Upregulation of the coagulation factor VII gene during glucose deprivation is mediated by activating transcription factor 4

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Cronin, Katherine R ^a   Mangan, Thomas P ^a   Carew, Josephine A ^a,b  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BLOOD CLOTTING FACTOR 7; GLUCOSE; MESSENGER RNA; SMALL INTERFERING RNA;

ARTICLE; BLOOD CLOTTING; BLOOD CLOTTING FACTOR 7 GENE; CELL STRAIN HEPG2; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL MOBILITY SHIFT ASSAY; GENE; GENE EXPRESSION; GENETIC TRANSFECTION; GLUCOSE DEPRIVATION; HUMAN; HUMAN CELL; PLASMID; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; STEADY STATE; STRESS; UPREGULATION; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 4; FACTOR VII; GLUCOSE; HEP G2 CELLS; HUMANS; RESPONSE ELEMENTS; RNA, SMALL INTERFERING; SWEETENING AGENTS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84864412899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040994     Document Type: Article

References (96)

1. Fair DS, Plow EF,((1983)) Synthesis and secretion of the fibrinolytic components, including alpha 2-antiplasmin, by a human hepatoma cell line. J Lab Clin Med 101:: 372--384.
2. Hagen FS, Gray CL, O'Hara P, Grant FJ, Saari GC, et al.((1986)) Characterization of a cDNA coding for human factor VII. Proc Natl Acad Sci USA 83:: 2412--2416.
3. Monroe DM, Hoffman M,((2006)) What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol 26:: 41--48.
4. Mackman N,((2006)) Role of tissue factor in hemostasis and thrombosis. Blood Cells Mol Dis 36:: 104--107.
5. Dahlback B, Villoutreix BO,((2005)) Regulation of blood coagulation by the protein C anticoagulant pathway: novel insights into structure-function relationships and molecular recognition. Arterioscler Thromb Vasc Biol 25:: 1311--1320.
6. Heeb MJ,((2008)) Role of the PROS1 gene in thrombosis: lessons and controversies. Expert Review of Hematology 1:: 9--12.
7. Monroe DM, Key NS,((2007)) The tissue factor-factor VIIa complex: procoagulant activity, regulation, and multitasking. J Thromb Haemost 5:: 1097--1105.
8. Romisch J, Feussner A, Vermohlen S, Stohr HA,((1999)) A protease isolated from human plasma activating factor VII independent of tissue factor. Blood Coagulation & Fibrinolysis 10:: 471--479.
9. Mackman N,((2005)) Tissue-specific hemostasis in mice. Arterioscler Thromb Vasc Biol 25:: 2273--2281.
10. Bach RR,((2006)) Tissue factor encryption. Arterioscler Thromb Vasc Biol 26:: 456--461.
11. Wolberg AS, Monroe DM, Roberts HR, Hoffman MR,((1999)) Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and-independent mechanisms. Blood Coagulation & Fibrinolysis 10:: 201--210.
12. Bach R, Rifkin DB,((1990)) Expression of tissue factor procoagulant activity: regulation by cytosolic calcium. Proc Natl Acad Sci USA 87:: 6995--6999.
13. Dietzen DJ, Page KL, Tetzloff TA,((2004)) Lipid rafts are necessary for tonic inhibition of cellular tissue factor procoagulant activity. Blood 103:: 3038--3044.
14. Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, et al.((2006)) Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 45:: 12020--12028.
15. Ahamed J, Versteeg HH, Kerver M, Chen VM, Mueller BM, et al.((2006)) Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 103:: 13932--13937.
16. Parry GC, Erlich JH, Carmeliet P, Luther T, Mackman N,((1998)) Low levels of tissue factor are compatible with development and hemostasis in mice. J Clin Invest 101:: 560--569.
17. Arbini AA, Pollak ES, Bayleran JK, High KA, Bauer KA,((1997)) Severe factor VII deficiency due to a mutation disrupting a hepatocyte nuclear factor 4 binding site in the factor VII promoter. Blood 89:: 176--182.
18. Carew JA, Pollak ES, High KA, Bauer KA,((1998)) Severe factor VII deficiency due to a mutation disrupting an Sp1 binding site in the factor VII promoter. Blood 92:: 1639--1645.
19. Carew JA, Pollak ES, Lopaciuk S, Bauer KA,((2000)) A new mutation in the HNF4 binding region of the factor VII promoter in a patient with severe factor VII deficiency. Blood 96:: 4370--4372.
