Lithium activates the Wnt and phosphatidylinositol 3-kinase Akt signaling pathways to promote cell survival in the absence of soluble survival factors

American Journal of Physiology - Renal Physiology

Volumn 288, Issue 4 57-4, 2005, Pages

  Sinha, Diviya ^a   Wang, Zhiyong ^a   Ruchalski, Kathleen L ^a   Levine, Jerrold S ^b   Krishnan, Selvi ^a   Lieberthal, Wilfred ^a   Schwartz, John H ^a   Borkan, Steven C ^a,c  

^a BOSTON MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c BOSTON UNIVERSITY   (United States)

Author keywords

Apoptosis; Glycogen synthase kinase 3 ; Insulin like growth factors; Renal epithelial cells; Serum deprivation; catenin

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2'3' 6 BROMOINDIRUBIN 3' OXIME; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; LITHIUM; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN BINDING PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; KIDNEY EPITHELIUM; KIDNEY PROXIMAL TUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 15044342829     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00189.2004     Document Type: Article

References (76)

1. Aberle H, Schwartz H, and Kemler R. Cadherin-catenin complex; protein interactions and their implications for cadherin function. J Cell Biochem 61: 514-523, 1996.
2. Alessi DR and Cohen P. Mechanism of activation and function of protein kinase B. Curr Opin Genet Dev 8: 55-62, 1998.
3. Bonegio R and Lieberthal W. Role of apoptosis in the pathogenesis of acute renal failure. Curr Opin Nephrol Hypertens 11: 301-308, 2002.
4. Bournat JC, Brown AM, and Soler AP. Wnt-1-dependent activation of the survival factor NF-κB in PC12 cells. J Neurosci Res 61: 21-32, 2000.
5. Brazil DP and Hemmings BA. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 26: 657-664, 2001.
6. Cadigan KM and Nusse R. Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-3305, 1997.
7. Carmichael J, Sugars KL, Bao YP, and Rubinsztein DC. Glycogen synthase kinase-3β inhibitors prevent cellular polyglutamine toxicity caused by the Huntington's disease mutation. J Biol Chem 277: 33791-33798, 2002.
8. Chalecka-Franaszek E and Chuang DM. Lithium activates the serine/ threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci USA 96: 8745-8750, 1999.
9. Chen RW and Chuang DM. Long-term lithium treatment suppresses p53 and Bax expression but increases Bcl-2 expression. A prominent role in neuroprotection against excitotoxicity. J Biol Chem 274: 6039-6042, 1999.
10. Chen S, Guttridge DC, You Z, Zhang Z, Fribley A, Mayo MW, Kitajewski J, and Wang CY. Wnt-1 signaling inhibits apoptosis by activating β-catenin/T cell factor-mediated transcription. J Cell Biol 152: 87-96, 2001.
11. Cross DA, Alessi DR, Cohen P, Andjelkovich M, and Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789, 1995.
12. Cross DA, Culbert AA, Chalmers KA, Facci L, Skaper SD, and Reith AD. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J Neurochem 77: 94-102, 2001.
13. Datta SR, Brunet A, and Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927, 1999.
14. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, and Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241, 1997.
15. Doble BW and Woodgett JR. GSK-3: tricks of the trade for a multitasking kinase. J Cell Sci 116: 1175-1186, 2003.
16. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol 10: 262-267, 1998.
17. Evan G and Littlewood T. A matter of life and cell death. Science 281: 1317-1322, 1998.
18. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, and Hancock DC. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128, 1992.
19. Ferkey DM and Klmelman D. GSK-3: new thoughts on an old enzyme. Dev Biol 225: 471-479, 2000.
20. Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, and Rotwein PS. "Spontaneous" differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J Biol Chem 266: 15917-15923, 1991.
21. Frame S and Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1-16, 2001.
22. Fukumoto S, Hsieh CM, Maemura K, Layne MD, Yet SF, Lee KH, Matsui T, Rosenzweig A, Taylor WG, Rubin JS, Perrella MA, and Lee ME. Akt participation in the Wnt signaling pathway through Dishevelled. J Biol Chem 276: 17479-17483, 2001.
23. Gagnon A, Dods P, Roustan-Delatour N, Chen CS, and Sorisky A. Phosphatidylinositol-3,4,5-trisphosphate is required for insulin-like growth factor 1-mediated survival of 3T3-L1 preadipocytes. Endocrinology 142: 205-212, 2001.
