Neurotensin phosphorylates GSK-3α/β through the activation of PKC in human colon cancer cells

Neoplasia

Volumn 8, Issue 9, 2006, Pages 781-787

  Wang, Qingding ^a   Zhou, Yuning ^a   Evers, B Mark ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Cyclin D1; GSK 3; Intestinal cells; Neurotensin; PKC

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; LY 379196; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NEUROTENSIN; NEUROTENSIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C INHIBITOR;

ARTICLE; BINDING AFFINITY; CANCER CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELL STRAIN HCT116; CELL STRAIN HT29; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTESTINE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 33749076514     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.06259     Document Type: Article

References (60)

1. Townsend CM Jr, Bold RJ, and Ishizuka J (1994). Gastrointestinal hormones and cell proliferation. Surg Today 24, 772-777.
2. Evers BM (2002). Endocrine gene neurotensin: molecular mechanisms and a model of intestinal differentiation. World J Surg 26, 799-805.
3. Evers BM, Wang X, Zhou Z, Townsend CM Jr, McNeil GP, and Dobner PR (1995). Characterization of promoter elements required for cell-specific expression of the neurotensin/neuromedin N gene in a human endocrine cell line. Mol Cell Biol 15, 3870-3881.
4. 3H]oleic acid translocation across rat small intestine. Am J Physiol 251, G823-G829.
5. Thor K and Rosell S (1986). Neurotensin increases colonic motility. Gastroenterology 90, 27-31.
6. Evers BM, Izukura M, Chung DH, Parekh D, Yoshinaga K, Greeley GH Jr, Uchida T, Townsend CM Jr, and Thompson JC (1992). Neurotensin stimulates growth of colonic mucosa in young and aged rats. Gastroenterology 103, 86-91.
7. Chung DH, Evers BM, Shimoda I, Townsend CM Jr, Rajaraman S, and Thompson JC (1992). Effect of neurotensin on gut mucosal growth in rats with jejunal and ileal Thiry-Vella fistulas. Gastroenterology 103, 1254-1259.
8. Thomas RP, Hellmich MR, Townsend CM Jr, and Evers BM (2003). Role of gastrointestinal hormones in the proliferation of normal and neoplastic tissues. Endocr Rev 24, 571-599.
9. Maoret JJ, Pospai D, Rouyer-Fessard C, Couvineau A, Laboisse C, Voisin T, and Laburthe M (1994). Neurotensin receptor and its mRNA are expressed in many human colon cancer cell lines but not in normal colonic epithelium: binding studies and RT-PCR experiments. Biochem Biophys Res Commun 203, 465-471.
10. Ehlers RA, Zhang Y, Hellmich MR, and Evers BM (2000). Neurotensin-mediated activation of MAPK pathways and AP-1 binding in the human pancreatic cancer cell line, MIA PaCa-2. Biochem Biophys Res Commun 269, 704-708.
11. Ehlers RA II, Bonnor RM, Wang X, Hellmich MR, and Evers BM (1998). Signal transduction mechanisms in neurotensin-mediated cellular regulation. Surgery 124, 239-246 (discussion, 246-237).
12. Poinot-Chazel C, Portier M, Bouaboula M, Vita N, Pecceu F, Gully D, Monroe JG, Maffrand JP, Le Fur G, and Casellas P (1996). Activation of mitogen-activated protein kinase couples neurotensin receptor stimulation to induction of the primary response gene Krox-24. Biochem J 320 (Pt 1), 145-151.
13. Zhao D, Keates AC, Kuhnt-Moore S, Moyer MP, Kelly CP, and Pothoulakis C (2001). Signal transduction pathways mediating neurotensin-stimulated interleukin-8 expression in human colonocytes. J Biol Chem 276, 44464-44471.
14. Ryder NM, Guha S, Hines OJ, Reber HA, and Rozengurt E (2001). G protein-coupled receptor signaling in human ductal pancreatic cancer cells: neurotensin responsiveness and mitogenic stimulation. J Cell Physiol 186, 53-64.
15. i and protein kinase C. Cell Calcium 15, 162-174.
16. Hassan S, Dobner PR, and Carraway RE (2004). Involvement of MAP-kinase, PI3-kinase and EGF-receptor in the stimulatory effect of Neurotensin on DNA synthesis in PC3 cells. Regul Pept 120, 155-166.
