Gestational low protein diet selectively induces the amino acid response pathway target genes in the liver of offspring rats through transcription factor binding and histone modifications

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1809, Issue 10, 2011, Pages 549-556

  Zhou, Dan ^a   Pan, Yuan Xiang ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Epigenetic modification; Maternal programming; Pregnancy; Protein restriction

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ACTIVATING TRANSCRIPTION FACTOR 3; ACTIVATING TRANSCRIPTION FACTOR 4; AMINO ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; RNA POLYMERASE II; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEMALE; GENE INTERACTION; GENE TARGETING; GESTATION PERIOD; HISTONE ACETYLATION; HISTONE MODIFICATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; RAT; REGULATORY MECHANISM; TRANSCRIPTION INITIATION;

AMINO ACIDS; ANIMALS; DIET, PROTEIN-RESTRICTED; FEMALE; GENE EXPRESSION REGULATION; HISTONES; HUMANS; LIVER; MATERNAL EXPOSURE; PREGNANCY; PREGNANCY, ANIMAL; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

RATTUS;

EID: 80053446399     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.07.003     Document Type: Article

References (37)

1. Desai M., Hales C.N. Role of fetal and infant growth in programming metabolism in later life. Biol Rev Camb Philos Soc 1997, 72:329-348.
2. Endo Y., Fu Z., Abe K., Arai S., Kato H. Dietary protein quantity and quality affect rat hepatic gene expression. J Nutr 2002, 132:3632-3637.
3. Roseboom T.J., van der Meulen J.H., Ravelli A.C., Osmond C., Barker D.J., Bleker O.P. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 2001, 185:93-98.
4. Lillycrop K.A., Phillips E.S., Torrens C., Hanson M.A., Jackson A.A., Burdge G.C. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 2008, 100:278-282.
5. Hao S., Sharp J.W., Ross-Inta C.M., McDaniel B.J., Anthony T.G., Wek R.C., Cavener D.R., McGrath B.C., Rudell J.B., Koehnle T.J., Gietzen D.W. Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 2005, 307:1776-1778.
6. Thiaville M.M., Dudenhausen E.E., Zhong C., Pan Y.X., Kilberg M.S. Deprivation of protein or amino acid induces C/EBPbeta synthesis and binding to amino acid response elements, but its action is not an absolute requirement for enhanced transcription. Biochem J 2008, 410:473-484.
7. de Haro C., Mendez R., Santoyo J. The eIF-2alpha kinases and the control of protein synthesis. FASEB J 1996, 10:1378-1387.
8. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K., Cavener D.R. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 2002, 22:3864-3874.
9. Kilberg M.S., Shan J., Su N. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metab 2009, 20:436-443.
10. Hashimoto Y., Zhang C., Kawauchi J., Imoto I., Adachi M.T., Inazawa J., Amagasa T., Hai T., Kitajima S. An alternatively spliced isoform of transcriptional repressor ATF3 and its induction by stress stimuli. Nucleic Acids Res 2002, 30:2398-2406.
11. Katz S., Aronheim A. Differential targeting of the stress mitogen-activated protein kinases to the c-Jun dimerization protein 2. Biochem J 2002, 368:939-945.
12. Liang G., Wolfgang C.D., Chen B.P., Chen T.H., Hai T. ATF3 gene. Genomic organization, promoter, and regulation. J Biol Chem 1996, 271:1695-1701.
13. Hai T., Hartman M.G. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 2001, 273:1-11.
14. Pan Y.X., Chen H., Thiaville M.M., Kilberg M.S. Activation of the ATF3 gene through a co-ordinated amino acid-sensing response programme that controls transcriptional regulation of responsive genes following amino acid limitation. Biochem J 2007, 401:299-307.
15. Jiang H.Y., Wek S.A., McGrath B.C., Lu D., Hai T., Harding H.P., Wang X., Ron D., Cavener D.R., Wek R.C. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol 2004, 24:1365-1377.
16. Andrulis I.L., Chen J., Ray P.N. Isolation of human cDNAs for asparagine synthetase and expression in Jensen rat sarcoma cells. Mol Cell Biol 1987, 7:2435-2443.
