Involvement of Akt2/protein kinase B β (PKBβ) in the 8-Cl-cAMP-induced cancer cell growth inhibition

Journal of Cellular Physiology

Volumn 228, Issue 4, 2013, Pages 890-902

  Choi, Ki Young ^a   Ahn, Young Ho ^a   Ahn, Hae Won ^a   Cho, Young Jun ^a   Hong, Seung Hwan ^a,b  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 AMINO 5 (3 BROMOPHENYL) 7 (6 MORPHOLINO 3 PYRIDINYL)PYRIDO[2,3 D]PYRIMIDINE; 5 AMINOIMIDAZOLE 4 CARBOXAMIDE RIBONUCLEOSIDE; 8 CHLOROADENOSINE 3',5' PHOSPHATE; ANTINEOPLASTIC AGENT; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B BETA; RIBONUCLEOSIDE DERIVATIVE; SMALL INTERFERING RNA; TRICIRIBINE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC AGENTS; CELL DEATH; CELL LINE, TUMOR; CELL PROLIFERATION; HELA CELLS; HUMANS; MCF-7 CELLS; NEOPLASMS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RIBONUCLEOTIDES;

EID: 84871680237     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24240     Document Type: Article

References (50)

1. Ahn YH, Jung JM, Hong SH. 2004. 8-Cl-cAMP and its metabolite, 8-Cl-adenosine induce growth inhibition in mouse fibroblast DT cells through the same pathways: Protein kinase C activation and cyclin B down-regulation. J Cell Physiol 201:277-285.
2. Ahn YH, Jung JM, Hong SH. 2005. 8-Chloro-cyclic AMP-induced growth inhibition and apoptosis is mediated by p38 mitogen-activated protein kinase activation in HL60 cells. Cancer Res 65:4896-4901.
3. Ahn YH, Han JH, Hong SH. 2006. Rap1 and p38 MAPK mediate 8-chloro-cAMP-induced growth inhibition in mouse fibroblast DT cells. J Cell Physiol 209:1039-1045.
4. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15:6541-6551.
5. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 7:261-269.
6. Bellacosa A, Testa JR, Staal SP, Tsichlis PN. 1991. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254:274-277.
7. Brazil DP, Hemmings BA. 2001. Ten years of protein kinase B signalling: A hard Akt to follow. Trends Biochem Sci 26:657-664.
8. Brennan P, Babbage JW, Burgering BM, Groner B, Reif K, Cantrell DA. 1997. Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. Immunity 7:679-689.
9. Burgering BM, Coffer PJ. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
10. Chen D, Niu M, Jiao X, Zhang K, Liang J, Zhang D. 2012. Inhibition of AKT2 enhances sensitivity to gemcitabine via regulating PUMA and NF-kappaB signaling pathway in human pancreatic ductal adenocarcinoma. Int J Mol Sci 13:1186-1208.
11. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB III, Kaestner KH, Bartolomei MS, Shulman GI, Birnbaum MJ. 2001a. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292:1728-1731.
12. Cho H, Thorvaldsen JL, Chu Q, Feng F, Birnbaum MJ. 2001b. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 276:38349-38352.
13. Ciardiello F, Tortora G, Kim N, Clair T, Ally S, Salomon DS, Cho-Chung YS. 1990. 8-Chloro-cAMP inhibits transforming growth factor alpha transformation of mammary epithelial cells by restoration of the normal mRNA patterns for cAMP-dependent protein kinase regulatory subunit isoforms which show disruption upon transformation. J Biol Chem 265:1016-1020.
14. Coffer PJ, Woodgett JR. 1991. Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur J Biochem 201:475-481.
15. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
16. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G. 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
