Cooperation between GLI and JUN enhances transcription of JUN and selected GLI target genes

Oncogene

Volumn 28, Issue 13, 2009, Pages 1639-1651

  Laner Plamberger, S ^a   Kaser, A ^a   Paulischta, M ^a   Hauser Kronberger, C ^b   Eichberger, T ^a   Frischauf, A M ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Activated JUN; Basal cell carcinoma; GLI1; GLI2; Hedgehog signaling; Keratinocytes

Indexed keywords

ONCOPROTEIN; PROTEIN JUN; SHORT HAIRPIN RNA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GENE INTERACTION; GENE TARGETING; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; HUMAN CELL; KERATINOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BASE SEQUENCE; BINDING SITES; CELL PROLIFERATION; CELLS, CULTURED; GENES, CDC; HEDGEHOG PROTEINS; HUMANS; KERATINOCYTES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

ERINACEIDAE;

EID: 64049102116     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.10     Document Type: Article

References (82)

1. Agren M, Kogerman P, Kleman MI, Wessling M, Toftgard R. (2004). Expression ofthe PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 330: 101-114.
2. Angel P, Allegretto EA, Okino ST, Hattori K, Boyle WJ, Hunter T et al. (1988a). Oncogene jun encodes a sequence-specific transactivator similar to AP-1. Nature 332: 166-171.
3. Angel P, Hattori K, Smeal T, Karin M. (1988b). The jun protooncogene is positively autoregulated by its product, Jun/AP-1. Cell 55: 875-885.
4. Bannister AJ, Oehler T, Wilhelm D, Angel P, Kouzarides T. (1995). Stimulation ofc-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11: 2509-2514.
5. Basuyaux JP, Ferreira E, Stehelin D, Buttice G. (1997). The Ets transcription factors interact with each other and with the c-Fos/c-Jun complex via distinct protein domains in a DNA-dependent and -independent manner. J Biol Chem 272: 26188-26195.
6. Beachy PA, Karhadkar SS, Berman DM. (2004). Tissue repair and stem cell renewal in carcinogenesis. Nature 432: 324-331.
7. Behrens A, Jochum W, Sibilia M, Wagner EF. (2000). Oncogenic transformation by ras and fos is mediated by c-Jun N-terminal phosphorylation. Oncogene 19: 2657-2663.
8. Behrens A, Sibilia M, Wagner EF. (1999). Amino-terminal phosphorylation ofc-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21: 326-329.
9. Bigelow RL, Jen EY, Delehedde M, Chari NS, McDonnell TJ. (2005). Sonic hedgehog induces epidermal growth factor dependent matrix infiltration in HaCaT keratinocytes. J Invest Dermatol 124: 457-465.
10. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA et al. (2000). Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20: 1436-1447.
11. Eferl R, Wagner EF. (2003). AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
12. Eichberger T, Kaser A, Pixner C, Schmid C, Klingler S, Winklmayr M et al. (2008). GLI2-specific transcriptional activation of the bone morphogenetic protein/activin antagonist follistatin in human epidermal cells. J Biol Chem 283: 12426-12437.
13. Eichberger T, Sander V, Schnidar H, Regl G, Kasper M, Schmid C et al. (2006). Overlapping and distinct transcriptional regulator properties ofthe GLI1 and GLI2 oncogenes. Genomics 87: 616-632.
14. Evangelista M, Tian H, de Sauvage FJ. (2006). The hedgehog signaling pathway in cancer. Clin Cancer Res 12: 5924-5928.
15. Ghali L, Wong ST, Green J, Tidman N, Quinn AG. (1999). Gli1 protein is expressed in basal cell carcinomas, outer root sheath keratinocytes and a subpopulation ofmesenchymal cells in normal human skin. J Invest Dermatol 113: 595-599.
16. Giesecke AV, Fang R, Joung JK. (2006). Synthetic protein-protein interaction domains created by shuffling Cys2His2 zinc-fingers. Mol Syst Biol 2: 2006.2011 Epub 21 March 2006.
