Regulation of c-Myc Protein Abundance by a Protein Phosphatase 2A-Glycogen Synthase Kinase 3β-Negative Feedback Pathway

Genes and Cancer

Volumn 3, Issue 1, 2012, Pages 23-36

  Liu, Lingfeng ^a   Eisenman, Robert N ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

degradation; GSK3 ; Myc; phosphorylation; PP2A

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MYC PROTEIN; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A B SUBUNIT 56 DELTA; SERINE; SMALL INTERFERING RNA; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PPP2R5D GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; TRANSCRIPTION REGULATION;

EID: 84868671065     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601912448067     Document Type: Article

References (69)

1. Eilers M,Eisenman RN.Myc's broad reach.Genes Dev. 2008;22:2755-66.
2. Meyer N,Penn LZ.Reflecting on 25 years with MYC.Nat Rev Cancer. 2008;8:976-90.
3. Dominguez-Sola D,Ying CY,Grandori C,et al.Non-transcriptional control of DNA replication by c-Myc.Nature. 2007;448:445-51.
4. Conacci-Sorrell M,Ngouenet C,Eisenman RN.Myc-nick: a cytoplasmic cleavage product of Myc that promotes alpha-tubulin acetylation and cell differentiation.Cell. 2010;142:480-93.
5. Liu J,Levens D.Making Myc.Curr Top Microbiol Immunol. 2006;302:1-32.
6. Levens D.You don't muck with MYC.Genes Cancer. 2010;1:547-54.
7. Vita M,Henriksson M.The Myc oncoprotein as a therapeutic target for human cancer.Semin Cancer Biol. 2006;16:318-30.
8. Kim SY,Herbst A,Tworkowski KA,Salghetti SE,Tansey WP.Skp2 regulates myc protein stability and activity.Mol Cell. 2003;11:1177-88.
9. von der Lehr N,Johansson S,Wu S,et al.The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription.Mol Cell. 2003;11:1189-200.
10. Moberg KH,Mukherjee A,Veraksa A,Artavanis-Tsakonas S,Hariharan IK.The Drosophila F box protein archipelago regulates dMyc protein levels in vivo.Curr Biol. 2004;14:965-74.
11. Welcker M,Orian A,Grim JA,Eisenman RN,Clurman BE.A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size.Curr Biol. 2004;14:1852-7.
12. Yada M,Hatakeyama S,Kamura T,et al.Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7.EMBO J. 2004;23:2116-25.
13. Zhao X,Heng JI,Guardavaccaro D,et al.The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein.Nat Cell Biol. 2008;10:643-53.
14. Choi SH,Wright JB,Gerber SA,Cole MD.Myc protein is stabilized by suppression of a novel E3 ligase complex in cancer cells.Genes Dev. 2010;24:1236-41.
15. Malempati S,Tibbitts D,Cunningham M,et al.Aberrant stabilization of c-Myc protein in some lymphoblastic leukemias.Leukemia. 2006;20:1572-81.
16. Cohn SL,Salwen H,Quasney MW,et al.Prolonged N-myc protein half-life in a neuroblastoma cell line lacking N-myc amplification.Oncogene. 1990;5:1821-7.
17. Gregory MA,Hann SR.c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells.Mol Cell Biol. 2000;20:2423-35.
18. Zhang X,Farrell AS,Daniel CJ,et al.Mechanistic insight into Myc stabilization in breast cancer involving aberrant Axin1 expression.Proc Natl Acad Sci U S A. 2011;109:2790-5.
19. Salghetti SE,Muratani M,Wijnen H,Futcher B,Tansey WP.Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis.Proc Natl Acad Sci U S A. 2000;97:3118-23.
20. Sears R,Nuckolls F,Haura E,Taya Y,Tamai K,Nevins JR.Multiple ras-dependent phosphorylation pathways regulate myc protein stability.Genes Dev. 2000;14:2501-14.
21. Sears R,Leone G,DeGregori J,Nevins JR.Ras enhances Myc protein stability.Mol Cell. 1999;3:169-79.
22. Welcker M,Orian A,Jin J,et al.The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation.Proc Natl Acad Sci U S A. 2004;101:9085-90.