17. Downward J. 1998. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol 10:262-267.
18. Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, Forman MS, Lee VM, Szabolcs M, de Jong R, Oltersdorf T, Ludwig T, Efstratiadis A, Birnbaum MJ. 2005. Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol Cell Biol 25:1869-1878.
19. Fischer-Posovszky P, Tews D, Horenburg S, Debatin KM, Wabitsch M. 2012. Differential function of Akt1 and Akt2 in human adipocytes. Mol Cell Endocrinol 358:135-143.
20. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
21. Gandhi V, Ayres M, Halgren RG, Krett NL, Newman RA, Rosen ST. 2001. 8-chloro-cAMP and 8-chloro-adenosine act by the same mechanism in multiple myeloma cells. Cancer Res 61:5474-5479.
22. Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL, Coskran T, Black SC, Brees DJ, Wicks JR, McNeish JD, Coleman KG. 2003. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 112:197-208.
23. Halgren RG, Traynor AE, Pillay S, Zell JL, Heller KF, Krett NL, Rosen ST. 1998. 8Cl-cAMP cytotoxicity in both steroid sensitive and insensitive multiple myeloma cell lines is mediated by 8Cl-adenosine. Blood 92:2893-2898.
24. Han JH, Ahn YH, Choi KY, Hong SH. 2009. Involvement of AMP-activated protein kinase and p38 mitogen-activated protein kinase in 8-Cl-cAMP-induced growth inhibition. J Cell Physiol 218:104-112.
25. Horie T, Ono K, Nagao K, Nishi H, Kinoshita M, Kawamura T, Wada H, Shimatsu A, Kita T, Hasegawa K. 2008. Oxidative stress induces GLUT4 translocation by activation of PI3-K/Akt and dual AMPK kinase in cardiac myocytes. J Cell Physiol 215:733-742.
26. Huang Q, Lan F, Zheng Z, Xie F, Han J, Dong L, Xie Y, Zheng F. 2011. Akt2 kinase suppresses glyceraldehyde-3-phosphate dehydrogenase (GAPDH)-mediated apoptosis in ovarian cancer cells via phosphorylating GAPDH at threonine 237 and decreasing its nuclear translocation. J Biol Chem 286:42211-42220.
27. Jensen PJ, Gunter LB, Carayannopoulos MO. 2010. Akt2 modulates glucose availability and downstream apoptotic pathways during development. J Biol Chem 285:17673-17680.
28. Jones PF, Jakubowicz T, Hemmings BA. 1991a. Molecular cloning of a second form of rac protein kinase. Cell Regul 2:1001-1009.
29. Jones PF, Jakubowicz T, Pitossi FJ, Maurer F, Hemmings BA. 1991b. Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc Natl Acad Sci USA 88:4171-4175.
30. Kim SN, Kim SG, Park JH, Lee MA, Park SD, Cho-Chung YS, Hong SH. 2000. Dual anticancer activity of 8-Cl-cAMP: Inhibition of cell proliferation and induction of apoptotic cell death. Biochem Biophys Res Commun 273:404-410.
31. Kim SN, Ahn YH, Kim SG, Park SD, Cho-Chung YS, Hong SH. 2001. 8-Cl-cAMP induces cell cycle-specific apoptosis in human cancer cells. Int J Cancer 93:33-41.
32. Kohn AD, Summers SA, Birnbaum MJ, Roth RA. 1996. Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem 271:31372-31378.
33. Konishi H, Kuroda S, Tanaka M, Matsuzaki H, Ono Y, Kameyama K, Haga T, Kikkawa U. 1995. Molecular cloning and characterization of a new member of the RAC protein kinase family: Association of the pleckstrin homology domain of three types of RAC protein kinase with protein kinase C subspecies and beta gamma subunits of G proteins. Biochem Biophys Res Commun 216:526-534.
34. Lange-Carter CA, Vuillequez JJ, Malkinson AM. 1993. 8-Chloroadenosine mediates 8-chloro-cyclic AMP-induced down-regulation of cyclic AMP-dependent protein kinase in normal and neoplastic mouse lung epithelial cells by a cyclic AMP-independent mechanism. Cancer Res 53:393-400.
