Inactivation of the 3-phosphoglycerate dehydrogenase gene in mice: Changes in gene expression and associated regulatory networks resulting from serine deficiency

Functional and Integrative Genomics

Volumn 8, Issue 3, 2008, Pages 235-249

  Furuya, Shigeki ^a,b   Yoshida, Kazuyuki ^b,c   Kawakami, Yuriko ^a   Yang, Jyung Hoon ^a   Sayano, Tomoko ^a   Azuma, Norihiro ^c   Tanaka, Hideyuki ^c   Kuhara, Satoru ^a   Hirabayashi, Yoshio ^b,d  

^a KYUSHU UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c UTSUNOMIYA UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Brain development; CREB; Knockout mouse; Metabolic disorder

Indexed keywords

GLYCINE; PHOSPHOGLYCERATE DEHYDROGENASE; SERINE;

AMINO ACID ANALYSIS; AMINO ACID BLOOD LEVEL; AMINO ACID DEFICIENCY; AMINO ACID METABOLISM; AMINOACYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CHONDROGENESIS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION; GENE IDENTIFICATION; GENE INACTIVATION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA TRANSLATION; RNA TRANSPORT; SERINE DEFICIENCY; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE; UPREGULATION; WILD TYPE;

ANIMALS; COMPUTATIONAL BIOLOGY; CROSSES, GENETIC; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HOMOZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOGLYCERATE DEHYDROGENASE; PROTEINS; REPRODUCIBILITY OF RESULTS; SERINE;

ANIMALIA; MUS;

EID: 45449091548     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-007-0072-5     Document Type: Article

References (57)