23. Sjostrom SK,Finn G,Hahn WC,Rowitch DH,Kenney AM.The Cdk1 complex plays a prime role in regulating N-myc phosphorylation and turnover in neural precursors.Dev Cell. 2005;9:327-38.
24. Frame S,Cohen P.GSK3 takes centre stage more than 20 years after its discovery.Biochem J. 2001;359:1-16.
25. Doble BW,Woodgett JR.GSK-3: tricks of the trade for a multi-tasking kinase.J Cell Sci. 2003;116:1175-86.
26. Cross DA,Alessi DR,Cohen P,Andjelkovich M,Hemmings BA.Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B.Nature. 1995;378:785-9.
27. Frame S,Cohen P,Biondi RM.A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation.Mol Cell. 2001;7:1321-7.
28. Arnold HK,Zhang X,Daniel CJ,et al.The Axin1 scaffold protein promotes formation of a degradation complex for c-Myc.EMBO J. 2009;28:500-12.
29. Virshup DM,Shenolikar S.From promiscuity to precision: protein phosphatases get a makeover.Mol Cell. 2009;33:537-45.
30. Yeh E,Cunningham M,Arnold H,et al.A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells.Nat Cell Biol. 2004;6:308-18.
31. Arnold HK,Sears RC.Protein phosphatase 2A regulatory subunit B56alpha associates with c-myc and negatively regulates c-myc accumulation.Mol Cell Biol. 2006;26:2832-44.
32. Schuhmacher M,Kohlhuber F,Holzel M,et al.The transcriptional program of a human B cell line in response to myc.Nucleic Acids Res. 2001;29:397-406.
33. Schuhmacher M,Staege MS,Pajic A,et al.Control of cell growth by c-Myc in the absence of cell division.Curr Biol. 1999;9:1255-8.
34. Cross SM,Sanchez CA,Morgan CA,et al.A p53-dependent mouse spindle checkpoint.Science. 1995;267:1353-6.
35. Yu JS,Yang SD.Protein kinase FA/glycogen synthase kinase-3 predominantly phosphorylates the in vivo site Thr97-Pro in brain myelin basic protein: evidence for Thr-Pro and Ser-Arg-X-X-Ser as consensus sequence motifs.J Neurochem. 1994;62:1596-603.
36. Meijer L,Skaltsounis AL,Magiatis P,et al.GSK-3-selective inhibitors derived from Tyrian purple indirubins.Chem Biol. 2003;10:1255-66.
37. Maurer U,Charvet C,Wagman AS,Dejardin E,Green DR.Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1.Mol Cell. 2006;21:749-60.
38. Rossig L,Badorff C,Holzmann Y,Zeiher AM,Dimmeler S.Glycogen synthase kinase-3 couples AKT-dependent signaling to the regulation of p21Cip1 degradation.J Biol Chem. 2002;277:9684-9.
39. Ivaska J,Nissinen L,Immonen N,Eriksson JE,Kahari VM,Heino J.Integrin alpha 2 beta 1 promotes activation of protein phosphatase 2A and dephosphorylation of Akt and glycogen synthase kinase 3 beta.Mol Cell Biol. 2002;22:1352-9.
40. Lin CF,Chen CL,Chiang CW,Jan MS,Huang WC,Lin YS.GSK-3beta acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis.J Cell Sci. 2007;120:2935-43.
41. Cohen P,Holmes CFB,Tsukitani Y.Okadaic acid: a new probe for the study of cellular regulation.Trends Biochem Sci. 1990;15:98-102.
42. Eilers M,Picard D,Yamamoto KR,Bishop JM.Chimeras of Myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells.Nature. 1989;340:66-8.
43. Littlewood TD,Hancock DC,Danielian PS,Parker MG,Evan GI.A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins.Nucleic Acids Res. 1995;23:1686-90.
44. Li X,Yost HJ,Virshup DM,Seeling JM.Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus.EMBO J. 2001;20:4122-31.
45. Mora A,Sabio G,Gonzalez-Polo RA,et al.Lithium inhibits caspase 3 activation and dephosphorylation of PKB and GSK3 induced by K+ deprivation in cerebellar granule cells.J Neurochem. 2001;78:199-206.
46. Lee YI,Seo M,Kim Y,et al.Membrane depolarization induces the undulating phosphorylation/dephosphorylation of glycogen synthase kinase 3beta, and this dephosphorylation involves protein phosphatases 2A and 2B in SH-SY5Y human neuroblastoma cells.J Biol Chem. 2005;280:22044-52.