20. Kavlie A, Hiltunen L, Rasi V, Prydz H,((2003)) Two novel mutations in the human coagulation factor VII promoter. Thromb Haemost 90:: 194--205.
21. Zheng XW, Kudaravalli R, Russell TT, DiMichele DM, Gibb C, et al.((2011)) Mutation in the factor VII hepatocyte nuclear factor 4alpha-binding site contributes to factor VII deficiency. Blood Coagulation & Fibrinolysis 22:: 624--627.
22. Rosen ED, Chan JC, Idusogie E, Clotman F, Vlasuk G, et al.((1997)) Mice lacking factor VII develop normally but suffer fatal perinatal bleeding. Nature 390:: 290--294.
23. Rosen ED, Xu H, Liang Z, Martin JA, Suckow M, et al.((2005)) Generation of genetically-altered mice producing very low levels of coagulation factorVII. Thromb Haemost 94:: 493--497.
24. Toomey JR, Kratzer KE, Lasky NM, Stanton JJ, Broze GJ Jr,((1996)) Targeted disruption of the murine tissue factor gene results in embryonic lethality. Blood 88:: 1583--1587.
25. Bugge TH, Xiao Q, Kombrinck KW, Flick MJ, Holmback K, et al.((1996)) Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci USA 93:: 6258--6263.
26. Schroder M, Kaufman RJ,((2005)) The mammalian unfolded protein response. Annual Review Biochem 74:: 739--789.
27. Harding HP, Zhang Y, Ron D,((1999)) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:: 271--274.
28. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al.((2000)) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Molecular Cell 6:: 1099--1108.
29. Hinnebusch AG,((2005)) eIF2alpha kinases provide a new solution to the puzzle of substrate specificity. Nature Structural & Molecular Biology 12:: 835--838.
30. Dever TE,((2002)) Gene-specific regulation by general translation factors. Cell 108:: 545--556.
31. Ma K, Vattem KM, Wek RC,((2002)) Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J Biol Chem 277:: 18728--18735.
32. Anthony TG, McDaniel BJ, Byerley RL, McGrath BC, Cavener DR, et al.((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.
33. Wek RC, Jiang HY, Anthony TG,((2006)) Coping with stress: eIF2 kinases and translational control. Biochemical Society Transactions 34:: 7--11.
34. Jiang HY, Wek RC,((2005)) GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation. Biochem J 385:: 371--380.
35. Ameri K, Harris AL,((2008)) Activating transcription factor 4. Int J Biochemistry & Cell Biology 40:: 14--21.
36. Chen C, Dudenhausen E, Chen H, Pan YX, Gjymishka A, et al.((2005)) Amino-acid limitation induces transcription from the human C/EBPbeta gene via an enhancer activity located downstream of the protein coding sequence. Biochem J 391:: 649--658.
37. Sato H, Nomura S, Maebara K, Sato K, Tamba M, et al.((2004)) Transcriptional control of cystine/glutamate transporter gene by amino acid deprivation. Biochem Biophys Res Commun 325:: 109--116.
38. Carlson SG, Fawcett TW, Bartlett JD, Bernier M, Holbrook NJ,((1993)) Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol Cell Biol 13:: 4736--4744.
39. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H,((2005)) TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. Embo J 24:: 1243--1255.
40. Wolfgang CD, Liang G, Okamoto Y, Allen AE, Hai T,((2000)) Transcriptional autorepression of the stress-inducible gene ATF3. J Biol Chem 275:: 16865--16870.
41. Barbosa-Tessmann IP, Chen C, Zhong C, Schuster SM, Nick HS, et al.((1999)) Activation of the unfolded protein response pathway induces human asparagine synthetase gene expression. J Biol Chem 274:: 31139--31144.
42. Barbosa-Tessmann IP, Chen C, Zhong C, Siu F, Schuster SM, et al.((2000)) Activation of the human asparagine synthetase gene by the amino acid response and the endoplasmic reticulum stress response pathways occurs by common genomic elements. J Biol Chem 275:: 26976--26985.
43. Palii SS, Chen H, Kilberg MS,((2004)) Transcriptional control of the human sodium-coupled neutral amino acid transporter system A gene by amino acid availability is mediated by an intronic element. J Biol Chem 279:: 3463--3471.
44. Bruhat A, Jousse C, Carraro V, Reimold AM, Ferrara M, et al.((2000)) Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol Cellular Biol 20:: 7192--7204.