1. Adhikary S, Eilers M (2005) Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 6:635-645
2. Anthony TG, McDaniel BJ, Byerley RL, McGrath BC, Cavener DR, McNurlan MA, Wek RC (2004) Preservation of liver protein synthesis during dietary leucine deprivation occurs at the expense of skeletal muscle mass in mice deleted for eIF2 kinase GCN2. J Biol Chem 279:36553-36561
3. Averous J, Bruhat A, Jousse C, Carraro V, Thiel G, Fafournoux P (2004) Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279:5288-5297
4. Bianco P, Fisher LW, Young MF, Termine JD, Robey PG (1991) Expression of bone sialoprotein (BSP) in developing human tissues. Calcif Tissue Int 49:421-426
5. Chen Z, Karaplis AC, Ackerman SL, Pogribny IP, Melnyk S, Lussier-Cacan S, Chen MF, Pai A, John SW, Smith RS, Bottiglieri T, Bagley P, Selhub J, Rudnicki MA, James SJ, Rozen R (2001) Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum Mol Genet 10:433-443
6. Cho HM, Jun DY, Bae MA, Ahn JD, Kim YH (2000) Nucleotide sequence and differential expression of the human 3-phosphoglycerate dehydrogenase gene. Gene 245:193-201
7. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F (2006) The c-Myc target gene network. Semin Cancer Biol 16:253-264
8. de Koning TJ (2006) Treatment with amino acids in serine deficiency disorders. J Inherit Metab Dis 29:347-351
9. de Koning TJ, Duran M, Van Maldergem L, Pineda M, Dorland L, Gooskens R, Jaeken J, Poll-The BT (2002) Congenital microcephaly and seizures due to 3-phosphoglycerate dehydrogenase deficiency: Outcome of treatment with amino acids. J Inherit Metab Dis 25:119-125
10. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 4:P3
11. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247-251
12. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, Cocito A, Amati B (2003) Genomic targets of the human c-Myc protein. Genes Dev 17:1115-1129
13. Fu TF, Rife JP, Schirch V (2001) The role of serine hydroxymethyltransferase isozymes in one-carbon metabolism in MCF-7 cells as determined by (13)C NMR. Arch Biochem Biophys 393:42-50
14. Furst DO, Osborn M, Weber K (1989) Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol 109:517-527
15. Furuya S (2008) An essential role for de novo biosynthesis of L-serine in CNS development. Asia Pac J Clin Nutr 17 (S1) (in press)
16. Furuya S, Watanabe M (2003) Novel neuroglial and glioglial relationships mediated by L-serine metabolism. Arch Histol Cytol 66:109-121
17. Furuya S, Tabata T, Mitoma J, Yamada K, Yamasaki M, Makino A, Yamamoto T, Watanabe M, Kano M, Hirabayashi Y (2000) L-Serine and glycine serve as major astroglia-derived trophic factors for cerebellar Purkinje neurons. Proc Natl Acad Sci U S A 97:11528-11533
18. Hao S, Sharp JW, Ross-Inta CM, McDaniel BJ, Anthony TG, Wek RC, Cavener DR, McGrath BC, Rudell JB, Koehnle TJ, Gietzen DW (2005) Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 307:1776-1778
19. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108
20. Hart CE, Race V, Achouri Y, Wiame E, Sharrard M, Olpin SE, Watkinson J, Bonham JR, Jaeken J, Matthijs G, Van Schaftingen E (2007) Phosphoserine aminotransferase deficiency: A novel disorder of the serine biosynthesis pathway. Am J Hum Genet 80:931-937
21. Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59:407-450
22. Hosack DA, Dennis G Jr., Sherman BT, Lane HC, Lempicki RA (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4:R70
23. Ichihara A, Greenberg DM (1955) Pathway of serine formation from carbohydrate in rat liver. Proc Natl Acad Sci U S A 41:605-609
24. Jaeken J, Detheux M, Van Maldergem L, Foulon M, Carchon H, Van Schaftingen E (1996) 3-Phosphoglycerate dehydrogenase deficiency: An inborn error of serine biosynthesis. Arch Dis Child 74:542-545
25. Jaeken J, Detheux M, Fryns JP, Collet JF, Alliet P, Van Schaftingen E (1997) Phosphoserine phosphatase deficiency in a patient with Williams syndrome. J Med Genet 34:594-596
26. Johannessen M, Delghandi MP, Moens U (2004) What turns CREB on? Cell Signal 16:1211-1227
27. Johnston JG, van der Kooy D (1989) Protooncogene expression identifies a transient columnar organization of the forebrain within the late embryonic ventricular zone. Proc Natl Acad Sci U S A 86:1066-1070
28. Jousse C, Oyadomari S, Novoa I, Lu P, Zhang Y, Harding HP, Ron D (2003) Inhibition of a constitutive translation initiation factor 2alpha phosphatase, CReP, promotes survival of stressed cells. J Cell Biol 163:767-775
29. Klomp LW, de Koning TJ, Malingre HE, van Beurden EA, Brink M, Opdam FL, Duran M, Jaeken J, Pineda M, Van Maldergem L, Poll-The BT, van den Berg IE, Berger R (2000) Molecular characterization of 3-phosphoglycerate dehydrogenase deficiency-a neurometabolic disorder associated with reduced L-serine biosynthesis. Am J Hum Genet 67:1389-1399
30. Li Z, Van Calcar S, Qu C, Cavenee WK, Zhang MQ, Ren B (2003) A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci U S A 100:8164-8169
31. Luscher B, Eisenman RN (1988) c-myc and c-myb protein degradation: effect of metabolic inhibitors and heat shock. Mol Cell Biol 8:2504-2512
