun, S., and Siideshmukh, R. (1995) Specific endonucleolytic cleavages of mouse albumin mRNA and their modulation during liver development. Nucleic Acids Res. 23, 641-646
30. Lim, S.-K., and Maquat, L. E. (1992) Human β-globin mRNAs that harbor a nonsense codon are degraded in murine erythroid tissues to intermediates lacking regions of exon I or exons I and II that have a cap-like structure at the 5′termmi. EMBO J. 11, 3271-3278
31. Belgrader, P., Cheng, J., Zhou, X., Stephenson, L. S., and Maquat, L. E. (1994) Mammalian nonsense codons can be cis effectors of nuclear mRNA half-life. Mol. Cell. Biol. 14, 8219-8228
32. Gallie, D. R., and Tanguay, R. (1994) Poly(A) binds to initiation factors and increases cap-dependent translation in vitro. J. Biol. Chem. 269, 17166-17173
33. Bonnieu, A., Piechaczyk, M., Marty, L., Cuny, M., Blanchard, J.-M., Fort, P., and Jeanteur, P. (1988) Sequence determinants of c-myc mRNA turn-over: influence of 3′ and 5′ non-coding regions. Oncogene Res. 3, 155-166
34. Moore, M. A., and Shenk, T. (1988) The adenovirus tripartite leader sequence can alter nuclear and cytoplasmic metabolism of a non-adenovirus mRNA within infected cells. Nucleic Acids Res. 16, 2247-2262
35. Babu, N., Raj, K., and Pitha, P. M. (1993) 65-kDa protein binds to destabilizing sequences in the IFN-β mRNA coding and 3′ UTR. FASEB J. 7, 702-710
36. Wellington, C. L., Greenberg, M. E., and Belasco, J. G. (1993) The destabilizing elements in the coding region of c-fos mRNA are recognized as RNA. Mol. Cell. Biol. 13, 5034-5042
37. Bachurski, C. J., Theodorakis, N. G., Coulson, R. M., and Cleveland, D. W. (1994) An amino-terminal tetrapeptide specifies cotranslational degradation of β-tubulin but not α-tubulin mRNAs. Mol. Cell. Biol. 14, 4076-4086
38. Nishizawa, K., and Okamoto, H. (1994) Mutation analysis of the role for the carboxy-terminus encoding region in NGF-induced stabilization of GAP-43 mRNA. Biochem. Biophys. Res. Commun. 205, 1380-1385
39. Ohh, M., and Takei, F. (1994) Interferon-γ- and phorbol myristate acetate-positive elements involved in intercellular adhesion molecule-1 mRNA stabilization. J. Biol. Chem. 269, 30117-30120
40. Harford, J. B., Rouault, T. A., and Klausner, R. D. (1994) The control of cellular iron homeostasis. In Iron Metabolism in Health and Disease (Brock, J. H., Halliday, J. W., Pippard, M. J., and Powell, L. W., eds) pp. 123-149, W. B. Saunders, Philadelphia
41. B, a second iron-responsive element-binding protein. J. Biol. Chem 269, 6405-6409
42. Sureau, A., and Perbal, B. (1994) Several mRNAs with variable 3′ untranslated regions and different stability encode the human PR264/SC35 splicing factor. Proc. Natl. Acad. Sci. USA 91, 932-936
43. Zubiaga, A. M., Belasco, J. G., and Greenberg, M. E. (1995) The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15, 2219-2230
44. Bohjanen, P. R., Petryniak, B., June, C. H., Thompson, C. B., and Lindsten, T. (1992) AU RNA-binding factors differ in their binding specificities and affinities. J. Biol. Chem. 267, 6302-6309
45. Gorospe, M., and Baglioni, C. (1994) Degradation of unstable interleukin-1α mRNA in a rabbit reticulocyte cell-free system. Localization of an instability determinant to a cluster of AUUUA motifs. J. Biol. Chem. 269, 11845-11851