35. Langeveld CH, Jongenelen CA, Heimans JJ, Stoof JC. 1992. Growth inhibition of human glioma cells induced by 8-chloroadenosine, an active metabolite of 8-chloro cyclic adenosine 3′:5′-monophosphate. Cancer Res 52:3994-3999.
36. Leavens KF, Easton RM, Shulman GI, Previs SF, Birnbaum MJ. 2009. Akt2 is required for hepatic lipid accumulation in models of insulin resistance. Cell Metab 10:405-418.
37. Li X, Mikhalkova D, Gao E, Zhang J, Myers V, Zincarelli C, Lei Y, Song J, Koch WJ, Peppel K, Cheung JY, Feldman AM, Chan TO. 2011. Myocardial injury after ischemia-reperfusion in mice deficient in Akt2 is associated with increased cardiac macrophage density. Am J Physiol Heart Circ Physiol 301:H1932-H1940.
38. Lucchi S, Calebiro D, de Filippis T, Grassi ES, Borghi MO, Persani L. 2011. 8-Chloro-cyclic AMP and protein kinase A I-selective cyclic AMP analogs inhibit cancer cell growth through different mechanisms. PLoS ONE 6:e20785.
39. Marte BM, Rodriguez-Viciana P, Wennstrom S, Warne PH, Downward J. 1997. R-Ras can activate the phosphoinositide 3-kinase but not the MAP kinase arm of the Ras effector pathways. Curr Biol 7:63-70.
40. Mu J, Brozinick JT, Jr., Valladares O, Bucan M, Birnbaum MJ. 2001. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7:1085-1094.
41. Mukherjee A, Wilson EM, Rotwein P. 2010. Selective signaling by Akt2 promotes bone morphogenetic protein 2-mediated osteoblast differentiation. Mol Cell Biol 30:1018-1027.
42. Rotte A, Pasham V, Bhandaru M, Eichenmuller M, Yang W, Qadri SM, Kempe DS, Puchchakayala G, Pearce D, Birnbaum MJ, Lang F. 2010. Regulation of gastric acid secretion by PKB/Akt2. Cell Physiol Biochem 25:695-704.
43. Shaw M, Cohen P, Alessi DR. 1997. Further evidence that the inhibition of glycogen synthase kinase-3beta by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216. FEBS Lett 416:307-311.
44. Tagliaferri P, Katsaros D, Clair T, Ally S, Tortora G, Neckers L, Rubalcava B, Parandoosh Z, Chang YA, Revankar GR, Crabtree GW, Robins RK, Cho-Chung YS. 1988a. Synergistic inhibition of growth of breast and colon human cancer cell lines by site-selective cyclic AMP analogues. Cancer Res 48:1642-1650.
45. Tagliaferri P, Katsaros D, Clair T, Neckers L, Robins RK, Cho-Chung YS. 1988b. Reverse transformation of Harvey murine sarcoma virus-transformed NIH/3T3 cells by site-selective cyclic AMP analogs. J Biol Chem 263:409-416.
46. Thomas CC, Deak M, Alessi DR, van Aalten DM. 2002. High-resolution structure of the pleckstrin homology domain of protein kinase b/akt bound to phosphatidylinositol (3, 4, 5)-trisphosphate. Curr Biol 12:1256-1262.
47. Tortora G, Pepe S, Yokozaki H, Meissner S, Cho-Chung YS. 1991. Cooperative effect of 8-Cl-cAMP and rhGM-CSF on the differentiation of HL-60 human leukemia cells. Biochem Biophys Res Commun 177:1133-1140.
48. Van Lookeren Campagne MM, Villalba Diaz F, Jastorff B, Kessin RH. 1991. 8-Chloroadenosine 3′, 5′-monophosphate inhibits the growth of Chinese hamster ovary and Molt-4 cells through its adenosine metabolite. Cancer Res 51:1600-1605.
49. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E, Hemmings BA. 2003. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem 278:32124-32131.
50. Yang W, Ju JH, Lee KM, Shin I. 2011. Akt isoform-specific inhibition of MDA-MB-231 cell proliferation. Cell Signal 23:19-26.