24. Geiger B and Ayalon O. Cadherins. Annu Rev Cell Biol 8: 307-332, 1992.
25. Ghribi O, Herman MM, Spaulding NK, and Savory J. Lithium inhibits aluminum-induced apoptosis in rabbit hippocampus, by preventing cytochrome c translocation, Bcl-2 decrease, Bax elevation and caspase-3 activation. J Neurochem 82: 137-145, 2002.
26. Grimes CA and Jope RS. The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog Neurobiol 65: 391-426, 2001.
27. Hall AC, Brennan A, Goold RG, Cleverley K, Lucas FR, Gordon-Weeks PR, and Saunas PC. Valproate regulates GSK-3-mediated axonal remodeling and synapsin I clustering in developing neurons. Mol Cell Neurosci 20: 257-270, 2002.
28. Hashimoto R, Senatorov V, Kanai H, Leeds P, and Chuang DM. Lithium stimulates progenitor proliferation in cultured brain neurons. Neuroscience 117: 55-61, 2003.
29. Hazeki O, Hazeki K, Katada T, and Ui M. Inhibitory effect of wortmannin on phosphatidylinositol 3-kinase-mediated cellular events. J Lipid Mediat Cell Signal 14: 259-261, 1996.
30. He TC, Chan TA, Vogelstein B, and Kinzler KW. PPARΔ is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 99: 335-345, 1999.
31. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, and Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512, 1998.
32. Hershko A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr Opin Cell Biol 9: 788-799, 1997.
33. Iglesias J, Abernethy VE, Wang Z, Lieberthal W, Koh JS, and Levine JS. Albumin is a major serum survival factor for renal tubular cells and macrophages through scavenging of ROS. Am J Physiol Renal Physiol 277: F711-F722, 1999.
34. Jones SM, Klinghoffer R, Prestwich GD, Toker A, and Kazlauskas A. PDGF induces an early and a late wave of PI 3-kinase activity, and only the late wave is required for progression through G1. Curr Biol 9: 512-521, 1999.
35. Kang EP, Urbonas A, Baddoo A, Baskin S, Malhotra A, and Meggs LG. IGF-1 inhibits the mitochondrial apoptosis program in mesangial cells exposed to high glucose. Am J Physiol Renal Physiol 285: F1013-F1024, 2003.
36. Klein PS and Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93: 8455-8459, 1996.
37. Kolligs FT, Hu G, Dang CV, and Fearon ER. Neoplastic transformation of RK3E by mutant β-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol Cell Biol 19: 5696-5706, 1999.
38. Kronfeld-Kinar Y, Vilchik S, Hyman T, Leibkowicz F, and Salzberg S. Involvement of PKR in the regulation of myogenesis. Cell Growth Differ 10: 201-212, 1999.
39. Lieberthal W and Levine JS. Mechanisms of apoptosis and its potential role in renal tubular epithelial cell injury. Am J Physiol Renal Fluid Electrolyte Physiol 271: F477-F488, 1996.
40. Lieberthal W, Menza SA, and Levine JS. Graded ATP depletion can cause necrosis or apoptosis of cultured mouse proximal tubular cells. Am J Physiol Renal Physiol 274: F315-F327, 1998.
41. Lieberthal W, Triaca V, Koh JS, Pagano PJ, and Levine JS. Role of superoxide in apoptosis induced by growth factor withdrawal. Am J Physiol Renal Physiol 275: F691-F702, 1998.
42. Loberg RD, Vesely E, and Brosius FC III. Enhanced glycogen synthase kinase-3β activity mediates hypoxia-induced apoptosis of vascular smooth muscle cells and is prevented by glucose transport and metabolism. J Biol Chem 277: 41667-41673, 2002.
43. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS, and MacDougald OA. Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulin-like growth factors. J Biol Chem 277: 38239-38244, 2002.
44. Magun R, Boone BL, Tsang BK, and Sorisky A. The effect of adipocyte differentiation on the capacity of 3T3-L1 cells to undergo apoptosis in response to growth factor deprivation. Int J Obes Relat Metab Disord 22: 567-571, 1998.
45. Magun R, Gagnon A, Yaraghi Z, and Sorisky A. Expression and regulation of neuronal apoptosis inhibitory protein during adipocyte differentiation. Diabetes 47: 1948-1952, 1998.
46. Martinez A, Castro A, Dorronsoro I, and Alonso M. Glycogen synthase kinase 3 (GSK-3) inhibitors as new promising drugs for diabetes, neurodegeneration, cancer, and inflammation. Med Res Rev 22: 373-384, 2002.
47. + deprivation in cerebellar granule cells. J Neurochem 78: 199-206, 2001.
48. Morali OG, Delmas V, Moore R, Jeanney C, Thiery JP, and Larue L. IGF-II induces rapid β-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 20: 4942-4950, 2001.
49. Morin PJ, Vogelstein B, and Kinzler KW. Apoptosis and APC in colorectal tumorigenesis. Proc Natl Acad Sci USA 93: 7950-7954, 1996.