17. Jousse C., Bruhat A., Ferrara M., Fafournoux P. Evidence for multiple signaling pathways in the regulation of gene expression by amino acids in human cell lines. J Nutr 2000, 130:1555-1560.
18. Hill J.M., Roberts J., Loeb E., Khan A., MacLellan A., Hill R.W. L-asparaginase therapy for leukemia and other malignant neoplasms. Remission in human leukemia. JAMA 1967, 202:882-888.
19. Lorenzi P.L., Weinstein J.N. Asparagine synthetase: a new potential biomarker in ovarian cancer. Drug News Perspect 2009, 22:61-64.
20. Fafournoux P., Bruhat A., Jousse C. Amino acid regulation of gene expression. Biochem J 2000, 351:1-12.
21. Pan Y., Chen H., Siu F., Kilberg M.S. Amino acid deprivation and endoplasmic reticulum stress induce expression of multiple activating transcription factor-3 mRNA species that, when overexpressed in HepG2 cells, modulate transcription by the human asparagine synthetase promoter. J Biol Chem 2003, 278:38402-38412.
22. Chen H., Pan Y.X., Dudenhausen E.E., Kilberg M.S. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive basic region/leucine zipper transcription factors as well as localized histone acetylation. J Biol Chem 2004, 279:50829-50839.
23. Su N., Kilberg M.S. C/EBP homology protein (CHOP) interacts with activating transcription factor 4 (ATF4) and negatively regulates the stress-dependent induction of the asparagine synthetase gene. J Biol Chem 2008, 283:35106-35117.
24. Strakovsky R.S., Zhou D., Pan Y.X. A low-protein diet during gestation in rats activates the placental mammalian amino acid response pathway and programs the growth capacity of offspring. J Nutr 2010.
25. Sandoval J., Rodriguez J.L., Tur G., Serviddio G., Pereda J., Boukaba A., Sastre J., Torres L., Franco L., Lopez-Rodas G. RNAPol-ChIP: a novel application of chromatin immunoprecipitation to the analysis of real-time gene transcription. Nucleic Acids Res 2004, 32:e88.
26. Shan J., Ord D., Ord T., Kilberg M.S. Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAAT enhancer-binding protein-activating transcription factor response elements. J Biol Chem 2009, 284:21241-21248.
27. Thiaville M.M., Pan Y.X., Gjymishka A., Zhong C., Kaufman R.J., Kilberg M.S. MEK signaling is required for phosphorylation of eIF2alpha following amino acid limitation of HepG2 human hepatoma cells. J Biol Chem 2008, 283:10848-10857.
28. Gjymishka A., Palii S.S., Shan J., Kilberg M.S. Despite increased ATF4 binding at the C/EBP-ATF composite site following activation of the unfolded protein response, system A transporter 2 (SNAT2) transcription activity is repressed in HepG2 cells. J Biol Chem 2008, 283:27736-27747.
29. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87:953-959.
30. Bernstein B.E., Kamal M., Lindblad-Toh K., Bekiranov S., Bailey D.K., Huebert D.J., McMahon S., Karlsson E.K., Kulbokas E.J., Gingeras T.R., Schreiber S.L., Lander E.S. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005, 120:169-181.
31. Schubeler D., MacAlpine D.M., Scalzo D., Wirbelauer C., Kooperberg C., van Leeuwen F., Gottschling D.E., O'Neill L.P., Turner B.M., Delrow J., Bell S.P., Groudine M. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004, 18:1263-1271.
32. Lachner M., Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol 2002, 14:286-298.
33. Snowden A.W., Gregory P.D., Case C.C., Pabo C.O. Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo. Curr Biol 2002, 12:2159-2166.
34. Szyf M., Weaver I., Meaney M. Maternal care, the epigenome and phenotypic differences in behavior. Reprod Toxicol 2007, 24:9-19.
35. Kim J.Y., Lee S.H., Song E.H., Park Y.M., Lim J.Y., Kim D.J., Choi K.H., Park S.I., Gao B., Kim W.H. A critical role of STAT1 in streptozotocin-induced diabetic liver injury in mice: controlled by ATF3. Cell Signal 2009, 21:1758-1767.
36. Allen-Jennings A.E., Hartman M.G., Kociba G.J., Hai T. The roles of ATF3 in liver dysfunction and the regulation of phosphoenolpyruvate carboxykinase gene expression. J Biol Chem 2002, 277:20020-20025.
37. Szyf M. The early life environment and the epigenome. Biochim Biophys Acta 2009, 1790:878-885.