Angiotensin II-inducible platelet-derived growth factor-D transcription requires specific Ser/Thr residues in the second zinc finger region of Sp1

Circulation Research

Volumn 102, Issue 4, 2008, Pages

  Tan, Nicole Y ^a   Midgley, Valerie C ^a   Kavurma, Mary M ^a   Santiago, Fernando S ^a   Luo, Xiao ^a   Peden, Ryan ^a   Fahmy, Roger G ^a   Berndt, Michael C ^b   Molloy, Mark P ^c   Khachigian, Levon M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

PDGF D; PKC ; Sp1 phosphorylation; Transcription

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; PEPTIDE ANTIBODY; PLATELET DERIVED GROWTH FACTOR D; PROTEIN KINASE C ZETA; SERINE; THREONINE; TRANSCRIPTION FACTOR SP1; ANTIBODY; LYMPHOKINE; PDGFD PROTEIN, HUMAN; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE C; SCDGFB PROTEIN, RAT; UNCLASSIFIED DRUG; VASOCONSTRICTOR AGENT; ZINC FINGER PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; CAROTID ARTERY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; GENE ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RAT; SMOOTH MUSCLE FIBER; ZINC FINGER MOTIF; ANIMAL; BALLOON DILATATION; CAROTID ARTERY DISEASE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; GENETICS; IMMUNOLOGY; METABOLISM; MUTAGENESIS; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; ANTIBODIES; BALLOON DILATATION; CAROTID ARTERY DISEASES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HUMANS; LYMPHOKINES; MUSCLE, SMOOTH, VASCULAR; MUTAGENESIS; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROMOTER REGIONS (GENETICS); PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; SERINE; SP1 TRANSCRIPTION FACTOR; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THREONINE; TRANSCRIPTION, GENETIC; VASOCONSTRICTOR AGENTS; ZINC FINGERS;

EID: 41949103861     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.167395     Document Type: Article

References (58)

