Profiling of the fetal and adult rat liver transcriptome and translatome reveals discordant regulation by the mechanistic target of rapamycin (mTOR)

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 309, Issue 1, 2015, Pages R22-R35

  Boylan, Joan M ^a   Sanders, Jennifer A ^a,b   Neretti, Nicola ^b   Gruppuso, Philip A ^a,b  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Fetus; Liver; Protein synthesis; Rapamycin; Regeneration; Translation initiation

Indexed keywords

DIMETHYL SULFOXIDE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PROTEIN; RAPAMYCIN; RIBOSOME PROTEIN; TRANSCRIPTOME; TRANSLATOME; UNCLASSIFIED DRUG; MTOR PROTEIN, RAT; TARGET OF RAPAMYCIN KINASE;

ACUTE PHASE RESPONSE; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; FETUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; IN VIVO STUDY; LIVER; LIVER CELL; LIVER REGENERATION; LIVER RESECTION; LYSOSOME; MOLECULAR BIOLOGY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; RNA PROCESSING; SIGNAL TRANSDUCTION; STEROID METABOLISM; TRANSLATION INITIATION; AGE; ANIMAL; ANTAGONISTS AND INHIBITORS; CLUSTER ANALYSIS; COMPARATIVE STUDY; DIET RESTRICTION; DNA MICROARRAY; DRUG EFFECTS; DRUG RESISTANCE; EATING; GENE EXPRESSION REGULATION; GENETICS; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROCEDURES; RNA TRANSLATION; SPRAGUE DAWLEY RAT; SURGERY;

AGE FACTORS; ANIMALS; CELL PROLIFERATION; CLUSTER ANALYSIS; DRUG RESISTANCE; EATING; FASTING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HEPATECTOMY; LIVER; LIVER REGENERATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSCRIPTOME;

EID: 84935492298     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00114.2015     Document Type: Article

References (42)