45. Chen C, Dudenhausen EE, Pan YX, Zhong C, Kilberg MS,((2004)) Human CCAAT/enhancer-binding protein beta gene expression is activated by endoplasmic reticulum stress through an unfolded protein response element downstream of the protein coding sequence. J Biol Chem 279:: 27948--27956.
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. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, et al.((2003)) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molecular Cell 11:: 619--633.
48. Ron D, Walter P,((2007)) Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology 8:: 519--529.
49. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D,((2000)) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nature Cell Biology 2:: 326--332.
50. Liu CY, Schroder M, Kaufman RJ,((2000)) Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 275:: 24881--24885.
51. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, et al.((2000)) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Molecular Cell 6:: 1355--1364.
52. Hollien J, Weissman JS,((2006)) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:: 104--107.
53. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K,((2001)) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:: 881--891.
54. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, et al.((2002)) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes & Development 16:: 452--466.
55. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al.((2002)) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:: 92--96.
56. Kilberg MS, Pan YX, Chen H, Leung-Pineda V,((2005)) Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 25:: 59--85.
57. Brush MH, Weiser DC, Shenolikar S,((2003)) Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Molecular Cellular Biology 23:: 1292--1303.
58. Teske BF, Wek SA, Bunpo P, Cundiff JK, McClintick JN, et al.((2011)) The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Molecular Biology of the Cell 22:: 4390--4405.
59. Huang CC, Li Y, Lopez AB, Chiang CM, Kaufman RJ, et al.((2010)) Temporal regulation of Cat-1 (cationic amino acid transporter-1) gene transcription during endoplasmic reticulum stress. Biochem J 429:: 215--224.
60. Armstrong JL, Flockhart R, Veal GJ, Lovat PE, Redfern CP,((2010)) Regulation of endoplasmic reticulum stress-induced cell death by ATF4 in neuroectodermal tumor cells. J Biol Chem 285:: 6091--6100.
61. Costa-Mattioli M, Gobert D, Stern E, Gamache K, Colina R, et al.((2007)) eIF2alpha phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory. Cell 129:: 195--206.
62. Moneva MH, Dagogo-Jack S,((2002)) Multiple drug targets in the management of type 2 diabetes. Current Drug Targets 3:: 203--221.
63. Jackson AA, Cronin KR, Zachariah R, Carew JA,((2007)) CCAAT/enhancer-binding protein-beta participates in insulin-responsive expression of the factor VII gene. J Biol Chem 282:: 31156--31165.
64. Vallejo M, Ron D, Miller CP, Habener JF,((1993)) C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc Natl Acad Sci USA 90:: 4679--4683.
65. Gombart AF, Grewal J, Koeffler HP,((2007)) ATF4 differentially regulates transcriptional activation of myeloid-specific genes by C/EBPepsilon and C/EBPalpha. J Leukocyte Biology 81:: 1535--1547.
66. Descombes P, Schibler U,((1991)) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67:: 569--579.
67. Hoffman M, Colina CM, McDonald AG, Arepally GM, Pedersen L, et al.((2007)) Tissue factor around dermal vessels has bound factor VII in the absence of injury. J Thromb Haemost 5:: 1403--1408.
68. Connelly S, Andrews JL, Gallo-Penn AM, Tagliavacca L, Kaufman RJ, et al.((1999)) Evaluation of an adenoviral vector encoding full-length human factor VIII in hemophiliac mice. Thromb Haemost 81:: 234--239.
69. Miao HZ, Sirachainan N, Palmer L, Kucab P, Cunningham MA, et al.((2004)) Bioengineering of coagulation factor VIII for improved secretion. Blood 103:: 3412--3419.
70. Selvaraj SR, Scheller AN, Miao HZ, Kaufman RJ, Pipe SW,((2012)) Bioengineering of coagulation factor VIII for efficient expression through elimination of a dispensable disulfide loop. J Thromb Haemost 10:: 107--115.
71. Thiaville MM, Dudenhausen EE, Zhong C, Pan YX, Kilberg MS,((2008)) 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 410:: 473--484.
72. Li Y, Bevilacqua E, Chiribau CB, Majumder M, Wang C, et al.((2008)) Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J Biol Chem 283:: 22443--22456.
73. Estes SD, Stoler DL, Anderson GR,((1995)) Normal fibroblasts induce the C/EBP beta and ATF-4 bZIP transcription factors in response to anoxia. Exp Cell Res 220:: 47--54.
