Protein phosphatase 2A and rapamycin regulate the nuclear localization and activity of the transcription factor GLI3

Cancer Research

Volumn 68, Issue 12, 2008, Pages 4658-4665

  Krauß, Sybille ^a,b   Foerster, John ^d   Schneider, Rainer ^b,c   Schweiger, Susann ^b,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d NINEWELLS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN PHOSPHATASE 2A; RAPAMYCIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; CYCLIN D; CYCLINE; ENHANCED GREEN FLUORESCENT PROTEIN; G PROTEIN COUPLED RECEPTOR; GLI1 PROTEIN, HUMAN; GLI2 PROTEIN, HUMAN; GLI3 PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; IGBP1 PROTEIN, HUMAN; IMMUNOSUPPRESSIVE AGENT; KRUPPEL LIKE FACTOR; MESSENGER RNA; MTORC1 PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2; SHH PROTEIN, HUMAN; SIGNAL PEPTIDE; TASTE RECEPTORS, TYPE 2; TRANSCRIPTION FACTOR;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION; CELL CULTURE; CELL FRACTIONATION; CELL NUCLEUS; CYTOSOL; DRUG ANTAGONISM; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

CELL NUCLEUS; CYCLINS; CYTOSOL; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NEOPLASMS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEIN PHOSPHATASE 2; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 49649085367     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-6174     Document Type: Article

References (49)

