GSK-3 promotes cell survival, growth, and PAX3 levels in human melanoma cells

Molecular Cancer Research

Volumn 10, Issue 8, 2012, Pages 1065-1076

  Kubic, Jennifer D ^a   Mascarenhas, Joseph B ^a   Iizuka, Takumi ^a   Wolfgeher, Don ^a   Lang, Deborah ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR PAX3;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL GROWTH; CELL LEVEL; CELL MIGRATION; CELL PROLIFERATION; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MELANOMA CELL; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INDOLES; MALEIMIDES; MELANOMA; PAIRED BOX TRANSCRIPTION FACTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84865294455     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0387     Document Type: Article

References (48)

1. Doble BW, Woodgett JR. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003;116:1175-86.
2. Woodgett JR. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 1990;9:2431-8.
3. Yao HB, Shaw PC, Wong CC, Wan DC. Expression of glycogen synthase kinase-3 isoforms in mouse tissues and their transcription in the brain. J Chem Neuroanat 2002;23:291-7.
4. Lau KF, Miller CC, Anderton BH, Shaw PC. Expression analysis of glycogen synthase kinase-3 in human tissues. J Pept Res 1999;54:85-91.
5. Sutherland C, Leighton IA, Cohen P. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem J 1993;296:15-9.
6. Sutherland C, Cohen P. The alpha-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase orMAPkinase- activated protein kinase-1 in vitro. FEBS Lett 1994;338:37-42.
7. Ding VW, Chen RH, McCormick F. Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 2000;275:32475-81.
8. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR. Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series ofembryonic stem cell lines. Dev Cell 2007;12:957-71.
9. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000;406:86-90.
10. Liu KJ, Arron JR, Stankunas K, Crabtree GR, Longaker MT. Chemical rescue of cleft palate and midline defects in conditional GSK-3beta mice. Nature 2007;446:79-82.
11. Kerkela R, Kockeritz L, Macaulay K, Zho J, Doble BW, Beahm C, et al. Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J Clin Invest 2008;118:3609-18.
12. MacAulay K, Doble BW, Patel S, Hansotia T, Sinclair EM, Drucker DJ, et al. Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell Metab 2007;6:329-37.
13. Chien AJ, Moore EC, Lonsdorf AS, Kulikauskas RM, Rothberg BG, Berger AJ, et al. Activated Wnt/beta-catenin signaling in melanoma is associated with decreased proliferation in patient tumors and a murine melanoma model. Proc Natl Acad Sci U S A 2009;106:1193-8.
14. Panka DJ, Cho DC, Atkins MB, Mier JW. GSK-3beta inhibition enhances sorafenib-induced apoptosis in melanoma cell lines. J Biol Chem 2008;283:726-32.
15. Bellei B, Flori E, Izzo E, Maresca V, Picardo M. GSK3beta inhibition promotes melanogenesis in mouse B16 melanoma cells and normal human melanocytes. Cell Signal 2008;20:1750-61.
16. Jin EJ, Erickson CA, Takada S, Burrus LW. Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev Biol 2001;233:22-37.
17. Watanabe A, Takeda K, Ploplis B, Tachibana M. Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat Genet 1998;18:283-6.
18. Lang D, Lu MM, Huang L, Engleka KA, Zhang M, Chu EY, et al. Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 2005;433:884-7.
19. Hornyak T, Hayes D, Chiu L-Y, Ziff E. Transcription factors in melanocyte development: distinct roles for Pax-3 and Mitf. Mech Dev 2001;101:47-59.
20. Scholl FA, Kamarashev J, Murmann OV, Geertsen R, Dummer R, Schafer BW. PAX3 is expressed in human melanomas and contributes to tumor cell survival. Cancer Res 2001;61:823-6.
21. Plummer RS, Shea CR, Nelson M, Powell SK, Freeman DM, Dan CP, et al. PAX3 expression in primary melanomas and nevi. Mod Pathol 2008;21:525-30.
22. Mascarenhas JB, Littlejohn EL, Wolsky RJ, Young KP, Nelson M, Salgia R, et al. PAX3 and SOX10 activate MET receptor expression in melanoma. Pigment Cell Melanoma Res 2010;23:225-37.
23. Natali PG, Nicotra MR, Di Renzo MF, Di Renzo MF, Prat M, Bigotti A, et al. Expression of the c-Met/HGF receptor in human melanocytic neoplasms: demonstration of the relationship to malignant melanoma tumour progression. Br J Cancer 1993;68:746-50.