17. Ginsberg M, Czeko E, Muller P, Ren Z, Chen X, Darnell Jr JE. (2007). Amino acid residues required for physical and cooperative transcriptional interaction of STAT3 and AP-1 proteins c-Jun and c-Fos. Mol Cell Biol 27: 6300-6308.
18. Grachtchouk M, Mo R, Yu S, Zhang X, Sasaki H, Hui CC et al. (2000). Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat Genet 24: 216-217.
19. Gramigni C, Penco S, Bianchi-Scarra G, Ravazzolo R, Garre C. (1998). An upstream negative regulatory element in human granulocyte-macrophage colony-stimulating factor promoter is recognised by AP1 family members. FEBS Lett 440: 119-124.
20. Hahn H, Wicking C, Zaphiropoulous PG, Gailani MR, Shanley S, Chidambaram A et al. (1996). Mutations ofthe human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85: 841-851.
21. Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E et al. (2006). Genome-wide prediction ofmammalia n enhancers based on analysis of transcription-factor binding affinity. Cell 124: 47-59.
22. Hayakawa J, Mittal S, Wang Y, Korkmaz KS, Adamson E, English C et al. (2004). Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol Cell 16: 521-535.
23. Hebrok M. (2003). Hedgehog signaling in pancreas development. Mech Dev 120: 45-57.
24. Herber B, Truss M, Beato M, Muller R. (1994). Inducible regulatory elements in the human cyclin D1 promoter. Oncogene 9: 1295-1304.
25. Hess J, Angel P, Schorpp-Kistner M. (2004). AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 117: 5965-5973.
26. Hibi M, Lin A, Smeal T, Minden A, Karin M. (1993). Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7: 2135-2148.
27. Hooper JE, Scott MP. (2005). Communicating with Hedgehogs. Nat Rev Mol Cell Biol 6: 306-317.
28. Huangfu D, Anderson KV. (2006). Signaling from Smo to Ci/Gli: conservation and divergence ofHedgehog pathways from Drosophila to vertebrates. Development 133: 3-14.
29. Ikram MS, Neill GW, Regl G, Eichberger T, FrischaufAM, Aberger F et al. (2004). GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J Invest Dermatol 122: 1503-1509.
30. Ingham PW, McMahon AP. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15: 3059-3087.
31. Jochum W, Passegue E, Wagner EF. (2001). AP-1 in mouse development and tumorigenesis. Oncogene 20: 2401-2412.
32. Johnson GL, Nakamura K. (2007). The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta 1773: 1341-1348.
33. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM et al. (1996). Human homolog of patched , a candidate gene for the basal cell nevus syndrome. Science 272: 1668-1671.
34. Johnson RS, van Lingen B, Papaioannou VE, Spiegelman BM. (1993). A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev 7: 1309-1317.
35. Kasper M, Regl G, Eichberger T, FrischaufAM, Aberger F. (2007). Efficient manipulation of Hedgehog/GLI signaling using retroviral expression systems. Methods Mol Biol 397: 67-78.
36. Kasper M, Regl G, FrischaufAM, Aberger F. (2006a). GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur J Cancer 42: 437-445.
37. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S, Blaas L et al. (2006b). Selective modulation ofHedgehog/GL I target gene expression by epidermal growth factor signaling in human keratinocytes. Mol Cell Biol 26: 6283-6298.
38. Kim S, Denny CT, Wisdom R. (2006). Cooperative DNA binding with P-1 proteins is required for transformation by EWS-Ets fusion proteins. Mol Cell Biol 26: 2467-2478.
39. Kinzler KW, Vogelstein B. (1990). The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol Cell Biol 10: 634-642.
40. Kogerman P, Grimm T, Kogerman L, Krause D, Unden AB, Sandstedt B et al. (1999). Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling ofGli-1. Nat Cell Biol 1: 312-319.
41. Lauth M, Bergstrom A, Toftgard R. (2007). Phorbol esters inhibit the Hedgehog signalling pathway downstream ofsuppressor off used, but upstream of Gli. Oncogene 26: 5163-5168.