1. Abraham RT. Making sense of amino acid sensing. Science 347: 128–129, 2014.
2. Anand P, Boylan JM, Ou Y, Gruppuso PA. Insulin signaling during perinatal liver development in the rat. Am J Physiol Endocrinol Metab 283: E844–E852, 2002.
3. Anand P, Gruppuso PA. Rapamycin inhibits liver growth during refeed-ing in rats via control of ribosomal protein translation but not cap-dependent translation initiation. J Nutr 136: 27–33, 2006.
4. Awad MM, Gruppuso PA. Cell cycle control during liver development in the rat: evidence indicating a role for cyclin D1 posttranscriptional regulation. Cell Growth Differ 11: 325–334, 2000.
5. Boylan JM, Anand P, Gruppuso PA. Ribosomal protein S6 phosphor-ylation and function during late gestation liver development in the rat. J Biol Chem 276: 44457–44463, 2001.
6. Braun L, Gruppuso P, Mikumo R, Fausto N. Transforming growth factor beta 1 in liver carcinogenesis: messenger RNA expression and growth effects. Cell Growth Differ 1: 103–111, 1990.
7. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 105: 17414–17419, 2008.
8. Cornu M, Albert V, Hall MN. mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 23: 53–62, 2013.
9. Dever TE. Gene-specific regulation by general translation factors. Cell 108: 545–556, 2002.
10. Efeyan A, Sabatini DM. mTOR and cancer: many loops in one pathway. Curr Opin Cell Biol 22: 169–176, 2010.
11. Gruppuso PA, Awad M, Bienieki TC, Boylan JM, Fernando S, Faris RA. Modulation of mitogen-independent hepatocyte proliferation during the perinatal period in the rat. In Vitro Cell Dev Biol Anim 33: 562–568, 1997.
12. Gruppuso PA, Boylan JM, Anand P, Bienieki TC. Effects of maternal starvation on hepatocyte proliferation in the late gestation fetal rat. Pediatr Res 57: 185–191, 2005.
13. Gruppuso PA, Boylan JM, Sanders JA. The physiology and pathophys-iology of rapamycin resistance: Implications for cancer. Cell Cycle 10: 1050–1058, 2011.
14. Gruppuso PA, Tsai SW, Boylan JM, Sanders JA. Hepatic translation control in the late-gestation fetal rat. Am J Physiol Regul Integr Comp Physiol 295: R558–R567, 2008.
15. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 12: 9–22, 2007.
16. Hershey JW. Translational control in mammalian cells. Annu Rev Biochem 60: 717–755, 1991.
17. Huang S, Bjornsti MA, Houghton PJ. Rapamycins: mechanism of action and cellular resistance. Cancer Biol Ther 2: 222–232, 2003.
18. Jefferies HB, Reinhard C, Kozma SC, Thomas G. Rapamycin selectively represses translation of the “polypyrimidine tract” mRNA family. Proc Natl Acad Sci USA 91: 4441–4445, 1994.
19. Jimenez RH, Lee JS, Francesconi M, Castellani G, Neretti N, Sanders JA, Sedivy J, Gruppuso PA. Regulation of gene expression in hepatic cells by the mammalian Target of Rapamycin (mTOR). PLoS One 5: e9084, 2010.
20. Kurmasheva RT, Huang S, Houghton PJ. Predicted mechanisms of resistance to mTOR inhibitors. Br J Cancer 95: 955–960, 2006.
21. Lamming DW, Demirkan G, Boylan JM, Mihaylova MM, Peng T, Ferreira J, Neretti N, Salomon A, Sabatini DM, Gruppuso PA. Hepatic signaling by the mechanistic target of rapamycin complex 2 (mTORC2). FASEB J 28: 300–315, 2013.
22. Laplante M, Sabatini DM. mTOR signaling. Cold Spring Harb Perspect Biol 4: a011593, 2012.
23. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 149: 274–293, 2012.
24. Laplante M, Sabatini DM. Regulation of mTORC1 and its impact on gene expression at a glance. J Cell Sci: 1713–1719, 2013.
25. Liu B, Qian SB. Translational regulation in nutrigenomics. Adv Nutr 2: 511–519, 2011.
26. Livingstone M, Bidinosti M. Rapamycin-insensitive mTORC1 activity controls eIF4E:4E-BP1 binding. F1000Res 1: 4, 2012.
27. Pestova TV, Kolupaeva VG, Lomakin IB, Pilipenko EV, Shatsky IN, Agol VI, Hellen CU. Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci USA 98: 7029–7036, 2001.
28. Prevot D, Darlix JL, Ohlmann T. Conducting the initiation of protein synthesis: the role of eIF4G. Biol Cell 95: 141–156, 2003.
29. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet 38: 500–501, 2006.
30. Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433: 477–480, 2005.
31. Sanders JA, Gruppuso PA. Hepatic, pancreatic and biliary cancers. In: Translation and Its Regulation in Cancer Biology and Medicine, edited by Parsyan A. London, UK: Springer, 2014.
32. Sanders JA, Lakhani A, Phornphutkul C, Wu KY, Gruppuso PA. The effect of rapamycin on DNA synthesis in multiple tissues from late gestation fetal and postnatal rats. Am J Physiol Cell Physiol 295: C406–C413, 2008.
33. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40: 310–322, 2010.
34. Shatsky IN, Dmitriev SE, Andreev DE, Terenin IM. Transcriptome-wide studies uncover the diversity of modes of mRNA recruitment to eukaryotic ribosomes. Crit Rev Biochem Mol Biol 49: 164–177, 2014.
35. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731–745, 2009.
36. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440–9445, 2003.
37. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP. GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics 23: 3251–3253, 2007.
38. Tcherkezian J, Cargnello M, Romeo Y, Huttlin EL, Lavoie G, Gygi SP, Roux PP. Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5=TOP mRNA translation. Genes Dev 28: 357–371, 2014.
39. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Saba-tini DM. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485: 109–113, 2012.
40. Villa N, Fraser CS. Diverse mechanisms of translation regulation and their role in cancer. In: Translation and Its Regulation in Cancer Biology and Medicine, edited by Parsyan A. London, UK: Springer, 2014, p. 39–72.
41. Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13: 227–232, 2012.
42. Williams-Hill DM, Duncan RF, Nielsen PJ, Tahara SM. Differential expression of the murine eukaryotic translation initiation factor isogenes eIF4A(I) and eIF4A(II) is dependent upon cellular growth status. Arch Biochem Biophys 338: 111–120, 1997.