Transcriptional regulation of N-acetylglutamate synthase

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Heibel, Sandra Kirsch ^a,b   Lopez, Giselle Yvette ^c   Panglao, Maria ^d   Sodha, Sonal ^e   Mariño Ramírez, Leonardo ^f   Tuchman, Mendel ^a   Caldovic, Ljubica ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUTAMATE ACETYLTRANSFERASE; HEPATOCYTE NUCLEAR FACTOR 1; NUCLEAR FACTOR Y; SMAD3 PROTEIN; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR SP1; AMINO ACID ACETYLTRANSFERASE; CARBAMOYL PHOSPHATE SYNTHASE; CCAAT BINDING FACTOR; CREB1 PROTEIN, HUMAN; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HNF1A PROTEIN, HUMAN; SMAD3 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENHANCER REGION; GENE; HUMAN; HUMAN CELL; LIVER; MOUSE; N ACETYLGLUTAMATE SYNTHASE GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN MOTIF; REAL TIME POLYMERASE CHAIN REACTION; SMALL INTESTINE; TATA BOX MOTIF; TRANSCRIPTION FACTOR BINDING MOTIF; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSLATION INITIATION; UREA CYCLE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE;

MAMMALIA;

AMINO-ACID N-ACETYLTRANSFERASE; ANIMALS; BASE SEQUENCE; CARBAMOYL-PHOSPHATE SYNTHASE (AMMONIA); CCAAT-BINDING FACTOR; CCAAT-ENHANCER-BINDING PROTEINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEPATOCYTE NUCLEAR FACTOR 1-ALPHA; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, NUCLEIC ACID; SMAD3 PROTEIN; SP1 TRANSCRIPTION FACTOR; SPECIES SPECIFICITY; TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION, GENETIC;

EID: 84857584751     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029527     Document Type: Article

References (94)

1. Caldovic L, Morizono H, Gracia Panglao M, Gallegos R, Yu X, et al. (2002) Cloning and expression of the human N-acetylglutamate synthase gene. Biochem Biophys Res Commun 299: 581-586.
2. Caldovic L, Morizono H, Yu X, Thompson M, Shi D, et al. (2002) Identification, cloning and expression of the mouse N-acetylglutamate synthase gene. Biochem J 364: 825-831.
3. Schimke RT, (1962) Differential effects of fasting and protein-free diets on levels of urea cycle enzymes in rat liver. J Biol Chem 237: 1921-1924.
4. Kawamoto S, Ishida H, Mori M, Tatibana M, (1982) Regulation of N-acetylglutamate synthetase in mouse liver. Postprandial changes in sensitivity to activation by arginine. Eur J Biochem 123: 637-641.
5. Tatibana M, Kawamoto S, Sonoda T, Mori M, (1982) Enzyme regulation of n-acetylglutamate synthesis in mouse and rat liver. Adv Exp Med Biol 153: 207-216.
6. Shigesada K, Tatibana M, (1978) N-Acetylglutamate synthetase from rat-liver mitochondria. Partial purification and catalytic properties. Eur J Biochem 84: 285-291.
7. Goping IS, Shore GC, (1994) Interactions between repressor and anti-repressor elements in the carbamyl phosphate synthetase I promoter. J Biol Chem 269: 3891-3896.
8. Howell BW, Lagace M, Shore GC, (1989) Activity of the carbamyl phosphate synthetase I promoter in liver nuclear extracts is dependent on a cis-acting C/EBP recognition element. Mol Cell Biol 9: 2928-2933.
9. Lagace M, Goping IS, Mueller CR, Lazzaro M, Shore GC, (1992) The carbamyl phosphate synthetase promoter contains multiple binding sites for C/EBP-related proteins. Gene 118: 231-238.
10. Schoneveld OJ, Gaemers IC, Hoogenkamp M, Lamers WH, (2005) The role of proximal-enhancer elements in the glucocorticoid regulation of carbamoylphosphate synthetase gene transcription from the upstream response unit. Biochimie 87: 1033-1040.
11. Kimura A, Nishiyori A, Murakami T, Tsukamoto T, Hata S, et al. (1993) Chicken ovalbumin upstream promoter-transcription factor (COUP-TF) represses transcription from the promoter of the gene for ornithine transcarbamylase in a manner antagonistic to hepatocyte nuclear factor-4 (HNF-4). J Biol Chem 268: 11125-11133.