17. Guha S, Rey O, and Rozengurt E (2002). Neurotensin induces protein kinase C-dependent protein kinase D activation and DNA synthesis in human pancreatic carcinoma cell line PANC-1. Cancer Res 62, 1632-1640.
18. Goode N, Hughes K, Woodgett JR, and Parker PJ (1992). Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 267, 16878-16882.
19. Fang X, Yu S, Tanyi JL, Lu Y, Woodgett JR, and Mills GB (2002). Convergence of multiple signaling cascades at glycogen synthase kinase 3: EDG receptor-mediated phosphorylation and inactivation by lysophosphatidic acid through a protein kinase C-dependent intracellular pathway. Mol Cell Biol 22, 2099-2110.
20. Hofmann J (2004). Protein kinase C isozymes as potential targets for anticancer therapy. Curr Cancer Drug Targets 4, 125-146.
21. Umar S, Sellin JH, and Morris AP (2000). Murine colonic mucosa hyperproliferation: II. PKC-beta activation and cPKC-mediated cellular CFTR overexpression. Am J Physiol Gastrointest Liver Physiol 278, G765-G774.
22. Parhamifar L, Jeppsson B, and Sjolander A (2005). Activation of cPLA2 is required for leukotriene D4-induced proliferation in colon cancer cells. Carcinogenesis 26, 1988-1998.
23. Amar S, Kitabgi P, and Vincent JP (1986). Activation of phosphatidylinositol turnover by neurotensin receptors in the human colonic adenocarcinoma cell line HT29. FEBS Lett 201, 31-36.
24. Bozou JC, Rochet N, Magnaldo I, Vincent JP, and Kitabgi P (1989). Neurotensin stimulates inositol trisphosphate-mediated calcium mobilization but not protein kinase C activation in HT29 cells. Involvement of a G-protein. Biochem J 264, 871-878.
25. Guha S, Lunn JA, Santiskulvong C, and Rozengurt E (2003). Neurotensin stimulates protein kinase C-dependent mitogenic signaling in human pancreatic carcinoma cell line PANC-1. Cancer Res 63, 2379-2387.
26. Doble BW and Woodgett JR (2003). GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116, 1175-1186.
27. Korswagen HC, Coudreuse DY, Betist MC, van de Water S, Zivkovic D, and Clevers HC (2002). The Axin-like protein PRY-1 is a negative regulator of a canonical Wnt pathway in C. elegans. Genes Dev 16, 1291-1302.
28. Pap M and Cooper GM (1998). Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273, 19929-19932.
29. Cui H, Meng Y, and Bulleit RF (1998). Inhibition of glycogen synthase kinase 3beta activity regulates proliferation of cultured cerebellar granule cells. Brain Res Dev Brain Res 111, 177-188.
30. Ali A, Hoeflich KP, and Woodgett JR (2001). Glycogen synthase kinase-3: properties, functions, and regulation. Chem Rev 101, 2527-2540.
31. Plyte SE, Hughes K, Nikolakaki E, Pulverer BJ, and Woodgett JR (1992). Glycogen synthase kinase-3: functions in oncogenesis and development. Biochim Biophys Acta 1114, 147-162.
32. Woodgett JR (1990). Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 9, 2431-2438.
33. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, and Woodgett JR (2000). Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406, 86-90.
34. Cross DA, Alessi DR, Cohen P, Andjelkovich M, and Hemmings BA (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
35. De Mesquita DD, Zhan Q, Crossley L, and Badwey JA (2001). p90-RSK and Akt may promote rapid phosphorylation/inactivation of glycogen synthase kinase 3 in chemoattractant-stimulated neutrophils. FEBS Lett 502, 84-88.
36. Wang Q, Wang X, and Evers BM (2003). Induction of cIAP-2 in human colon cancer cells through PKC delta/NF-kappa B. J Biol Chem 278, 51091-51099.
37. Brady MJ, Bourbonais FJ, and Saltiel AR (1998). The activation of glycogen synthase by insulin switches from kinase inhibition to phosphatase activation during adipogenesis in 3T3-L1 cells. J Biol Chem 273, 14063-14066.
38. Zhao D, Zhan Y, Zeng H, Koon HW, Moyer MP, and Pothoulakis C (2005). Neurotensin stimulates interleukin-8 expression through modulation of IkappaBalpha phosphorylation and p65 transcriptional activity: involvement of protein kinase Calpha. Mol Pharmacol 67, 2025-2031.