74. Dey S, Baird TD, Zhou D, Palam LR, Spandau DF, et al.((2010)) Both transcriptional regulation and translational control of ATF4 are central to the integrated stress response. J Biol Chem 285:: 33165--33174.
75. Siu F, Chen C, Zhong C, Kilberg MS,((2001)) CCAAT/enhancer-binding protein-beta is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem 276:: 48100--48107.
76. Malabanan KP, Khachigian LM,((2010)) Activation transcription factor-4 and the acute vascular response to injury. J Mol Med 88:: 545--552.
77. Tominaga H, Maeda S, Hayashi M, Takeda S, Akira S, et al.((2008)) CCAAT/enhancer-binding protein beta promotes osteoblast differentiation by enhancing Runx2 activity with ATF4. Mol Biol Cell 19:: 5373--5386.
78. Lee PD, Giudice LC, Conover CA, Powell DR,((1997)) Insulin-like growth factor binding protein-1: recent findings and new directions. Proc Soc Exp Biol Med 216:: 319--357.
79. Marchand A, Tomkiewicz C, Magne L, Barouki R, Garlatti M,((2006)) Endoplasmic reticulum stress induction of insulin-like growth factor-binding protein-1 involves ATF4. J Biol Chem 281:: 19124--19133.
80. Roybal CN, Hunsaker LA, Barbash O, Vander Jagt DL, Abcouwer SF,((2005)) The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. J Biol Chem 280:: 20331--20339.
81. Oskolkova OV, Afonyushkin T, Leitner A, von Schlieffen E, Gargalovic PS, et al.((2008)) ATF4-dependent transcription is a key mechanism in VEGF up-regulation by oxidized phospholipids: critical role of oxidized sn-2 residues in activation of unfolded protein response. Blood 112:: 330--339.
82. Pereira ER, Liao N, Neale GA, Hendershot LM,((2010)) Transcriptional and post-transcriptional regulation of proangiogenic factors by the unfolded protein response. PloS ONE 5 (9):: e12521 doi:10.1371/journal.pone.0012521.
83. Muth H, Kreis I, Zimmermann R, Tillmanns H, Holschermann H,((2005)) Differential gene expression in activated monocyte-derived macrophages following binding of factor VIIa to tissue factor. Thromb Haemost 94:: 1028--1034.
84. Rao LV, Pendurthi UR,((2005)) Tissue factor-factor VIIa signaling. Arterioscler Thromb Vasc Biol 25:: 47--56.
85. Xu Z, Xu H, Ploplis VA, Castellino FJ,((2010)) Factor VII deficiency impairs cutaneous wound healing in mice. Mol Med 16:: 167--176.
86. Xu H, Noria F, Sandoval-Cooper MJ, Menchen H, Donahue DL, et al.((2009)) Severe deficiency of coagulation Factor VII results in spontaneous cardiac fibrosis in mice. J Pathol 217:: 362--371.
87. Shinagawa K, Ploplis VA, Castellino FJ,((2009)) A severe deficiency of coagulation factor VIIa results in attenuation of the asthmatic response in mice. Am J Physiol Lung Cellular Molecular Physiol 296:: L763--770.
88. Xu H, Ploplis VA, Castellino FJ,((2006)) A coagulation factor VII deficiency protects against acute inflammatory responses in mice. J Pathol 210:: 488--496.
89. Oyadomari S, Harding HP, Zhang Y, Oyadomari M, Ron D,((2008)) Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab 7:: 520--532.
90. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, et al.((2004)) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:: 457--461.
91. Boden G, Song W, Duan X, Cheung P, Kresge K, et al.((2011)) Infusion of glucose and lipids at physiological rates causes acute endoplasmic reticulum stress in rat liver. Obesity 19:: 1366--1373.
92. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, et al.((2006)) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:: 1137--1140.
93. Ji C, Kaplowitz N,((2006)) ER stress: can the liver cope? J Hepatol 45:: 321--333.
94. Dara L, Ji C, Kaplowitz N,((2011)) The contribution of endoplasmic reticulum stress to liver diseases. Hepatol 53:: 1752--1763.
95. Carr ME,((2001)) Diabetes mellitus: a hypercoagulable state. J Diabetes Complications 15:: 44--54.
96. Hadzopoulou-Cladaras M, Kistanova E, Evagelopoulou C, Zeng S, Cladaras C, et al.((1997)) Functional domains of the nuclear receptor hepatocyte nuclear factor 4. J Biol Chem 272:: 539--550.