42. Maeda S, Karin M. (2003). Oncogene at lastc-Jun promotes liver cancer in mice. Cancer Cell 3: 102-104.
43. Maniatis T, Falvo JV, Kim TH, Kim TK, Lin CH, Parekh BS et al. (1998). Structure and function of the interferon-beta enhanceosome. Cold Spring Harb Symp Quant Biol 63: 609-620.
44. Martin KJ, Graner E, Li Y, Price LM, Kritzman BM, Fournier MV et al. (2001). High-sensitivity array analysis ofgene expression for the early detection of dissemina ted breast tumor cells in peripheral blood. Proc Natl Acad Sci USA 98: 2646-2651.
45. Mechta-Grigoriou F, Gerald D, Yaniv M. (2001). The mammalian Jun proteins: redundancy and specificity. Oncogene 20: 2378-2389.
46. Mimeault M, Johansson SL, Vankatraman G, Moore E, Henichart JP, Depreux P et al. (2007). Combined targeting of epidermal growth factor receptor and hedgehog signaling by gefitinib and cyclopamine cooperatively improves the cytotoxic effects of docetaxel on metastatic prostate cancer cells. Mol Cancer Ther 6: 967-978.
47. Nateri AS, Spencer-Dene B, Behrens A. (2005). Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285.
48. Neill GW, Harrison WJ, Ikram MS, Williams TD, Bianchi LS, Nadendla SK et al. (2008). GLI1 repression ofERK activity correlates with colony formation and impaired migration in human epidermal keratinocytes. Carcinogenesis 29: 738-746.
49. Nilsson M, Unden AB, Krause D, Malmqwist U, Raza K, Zaphiropoulos PG et al. (2000). Induction ofbasal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc Natl Acad Sci USA 97: 3438-3443.
50. Panne D. (2008). The enhanceosome. Curr Opin Struct Biol 18: 236-242.
51. Pasca di Magliano M, Hebrok M. (2003). Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer 3: 903-911.
52. Pasca di Magliano M, Sekine S, Ermilov A, Ferris J, Dlugosz AA, Hebrok M. (2006). Hedgehog/Ras interactions regulate early stages of pancrea tic cancer. Genes Dev 20: 3161-3173.
53. Pearse II RV, Collier LS, Scott MP, Tabin CJ. (1999). Vertebrate homologs of Drosophila suppressor off used interact with the gli family of transcriptional regulators. Dev Biol 212: 323-336.
54. Regl G, Kasper M, Schnidar H, Eichberger T, Neill GW, Ikram MS et al. (2004a). The zinc-finger transcription factor GLI2 antagonizes contact inhibition and differentiation of human epidermal cells. Oncogene 23: 1263-1274.
55. Regl G, Kasper M, Schnidar H, Eichberger T, Neill GW, Philpott MP et al. (2004b). Activation ofthe BCL2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res 64: 7724-7731.
56. Regl G, Neill GW, Eichberger T, Kasper M, Ikram MS, Koller J et al. (2002). Human GLI2 and GLI1 are part ofa positive feedback mechanism in basal cell carcinoma. Oncogene 21: 5529-5539.
57. Riobo NA, Haines GM, Emerson Jr CP. (2006a). Protein kinase C-delta and mitogen-activated protein/extracellular signal-regulated kinase-1 control GLI activation in hedgehog signaling. Cancer Res 66: 839-845.
58. Riobo NA, Lu K, Ai X, Haines GM, Emerson Jr CP. (2006b). Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc Natl Acad Sci USA 103: 4505-4510.
59. Roessler E, Ermilov AN, Grange DK, Wang A, Grachtchouk M, Dlugosz AA et al. (2005). A previously unidentified amino-terminal domain regulates transcriptional activity ofwild-type and diseaseassociated human GLI2. Hum Mol Genet 14: 2181-2188.
60. Roth FP, Hughes JD, Estep PW, Church GM. (1998). Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation. Nat Biotechnol 16: 939-945.
61. Rubin LL, de Sauvage FJ. (2006). Targeting the Hedgehog pathway in cancer. Nat Rev Drug Discov 5: 1026-1033.
62. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J et al. (2003). A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33: 401-406.