1. Wetmore C. Sonic hedgehog in normal and neoplastic proliferation: insight gained from human tumors and animal models. Curr Opin Genet Dev 2003;13:34-42.
2. Berman DM, Karhadkar SS, Maitra A, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003;425:846-51.
3. Watkins DN, Berman DM, Burkholder SG, Wang B, Beachy PA, Baylin SB. Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 2003;422:313-7.
4. Thayer SP, di Magliano MP, Heiser PW, et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003;425:851-6.
5. Sanchez P, Hernandez AM, Stecca B, et al. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci U S A 2004;101:12561-6.
6. Murone M, Rosenthal A, de Sauvage FJ. Hedgehog signal transduction: from flies to vertebrates. Exp Cell Res 1999;253:25-33.
7. Jacob J, Briscoe J. Gli proteins and the control of spinal-cord patterning. EMBO Rep 2003;4:761-5.
8. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J Biol Chem 1999;274:8143-52.
9. Janssens V, Goris J, Van Hoof C. PP2A: the expected tumor suppressor. Curr Opin Genet Dev 2005;15:34-41.
10. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell 2000;103:253-62.
11. Yang Q, Guan KL. Expanding mTOR signaling. Cell Res 2007;17:666-81.
12. Goldberg Y. Protein phosphatase 2A: who shall regulate the regulator? Biochem Pharmacol 1999;57:321-8.
13. Trockenbacher A, Suckow V, Foerster J, et al. MID1, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation. Nat Genet 2001;29:287-94.
14. Bjornsti MA, Houghton PJ. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004;4:335-48.
15. Peterson RT, Desai BN, Hardwick JS, Schreiber SL. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycinassociated protein. PNAS 1999;96:4438-42.
16. + (α4) is associated with a rapamycin-sensitive signal transduction in lymphocytes through direct binding to the catalytic subunit of protein phosphatase 2A. Blood 1998;92:539-46.
17. Nanahoshi M, Nishiuma T, Tsujishita Y, et al. Regulation of protein phosphatase 2A catalytic activity by α4 protein and its yeast homolog Tap42. Biochem Biophys Res Commun 1998;251:520.
18. Murata K, Wu J, Brautigan DL. B cell receptor-associated protein α4 displays rapamycin-sensitive binding directly to the catalytic subunit of protein phosphatase 2A. Proc Natl Acad Sci U S A 1997;94:10624-9.
19. Hartley D, Cooper GM. Role of mTOR in the degradation of IRS-1: regulation of PP2A activity. J Cell Biochem 2002;85:304-14.
20. Mill P, Mo R, Hu MC, Dagnino L, Rosenblum ND, Hui CC. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev Cell 2005;9:293-303.
21. Li Y, Zhang H, Choi SC, Litingtung Y, Chiang C. Sonic hedgehog signaling regulates Gli3 processing, mesenchymal proliferation, and differentiation during mouse lung organogenesis. Dev Biol 2004;270:214-31.
22. Hu MC, Mo R, Bhella S, et al. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 2006;133:569-78.
23. Weaver M, Batts L, Hogan BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 2003;258:169-84.
24. Walsh AH, Cheng A, Honkanen RE. Fostriecin, an antitumor antibiotic with inhibitory activity against serine/threonine protein phosphatases types 1 (PP1) and 2A (PP2A), is highly selective for PP2A. FEBS Lett 1997;416:230-4.
25. Kong M, Fox CJ, Mu J, et al. The PP2A-associated protein α4 is an essential inhibitor of apoptosis. Science 2004;306:695-8.
26. Donahue AC, Fruman DA. Distinct signaling mechanisms activate the target of rapamycin in response to different B-cell stimuli. Eur J Immunol 2007;37:2923-36.
27. Wyeth. Summary of product characteristics-rapamune: Wyeth Europe Ltd.; 2001.
28. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999;126:3915-24.
29. Bai CB, Joyner AL. Gli1 can rescue the in vivo function of Gli2. Development 2001;128:5161-72.
30. Wang B, Fallon JF, Beachy PA. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 2000;100:423-34.
31. Aza-Blanc P, Lin HY, Ruiz i Altaba A, Kornberg TB. Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 2000;127:4293-301.
32. Buttitta L, Mo R, Hui CC, Fan CM. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 2003;130:6233-43.
33. Vanderlaan G, Tyurina OV, Karlstrom RO, Chandrasekhar A. Gli function is essential for motor neuron induction in zebrafish. Dev Biol 2005;282:550-70.
34. Karim R, Tse G, Putti T, Scolyer R, Lee S. The significance of the Wnt pathway in the pathology of human cancers. Pathology 2004;36:120-8.
35. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS, Jr. NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 1999;19:5785-99.
36. Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, Strauss M. NF-κB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol Cell Biol 1999;19:2690-8.
37. Joyce D, Bouzahzah B, Fu M, et al. Integration of Rac-dependent regulation of cyclin D1 transcription through a nuclear factor-κB- dependent pathway. J Biol Chem 1999;274:25245-9.
38. von Wichert G, Haeussler U, Greten FR, et al. Regulation of cyclin D1 expression by autocrine IGF-I in human BON neuroendocrine tumour cells. Oncogene 2005;24:1284-9.
39. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001;20:2390-400.
40. Li Y, Zhang H, Choi SC, Litingtung Y, Chiang C. Sonic hedgehog signaling regulates Gli3 processing, mesenchymal proliferation, and differentiation during mouse lung organogenesis. Dev Biol 2004;270:214.
41. Mill P, Mo R, Hu MC, Dagnino L, Rosenblum ND, Hui C-c. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev Cell 2005;9:293.
42. Frost P, Shi Y, Hoang B, Lichtenstein A. AKT activity regulates the ability of mTOR inhibitors to prevent angiogenesis and VEGF expression in multiple myeloma cells. Oncogene 2006;26:2255-62.
43. Guba M, von Breitenbuch P, Steinbauer M, et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med 2002;8:128-35.
44. Marx SO, Jayaraman T, Go LO, Marks AR. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ Res 1995;76:412-7.
45. Costa LJ. Aspects of mTOR biology and the use of mTOR inhibitors in non-Hodgkin's lymphoma. Cancer Treat Rev 2007;33:78-84.
46. Hashemolhosseini S, Nagamine Y, Morley SJ, Desrivieres S, Mercep L, Ferrari S. Rapamycin inhibition of the G1 to S transition is mediated by effects on cyclin D1 mRNA and protein stability. J Biol Chem 1998;273:14424-9.
47. Ong CT, Khoo YT, Mukhopadhyay A, et al. mTOR as a potential therapeutic target for treatment of keloids and excessive scars. Exp Dermatol 2007;16:394-404.
48. Chen W, Possemato R, Campbell KT, Plattner CA, Pallas DC, Hahn WC. Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 2004;5:127-36.
49. Tsuchiya A, Tashiro E, Yoshida M, Imoto M. Involvement of protein phosphatase 2A nuclear accumulation and subsequent inactivation of activator protein-1 in leptomycin B-inhibited cyclin D1 expression. Oncogene 2007;26:1522-32.