47. Hill JJ,Callaghan DA,Ding W,Kelly JF,Chakravarthy BR.Identification of okadaic acid-induced phosphorylation events by a mass spectrometry approach.Biochem Biophys Res Commun. 2006;342:791-9.
48. Goedert M,Jakes R,Qi Z,Wang JH,Cohen P.Protein phosphatase 2A is the major enzyme in brain that dephosphorylates tau protein phosphorylated by proline-directed protein kinases or cyclic AMP-dependent protein kinase.J Neurochem. 1995;65:2804-7.
49. Seeling JM,Miller JR,Gil R,Moon RT,White R,Virshup DM.Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A.Science. 1999;283:2089-91.
50. Virshup DM.Protein phosphatase 2A: a panoply of enzymes.Curr Opin Cell Biol. 2000;12:180-5.
51. Xu Y,Xing Y,Chen Y,et al.Structure of the protein phosphatase 2A holoenzyme.Cell. 2006;127:1239-51.
52. Sontag E.Protein phosphatase 2A: the Trojan Horse of cellular signaling.Cell Signal. 2001;13:7-16.
53. McCright B,Rivers AM,Audlin S,Virshup DM.The B56 family of protein phosphatase 2A (PP2A) regulatory subunits encodes differentiation-induced phosphoproteins that target PP2A to both nucleus and cytoplasm.J Biol Chem. 1996;271:22081-9.
54. McCright B,Brothman AR,Virshup DM.Assignment of human protein phosphatase 2A regulatory subunit genes b56alpha, b56beta, b56gamma, b56delta, and b56epsilon (PPP2R5A-PPP2R5E), highly expressed in muscle and brain, to chromosome regions 1q41, 11q12, 3p21, 6p21.1, and 7p11.2 --> p12.Genomics. 1996;36:168-70.
55. Blackwood EM,Eisenman RN.Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA binding complex with Myc.Science. 1991;251:1211-7.
56. Amati B.Myc degradation: dancing with ubiquitin ligases.Proc Natl Acad Sci U S A. 2004;101:8843-4.
57. Westermarck J,Hahn WC.Multiple pathways regulated by the tumor suppressor PP2A in transformation.Trends Mol Med. 2008;14:152-60.
58. Batut J,Schmierer B,Cao J,Raftery LA,Hill CS,Howell M.Two highly related regulatory subunits of PP2A exert opposite effects on TGF-beta/activin/nodal signalling.Development. 2008;135:2927-37.
59. Kapfhamer D,Berger KH,Hopf FW,et al.Protein phosphatase 2a and glycogen synthase kinase 3 signaling modulate prepulse inhibition of the acoustic startle response by altering cortical M-Type potassium channel activity.J Neurosci. 2010;30:8830-40.
60. Junttila MR,Puustinen P,Niemela M,et al.CIP2A inhibits PP2A in human malignancies.Cell. 2007;130:51-62.
61. Gregory MA,Qi Y,Hann SR.Phosphorylation by glycogen synthase kinase-3 controls c-Myc proteolysis and subnuclear localization.J Biol Chem. 2003;278:51606-12.
62. Cartwright P,McLean C,Sheppard A,Rivett D,Jones K,Dalton S.LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism.Development. 2005;132:885-96.
63. Mannava S,Omilian AR,Wawrzyniak JA,et al.PP2A-B56alpha controls oncogene-induced senescence in normal and tumor human melanocytic cells.Oncogene. 2012;31:1484-92.
64. Kerosuo L,Fox H,Perala N,et al.CIP2A increases self-renewal and is linked to Myc in neural progenitor cells.Differentiation. 2010;80:68-77.
65. Khanna A,Bockelman C,Hemmes A,et al.MYC-dependent regulation and prognostic role of CIP2A in gastric cancer.J Natl Cancer Inst. 2009;101:793-805.
66. Cegielska A,Shaffer S,Derua R,Goris J,Virshup DM.Different oligomeric forms of protein phosphatase 2A activate and inhibit simian virus 40 DNA replication.Mol Cell Biol. 1994;14:4616-23.
67. Klockenbusch C,Kast J.Optimization of formaldehyde cross-linking for protein interaction analysis of non-tagged integrin beta1.J Biomed Biotechnol. 2010;2010:927585.
68. Aljanabi SM,Martinez I.Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques.Nucleic Acids Res. 1997;25:4692-3.
69. Heckman KL,Pease LR.Gene splicing and mutagenesis by PCR-driven overlap extension.Nat Protoc. 2007;2:924-32.