12. Kimura T, Chowdhury S, Tanaka T, Shimizu A, Iwase K, et al. (2001) CCAAT/enhancer-binding protein beta is required for activation of genes for ornithine cycle enzymes by glucocorticoids and glucagon in primary-cultured hepatocytes. FEBS Lett 494: 105-111.
13. Murakami T, Nishiyori A, Takiguchi M, Mori M, (1990) Promoter and 11-kilobase upstream enhancer elements responsible for hepatoma cell-specific expression of the rat ornithine transcarbamylase gene. Mol Cell Biol 10: 1180-1191.
14. Nishiyori A, Tashiro H, Kimura A, Akagi K, Yamamura K, et al. (1994) Determination of tissue specificity of the enhancer by combinatorial operation of tissue-enriched transcription factors. Both HNF-4 and C/EBP beta are required for liver-specific activity of the ornithine transcarbamylase enhancer. J Biol Chem 269: 1323-1331.
15. Guei TR, Liu MC, Yang CP, Su TS, (2008) Identification of a liver-specific cAMP response element in the human argininosuccinate synthetase gene. Biochem Biophys Res Commun 377: 257-261.
16. Anderson GM, Freytag SO, (1991) Synergistic activation of a human promoter in vivo by transcription factor Sp1. Mol Cell Biol 11: 1935-1943.
17. Boyce FM 3rd, Pogulis RJ, Freytag SO, (1989) Paradoxical regulation of human argininosuccinate synthetase cDNA minigene in opposition to endogenous gene: evidence for intragenic control sequences. Somat Cell Mol Genet 15: 123-129.
18. Matsubasa T, Takiguchi M, Matsuda I, Mori M, (1994) Rat argininosuccinate lyase promoter: the dyad-symmetric CCAAT box sequence CCAATTGG in the promoter is recognized by NF-Y. J Biochem 116: 1044-1055.
19. Dorn A, Bollekens J, Staub A, Benoist C, Mathis D, (1987) A multiplicity of CCAAT box-binding proteins. Cell 50: 863-872.
20. Hooft van Huijsduijnen R, Li XY, Black D, Matthes H, Benoist C, et al. (1990) Co-evolution from yeast to mouse: cDNA cloning of the two NF-Y (CP-1/CBF) subunits. EMBO J 9: 3119-3127.
21. Santoro C, Mermod N, Andrews PC, Tjian R, (1988) A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature 334: 218-224.
22. Takiguchi M, Mori M, (1991) In vitro analysis of the rat liver-type arginase promoter. J Biol Chem 266: 9186-9193.
23. Morris SM Jr, (2002) Regulation of enzymes of the urea cycle and arginine metabolism. Annu Rev Nutr 22: 87-105.
24. Morris SM Jr, Moncman CL, Rand KD, Dizikes GJ, Cederbaum SD, et al. (1987) Regulation of mRNA levels for five urea cycle enzymes in rat liver by diet, cyclic AMP, and glucocorticoids. Arch Biochem Biophys 256: 343-353.
25. Takiguchi M, Mori M, (1995) Transcriptional regulation of genes for ornithine cycle enzymes. Biochem J 312 (Pt 3): 649-659.
26. Nebes VL, Morris SM Jr, (1988) Regulation of messenger ribonucleic acid levels for five urea cycle enzymes in cultured rat hepatocytes. Requirements for cyclic adenosine monophosphate, glucocorticoids, and ongoing protein synthesis. Mol Endocrinol 2: 444-451.
27. Ryall JC, Quantz MA, Shore GC, (1986) Rat liver and intestinal mucosa differ in the developmental pattern and hormonal regulation of carbamoyl-phosphate synthetase I and ornithine carbamoyl transferase gene expression. Eur J Biochem 156: 453-458.
28. Schimke RT, (1963) Studies on factors affecting the levels of urea cycle enzymes in rat liver. J Biol Chem 238: 1012-1018.
29. Hazra A, DuBois DC, Almon RR, Snyder GH, Jusko WJ, (2008) Pharmacodynamic modeling of acute and chronic effects of methylprednisolone on hepatic urea cycle genes in rats. Gene Regul Syst Bio 2: 1-19.
