Non-Canonical Smads Phosphorylation Induced by the Glutamate Release Inhibitor, Riluzole, through GSK3 Activation in Melanoma

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Abushahba, Walid ^a   Olabisi, Oyenike O ^a   Jeong, Byeong Seon ^a   Boregowda, Rajeev K ^a   Wen, Yu ^a   Liu, Fang ^b   Goydos, James S ^a   Lasfar, Ahmed ^c   Cohen Solal, Karine A ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; METABOTROPIC RECEPTOR 1; PROTEIN KINASE B; RILUZOLE; SERINE; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; IN VITRO STUDY; INHBB GENE; MELANOMA; PLAU GENE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR CELL LINE; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MELANOMA; MICE; PHOSPHORYLATION; RILUZOLE; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS; UP-REGULATION;

EID: 84867413455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047312     Document Type: Article

References (61)

1. Javelaud D, Alexaki VI, Mauviel A, (2008) Transforming growth factor-beta in cutaneous melanoma. Pigment Cell Melanoma Res 21: 123-132.
2. Lasfar A, Cohen-Solal KA, (2010) Resistance to transforming growth factor beta-mediated tumor suppression in melanoma: are multiple mechanisms in place? Carcinogenesis 31: 1710-1717.
3. Abdollah S, Macias-Silva M, Tsukazaki T, Hayashi H, Attisano L, et al. (1997) TbetaRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling. J Biol Chem 272: 27678-27685.
4. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, et al. (1997) TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. Embo J 16: 5353-5362.
5. Souchelnytskyi S, Tamaki K, Engstrom U, Wernstedt C, ten Dijke P, et al. (1997) Phosphorylation of Ser465 and Ser467 in the C terminus of Smad2 mediates interaction with Smad4 and is required for transforming growth factor-beta signaling. J Biol Chem 272: 28107-28115.
6. Massague J, (2008) TGFbeta in Cancer. Cell 134: 215-230.
7. Siegel PM, Massague J, (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3: 807-821.
8. Alarcon C, Zaromytidou AI, Xi Q, Gao S, Yu J, et al. (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139: 757-769.
9. Chen D, Lin Q, Box N, Roop D, Ishii S, et al. (2009) SKI knockdown inhibits human melanoma tumor growth in vivo. Pigment Cell Melanoma Res 22: 761-772.
10. Cohen-Solal KA, Merrigan KT, Chan JL, Goydos JS, Chen W, et al. (2011) Constitutive Smad linker phosphorylation in melanoma: a mechanism of resistance to transforming growth factor-beta-mediated growth inhibition. Pigment Cell Melanoma Res 24: 512-524.
11. Gao S, Alarcon C, Sapkota G, Rahman S, Chen PY, et al. (2009) Ubiquitin ligase Nedd4L targets activated Smad2/3 to limit TGF-beta signaling. Mol Cell 36: 457-468.
12. Kamaraju AK, Roberts AB, (2005) Role of Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-beta-mediated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J Biol Chem 280: 1024-1036.
13. Kretzschmar M, Doody J, Timokhina I, Massague J, (1999) A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev 13: 804-816.
14. Liu F, (2006) Smad3 phosphorylation by cyclin-dependent kinases. Cytokine Growth Factor Rev 17: 9-17.
15. Matsuura I, Denissova NG, Wang G, He D, Long J, et al. (2004) Cyclin-dependent kinases regulate the antiproliferative function of Smads. Nature 430: 226-231.
16. Matsuura I, Wang G, He D, Liu F, (2005) Identification and characterization of ERK MAP kinase phosphorylation sites in Smad3. Biochemistry 44: 12546-12553.
17. Millet C, Yamashita M, Heller M, Yu LR, Veenstra TD, et al. (2009) A negative feedback control of transforming growth factor-beta signaling by glycogen synthase kinase 3-mediated Smad3 linker phosphorylation at Ser-204. J Biol Chem 284: 19808-19816.
18. Mori S, Matsuzaki K, Yoshida K, Furukawa F, Tahashi Y, et al. (2004) TGF-beta and HGF transmit the signals through JNK-dependent Smad2/3 phosphorylation at the linker regions. Oncogene 23: 7416-7429.
19. Sekimoto G, Matsuzaki K, Yoshida K, Mori S, Murata M, et al. (2007) Reversible Smad-dependent signaling between tumor suppression and oncogenesis. Cancer Res 67: 5090-5096.
20. Wang G, Matsuura I, He D, Liu F, (2009) Transforming growth factor-beta-inducible phosphorylation of Smad3. J Biol Chem 284: 9663-9673.
21. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 378: 785-789.