1. Philipsen S, Suske G. A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res. 1999;27:2991-3000.
2. Jackson SP, Tjian R. O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation. Cell. 1988;55:125-133.
3. Jackson SP, MacDonald JJ, Lees-Miller S, Tjian R. GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell. 1990;5:155-165.
4. Lin M-C, Almus-Jacobs F, Chen H-H, Parry GCN, Mackmann N, Shyy JY, Chen S. Shear stress induction of the tissue factor gene. J Clin Invest. 1997;99:737-744.
5. Reisinger K, Kaufmann R, Gille J. Increased Sp1 phosphorylation as a mechanism of hepatocyte growth factor (HGF/SF)-induced vascular endothelial growth factor (VEGF/VPF) transcription. J Cell Science. 2003;116:225-238.
6. Zheng XL, Matsubara S, Diao C, Hollenberg MD, Wong NC. Epidermal growth factor induction of apolipoprotein A-I is mediated by the Ras-MAP kinase cascade and Sp1. J Biol Chem. 2001;276:13822-13829.
7. Wu Z, Kim HP, Xue HH, Liu H, Zhao K, Leonard WJ. Interleukin-21 receptor gene induction in human T cells is mediated by T-cell receptor-induced Sp1 activity. Mol Cell Biol. 2005;25:9741-9752.
8. Larouche K, Leclerc S, Salesse C, Guerin SL. Expression of the alpha 5 integrin subunit gene promoter is positively regulated by the extracellular matrix component fibronectin through the transcription factor Sp1 in corneal epithelial cells in vitro. J Biol Chem. 2000;275:39182-39192.
9. Benasciutti E, Pages G, Kenzior O, Folk W, Blasi F, Crippa MP. MAPK and JNK transduction pathways can phosphorylate Sp1 to activate the uPA minimal promoter element and endogenous gene transcription. Blood. 2004;104:256-262.
10. Chupreta S, Du M, Todisco A, Merchant JL. EGF stimulates gastrin promoter through activation of Sp1 kinase activity. Am J Physiol Cell Physiol. 2000;278:C697-708.
11. Armstrong SA, Barry DA, Leggett RW, Mueller CR. Casein kinase II-mediated phosphorylation of the C terminus of Sp1 decreases its DNA binding activity. J Biol Chem. 1997;272:13489-13495.
12. Chun RF, O.J. S, Neuveut C, Jeang KT. Modulation of Sp1 phosphorylation by human immunodeficiency virus type 1 Tat. J Virol. 1998;72:2615-2629.
13. Kavurma MM, Santiago FS, Bonfoco E, Khachigian LM. Sp1 phosphorylation regulates apoptosis via extracellular FasL-Fas engagement. J Biol Chem. 2001;276:4964-4971.
14. Rafty LA, Khachigian LM. Sp1 phosphorylation regulates inducible expression of platelet-derived growth factor B-chain gene via atypical protein kinase C-zeta. Nucleic Acids Res. 2001;29:1027-1033.
15. Pal S, Claffey KP, Cohen HT, Mukhopadhyay D. Activation of Sp1-mediated vascular permeability factor/vascular endothelial growth factor transcription requires specific interaction with protein kinase C zeta. J Biol Chem. 1998;273:26277-26280.
16. Neid M, Datta K, Stephan S, Khanna I, Pal S, Shaw L, White M, Mukhopadhyay D. Role of insulin receptor substrates and protein kinase C-zeta in vascular permeability factor/vascular endothelial growth factor expression in pancreatic cancer cells. J Biol Chem. 2004;279:3941-3948.
17. Zhang Y, Liao M, Dufau ML. Phosphatidylinositol 3-kinase/protein kinase Czeta-induced phosphorylation of Sp1 and p107 repressor release have a critical role in histone deacetylase inhibitor-mediated depression of transcription of the luteinizing hormone receptor gene. Mol Cell Biol. 2006;26:6748-6761.
18. Toker A. Signalling through protein kinase C. Front Biosci. 1998;3:1134-1147.
19. Buteau J, Foisy S, Rhodes CJ, Carpenter L, Biden TJ, Prentki M. Protein kinase C-zeta activation mediates glucagon-like peptide-1-induced pancreatic beta-cell proliferation. Diabetes. 2001;50:2237-2243.
20. Le Good JA, Ziegler WH, Parekh DB, Alessi DR, Cohen P, Parker PJ. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science. 1998;281:2042-2045.
21. Huntley CC, De BP, Murray NR, Fields AP, Banerjee AK. Human parainfluenza virus type 3 phosphoprotein: identification of serine 333 as the major site for PKC zeta phosphorylation. Virology. 1995;211:561-567.
22. Khachigian LM, Collins T. Inducible expression of Egr-1-dependent genes: a paradigm of transcriptional activation in vascular endothelium. Circ Res. 1997;81:457-461.
23. Delbridge GJ, Khachigian LM. FGF-1-induced PDGF A-chain gene expression in vascular endothelial cells involves transcriptional activation by Egr-1. Circ Res. 1997;81:282-288.
24. Resnick N, Yahav H, Khachigian LM, Collins T, Anderson KR, Dewey FC, Gimbrone MA Jr. Endothelial gene regulation by laminar shear stress. Adv Exp Med Biol. 1997;430:155-164.
25. Berk BC, Alexander RW, Brock TA, Gimbrone MA Jr, Webb RC. Vasoconstriction: a new activity for platelet-derived growth factor. Science. 1986;232:87-90.
26. Khachigian LM, Williams AJ, Collins T. Interplay of Sp1 and Egr-1 in the proximal PDGF-A promoter in cultured vascular endothelial cells. J Biol Chem. 1995;270:27679-27686.
27. Khachigian LM, Lindner V, Williams AJ, Collins T. Egr-1-induced endothelial gene expression: a common theme in vascular injury. Science. 1996;271:1427-1431.
28. Midgley VC, Khachigian LM. Fibroblast growth factor-2 induction of platelet-derived growth factor-C chain transcription in vascular smooth muscle cells is ERK-dependent but not JNK-dependent and mediated by Egr-1. J Biol Chem. 2004;279:40289-40295.
29. Liu MY, Eyries M, Zhang C, Santiago FS, Khachigian LM. Inducible platelet-derived growth factor D-chain expression by angiotensin II and hydrogen peroxide involves transcriptional regulation by Ets-1 and Sp1. Blood. 2006;107:2322-2329.
