PIKE GTPase are phosphoinositide-3-kinase enhancers, suppressing programmed cell death

Journal of Cellular and Molecular Medicine

Volumn 11, Issue 1, 2007, Pages 39-53

  Chan, Chi Bun ^a   Ye, Keqiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Akt; Apoptosis; GTPase; PI3K; PIKE

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL; APOPTOSIS; ARTICLE; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN; METABOLISM; TISSUE DISTRIBUTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HUMANS; TISSUE DISTRIBUTION;

ESOCIDAE;

EID: 33947306609     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2007.00014.x     Document Type: Article

References (80)

1. Sofroniew MV, Howe CL, Mobley WC. Nerve growth factor signaling, neuropprotection, and neural repair. Annu Rev Neurosci. 2001; 24: 1217-281.
2. Arévalo JC, Wu SH. Neurotrophin signaling: many exciting surprises. Cell Mol Life Sci. 2006; 63: 1523-37.
3. Katso R, Okkenhaug K, Ahmadi K, White S, Timms S, Waterfield MD. Cellular function of phosphoinositide 3-kinases: implication for development, immunity, homeostatsis and cancer. Annu Rev Cell Dev Biol. 2001; 17: 615-75.
4. Stephens RM, Loeb DM, Copeland TD, Pawson T, Greene LA, Kaplan DR. Trk receptors use redundant signal transduction pathways involving SHC and PLC-gammato mediate NGF responses. Neuron. 1994; 12: 691-705.
5. Holgado-Madruga M, Moscatello DK, Emlet DR, Diererich R, Wong AJ. Grb2-associated binder-1 mediates phosphatidylinositol-3-OH kinase activation and the promotion of cell survival by nerve growth factor. Proc Natl Acad Sci USA. 1997; 94: 12419-24.
6. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev. 1999; 13: 2905-27.
7. Datta SR, Dedek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997; 91: 231-41.
8. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC. Regulation of cell death protease caspase-9 by phosphorylation. Science. 1998; 282: 1318-21.
9. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999; 96: 857-68.
10. Kane LP, Shapiro VS, Stokoe D, Weiss A. Induction of NF-κB by the Akt/PKB kinase. Curr Biol. 1999; 9: 601-4.
11. Neri LM, Milani D, Bertolaso L, Stroscio M, Bertagnolo V, Capitani S. Nuclear translocation of phosphatidylinositol 3-kinase in rat pheochromocytoma PC 12 cells after treatment with nerve growth factor. Cell Mol Biol. 1994; 40: 619-26.
12. Lu PJ, Hsu AL, Wang DS, Yan HY, Yin HL, Chen CS. Phosphoinositide 3-kinase in rat liver nuclei. Biochemistry. 1998; 37: 5738-45.
13. Kim SJ. Insulin rapidly induces nuclear translocation of PI3-kinase in HeG2 cells. Biochem Mol Biol Int. 1998; 46: 187-96.
14. Martelli AM, Borgatti P, Bortul R, Manfredini M, Massari L, Capitani S, Neri LM. Phosphatidylinositol 3-kinase translocates to the nucleus of osteoblast-like MC3T3-E1 cells in response to insulin-like growth factor I and platelet-derived growth factor but not to the proapoptotic cytokine tumor necrosis factor alpha. J Bone Miner Res. 2000; 15: 1716-30.
15. Didichenko SA, Thelen M. Phosphatidylinositol 3-kinase C2α contains a nuclear localization sequence and associates with nuclear speckles. J Biol Chem. 2001; 276: 48135-42.
16. Metjian A, Roll RL, Ma AD, Abrams CS. Agonists cause nuclear translocation of phosphatidylinositol 3-kinaseγ: a Gßγ- dependent pathway that requires the p110-γ amino terminus. J Biol Chem. 1999; 274: 27943-7.
17. Ahn JY, Rong R, Liu X, Ye K. PIKE/nuclear PI 3-kinase signaling mediates the anti-apoptotic actions of NGF in the nucleus. EMBO J. 2004; 23: 3995-4006.
18. 3 receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD. Mol Cell. 2005; 18: 435-45.