22. Bellingham MC, (2011) A review of the neural mechanisms of action and clinical efficiency of riluzole in treating amyotrophic lateral sclerosis: what have we learned in the last decade? CNS Neurosci Ther 17: 4-31.
23. Lee HJ, Wall BA, Wangari-Talbot J, Shin SS, Rosenberg S, et al. (2011) Glutamatergic Pathway Targeting in Melanoma: Single-Agent and Combinatorial Therapies. Clin Cancer Res 17: 7080-7092.
24. Namkoong J, Shin SS, Lee HJ, Marin YE, Wall BA, et al. (2007) Metabotropic glutamate receptor 1 and glutamate signaling in human melanoma. Cancer Res 67: 2298-2305.
25. Le MN, Chan JL, Rosenberg SA, Nabatian AS, Merrigan KT, et al. (2010) The glutamate release inhibitor Riluzole decreases migration, invasion, and proliferation of melanoma cells. J Invest Dermatol 130: 2240-2249.
26. Mehnert JM, Wen Y, Lee JH, Dudek L, Pruski-Clark L, et al. (2011) A phase II trial of riluzole, an antagonist of metabotropic glutamate receptor (GRM1) signaling, in advanced melanoma; Paper presented at: 2011 Annual Meeting of ASCO (American Society of Clinical Oncology) (Chicago).
27. Yip D, Le MN, Chan JL, Lee JH, Mehnert JA, et al. (2009) A phase 0 trial of riluzole in patients with resectable stage III and IV melanoma. Clin Cancer Res 15: 3896-3902.
28. Pollock PM, Cohen-Solal K, Sood R, Namkoong J, Martino JJ, et al. (2003) Melanoma mouse model implicates metabotropic glutamate signaling in melanocytic neoplasia. Nat Genet 34: 108-112.
29. Satyamoorthy K, Li G, Gerrero MR, Brose MS, Volpe P, et al. (2003) Constitutive mitogen-activated protein kinase activation in melanoma is mediated by both BRAF mutations and autocrine growth factor stimulation. Cancer Res 63: 756-759.
30. Welch DR, Bisi JE, Miller BE, Conaway D, Seftor EA, et al. (1991) Characterization of a highly invasive and spontaneously metastatic human malignant melanoma cell line. Int J Cancer 47: 227-237.
31. Bittner M, Meltzer P, Chen Y, Jiang Y, Seftor E, et al. (2000) Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 406: 536-540.
32. Carlson BA, Dubay MM, Sausville EA, Brizuela L, Worland PJ, (1996) Flavopiridol induces G1 arrest with inhibition of cyclin-dependent kinase (CDK) 2 and CDK4 in human breast carcinoma cells. Cancer Res 56: 2973-2978.
33. Rizzolio F, Tuccinardi T, Caligiuri I, Lucchetti C, Giordano A, (2010) CDK inhibitors: from the bench to clinical trials. Curr Drug Targets 11: 279-290.
34. Sedlacek HH, (2001) Mechanisms of action of flavopiridol. Crit Rev Oncol Hematol 38: 139-170.
35. Chu XJ, DePinto W, Bartkovitz D, So SS, Vu BT, et al. (2006) Discovery of [4-Amino-2-(1-methanesulfonylpiperidin-4-ylamino)pyrimidin-5-yl](2,3-diflu oro-6- methoxyphenyl)methanone (R547), a potent and selective cyclin-dependent kinase inhibitor with significant in vivo antitumor activity. Journal of Medicinal Chemistry 49: 6549-6560.
36. DePinto W, Chu XJ, Yin X, Smith M, Packman K, et al. (2006) In vitro and in vivo activity of R547: a potent and selective cyclin-dependent kinase inhibitor currently in phase I clinical trials. Mol Cancer Ther 5: 2644-2658.
37. Tighe A, Ray-Sinha A, Staples OD, Taylor SS, (2007) GSK-3 inhibitors induce chromosome instability. BMC Cell Biology 8: 34.
38. Polakis P, (1999) The oncogenic activation of beta-catenin. Curr Opin Genet Dev 9: 15-21.
39. Yost C, Torres M, Miller JR, Huang E, Kimelman D, et al. (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10: 1443-1454.
40. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, et al. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
41. Ohtani Y, Harada T, Funasaka Y, Nakao K, Takahara C, et al. (2008) Metabotropic glutamate receptor subtype-1 is essential for in vivo growth of melanoma. Oncogene 27: 7162-7170.
42. Khan AJ, Wall B, Ahlawat S, Green C, Schiff D, et al. (2011) Riluzole enhances ionizing radiation-induced cytotoxicity in human melanoma cells that ectopically express metabotropic glutamate receptor 1 in vitro and in vivo. Clin Cancer Res 17: 1807-1814.