46. Zhang, W., Wagner, B. J., Ehrenman, K., Schaefer, A. W., DeMaria, C. T., Crater, D., DeHaven, K., Long, L., and Biewer, G. (1993) Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13, 7652-7665
47. Luscher, B., Stauber, C., Schindler, R., and Schumperli, D. (1985) Faithful cell cycle regulation of a recombinant mouse histone H4 gene is controlled by sequences in the 3′-terminal part of the gene. Proc. Natl. Acad. Sci. USA 82, 4389-4393
48. Williams, A. S., Ingledue, T. C., Kay, B. K., and Marzluff, W. F. (1994) Changes in the stem-loop at the 3′ terminus of histone mRNA affects its nucleocytoplasmic transport and cytoplasmic regulation. Nucleic Acids Res 22, 4660-4666
49. Wahle, E. (1995) Poly(A) tail length control is caused by termination of processive synthesis. J. Biol. Chem. 270, 2800-2808
50. Brawerman, G. (1991) The role of poly(A) sequence in mammalian messenger RNA. CRC Crit. Rev. Biochem. 10, 1-38
51. Schiavi, S. C., Wellington, C. L., Shyu, A.-B., Chen, C.-Y. A., Greenberg, M. E., and Belasco, J. G. (1994) Multiple elements in the c-fos protein-coding region facilitate deadenylation and decay by a mechanism coupled to translation. J. Biol. Chem. 269, 3441-3448
52. Helper, J. E., Van Wyk, J. J., and Lund, P. K. (1990) Different half-lives of insulin-like growth factor I mRNAs that differ in length of 3′ untranslated sequence. Endocrinology 127, 1550-1552
53. Chew, L.-J., Murphy, D., and Carter, D. A. (1994) Alternatively polyadenylated vasoactive intestinal peptide mRNAs are differentially regulated at the level of stability. Mol. Endocrin. 8, 603-613
54. Nesic, D., Cheng, J., and Maquat, L E. (1993) Sequences within the last intron function in RNA 3′-end formation in cultured cells. Mol. Cell. Biol. 13, 3359-3369
55. Ross, J. (1994) Analysis of messenger RNA turnover in cell-free extracts from mammalian cells. In RNA Processing - A Practical Approach (Hames, B. D., and Higgins, S. J., eds) pp. 107-133, IRL Press, London
56. Ostareck-Lederer, A., Ostareck, D. H., Standart, N., and Thiele, B. J. (1994) Translation of 15-lipoxygenase mRNA is inhibited by a protein that binds to a repeated sequence in the 3′ untranslated region. EMBO J. 13, 1476-1481
57. Tanguay, R. L., and Gallie, D. R. (1996) Translational efficiency is regulated by the length of the 3′ untranslated region. Mol. Cell. Biol. 16, 146-156
58. Aloni, R., Peleg, D., and Meyuhas, O. (1992) Selective translational control and nonspecific posttranscriptional regulation of ribosomal protein gene expression during development and regeneration of rat liver. Mol. Cell. Biol. 12, 2203-2212
59. Knopp, J., Brtko, J., and Filipcík, P. (1992) Effect of triiodothyronine on rat liver polysome profiles and translational activity of mRNA after partial hepatectomy. Endocrine Regul. 26, 67-72
60. St Johnston, D. (1995) The intracellular localization of messenger RNAs. Cell 81, 161-170
61. Hovland, R., Campbell, G., Pryme, I., and Hesketh, J. (1995) The mRNAs for cyclin A, c-myc and ribosomal proteins L4 and S6 are associated with cytoskeletal-bound polysomes in HepG2 cells. Biochem. J. 310, 193-196
62. Mason, J. O., Williams, G. T., and Neuberg, M. S. (1988) The half-life of immunoglobin mRNA increases during B-cell differentiation: a possible role for targeting to membrane-bound polysomes. Genes & Dev. 2, 1003-1011