50. Niesler CU, Urso B, Prins JB, and Siddle K. IGF-I inhibits apoptosis induced by serum withdrawal, but potentiates TNF-α-induced apoptosis, in 3T3-L1 preadipocytes. J Endocrinol 167: 165-174, 2000.
51. Nonaka S and Chuang DM. Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats. Neuroreport 9: 2081-2084, 1998.
52. Nonaka S, Hough CJ, and Chuang DM. Chronic lithium treatment robustly protects neurons in the central nervous system against excitotoxicity by inhibiting N-methyl-D-aspartate receptor-mediated calcium influx. Proc Natl Acad Sci USA 95: 2642-2647, 1998.
53. Nonaka S, Katsube N, and Chuang DM. Lithium protects rat cerebellar granule cells against apoptosis induced by anticonvulsants, phenytoin and carbamazepine. J Pharmacol Exp Ther 286: 539-547, 1998.
54. Olanow CW and Tatton WG. Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 22: 123-144, 1999.
55. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, and Klein PS. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741, 2001.
56. Playford MP, Bicknell D, Bodmer WF, and Macaulay VM. Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of β-catenin. Proc Natl Acad Sci USA 97: 12103-12108, 2000.
57. Raff MC. Social controls on cell survival and cell death. Nature 356: 397-400, 1992.
58. Rana A, Sathyanarayana P, and Lieberthal W. Role of apoptosis of renal tubular cells in acute renal failure: therapeutic implications. Apoptosis 6: 83-102, 2001.
59. Rao R, Hao CM, and Breyer MD. Hypertonic stress activates glycogen synthase kinase 3β-mediated apoptosis of renal medullary interstitial cells, suppressing an NFκB-driven cyclooxygenase-2-dependent survival pathway. J Biol Chem 279: 3949-3955, 2004.
60. Robertson H, Ali S, McDonnell BJ, Burt AD, and Kirby JA. Chronic renal allograft dysfunction: the role of T cell-mediated tubular epithelial to mesenchymal cell transition. J Am Soc Nephrol 15: 390-397, 2004.
61. Sato N, Meijer L, Skaltsounis L, Greengard P, and Brivanlou AH. Maintenance of pluripotency in human arid mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10: 55-63, 2004.
62. Satyamoorthy K, Li G, Vaidya B, Patel D, and Herlyn M. Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and β-catenin pathways. Cancer Res 61: 7318-7324, 2001.
63. Sharma M, Chuang WW, and Sun Z. Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3β inhibition and nuclear β-catenin accumulation. J Biol Chem 277: 30935-30941, 2002.
64. Shinohara K, Tomioka M, Nakano H, Tone S, Ito H, and Kawashima S. Apoptosis induction resulting from proteasome inhibition. Biochem J 317: 385-388, 1996.
65. Sinha D, Bannergee S, Schwartz JH, Lieberthal W, and Levine JS. Inhibition of ligand-independent ERK1/2 activity in kidney proximal tubular cells deprived of soluble survival factors upregulates Akt and prevents apoptosis. J Biol Chem 279: 10962-10972, 2004.
66. Sinha D, Wang Z, Price VR, Schwartz JH, and Lieberthal W. Chemical anoxia of tubular cells induces activation of c-Src and its translocation to the zonula adherens. Am J Physiol Renal Physiol 284: F488-F497, 2003.
67. Smalley MJ and Dale TC. Wnt signalling in mammalian development and cancer. Cancer Metastasis Rev 18: 215-230, 1999.
68. Somervaille TC, Linch DC, and Khwaja A. Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood 98: 1374-1381, 2001.
69. Stambolic V, Mak TW, and Woodgett JR. Modulation of cellular apoptotic potential: contributions to oncogenesis. Oncogene 18: 6094-6103, 1999.
70. Tetsu O and McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426, 1999.
71. Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, and Thompson CB. Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 21: 5899-5912, 2001.
72. Waltzer L and Bienz M. The control of β-catenin and TCF during embryonic development and cancer. Cancer Metastasis Rev 18: 231-246, 1999.
73. Williams RS, Cheng L, Mudge AW, and Harwood AJ. A common mechanism of action for three mood-stabilizing drugs. Nature 417: 292-295, 2002.
74. Wright BE, Longacre A, and Reimers JM. Hypermutation in derepressed operons of Escherichia coli K12. Proc Natl Acad Sci USA 96: 5089-5094, 1999.
75. Yin H, Chao L, and Chao J. Adrenomedullin protects against myocardial apoptosis after ischemia/reperfusion through activation of Akt-GSK signaling. Hypertension 43: 109-116, 2004.
76. Zeisberg M and Kalluri R. The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 82: 175-181, 2004.