19. York JD, Majerus PW. Nuclear phosphatidylinositols decrease during S-phase of the cell cycle in HeLa cells. J Biol Chem. 1994; 269: 7847-50.
20. Neri LM, Bortul R, Tabellini G, Borgatti P, Baldini G, Celeghini C, Capitani S, Martelli AM. Erythropoietin-induced erythroid differentiation of K562 cells is accompanied by the nuclear translocation of phosphatidylinositoi 3-kinase and intranuclear generation of phosphatidylinositol (3,4,5) trisphosphate. Cell Signal. 2002; 14: 21-9.
21. Rong R, Ahn JY, Huang H, Nagata E, Kalman D, Kapp JA, Tu J, Worley PF, Synder SH, Ye K. PI3 kinase enhancer-Homer complex couples mGIuRI to PI3 kinase, preventing neuronal apoptosis. Nat Neurosci. 2003; 6: 1153-61.
22. Ahn JY, Rong R, Kroll TG, Van Meir EG, Snyder SH, Ye K. PIKE (phosphatidylinositoi 3-kinase enhancer)-A GTPase stimulates Akt activity and mediates cellular invasion. J Biol Chem. 2004; 279: 16441-51.
23. Ye K, Hurt KJ, Wu FY, Fang M, Luo HR, Hong JJ, Blackshaw S, Ferris CD, Snyder SH. Pike: a nuclear GTPase that enhances PI3 kinase activity and is regulated by protein 4.1N. Cell. 2000; 103: 919-30.
24. Nagase T, Seki N, Ishikawa K, Tanaka A, Nomura N. Prediction of the coding sequences of 40 new genes (KIAA0161-KIAA0200) deduced by analysis of cDNA clones from human cell line KG-1. DNA Res. 1996; 3: 17-24.
25. Elkahloun AG, Krizman DB, Wang Z, Hofmann TA, Roe B, Meltzer PS. Transcript mapping in a 46-kb sequenced region at the core of 12q13.3 amplification in human cancers. Genomics. 1997; 42: 295-301.
26. Xia C, Ma W, Stafford LJ, Liu C, Gong L, Martin JF, Liu M. GGAPs, a new family of bifunctional GTP-binding and GTPase-activating proteins. Mol Cell Biol. 2003; 23: 2476-88.
27. Ahn JY, Hu Y, Kroll TG, Allard P, Ye K. PIKE-A is amplified in human cancers and prevents apoptosis by up-regulating Akt. Proc Natl Acad Sci USA. 2004; 101: 6993-8.
28. Liu X, Hu Y, Hao C, Rempel S, Ye K. PIKE-A is a proto-oncogene, promoting cell growth, transformation and invasion. Oncogens 2007, in press.
29. Hu Y, Liu Z, Ye K. Phosphoinositol lipids bind to phosphatidylinositol 3 (PI3)-kinase enhancer GTPase and mediates its stimulatory effect on PI3-kinase and Akt signalings. Proc Natl Acad Sci USA. 2005; 102: 16853-8.
30. Pemberton LF, Paschal BM. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005; 6: 187-98.
31. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev 2001; 81: 153-208.
32. Mattagajasingh SN, Huang SC, Hartenstein JS, Snyder M, Marchesi VT, Benz EJ. A nonerythroid isoform of protein 4.1R interacts with the nuclear mitotic apparatus (NuMA) protein. J Cell Biol. 199; 145: 29-43.
33. Lallena MJ, Martinez C, Valcarcel J, Correas I. Functional association of nuclear protein 4.1 with premRNA splicing factors. J Cell Sci. 1998; 111: 1963-71.
34. Takakuwa Y. Protein 4.1, a multifunctional protein of the erythrocyte membrane skeleton: structure and functions in erythrocytes and nonerythroid cells. Int J Hematol. 2000; 72: 298-309.
35. Ye K, Compton DA, Lai MM, Walensky LD, Snyder SH. Protein 4.1N binding to nuclear mitotic apparatus protein in PC12 cells mediates the antiproliferative actions of nerve growth factor. J Neurosci. 1999; 19: 10747-56.
36. Yu H, Chen JK, Feng S, Dalgarno DC, Brauer AW, Schreiber SL. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Cell. 1994; 76: 933-45.
37. Li SS. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J. 2005; 390: 641-53.
38. Ye K, Aghdasi B, Luo HR, Moriarity JL, Wu FY, Hong JJ, Hurt KJ, Base SS, Suh P, Synder SH. Phospholipase C-γ1 is a physiological guanine nucleotide exhange factor for the nuclear GTPase PIKE. Nature. 2002; 415: 541-44.