39. Lin WW and Chen BC (1998). Distinct PKC isoforms mediate the activation of cPLA2 and adenylyl cyclase by phorbol ester in RAW264.7 macrophages. Br J Pharmacol 125, 1601-1609.
40. Wen HC, Huang WC, Ali A, Woodgett JR, and Lin WW (2003). Negative regulation of phosphatidylinositol 3-kinase and Akt signalling pathway by PKC. Cell Signal 15, 37-45.
41. Rouet-Benzineb P, Aparicio T, Guilmeau S, Pouzet C, Descatoire V, Buyse M, and Bado A (2004). Leptin counteracts sodium butyrate-induced apoptosis in human colon cancer HT-29 cells via NF-kappaB signaling. J Biol Chem 279, 16495-16502.
42. 1-phase progression. Genes Dev 13, 1501-1512.
43. Weinstein IB (2000). Disorders in cell circuitry during multistage carcinogenesis: the role of homeostasis. Carcinogenesis 21, 857-864.
44. Hamelers IH, van Schaik RF, Sipkema J, Sussenbach JS, and Steenbergh PH (2002). Insulin-like growth factor I triggers nuclear accumulation of cyclin D1 in MCF-7S breast cancer cells. J Biol Chem 277, 47645-47652.
45. Diehl JA, Cheng M, Roussel MF, and Sherr CJ (1998). Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12, 3499-3511.
46. Diehl JA, Zindy F, and Sherr CJ (1997). Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 11, 957-972.
47. Coghlan MP, Culbert AA, Cross DA, Corcoran SL, Yates JW, Pearce NJ, Rausch OL, Murphy GJ, Carter PS, Roxbee Cox L, et al. (2000). Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem Biol 7, 793-803.
48. Sadot E, Conacci-Sorrell M, Zhurinsky J, Shnizer D, Lando Z, Zharhary D, Kam Z, Ben-Ze'ev A, and Geiger B (2002). Regulation of S33/S37 phosphorylated beta-catenin in normal and transformed cells. J Cell Sci 115, 2771-2780.
49. Wong NA and Pignatelli M (2002). Beta-catenin - a linchpin in colorectal carcinogenesis? Am J Pathol 160, 389-401.
50. Wang Q, Wang X, Hernandez A, Hellmich MR, Gatalica Z, and Evers BM (2002). Regulation of TRAIL expression by the phosphatidylinositol 3-kinase/Akt/GSK-3 pathway in human colon cancer cells. J Biol Chem 277, 36602-36610.
51. Cross DA, Alessi DR, Vandenheede JR, McDowell HE, Hundal HS, and Cohen P (1994). The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem J 303 (Pt 1), 21-26.
52. Sutherland C, Leighton IA, and Cohen P (1993). Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem J 296 (Pt 1), 15-19.
53. Krause U, Bertrand L, Maisin L, Rosa M, and Hue L (2002). Signalling pathways and combinatory effects of insulin and amino acids in isolated rat hepatocytes. Eur J Biochem 269, 3742-3750.
54. Fang X, Yu SX, Lu Y, Bast RC Jr, Woodgett JR, and Mills GB (2000). Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 97, 11960-11965.
55. Vilimek D and Duronio V (2006). Cytokine-stimulated phosphorylation of GSK-3 is primarily dependent upon PKCs, not PKB. Biochem Cell Biol 84, 20-29.
56. Jirousek MR, Gillig JR, Gonzalez CM, Heath WF, McDonald JH III, Neel DA, Rito CJ, Singh U, Stramm LE, Melikian-Badalian A, et al. (1996). (S)-13-[(Dimethylamino)methyl]-10,11,14,15-tetrahydro-4,9:16, 21-dimetheno-1H, 13H-dibenzo[e,k]pyrrolo[3,4-h][1,4,13]oxadiazacyclohexadecene-1,3(2H)-dione (LY333531) and related analogues: isozyme selective inhibitors of protein kinase C beta. J Med Chem 39, 2664-2671.
57. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marme D, and Schachtele C (1993). Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem 268, 9194-9197.
58. Maoret JJ, Anini Y, Rouyer-Fessard C, Gully D, and Laburthe M (1999). Neurotensin and a non-peptide neurotensin receptor antagonist control human colon cancer cell growth in cell culture and in cells xenografted into nude mice. Int J Cancer 80, 448-454.
59. Farago M, Dominguez I, Landesman-Bollag E, Xu X, Rosner A, Cardiff RD, and Seldin DC (2005). Kinase-inactive glycogen synthase kinase 3beta promotes Wnt signaling and mammary tumorigenesis. Cancer Res 65, 5792-5801.
60. Cohen P and Frame S (2001). The renaissance of GSK3. Nat Rev Mol Cell Biol 2, 769-776.