30. Abdullah Abu Musa DM, Kobayashi K, Yasuda I, Iijima M, Christoffels VM, et al. (1999) Involvement of a cis-acting element in the suppression of carbamoyl phosphate synthetase I gene expression in the liver of carnitine-deficient mice. Mol Genet Metab 68: 346-356.
31. Schoneveld OJ, Hoogenkamp M, Stallen JM, Gaemers IC, Lamers WH, (2007) cyclicAMP and glucocorticoid responsiveness of the rat carbamoylphosphate synthetase gene requires the interplay of upstream regulatory units. Biochimie 89: 574-580.
32. Murakami T, Takiguchi M, Inomoto T, Yamamura K, Mori M, (1989) Tissue- and developmental stage-specific expression of the rat ornithine carbamoyltransferase gene in transgenic mice. Dev Genet 10: 393-401.
33. Sladek FM, Zhong WM, Lai E, Darnell JE Jr, (1990) Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev 4: 2353-2365.
34. Boyce FM, Anderson GM, Rusk CD, Freytag SO, (1986) Human argininosuccinate synthetase minigenes are subject to arginine-mediated repression but not to trans induction. Mol Cell Biol 6: 1244-1252.
35. Boyce FM 3rd, Freytag SO, (1989) Regulation of human argininosuccinate synthetase gene: induction by positive-acting nuclear mechanism in canavanine-resistant cell variants. Somat Cell Mol Genet 15: 113-121.
36. Jackson MJ, Allen SJ, Beaudet AL, O'Brien WE, (1988) Metabolite regulation of argininosuccinate synthetase in cultured human cells. J Biol Chem 263: 16388-16394.
37. Sunyakumthorn P, Boonsaen T, Boonsaeng V, Wallace JC, Jitrapakdee S, (2005) Involvement of specific proteins (Sp1/Sp3) and nuclear factor Y in basal transcription of the distal promoter of the rat pyruvate carboxylase gene in beta-cells. Biochem Biophys Res Commun 329: 188-196.
38. Snodgrass PJ, (1991) Dexamethasone and glucagon cause synergistic increases of urea cycle enzyme activities in livers of normal but not adrenalectomized rats. Enzyme 45: 30-38.
39. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
40. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, et al. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32: 1372-1381.
41. Marino-Ramirez L, Spouge JL, Kanga GC, Landsman D, (2004) Statistical analysis of over-represented words in human promoter sequences. Nucleic Acids Res 32: 949-958.
42. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
43. Kim HJ, Ko MS, Kim HK, Cho WJ, Lee SH, et al. Transcription factor Sp1 regulates basal transcription of the human DRG2 gene. Biochim Biophys Acta 1809: 184-190.
44. Zhang W, Tian Z, Sha S, Cheng LY, Philipsen S, et al. Functional and sequence analysis of human neuroglobin gene promoter region. Biochim Biophys Acta 1809: 236-244.
45. Convertini P, Infantino V, Bisaccia F, Palmieri F, Iacobazzi V, Role of FOXA and Sp1 in mitochondrial acylcarnitine carrier gene expression in different cell lines. Biochem Biophys Res Commun 404: 376-381.
46. Michels AJ, Hagen TM, (2009) Hepatocyte nuclear factor 1 is essential for transcription of sodium-dependent vitamin C transporter protein 1. Am J Physiol Cell Physiol 297: C1220-1227.
47. Wang Z, Burke PA, Hepatocyte nuclear factor-4alpha interacts with other hepatocyte nuclear factors in regulating transthyretin gene expression. FEBS J 277: 4066-4075.
48. Tue NT, Yoshioka Y, Yamaguchi M, NF-Y transcriptionally regulates the Drosophila p53 gene. Gene 473: 1-7.
49. Pallai R, Simpkins H, Chen J, Parekh HK, The CCAAT box binding transcription factor, nuclear factor-Y (NF-Y) regulates transcription of human aldo-keto reductase 1C1 (AKR1C1) gene. Gene 459: 11-23.
50. Xiang H, Wang J, Boxer LM, (2006) Role of the cyclic AMP response element in the bcl-2 promoter in the regulation of endogenous Bcl-2 expression and apoptosis in murine B cells. Mol Cell Biol 26: 8599-8606.