32. Lyons GE, Ontell M, Cox R, Sassoon D, Buckingham M (1990) The expression of myosin genes in developing skeletal muscle in the mouse embryo. J Cell Biol 111:1465-1476
33. Maurin AC, Jousse C, Averous J, Parry L, Bruhat A, Cherasse Y, Zeng H, Zhang Y, Harding HP, Ron D, Fafournoux P (2005) The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores. Cell Metab 1:273-277
34. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599-609
35. Menssen A, Hermeking H (2002) Characterization of the c-MYC-regulated transcriptome by SAGE: Identification and analysis of c-MYC target genes. Proc Natl Acad Sci U S A 99:6274-6279
36. Mitoma J, Furuya S, Hirabayashi Y (1998a) A novel metabolic communication between neurons and astrocytes: Non-essential amino acid l -serine released from astrocytes is essential for developing hippocampal neurons. Neurosci Res 30:195-199
37. Mitoma J, Kasama T, Furuya S, Hirabayashi Y (1998b) Occurrence of an unusual phospholipid, phosphatidyl- l -threonine, in cultured hippocampal neurons. Exogenous L-serine is required for the synthesis of neuronal phosphatidyl-l-serine and sphingolipids. J Biol Chem 273:19363-19366
38. Moberg KH, Logan TJ, Tyndall WA, Hall DJ (1992) Three distinct elements within the murine c-myc promoter are required for transcription. Oncogene 7:411-421
39. Nakano I, Dougherty JD, Kim K, Klement I, Geschwind DH, Kornblum HI (2007) Phosphoserine phosphatase is expressed in the neural stem cell niche and regulates neural stem and progenitor cell proliferation. Stem Cells 25:1975-1984
40. Nikiforov MA, Chandriani S, O'Connell B, Petrenko O, Kotenko I, Beavis A, Sedivy JM, Cole MD (2002) A functional screen for Myc-responsive genes reveals serine hydroxymethyltransferase, a major source of the one-carbon unit for cell metabolism. Mol Cell Biol 22:5793-5800
41. Pind S, Slominski E, Mauthe J, Pearlman K, Swoboda KJ, Wilkins JA, Sauder P, Natowicz MR (2002) V490M, a common mutation in 3-phosphoglycerate dehydrogenase deficiency, causes enzyme deficiency by decreasing the yield of mature enzyme. J Biol Chem 277:7136-7143
42. Pohjanpelto P, Holtta E (1990) Deprivation of a single amino acid induces protein synthesis-dependent increases in c-jun, c-myc, and ornithine decarboxylase mRNAs in Chinese hamster ovary cells. Mol Cell Biol 10:5814-5821
43. Remondini D, O'Connell B, Intrator N, Sedivy JM, Neretti N, Castellani GC, Cooper LN (2005) Targeting c-Myc-activated genes with a correlation method: Detection of global changes in large gene expression network dynamics. Proc Natl Acad Sci U S A 102:6902-6906
44. Saxe JP, Wu H, Kelly TK, Phelps ME, Sun YE, Kornblum HI, Huang J (2007) A phenotypic small-molecule screen identifies an orphan ligand-receptor pair that regulates neural stem cell differentiation. Chem Biol 14:1019-1030
45. Shimizu-Albergine M, Ippolito DL, Beavo JA (2001) Downregulation of fasting-induced cAMP response element-mediated gene induction by leptin in neuropeptide Y neurons of the arcuate nucleus. J Neurosci 21:1238-1246
46. Siu F, Bain PJ, LeBlanc-Chaffin R, Chen H, Kilberg MS (2002) ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem 277:24120-24127
47. Snell K (1984) Enzymes of serine metabolism in normal, developing and neoplastic rat tissues. Adv Enzyme Regul 22:325-400
48. Suo S, Kimura Y, Van Tol HH (2006) Starvation induces cAMP response element-binding protein-dependent gene expression through octopamine-Gq signaling in Caenorhabditis elegans. J Neurosci 26:10082-10090
49. Takasaki C, Miura E, Watanabe M (2007) Segmental and complementary expression of l-serine biosynthetic enzyme 3-phosphoglycerate dehydrogenase and neutral amino acid transporter ASCT1 in the mouse kidney. Biomed Res 28:61-69
50. Wek RC, Jiang HY, Anthony TG (2006) Coping with stress: EIF2 kinases and translational control. Biochem Soc Trans 34:7-11
51. Wisdom R, Lee W (1991) The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev 5:232-243
52. Wu SX, Goebbels S, Nakamura K, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N (2005) Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci U S A 102:17172-17177
53. Yamasaki M, Yamada K, Furuya S, Mitoma J, Hirabayashi Y, Watanabe M (2001) 3-Phosphoglycerate dehydrogenase, a key enzyme for l-serine biosynthesis, is preferentially expressed in the radial glia/astrocyte lineage and olfactory ensheathing glia in the mouse brain. J Neurosci 21:7691-7704
54. Yoshida K, Furuya S, Osuka S, Mitoma J, Shinoda Y, Watanabe M, Azuma N, Tanaka H, Hashikawa T, Itohara S, Hirabayashi Y (2004) Targeted disruption of the mouse 3-phosphoglycerate dehydrogenase gene causes severe neurodevelopmental defects and results in embryonic lethality. J Biol Chem 279:3573-3577
55. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, Ooi HS, Orlov YL, Shahab A, Yong HC, Fu Y, Weng Z, Kuznetsov VA, Sung WK, Ruan Y, Dang CV, Wei CL (2006) Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci U S A 103:17834-17839
56. Zhang P, McGrath BC, Reinert J, Olsen DS, Lei L, Gill S, Wek SA, Vattem KM, Wek RC, Kimball SR, Jefferson LS, Cavener DR (2002) The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol 22:6681-6688
57. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102:4459-4464