39. Smith MR, Liu YL, Matthews NT, Rhee SG, Sung WK, Kung HF. Phospholipase C-gamma 1 can induce DNA synthesis by a mechanism independent of its lipase activity. Proc Natl Acad Sci USA. 1994; 91: 6554-8.
40. Huang PS, Davis L, Huber H, Goodhart PJ, Wegrzyn RE, Oliff A, Heimbrook DC. An SH3 domain is required for the mitogenic activity of microinjected phospholipase C-gamma 1. FEBS Lett. 1995; 358: 287-92.
41. Rebecchi MJ, Pentyala SN. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev. 2000; 80: 1291-335.
42. Manzoli L, Martelli AM, Billi AM, Faenza I, Fiume R, Cocco L. Nuclear phospholipase C: Involvement in signal transduction. Prog Lip Res. 2005; 44: 185-206.
43. Klein C, Gensburger C, Freyermuth S, Nair BC, Labourdette G, Malviya AN. A 120 kDa nuclear phospholipase C(1 protein fragment is stimulated in vivo by EGF signal phosphorylating nuclear membrane EGFR. Biochemistry. 2004; 43: 15873-83.
44. Malviya AN, Klein C. Mechanism regulating nuclear calcium signaling. Can J Physiol Pharmacol. 2006; 84: 403-22.
45. Gomes DA, Leite MF, Bennett AM, Nathanson MH. Calcium signaling in the nucleus. Can J Physiol Pharmacol. 2006; 84: 325-32.
46. Vaudry D, Stork PJS, Lazarovici, Eiden LE. Signaling pathways for PC12 cell differentiation: making the right connections. Science. 2002 296: 1648-9.
47. Beneken J, Tu JC, Xiao B, Nuriya M, Yuan JP, Worley PF, Leahy DJ. Structure of the Homer EVH1 domain-peptide complex reveals a new twist in polyproline recognition. Neuron. 2000; 26:143-54.
48. Ango F, Pin JP, Tu JC, Xiao B, Worley PF, Bockaert J, Fagni L. Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation. J Neurosci. 2000; 20: 8710-6.
49. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron. 1998; 21: 717-26.
50. Feng W, Tu J, Yang T, Vernon PS, Allen PD, Worley PF, Pessah IN. Homer regulates gain of ryanodine receptor type 1 channel complex. J Biol Chem. 2002; 277: 44722-30.
51. Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF. Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell. 2003; 114: 777-89.
52. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PR Coupling of mGIuR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron. 1999; 23: 583-92.
53. Xiao B, Tu JC, Worley PF. Homer: a link between neural activity and glutamate receptor function. Curr Opin Neurobiol. 2000; 10: 370-4.
54. Copani A, Bruno VM, Barresi V, Battaglia G, Condorelli DF, Nicoletti F. Activation of metabotropic glutamate receptors prevents neuronal apoptosis in culture. J Neurochem. 1995; 64: 101-8.
55. Vincent AM, Maiese K. The metabotropic glutamate system promotes neuronal survival through distinct pathways of programmed cell death. Exp Neurol. 2000; 166: 65-82.
56. Rong R, Tang X, Gutmann DH, Ye K. Neurofibromatosis 2 (NF2) tumor suppressor merlin inhibits phosphatidylinositol 3-kinase through binding to PIKE-L. Proc Natl Acad Sci USA. 2004; 101: 18200-5.
57. Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, Pulst SM, Lenoir G, Bijlsma E, Fashold R, Dumanski J, de Jong P, Parry D, Eldrige R, Aurias A, Delattre O, Thomas G. Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature. 1993; 363: 515-21.
58. Twist EC, Ruttledge MH, Rousseau M, Sanson M, Papi L, Merel P, Delattre O, Thomas G, Rouleau GA. The neurofibromatosis type 2 gene is inactivated in schwannomas. Hum Mol Genet. 1994: 3: 147-51.
59. Bianchi AB, Hara T, Ramesh V, Gao J, Klein-Szanto AJP, Morin F, Menon AG, Trofatter JA, Gusella JF, Seizinger BR, Kley KN. Mutations in transcript isoforms of the neurofibromatosis 2 gene in multiple human tumour types. Nat Genet. 1994; 6: 185-92.