24. He SJ, Stevens G, Braithwaite AW, Eccles MR. Transfection of melanoma cells with antisense PAX3 oligonucleotides additively complements cisplatin-induced cytotoxicity. Mol Cancer Ther 2005;4:996-1003.
25. Amstutz R, Wachtel M, Troxler H, Kleinert P, Ebauer M, Haneke T, et al. Phosphorylation regulates transcriptional activity of PAX3/FKHR and reveals novel therapeutic possibilities. Cancer Res 2008;68:3767-76.
26. Miller PJ, Hollenbach AD. The oncogenic fusion protein Pax3-FKHR has a greater post-translational stability relative to Pax3 during early myogenesis. Biochim Biophys Acta 2007;1770:1450-8.
27. Miller PJ, Dietz KN, Hollenbach AD. Identification of serine 205 as a site of phosphorylation on Pax3 in proliferating but not differentiating primary myoblasts. Protein Sci 2008;17:1979-86.
28. Dietz KN, Miller PJ, Hollenbach AD. Phosphorylation of serine 205 by the protein kinase CK2 persists on Pax3-FOXO1, but not Pax3, throughout early myogenic differentiation. Biochemistry 2009;48:11786-95.
29. Dietz KN, Miller PJ, Iyengar AS, Loupe JM, Hollenbach AD. Identification of serines 201 and 209 as sites of Pax3 phosphorylation and the altered phosphorylation status of Pax3-FOXO1 during early myogenic differentiation. Int J Biochem Cell Biol 2011;43:936-45.
30. He X, Saint-Jeannet JP, Woodgett JR, Varmus HE, Dawid IB. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 1995;374:617-22.
31. Lang D, Epstein JA. Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum Mol Genet 2003;12:937-45.
32. Coghlan MP, Culbert AA, Cross DA, Corcoran SL, Yates JW, Pearce NJ, et al. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem Biol 2000;7:793-803.
33. Fiol CJ, Wang A, Roeske RW, Roach PJ. Ordered multisite protein phosphorylation. Analysis of glycogen synthase kinase 3 action using model peptide substrates. J Biol Chem 1990;265:6061-5.
34. Hagen T, Di Daniel E, Culbert AA, Reith AD. Expression and characterization of GSK-3 mutants and their effect on beta-catenin phosphorylation in intact cells. J Biol Chem 2002;277:23330-5.
35. Kubic JD, Young KP, Plummer RS, Ludvik AE, Lang D. Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res 2008;21:627-45.
36. Turenne GA, Price BD. Glycogen synthase kinase3 beta phosphorylates serine 33 of p53 and activates p530s transcriptional activity. BMC Cell Biol 2001;2:12.
37. Ougolkov AV, Fernandez-Zapico ME, Bilim VN, Smyrk TC, Chari ST, Billadeau DD. Aberrant nuclear accumulation of glycogen synthase kinase-3beta in human pancreatic cancer: association with kinase activity and tumor dedifferentiation. Clin Cancer Res 2006;12:5074-81.
38. Ougolkov AV, Fernandez-Zapico ME, Savoy DN, Urrutia RA, Billadeau DD. Glycogen synthase kinase-3beta participates in nuclear factor kappaB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res 2005;65:2076-81.
39. Bilim V, Ougolkov A, Yuuki K, Naito D, Kawazoe H, Muto A, et al. Glycogen synthase kinase-3: a new therapeutic target in renal cell carcinoma. Br J Cancer 2009;101:2005-14.
40. Romero-Graillet C, Aberdam E, Clement M, Ortonne JP, Ballotti R. Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J Clin Invest 1997;99:635-42.
41. Phelan SA, Ito M, Loeken MR. Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis. Diabetes 1997;46:1189-97.
42. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 1997;16:3797-804.
43. Tsuchiya K, Nakamura T, Okamoto R, Kanai T, Watanabe M. Reciprocal targeting of Hath1 and beta-catenin by Wnt glycogen synthase kinase 3beta in human colon cancer. Gastroenterology 2007;132:208-20.
44. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 2005;438:873-7.
45. Takeda K, Takemoto C, Kobayashi I, Watanabe A, Nobukuni Y, Fisher DE, et al. Ser298 of MITF, a mutation site in Waardenburg syndrome type 2, is a phosphorylation site with functional significance. Hum Mol Genet 2000;9:125-32.
46. Barr FG, Galili N, Holick J, Biegel JA, Rovera G, Emanuel BS. Rearrangement of the PAX3 paired box gene in the paediatric solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;3:113-7.
47. Boutet SC, Disatnik MH, Chan LS, Iori K, Rando TA. Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 2007;130:349-62.
48. Olsten ME, Litchfield DW. Order or chaos? An evaluation of the regulation of protein kinase CK2. Biochem Cell Biol 2004;82:681-93.