51. Callens N, Baert JL, Monte D, Sunesen M, Van Lint C, et al. (2003) Transcriptional regulation of the murine brca2 gene by CREB/ATF transcription factors. Biochem Biophys Res Commun 312: 702-707.
52. Deng WG, Zhu Y, Montero A, Wu KK, (2003) Quantitative analysis of binding of transcription factor complex to biotinylated DNA probe by a streptavidin-agarose pulldown assay. Anal Biochem 323: 12-18.
53. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A, Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
54. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
55. Christoffels VM, van den Hoff MJ, Lamers MC, van Roon MA, de Boer PA, et al. (1996) The upstream regulatory region of the carbamoyl-phosphate synthetase I gene controls its tissue-specific, developmental, and hormonal regulation in vivo. J Biol Chem 271: 31243-31250.
56. Christoffels VM, Grange T, Kaestner KH, Cole TJ, Darlington GJ, et al. (1998) Glucocorticoid receptor, C/EBP, HNF3, and protein kinase A coordinately activate the glucocorticoid response unit of the carbamoylphosphate synthetase I gene. Mol Cell Biol 18: 6305-6315.
57. Christoffels VM, van den Hoff MJ, Moorman AF, Lamers WH, (1995) The far-upstream enhancer of the carbamoyl-phosphate synthetase I gene is responsible for the tissue specificity and hormone inducibility of its expression. J Biol Chem 270: 24932-24940.
58. Klein H, Vingron M, (2007) Using transcription factor binding site co-occurrence to predict regulatory regions. Genome Inform 18: 109-118.
59. Renga B, Mencarelli A, Cipriani S, D'Amore C, Zampella A, et al. The nuclear receptor FXR regulates hepatic transport and metabolism of glutamine and glutamate. Biochim Biophys Acta 1812: 1522-1531.
60. Emami KH, Burke TW, Smale ST, (1998) Sp1 activation of a TATA-less promoter requires a species-specific interaction involving transcription factor IID. Nucleic Acids Res 26: 839-846.
61. Muckenfuss H, Kaiser JK, Krebil E, Battenberg M, Schwer C, et al. (2007) Sp1 and Sp3 regulate basal transcription of the human APOBEC3G gene. Nucleic Acids Res 35: 3784-3796.
62. Schibler U, Sierra F, (1987) Alternative promoters in developmental gene expression. Annu Rev Genet 21: 237-257.
63. Hai T, Hartman MG, (2001) 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 273: 1-11.
64. De Cesare D, Sassone-Corsi P, (2000) Transcriptional regulation by cyclic AMP-responsive factors. Prog Nucleic Acid Res Mol Biol 64: 343-369.
65. Matuoka K, Yu Chen K, (1999) Nuclear factor Y (NF-Y) and cellular senescence. Exp Cell Res 253: 365-371.
66. Juang HH, Costello LC, Franklin RB, (1995) Androgen modulation of multiple transcription start sites of the mitochondrial aspartate aminotransferase gene in rat prostate. J Biol Chem 270: 12629-12634.
67. Pave-Preux M, Aggerbeck M, Veyssier C, Bousquet-Lemercier B, Hanoune J, et al. (1990) Hormonal discrimination among transcription start sites of aspartate aminotransferase. J Biol Chem 265: 4444-4448.
68. Kadonaga JT, Courey AJ, Ladika J, Tjian R, (1988) Distinct regions of Sp1 modulate DNA binding and transcriptional activation. Science 242: 1566-1570.
69. Li L, He S, Sun JM, Davie JR, (2004) Gene regulation by Sp1 and Sp3. Biochem Cell Biol 82: 460-471.
70. Solomon SS, Majumdar G, Martinez-Hernandez A, Raghow R, (2008) A critical role of Sp1 transcription factor in regulating gene expression in response to insulin and other hormones. Life Sci 83: 305-312.
71. Wierstra I, (2008) Sp1: emerging roles-beyond constitutive activation of TATA-less housekeeping genes. Biochem Biophys Res Commun 372: 1-13.
72. Montminy M, Koo SH, Zhang X, (2004) The CREB family: key regulators of hepatic metabolism. Ann Endocrinol (Paris) 65: 73-75.