63. Ruiz i Altaba A, Mas C, Stecca B. (2007). The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol 17: 438-447.
64. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H. (1999). Regulation ofGli2 and Gli3 activities by an amino-terminal repression domain: implication ofGli2 and Gli3 as primary mediators of Shh signaling. Development 126: 3915-3924.
65. Schaefer TS, Sanders LK, Nathans D. (1995). Cooperative transcriptional activity of Jun and Stat3 beta, a short form of Stat3. Proc Natl Acad Sci USA 92: 9097-9101.
66. Schutte J, Minna JD, Birrer MJ. (1989). Deregulated expression of human c-jun transforms primary rat embryo cells in cooperation with an activated c-Ha-ras gene and transforms rat-1a cells as a single gene. Proc Natl Acad Sci USA 86: 2257-2261.
67. Sheng H, Goich S, Wang A, Grachtchouk M, Lowe L, Mo R et al. (2002). Dissecting the oncogenic potential ofGli2: deletion ofan NH(2)-terminal fragment alters skin tumor phenotype. Cancer Res 62: 5308-5316.
68. Sibilia M, Fleischmann A, Behrens A, Stingl L, Carroll J, Watt FM et al. (2000). The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102: 211-220.
69. Smeal T, Binetruy B, Mercola D, Grover-Bardwick A, Heidecker G, Rapp UR et al. (1992). Oncoprotein-mediated signalling cascade stimulates c-Jun activity by phosphorylation ofserines 63 and 73. Mol Cell Biol 12: 3507-3513.
70. Speek M, Njunkova O, Pata I, Valdre E, Kogerman P. (2006). A potential role ofalternative splicing in the regulation ofthe transcriptional activity ofhuman GLI2 in gonadal tissues. BMC Mol Biol 7: 13.
71. Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V et al. (2007). Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci USA 104: 5895-5900.
72. Stecca B, Ruiz i Altaba A. (2002). The therapeutic potential of modulators ofthe Hedgehog-Gli signaling pathway. J Biol 1: 9.
73. Stein B, Angel P, van Dam H, Ponta H, Herrlich P, van der Eb A et al. (1992). Ultraviolet-radiation induced c-jun gene transcription: two AP-1 like binding sites mediate the response. Photochem Photobiol 55: 409-415.
74. Toualbi K, Guller MC, Mauriz JL, Labalette C, Buendia MA, Mauviel A et al. (2007). Physical and functional cooperation between AP-1 and beta-catenin for the regulation of TCF-dependent genes. Oncogene 26: 3492-3502.
75. Vezina CM, Bushman AW. (2007). Hedgehog signaling in prostate growth and benign prostate hyperplasia. Curr Urol Rep 8: 275-280. Weston CR, Davis RJ. (2007). The JNK signal transduction pathway. Curr Opin Cell Biol 19: 142-149.
76. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C et al. (1998). Activating smoothened mutations in sporadic basal-cell carcinoma. Nature 391: 90-92.
77. Yates S, Rayner TE. (2002). Transcription factor activation in response to cutaneous injury: role ofAP-1 in reepithelialization. Wound Repair Regen 10: 5-15.
78. Young MR, Li JJ, Rincon M, Flavell RA, Sathyanarayana BK, Hunziker R et al. (1999). Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc Natl Acad Sci USA 96: 9827-9832.
79. Zenz R, Scheuch H, Martin P, Frank C, Eferl R, Kenner L et al. (2003). c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev Cell 4: 879-889.
80. Zenz R, Wagner EF. (2006). Jun signalling in the epidermis: from developmental defects to psoriasis and skin tumors. Int J Biochem Cell Biol 38: 1043-1049.
81. Zhang G, Luo X, Sumithran E, Pua VS, Barnetson RS, Halliday GM et al. (2006). Squamous cell carcinoma growth in mice and in culture is regulated by c-Jun and its control ofmatrix metalloproteinase-2 and -9 expression. Oncogene 25: 7260-7266.
82. Zhao M, Qiao M, Harris SE, Chen D, Oyajobi BO, Mundy GR. (2006). The zinc finger transcription factor Gli2 mediates bone morphogenetic protein 2 expression in osteoblasts in response to hedgehog signaling. Mol Cell Biol 26: 6197-6208.