63. Zambetti, G., Stein, J., and Stein, G. (1990) Role of messenger RNA subcellular localization in the posttranscnptional regulation of human histone gene expression. J. Cell. Physiol. 144, 175-182
64. Lee, C. H., Bradley, G., and Ling, V. (1995) Overexpression of the class II P-glycoprotein gene in primary rat hepatocyte culture: evidence for increased mRNA stability. Cell Growth & Differ. 6, 347-354
65. Miller, A. C., Gafner, J., Clark, E. P., and Samid, D. (1993) Posttranscriptional down-regulation of ras oncogene expression by inhibitors of cellular glutathione. Mol. Cell. Biol. 13, 4416-4422
66. Hong, Y., and Malter, J. S. (1991) A redox switch and phosphorylation are involved in the posttranslational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore. J. Biol. Chem. 266, 3167-3171
67. Simonet, W. S., and Ness, G. C. (1989) Post-transcriptional regulation of 3-hydroxy-3-methylglutaryl-CoA reductase mRNA in rat liver. Glucocorticoids block the stabilization caused by thyroid hormones. J. Biol. Chem. 264, 569-573
68. Morello, D., Lavenu, A., Pournin, S., and Babinet, C. (1993) The 5′ and 3′ non-coding sequences of the c-myc gene, required in vitro for its post-transcriptional regulation, are dispensable in vivo. Oncogene 8, 1921-1929
69. Furth, P. A., St. Onge, L., Böger, H., Gruss, P., Gossen, M., Kistner, A., Bujard., II., and Hennighausen., L. (1994) Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. Proc. Natl. Acad. Sci. USA 91, 9302-9306
70. Milland, J., Tsykin, A., Thomas, T., Aldred, A. R., Cole, T., and Schreiber, G. (1990) Gene expression in regenerating and acute-phase rat liver. Am. J. Physiol. 259, G340-G347
71. Panduro, A., Lin-Lee, Y. C., Chan, L., and Shafritz, D. A. (1990) Transcriptional and posttranscriptional regulation of apolipoprotein E, A-I, and A-II gene expression in normal rat liver and during several pathophysiologic states. Biochemistry 29, 8430-8435
72. Agell, N., Pujol, M. J., Lopez-Girona, A., Bosch, M., Rosa, J. L., and Bachs, O. (1994) Calmodulin expression during rat liver regeneration. Hepatology 20, 1002-1008
73. Flodby, P., Antonson, P., Barlow, C., Blanck, A., Porsch-Hallstrom, I., and Xanthopoulos, K. G. (1993) Differential patterns of expression of three C/EBP isoforms, HNF-1, and HNF-4 after partial hepatectomy in rats. Exp. Cell Res. 208, 248-256
74. Lee, S. J., and Boyer, T. D. (1993) The effect of hepatic regeneration on the expression of the glutathione S-transferases. Biochem. J. 293, 137-142
75. Ferrero, M., Desiderio, M. A., Martinotti, A., Melani, C., Bernelli-Zazzera, A., Colombo, M. P., and Cairo, G. (1994) Expression of a growth arrest specific gene (gas-6) during liver regeneration: molecular mechanisms and signalling pathways. J. Cell. Physiol. 158, 263-269
76. Kren, B. T., Teel, A. L., and Steer, C. J. (1994) Transcriptional rate and steady-state changes of retinoblastoma mRNA in regenerating rat liver. Hepatology 19, 1214-1222
77. Rosa, J. L., Tauler, A., Lange, A. J., Pilkis, S. J., and Bartrons, R. (1992) Transcriptional and posttranscriptional regulation of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase during liver regeneration. Proc. Natl. Acad. Sci. USA 89, 3746-3750
78. Krumm, A., Hickey, L. B., and Groudine, M. (1995) Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes & Dev. 9, 559-572