43. Choi KY, Chang K, Pickel JM, Badger JD 2nd, Roche KW (2011) Expression of the metabotropic glutamate receptor 5 (mGluR5) induces melanoma in transgenic mice. Proc Natl Acad Sci U S A 108: 15219-15224.
44. Prickett TD, Wei X, Cardenas-Navia I, Teer JK, Lin JC, et al. (2011) Exon capture analysis of G protein-coupled receptors identifies activating mutations in GRM3 in melanoma. Nat Genet 43: 1119-1126.
45. Shin SS, Martino JJ, Chen S, (2008) Metabotropic glutamate receptors (mGlus) and cellular transformation. Neuropharmacology 55: 396-402.
46. Wei X, Walia V, Lin JC, Teer JK, Prickett TD, et al. (2011) Exome sequencing identifies GRIN2A as frequently mutated in melanoma. Nat Genet 43: 442-446.
47. McDowall M, Edwards NM, Jahoda CA, Hynd PI, (2008) The role of activins and follistatins in skin and hair follicle development and function. Cytokine Growth Factor Rev 19: 415-426.
48. Tobar N, Villar V, Santibanez JF, (2010) ROS-NFkappaB mediates TGF-beta1-induced expression of urokinase-type plasminogen activator, matrix metalloproteinase-9 and cell invasion. Mol Cell Biochem 340: 195-202.
49. Shiou SR, Datta PK, Dhawan P, Law BK, Yingling JM, et al. (2006) Smad4-dependent regulation of urokinase plasminogen activator secretion and RNA stability associated with invasiveness by autocrine and paracrine transforming growth factor-beta. J Biol Chem 281: 33971-33981.
50. Madhunapantula SV, Robertson GP, (2009) The PTEN-AKT3 signaling cascade as a therapeutic target in melanoma. Pigment Cell Melanoma Res 22: 400-419.
51. Biechele TL, Camp ND, Fass DM, Kulikauskas RM, Robin NC, et al. (2010) Chemical-genetic screen identifies riluzole as an enhancer of Wnt/beta-catenin signaling in melanoma. Chemistry & Biology 17: 1177-1182.
52. Matsuzaki K, Kitano C, Murata M, Sekimoto G, Yoshida K, et al. (2009) Smad2 and Smad3 phosphorylated at both linker and COOH-terminal regions transmit malignant TGF-beta signal in later stages of human colorectal cancer. Cancer Res 69: 5321-5330.
53. Wildi S, Kleeff J, Maruyama H, Maurer CA, Buchler MW, et al. (2001) Overexpression of activin A in stage IV colorectal cancer. Gut 49: 409-417.
54. Yoshinaga K, Inoue H, Utsunomiya T, Sonoda H, Masuda T, et al. (2004) N-cadherin is regulated by activin A and associated with tumor aggressiveness in esophageal carcinoma. Clin Cancer Res 10: 5702-5707.
55. Yoshinaga K, Mimori K, Yamashita K, Utsunomiya T, Inoue H, et al. (2003) Clinical significance of the expression of activin A in esophageal carcinoma. Int J Oncol 22: 75-80.
56. Yoshinaga K, Yamashita K, Mimori K, Tanaka F, Inoue H, et al. (2008) Activin a causes cancer cell aggressiveness in esophageal squamous cell carcinoma cells. Ann Surg Oncol 15: 96-103.
57. Zhang DF, Li XG, Su LJ, Meng QL, (2010) Expression of activin A and follistatin in glioblastoma and their effects on U87 in vitro. J Int Med Res 38: 1343-1353.
58. Stove C, Vanrobaeys F, Devreese B, Van Beeumen J, Mareel M, et al. (2004) Melanoma cells secrete follistatin, an antagonist of activin-mediated growth inhibition. Oncogene 23: 5330-5339.
59. Shapiro RL, Duquette JG, Roses DF, Nunes I, Harris MN, et al. (1996) Induction of primary cutaneous melanocytic neoplasms in urokinase-type plasminogen activator (uPA)-deficient and wild-type mice: cellular blue nevi invade but do not progress to malignant melanoma in uPA-deficient animals. Cancer Res 56: 3597-3604.
60. Gutierrez LS, Schulman A, Brito-Robinson T, Noria F, Ploplis VA, et al. (2000) Tumor development is retarded in mice lacking the gene for urokinase-type plasminogen activator or its inhibitor, plasminogen activator inhibitor-1. Cancer Res 60: 5839-5847.
61. Ulisse S, Baldini E, Sorrenti S, D'Armiento M, (2009) The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets 9: 32-71.