CD40-induced transcriptional activation of vascular endothelial growth factor involves a 68-bp region of the promoter containing a CpG island

American Journal of Physiology - Renal Physiology

Volumn 287, Issue 3 56-3, 2004, Pages

  Lapchak, Peter H ^a   Melter, Michael ^a   Pal, Soumitro ^a   Flaxenburg, Jesse A ^a   Geehan, Christopher ^a   Frank, Markus H ^a   Mukhopadhyay, Debabrata ^a,b   Briscoe, David M ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Angiogenesis; Angiogenesis factors; Base pair; Transactivation; Vascular endothelium

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; DNA; LUCIFERASE; METHYL CPG BINDING PROTEIN 2; VASCULOTROPIN;

ARTICLE; CELL TYPE; COMPUTER ANALYSIS; CONTROLLED STUDY; CPG ISLAND; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MECP2 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SECRETION; PROTEINURIA; REGULATORY MECHANISM; REPRESSOR GENE; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION;

EID: 4143061209     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00070.2004     Document Type: Article

References (69)

1. Alderson MR, Armitage RJ, Tough TW, Strockbine L, Fanslow WC, and Spriggs MK. CD40 expression by human monocytes: regulation by cytokines and activation of monocytes by the ligand for CD40. J Exp Med 178: 669-674, 1993.
2. Bailey E, Bottomley MJ, Westwell S, Pringle JH, Furness PN, Feehally J, Brenchley PE, and Harper SJ. Vascular endothelial growth factor mRNA expression in minimal change, membranous, and diabetic nephropathy demonstrated by non-isotopic in situ hybridisation. J Clin Pathol 52: 735-738, 1999.
3. Bianco T, Chenevix-Trench G, Walsh DC, Cooper JE, and Dobrovic A. Tumour-specific distribution of BRCAI promoter region methylation supports a pathogenetic role in breast and ovarian cancer. Carcinogenesis 21: 147-151. 2000.
4. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21, 2002.
5. Bird AP and Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell 99: 451-454, 1999.
6. Boyes J and Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64: 1123-1134, 1991.
7. Brown LF, Berse B, Tognazzi K, Manseau EJ, Van de Water L, Senger DR, Dvorak HF, and Rosen S. Vascular permeability factor mRNA and protein expression in human kidney. Kidney Int 42: 1457-1461. 1992.
8. Brown LF, Detmar M, Claffey K, Nagy JA, Feng D, Dvorak AM, and Dvorak HF. Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. EXS 79: 233-269, 1997.
9. Burley SK and Roeder RG. Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65: 769-799, 1996.
10. Campanero MR, Armstrong MI, and Flemington EK. CpG methylation as a mechanism for the regulation of E2F activity. Proc Natl Acad Sci USA 97: 6481-6486, 2000.
11. Chandler SP, Guschin D, Landsberger N, and Wolffe AP. The methyl-CpG binding transcriptional repressor MeCP2 stably associates with nucleosomal DNA. Biochemistry 38: 7008-7018, 1999.
12. Cho CS, Cho ML, Min SY, Kim WU, Min DJ, Lee SS, Park SH, Choe J, and Kim HY. CD40 engagement on synovial fibroblast upregulates production of vascular endothelial growth factor. J Immunol 164: 5055-5061, 2000.
13. Choi YJ, Chakrahorty S, Nguyen V, Nguyen C, Kim BK, Shim SI, Suki WN, and Truong LD. Peritubular capillary loss is associated with chronic tubulointerstitial injury in human kidney: altered expression of vascular endothelial growth factor. Hum Pathol 31: 1491-1497, 2000.
14. Cooper ME, Vranes D, Youssef S, Stacker SA, Cox AJ, Rizkalla B, Casley DJ, Bach LA, Kelly DJ, and Gilbert RE. Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 48: 2229-2239, 1999.
15. Cross SH, Charlton JA, Nan X, and Bird AP. Purification of CpG islands using a methylated DNA binding column. Nat Genet 6: 236-244, 1994.
16. Denton MD, Reul RM, Dharnidharka VR, Fang JC, Ganz P, and Briscoe OM. Central role for CD40/CD40 ligand (CD154) interactions in transplant rejection. Pediatr Transplant 2: 6-15, 1998.
17. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerher HP, Kikkawa Y, Miner JH, and Quaggin SE. Glomerular-specinc alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716, 2003.
18. Ferrara N and Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 18: 4-25, 1997.
19. Francis DA, Karras JG, Ke XY, Sen R, and Rothstein TL. Induction of the transcription factors NF-κB, AP-1, and NF-AT during B cell stimulation through the CD40 receptor. Int Immunol 7: 151-161, 1995.
20. Fujita N, Takebayashi S, Okumura K, Kudo S, Chiba T, Saya H, and Nakao M. Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBDI isoforms. Mol Cell Biol 19: 6415-6426, 1999.