30. Kavurma MM, Bobryshev Y, Khachigian LM. Ets-1 positively regulates Fas ligand transcription via cooperative interactions with Sp1. J Biol Chem. 2002;277:36244-36252.
31. Rafty LA, Santiago FS, Khachigian LM. NF1/X represses PDGF A-chain transcription by interacting with Sp1 and antagonizing Sp1 occupancy of the promoter. EMBO J. 2002;21:334-343.
32. Khachigian LM, Fahmy RG, Zhang G, Bobryshev YV, Kaniaros A. c-Jun regulates vascular smooth muscle cell growth and neointima formation after arterial injury: inhibition by a novel DNAzyme targeting c-Jun. J Biol Chem. 2002;277:22985-22991.
33. Santiago FS, Lowe HC, Kavurma MM, Chesterman CN, Baker A, Atkins DG, Khachigian LM. New DNA enzyme targeting Egr-1 mRNA inhibits vascular smooth muscle proliferation and regrowth factor injury. Nature Med. 1999;5:1264-1269.
34. Santiago FS, Lowe HC, Bobryshev YV, Khachigian LM. Induction of the transcriptional repressor Yin Yang-1 by vascular cell injury: autocrine/paracrine role of endogenous fibroblast growth factor-2. J Biol Chem. 2001;276:41143-41149.
35. Hsu S-M, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981;29:577-580.
36. Kim J, Camp DG II, Smith RD. Improved detection of multi-phosphorylated peptides in the presence of phosphoric acid in liquid chromatography/mass spectrometry. J Mass Spectrom. 2004;39:208-215.
37. Steen H, Jebanathirajah JA, Rush J, Morrice N, Kirschner MW. Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol Cell Proteomics. 2006;5:172-181.
38. Biemann K. Sequencing of peptides by tandem mass spectrometry and high-energy collision-induced dissociation. Methods Enzymol. 1990;193:455-479.
39. Mangin P, David T, Lavaud V, Cranmer SL, Pikovski I, Jackson SP, Berndt MC, Cazenave JP, Gachet C, Lanza F. Identification of a novel 14-3-3zeta binding site within the cytoplasmic tail of platelet glycoprotein Ibalpha. Blood. 2004;104:420-427.
40. Guthridge MA, Stomski FC, Barry EF, Winnall W, Woodcock JM, McClure BJ, Dottore M, Berndt MC, Lopez AF. Site-specific serine phosphorylation of the IL-3 receptor is required for hemopoietic cell survival. Mol Cell. 2000;6:99-108.
41. Watanabe T, Barker TA, Berk BC. Angiotensin II and the endothelium: diverse signals and effects. Hypertension. 2005;45:163-169.
42. Khachigian LM, Takuwa Y, Collins T. Mechanisms of angiotensin II-induced platelet-derived growth factor gene expression. Mol Cell Biochem. 2000;212:183-186.
43. Dixon BS, Sharma RV, Dickerson T, Fortune J. Bradykinin and angiotensin II: activation of protein kinase C in arterial smooth muscle. Am J Physiol. 1994;266:C1406-C1420.
44. Gomez-del Arco P, Maki K, Georgopoulos K. Phosphorylation controls Ikaros's ability to negatively regulate the G(1)-S transition. Mol Cell Biol. 2004;24:2797-2807.
45. Marden CM, Stefanidis D, Cunninghame-Graham DS, Casimir CM. Differentiation-dependent up-regulation of p47(phox) gene transcription is associated with changes in PU. 1 phosphorylation and increased binding affinity. Biochem Biophys Res Commun. 2003;305:193-202.
46. Fishel RS, Thourani V, Eisenberg SJ, Shai SY, Corson MA, Nabel EG, Bernstein KE, Berk BC. Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. Possible mediator of the response to vascular injury. J Clin Invest. 1995;95:377-387.
47. Parmentier JH, Zhang C, Estes A, Schaefer S, Malik KU. Essential role of PKC-zeta in normal and angiotensin II-accelerated neointimal growth after vascular injury. Am J Physiol Heart Circ Physiol. 2006;291:H1602-H1613.
48. Chen J, Han Y, Lin C, Zhen Y, Song X, Teng S, Chen C, Chen Y, Zhang Y, Hui R. PDGF-D contributes to neointimal hyperplasia in rat model of vessel injury. Biochem Biophys Res Commun. 2005;329:976-983.
49. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A. 1986;83:4913-4917.
50. Oka S, Shiraishi Y, Yoshida T, Ohkubo T, Sugiura Y, Kobayashi Y. NMR structure of transcription factor Sp1 DNA binding domain. Biochemistry. 2004;43:16027-16035.
51. Usukura J, Nishizawa Y, Shimomura A, Kobayashi K, Nagatsu T, Hagiwara M. Direct imaging of phosphorylation-dependent conformational change and DNA binding of CREB by electron microscopy. Genes Cells. 2000;5:515-522.
52. Vanden Berghe W, Vermeulen L, Delerive P, De Bosscher K, Staels B, Haegeman G. A paradigm for gene regulation: inflammation, NF-kappaB and PPAR. Adv Exp Med Biol. 2003;544:181-196.
53. Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, Weigel NL, Ingraham HA. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol Cell. 1999;3:521-526.
54. Bonello MR, Bobryshev YV, Khachigian LM. Peroxide-inducible Ets-1 mediates platelet-derived growth factor receptor-{alpha} gene transcription in vascular smooth muscle cells. Am J Pathol. 2005;167:1149-1159.
55. Fischer C, Sanchez-Ruderisch H, Welzel M, Wiedenmann B, Sakai T, Andre S, Gabius HJ, Khachigian L, Detjen KM, Rosewicz S. Galectin-1 interacts with the alpha 5beta 1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 2005;280:37266-37277.
56. Chu S, Ferro TJ. Sp1: regulation of gene expression by phosphorylation. Gene. 2005;348:1-11.
57. Bouwman P, Philipsen S. Regulation of the activity of Sp1-related transcription factors. Mol Cell Endocrinol. 2002;195:27-38.
58. Bonello MR, Khachigian LM. Fibroblast growth factor-2 represses platelet-derived growth factor receptor-alpha (PDGFR-alpha) transcription via ERK1/2-dependent Sp1 phosphorylation and an atypical cis-acting element in the proximal PDGFR-alpha promoter. J Biol Chem. 2004;279:2377-2382.