73. Mayr B, Montminy M, (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2: 599-609.
74. Heibel SK, Ah Mew N, Caldovic L, Daikhin Y, Yudkoff M, et al. N-carbamylglutamate enhancement of ureagenesis leads to discovery of a novel deleterious mutation in a newly defined enhancer of the NAGS gene and to effective therapy. Hum Mutat 32: 1153-1160.
75. Kuo CJ, Conley PB, Chen L, Sladek FM, Darnell JE Jr, et al. (1992) A transcriptional hierarchy involved in mammalian cell-type specification. Nature 355: 457-461.
76. Sladek FM, (1993) Orphan receptor HNF-4 and liver-specific gene expression. Receptor 3: 223-232.
77. Ktistaki E, Talianidis I, (1997) Modulation of hepatic gene expression by hepatocyte nuclear factor 1. Science 277: 109-112.
78. Strausberg RL, Feingold EA, Grouse LH, Derge JG, Klausner RD, et al. (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A 99: 16899-16903.
79. Lomenick JP, Melguizo MS, Mitchell SL, Summar ML, Anderson JW, (2009) Effects of meals high in carbohydrate, protein, and fat on ghrelin and peptide YY secretion in prepubertal children. J Clin Endocrinol Metab 94: 4463-4471.
80. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
81. Mitchell S, Murdock D, Summar M, (2008) Plasma peptide tyrosine tyrosine (PYY) levels are increased in urea cycle disorder patients. Mol Gen Metab 93: 258 (abstract).
82. Neill MA, Aschner J, Barr F, Summar ML, (2009) Quantitative RT-PCR comparison of the urea and nitric oxide cycle gene transcripts in adult human tissues. Mol Genet Metab 97: 121-127.
83. Myrsen-Axcrona U, Ekblad E, Sundler F, (1997) Developmental expression of NPY, PYY and PP in the rat pancreas and their coexistence with islet hormones. Regul Pept 68: 165-175.
84. Ekblad E, Sundler F, (2002) Distribution of pancreatic polypeptide and peptide YY. Peptides 23: 251-261.
85. Lundberg JM, Tatemoto K, Terenius L, Hellstrom PM, Mutt V, et al. (1982) Localization of peptide YY (PYY) in gastrointestinal endocrine cells and effects on intestinal blood flow and motility. Proc Natl Acad Sci U S A 79: 4471-4475.
86. Lukinius AI, Ericsson JL, Lundqvist MK, Wilander EM, (1986) Ultrastructural localization of serotonin and polypeptide YY (PYY) in endocrine cells of the human rectum. J Histochem Cytochem 34: 719-726.
87. Geng M, Li T, Kong X, Song X, Chu W, et al. Reduced expression of intestinal N-acetylglutamate synthase in suckling piglets: a novel molecular mechanism for arginine as a nutritionally essential amino acid for neonates. Amino Acids 40: 1513-1522.
88. Uchiyama C, Mori M, Tatibana M, (1981) Subcellular localization and properties of N-acetylglutamate synthase in rat small intestinal mucosa. J Biochem 89: 1777-1786.
89. Dubois N, Cavard C, Chasse JF, Kamoun P, Briand P, (1988) Compared expression levels of ornithine transcarbamylase and carbamylphosphate synthetase in liver and small intestine of normal and mutant mice. Biochim Biophys Acta 950: 321-328.
90. Ishihara K, Oshimura M, Nakao M, (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23: 733-742.
91. Renda M, Baglivo I, Burgess-Beusse B, Esposito S, Fattorusso R, et al. (2007) Critical DNA binding interactions of the insulator protein CTCF: a small number of zinc fingers mediate strong binding, and a single finger-DNA interaction controls binding at imprinted loci. J Biol Chem 282: 33336-33345.
92. Majumder P, Gomez JA, Chadwick BP, Boss JM, (2008) The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions. J Exp Med 205: 785-798.
93. Heibel SK, Ah Mew N, Caldovic L, Daikhin Y, Yudkoff M, et al. (2011) N-carbamylglutamate enhancement of ureagenesis leads to discovery of a novel deleterious mutation in a newly defined enhancer of the NAGS gene and to effective therapy. Hum Mutat 32: 1153-1160.
94. Luksan O, Jirsa M, Eberova J, Minks J, Treslova H, et al. (2010) Disruption of OTC promoter-enhancer interaction in a patient with symptoms of ornithine carbamoyltransferase deficiency. Hum Mutat 31: E1294-1303.