21. Haltia A, Solin ML, Jalanko H, Holmberg C, Miettinen A, and Holthofer H. Mechanisms of proteinuria: vascular permeability factor in congenital nephrotic syndrome of the Finnish type. Pediatr Res 40: 652-657, 1996.
22. Hendrich B and Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18: 6538-6547, 1998.
23. Henn V, Slupsky JR, Grafe M, Anagnostopoulos I, Forster R, Muller-Berghaus G, and Kroczek RA. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 391: 591-594, 1998.
24. Hollenbaugh D, Mischel-Petty N, Edwards CP, Simon JC, Denfeld RW, Kiener PA, and Aruffo A. Expression of functional CD40 by vascular endothelial cells. J Exp Med 182: 33-40, 1995.
25. Honkanen E, von Willehrand E, Koskinen P, Teppo AM, Tornroth T, Ruutu M, and Gronhagen-Riska C. Decreased expression of vascular endothelial growth factor in idiopathic membranous glomerulonephritis: relationships to clinical course. Am J Kidney Dis 42: 1139-1148, 2003.
26. Horita Y, Miyazaki M, Koji T, Kobayashi N, Shibuya M, Razzaque MS, Cheng M, Ozono Y, Kohno S, and Taguchi T, Expression of vascular endothelial growth factor and its receptors in rats with protein-overload nephrosis. Nephrol Dial Transplant 13: 2519-2528. 1998.
27. Huo L and Rothstein TL. Receptor-specific induction of individual AP-1 components in B lymphocytes. J Immunol 154: 3300-3309, 1995.
28. Hutchins AS, Mullen AC, Lee HW, Sykes KJ, High FA, Hendrich BD, Bird AP, and Reiner SL. Gene silencing quantitatively controls the function of a developmental trans-activator. Mol Cell 10: 81-91, 2002.
29. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, and Wolffe AP, Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187-191, 1998,
30. Kitamoto Y, Tokunaga H, Miyamoto K, and Tomita K. VEGF is an essential molecule for glomerular structuring. Nephrol Dial Transplant 17. Suppl 9: 25-27, 2002.
31. Klagsbrun M and D'Amore PA. Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev 7: 259-270. 1996.
32. Kudo S. Methyl-CpG-binding protein MeCP2 represses Sp1-activated transcription of the human leukosialin gene when the promoter is methylated. Mol Cell Biol 18: 5492-5499, 1998.
33. Kudo S and Fukuda M. Transcriptional activation of human leukosialin (CD43) gene by Sp1 through binding to a GGGTGG motif. Eur J Biochem 223: 319-327, 1994.
34. Laurinavicius A, Hurwitz S, and Rennke HG. Collapsing glomerulopathy in HIV and non-HIV patients: a clinicopathotogical and follow-up study. Kidney Int 56: 2203-2213, 1999.
35. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, and Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309, 1989.
36. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, and Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683, 2004.
37. Li H and Nord EP. CD40 ligation stimulates MCP-1 and IL-8 production, TRAF6 recruitment, and MAPK activation in proximal tubule cells. Am J Physiol Renal Physiol 282: F1020-F1033, 2002.
38. Luttun A and Carmeliet P. Soluble VEGF receptor FItI: the elusive preeclampsia factor discovered? J Clin Invest 111: 600-602, 2003.
39. Mattot V, Moons L, Lupu F, Chernavvsky D, Gomez RA, Collen D, and Carmeliet P. Loss of the VEGF(164) and VEGF(188) isoforms impairs postnatal glomerular angiogenesis and renal arteriogenesis in mice. J Am Soc Nephrol 13: 1548-1560, 2002.
40. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondai S, Lihermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, and Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sFItI) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658, 2003.
41. Melter M, Reinders ME, Sho M, Pal S, Geehan C, Denton MD, Mukhopadhyay D, and Briscoe DM. Ligation of CD40 induces the expression of vascular endothelial growth factor by endothelial cells and monocytes and promotes angiogenesis in vivo. Blood 96: 3801-3808. 2000.
42. Mukhopadhyay D, Knebelmann B, Cohen HT, Ananth S, and Sukhatme VP. The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity. Mol Cell Biol 17: 5629-5639, 1997.
43. Muller C, Readhead C, Diederichs S, Idos G, Yang R, Tidow N, Serve H, Berdel WE, and Koeffler HP. Methylation of the cyclin A1 promoter correlates with gene silencing in somatic cell lines, while tissue-specific expression of cyclin A1 is methylation independent. Mol Cell Biol 20: 3316-3329,2000.
44. Nan X, Campoy FJ, and Bird A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88: 471-481, 1997.
45. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, and Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389, 1998.
46. Nitta K, Uchida K, Kimata N, Honda K, Horita S, Hayashi T, Ishizuka T, Kobayashi H, Kawashima A, Yumura W, and Nihei H. Increased serum levels of vascular endothelial growth factor in human crescentic glomerulonephritis. Clin Nephrol 52: 76-82, 1999.
47. Noelle RJ, Roy M, Shepherd DM, Stamenkovic I, Ledbetter JA, and Aruffo A. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc Natl Acad Sci USA 89: 6550-6554, 1992.
48. Ostendorf T, Kunter U, Eitner F, Loos A, Regele H, Kerjaschki D, Henninger DD, Janjic N, and Floege J. VEGF(165) mediates glomerular endothelial repair. J Clin Invest 104: 913-923. 1999.
49. Pal S, Claffey KP, Cohen HT, and 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 273: 26277-26280, 1998.
50. Pal S, Datta K, Khosravi-Far R, and Mukhopadhyay D. Role of PKC z in Ras-mediated transcriptional activation of vascular permeability factor/vascular endothelial growth factor expression. J Biol Chem 276: 2395-2403, 2001.
51. Pilmore HL, Kris JM, Painter DM. Bishop GA, and McCaughan GW. Vascular endothelial growth factor expression in human chronic renal allograft rejection. Transplantation 67: 929-933, 1999.
52. Quandt K, Frech K, Karas H. Wingender E, and Werner T. MatInd and MaiInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23: 4878-4884. 1995.
53. Reinders ME, Sho M, Robertson SW, Geehan CS, and Briscoe DM. Proangiogenic function of CD40 ligand-CD40 interactions. J Immunol 171: 1534-1541, 2003.
54. Reul RM, Fang JC, Denton MD, Geehan C, Long C, Mitchell RN, Ganz P, and Briscoe DM. CD40 and CD40 ligand (CD 154) are coexpressed on microvessels in vivo in human cardiac allograft rejection. Transplantation 64: 1765-1774, 1997.
55. Robert B, Zhao X, and Abrahamson DR. Coexpression of neuropilin-1, Flk1, and VEGF(164) in developing and mature mouse kidney glomeruli. Am J Physiol Renal Physiol 279: F275-F282, 2000.
56. Schonbeck U and Libby P. The CD40/CD154 receptor/ligand dyad. Cell Mol Life Sci 58: 4-43, 2001.
57. Shahbazi M, Fryer AA, Pravica V, Brogan IJ. Ramsay HM, Hutchinson IV, and Harden PN. Vascular endothelial growth factor gene polymorphisms are associated with acute renal allograft rejection. J Am Soc Nephrol 13: 260-264, 2002.
58. Shihab FS, Bennett WM, Yi H, and Andoh TF. Expression of vascular endothelial growth factor and its receptors Fit-1 and KDR/Flk-1 in chronic cyclosporine nephrotoxicity. Transplantation 72: 164-168, 2001.
59. Shulman K, Rosen S, Tognazzi K, Manseau FJ, and Brown LF. Expression of vascular permeability factor (VPF/VEGF) is altered in many glomerular diseases. J Am Soc Nephrol 7: 661-666, 1996.
60. Somlo S and Mundel P. Getting a foothold in nephrotic syndrome. Nat Genet 24: 333-335, 2000.
61. Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, and Kalluri R. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-l) induces proteinuria. J Biol Chem 278: 12605-12608, 2003.
62. Tai YT, Podar K, Gupta D, Lin B, Young G, Akiyama M, and Anderson KC. CD40 activation induces p53-dependent vascular endothelial growth factor secretion in human multiple myeloma cells. Blood 99: 1419-1427, 2002.
63. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, and Abraham JA. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 266: 11947-11954, 1991.
64. Tufro A, Norwood VF, Carey RM, and Gomez RA. Vascular endothelial growth factor induces nephrogenesis and vasculogenesis. J Am Soc Nephrol 10: 2125-2134, 1999.
65. Van Kooten C and Banchereau J. CD40-CD40 ligand: a multifunctional receptor-ligand pair. Adv Immunol 61: 1-77, 1996.
66. Van Kooten C, van der Linde X, Woltman AM, van Es LA, and Daha MR. Synergistic effect of interleukin-1 and CD40L on the activation of human renal tubular epithelial cells. Kidney Int 56: 41-51, 1999.
67. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, and Rosenberg SA. A randomized trial of bevacizumab. an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349: 427-434, 2003.
68. Yellin MJ, Brett J, Baum D, Matsushima A, Szabolcs M, Stern D, and Chess L. Functional interactions of T cells with endotheliai cells: the role of CD40L-CD40-mediated signals. J Exp Med 182: 1857-1864, 1995.
69. Zeng H, Dvorak HF, and Mukhopadhyay D. Vascular permeability factor (VpF)/vascular endothelial growth factor (VEGF) peceptor-1 down-modulates VPFWEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 276: 26969-26979, 2001.