79. Wuarin, J., and Schibler, U. (1994) Physical isolation of nascent RNA chains transcribed by RNA polymerase II: evidence for cotranscriptional splicing. Mol. Cell. Biol. 14, 7219-7225
80. Muegge, K., Vila, M., Gusella, G. L., Musso, T., Herrlich, P., Stein, B., and Durum, S. K. (1993) Interleukin 1 induction of the c-jun promoter. Proc. Natl. Acad. Sci. USA 91, 7054-7058
81. Johnson, T. R., Rudin, S. D., Blossey, B. K., Ilan, J., and Ilan, J. (1991) Newly synthesized RNA: Simultaneous measurement in intact cells of transcription rates and RNA stability of insulin-like growth factor I, actin, and albumin in growth-hormone-stimulated hepatocytes. Proc. Natl. Acad. Sci. USA 88, 5287-5291
82. Christ, B., Nath, A., Heinrich, P. C., and Jungermann, K. (1994) Inhibition by recombinant human interleukin-6 of the glucagon-dependent induction of phosphoenolpyruvate carboxykinase and of the insulin-dependent induction of glucokinase gene expression in cultured rat hepatocytes: regulation of gene transcription and messenger RNA degradation. Hepatology 20, 1577-1583
83. Levy, J. R., and Hug, V. (1992) Regulation of insulin receptor gene expression. Cell cycle-mediated effects on insulin receptor mRNA stability. J. Biol. Chem. 267, 25289-25295
84. Lavenu, A., Pistoi, S., Pournin, S., Babinet, C., and Morello, D. (1995) Both coding exons of the c-myc gene contribute to its posttranscriptional regulation in the quiescent liver and regenerating liver and after protein synthesis inhibition. Mol. Cell. Biol. 15, 4410-4419
85. Ray, R., Panda, C. K., Chakraborty, B. K., Mukherji, S., Chaudhury, K., and Roychoudhury, J. (1994) Changes in UsnRNA biosynthesis during rat liver regeneration. Mol. Cell. Biochem. 141, 71-77
86. Diamond, R. H., Du, K., Lee, V. M., Mohn, K. L., Haber, B. A., Tewari, D. S., and Taub, R. (1993) Novel delayed-early and highly insulin-induced growth response genes. J. Biol. Chem. 268, 15185-15192
87. Caputi, M-, Melo, C. A., and Baralle, F. E. (1995) Regulation of fibronectin expression in rat regenerating liver. Nucleic Acids Res. 23, 238-243
88. Tsui, L. V., Guidotti, L. G., Ishikawa, T., and Chisari, F. V. (1995) Posttranscriptional clearance of hepatitis B virus RNA by cytotoxic T lymphocyte-activated hepatocytes. Proc. Natl. Acad. Sci. USA 92, 12398-12402
89. Nambu, S., Inoue, K., and Sasaki, H. (1987) Site-specific hypomethylation of the c-myc oncogene in human hepatocellular carcinoma. J. Cancer Res. 78, 695-704
90. Jost, J.-P. (1993) Nuclear extracts of chicken embryos promote an active demethylation of DNA by excision repair of 5-methyldeoxycytidine. Proc. Natl. Acad. Sci. USA 91, 4684-4688
91. Ingelbrecht, I., Van Houdt, H., Van Montagu, M., and Depicker, A. (1994) Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. Proc. Natl. Acad. Sci. USA 91, 10502-10506
92. Wainfan, E., and Poirier, L. A. (1992) Methyl groups in carcinogenesis: effects on DNA methylation and gene expression. Cancer Res. (Suppl.) 52, 2071s-2077s
93. Malyankar, U. M., Rittling, S. R., Connor, A., and Denhardt, D. T. (1994) The mitogen-regulated protein/proliferin transcript is degraded in primary mouse embryo fibroblast but not 3T3 nuclei: Altered RNA processing correlates with immortalization. Proc. Natl. Acad. Sci. USA 91, 335-339