60. Lasota J, Fetsch JF, Wozniak A, Wasag B, Sciot R, Miettinen M. The neurofibromatosis type 2 gene is mutated in perineurial cell turmors: A molecular genetic study of eight cases. Am J Pathol. 2001; 158: 1223-9.
61. Sheikh HA, Tometsko M, Niehouse L, Aldeeb D, Swalsky P, Finkelstein S, Barnes EL, Hunt JL. Molecular genotyping of medullary thyroid carcinoma can predict tumor recurrence. Am J Surg Pathol. 2004; 28: 101-6.
62. Pineau P, Marchio A, Nagamori S, Seki S, Tiollais P, DejeanA. Homozygous deleltion scanning in hepatobiliary tumor cell lines reveals alternative pathways for liver carcinogenesis. Hepatology. 2003 37: 852-61.
63. Schulze KM, Hanemann CO, Muller HW, Hanenberg H. Transduction of wild-type merlin into human schwannoma cells decreases schwannoma cell growth and induces apoptosis. Hum Mol Genet. 2002; 11: 69-76.
64. Xiao GH, Gallagher R, Shetler J, Skele K, Altomare DA, Pestell RG, Jhanwar S, Testa JR. The NF2 tumor suppressor gene product, merlin, inhibits cell proliferation and cell cycle progression by repressing cyclin D1 expression. Mol Cell Biol. 2005; 25: 2384-94.
65. Kissil JL, Wilker EW, Johnson KC, Eckman MS, Yaffe MB, Jacks T. Merlin, the product of the Nf2 tumor suppressor gene, is an inhibitor of the p21-activated kinase, Pak1. Mol Cell. 2003; 12: 841-9.
66. Shaw RJ, Paez JG, Curto M, Yaktine A, Pruitt WM, Saotome I, O'Bryan JP, Gupta V, Ratner N, Der CJ, Jacks T, McClatchey AI. The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev Cell. 2001; 1:63-72.
67. Osaki M, Oshimura M, Ito H. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis. 2004; 9: 667-76.
68. Touhara K, Inglese J, Pitcher JA, Shaw G, Lefkowitz RJ. Binding of G protein beta gamma-subunits to pleckstrin homology domains. J Biol Chem. 1994; 269: 10217-20.
69. Klippel A, Kavanaugh WM, Pot D, Williams LT. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol Cell Biol. 1997; 17:338-44.
70. Knobbe CB, Trampe-Kieslich A, Reifenberger G. Genetic alteration and expression of the phosphoinositol-3-kinase/Akt pathway genes PIK3CA and PIKE in human glioblastomas. Neuropath Appl Neurobiol. 2005; 31: 486-90.
71. Tang X, Ye K. PIKE tyrosine phosphorylation regulates its apoptotic cleavage during programmed cell death. Advan Enzyme Regul. 2006; 46: 289-300.
72. Tang X, Feng Y, Ye K. Src-family tyrosine kinase Fyn phosphrylates phosphatidylinositol 3-kinase enhancer-activating Akt, preventing its apoptotic cleavage and promoting cell survival. Cell Death Differ. 2007; 14: 368-77.
73. Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 2003; 22: 337-58.
74. Horwood JM, Dufour F, Laroche S, Davis S. Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci. 2006; 23: 3375-84.
75. Chen X, Garelick MG, Wang H, Lil V, Athos J, Storm DR. PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat Neurosci. 2005; 8: 925-31.
76. Eckert MJ, Racine RJ. Metabotropic glutamate receptors contribute to neocortical synaptic plasticity in vivo. Neuroreport. 2004; 15: 2685-9.
77. van der Heide LP, Ramakers GM, Smidt MP. Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol. 2006; 79: 205-21.
78. Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, Becker LE, MacDonald JF, Wang YT. 1997. Recruitment of functional GABA (A) receptors to postsynaptic domains by insulin. Nature. 1997; 388: 686-90.
79. Mill JF, Chao MV, Ishii DN. Insulin, insulin-like growth factor II, and nerve growth factor effects on tubulin mRNA levels and neurite formation. Proc Natl Acad Sci USA. 1985; 82: 7126-30.
80. Tanaka M, Sawada M, Yoshida S, Hanaoka F, Marunouchi T. Insulin prevents apoptosis of external granular neurons in rat cerebellar slice cultures. Neurosci Lett. 1995; 199: 37-40.