Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration

Journal of Neuroscience

Volumn 20, Issue 8, 2000, Pages 2875-2886

  Namikawa, Kazuhiko ^a   Honma, Masaru ^a   Abe, Koji ^a   Takeda, Masumi ^a   Mansur, Khalil ^a   Obata, Tatsuo ^a   Miwa, Akiko ^b,c   Okado, Haruo ^b,c   Kiyama, Hiroshi ^a,c  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Adenoviral gene transfer; Cell death; Hypoglossal; Nerve injury; Nerve regeneration; Neuronal survival

Indexed keywords

PROTEIN KINASE B;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL SURVIVAL; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE TRANSFER; HYPOGLOSSAL NERVE; IN SITU HYBRIDIZATION; MOTONEURON; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE INJURY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

EID: 0034655803     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-08-02875.2000     Document Type: Article

References (85)

1. Akli S, Caillaud C, Vigne E, Stratford-Perricaudet LD, Poenaru L, Perricaudet M, Kahn A, Peschanski MR (1993) Transfer of a foreign gene into the brain using adenovirus vectors. Nat Genet 3:224-228.
2. Batistatou A, Merry DE, Korsmeyer SJ, Greene LA (1993) Bcl-2 affects survival hut not neuronal differentiation of PC12 cells. J Neurosci 13:4422-4428.
3. Bergmann A, Agapite J, McCall K, Steller H (1998) The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331-341.
4. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
5. Burgering BM, Coffer PJ (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
6. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282:1318-1321.
7. Chen J, Nagayama T, Jin k, Stetler RA, Zhu RL, Graham SH, Simon RP (1998) Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18:4914-4928.
8. Cowley S, Paterson H, Kemp P, Marshall CJ (1994) Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
9. Creedon DJ, Johnson EM, Lawrence JC (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J Biol Chem 271:20713-20718.
10. 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.
11. Crowder RJ, Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18:2933-2943.
12. D'Mello SR, Borodezt K, Soltoff SP (1997) Insulin-like growth factor and potassium depolarization maintain neuronal survival by distinct pathways: possible involvement of PI 3-kinase in IGF-1 signaling. J Neurosci 17:1548-1560.
13. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg M E (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
14. Davidson BL, Allen ED, Kozarsky KF, Wilson JM, Roessler BJ (1993) A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat Genet 3:219-223.
15. Deckwerth TL, Elliott JL, Knudson CM, Johnson Jr EM, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
16. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nún̄ez G (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
17. Downward J (1998) Lipid-regulated kinases: some common themes at last. Science 279:673-674.
18. Du K, Montminy M (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273:32377-32379.
19. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661-665.
20. Farlie PG, Dringen R, Rees SM, Kannourakis G, Bernard O (1995) bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc Natl Acad Sci USA 92:4397-4401.
21. 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.
22. Fukuda M, Gotoh Y, Nishida E (1997) Interaction of MAP kinase with MAP kinase kinase: its possible role in the control of nucleocytoplasmic transport of MAP kinase. EMBO J 16:1901-1908.
23. Gravel C, Gotz R, Lorrain A, Sendtner M (1997) Adenoviral gene transfer of ciliary neurotrophic factor and brain-derived neurotrophic factor leads to long-term survival of axotomized motor neurons. Nat Med 3:765-770.
24. Hamburger V (1934) The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J Exp Zool 68:449-494.
25. Hanson Jr MG, Shen S, Wiemelt AP, McMorris FA, Barres BA (1998) Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18:7361-7371.
26. Harada H, Becknell B, Wilm M, Mann M, Huang LJ, Taylor SS, Scott JD, Korsmeyer SJ (1999) Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell 3:413-422.
27. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, Armanini M, Simmons L, Moffet B, Vandlen RA, Simpson LC, Moffet B, Vandlen RA, Koliatsos VE, Rosenthal A (1994) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266:1062-1064.
28. Hirota H, Kiyama H, Kishimoto T, Taga T (1996) Accelerated nerve regeneration in mice by upregulated expression of interleukin (IL) 6 and IL-6 receptor after trauma. J Exp Med 183:2627-2634.
29. Hu Y, Benedict MA, Wu D, Inohara N, Nún̄ez G (1998) Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci USA 95:4386-4391.
30. Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K (1996) A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol Pharm Bull 19:1518-1520.
31. Ito Y, Sakagami H, Kondo H (1996) Enhanced gene expression for phosphatidylinositol 3-kinase in the hypoglossal motoneurons following axonal crush. Mol Brain Res 37:329-332.
32. Kanegae Y, Makimura M, Saito I (1994) A simple and efficient method for purification of infectious recombinant adenovirus. Jpn J Med Sci Biol 47:157-166.
33. Kanegae Y, Lee G, Sato Y, Tanaka M, Nakai M, Sakaki T, Sugano S, Saito I (1995) Efficient gene activation in mammalian cells by using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acids Res 23:3816-3821.
34. Kaplan DR, Miller FD (1997) Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9:213-221.
35. Kermer P, Klocker N, Labes M, Bahr M (1998) Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci 18:4656-4662.
36. Kimura K, Hattori S, Kabuyama Y, Shizawa Y, Takayanagi J, Nakamura S, Toki S, Matsuda Y, Onodera K, Fukui Y (1994) Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J Biol Chem 269:18961-18967.
37. Kiryu S, Morita N, Ohno K, Maeno H, Kiyama H (1995a) Regulation of mRNA expression involved in Ras and PKA signal pathways during rat hypoglossal nerve regeneration. Mol Brain Res 29:147-156.
38. Kiryu S, Yao GL, Morita N, Kato H, Kiyama H (1995b) Nerve injury enhances rat neuronal glutamate transporter expression: identification by differential display PCR. J Neurosci 15:7872-7878.
39. Kita Y, Kimura KD, Kobayashi M, Ihara S, Kaibuchi K, Kuroda S, Ui M, Iba H, Konishi H, Kikkawa U, Nagata S, Fukui Y (1998) Microinjection of activated phosphatidylinositol-3 kinase induces process outgrowth in rat PC12 cells through the Rac-JNK signal transduction pathway. J Cell Sci 111:907-915.
40. Kitamura T, Ogawa W, Sakaue H, Hino Y, Kuroda S, Takata M, Matsumoto M, Maeda T, Konishi H, Kikkawa U, Kasuga M (1998) Requirement for activation of the serine-threonine kinase Akt (protein kinase B) in insulin stimulation of protein synthesis hut not of glucose transport. Mol Cell Biol 18:3708-3717.
41. Klesse LJ, Parada LF (1998) p21 ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF1 mutant sensory neurons. J Neurosci 18:10420-10428.
42. Klinz FJ, Wolff P, Heumann R (1996) Nerve growth factor-stimulated mitogen-activated protein kinase activity is not necessary for neurite outgrowth of chick dorsal root ganglion sensory and sympathetic neurons. J Neurosci Res 46:720-726.
43. Kohn AD, Takeuchi F, Roth RA (1996a) Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J Biol Chem 271:21920-21926.
44. Kohn AD, Summers SA, Birnbaum MJ, Roth RA (1996b) 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.
45. Kohn AD, Barthel A, Kovacina KS, Boge A, Wallach B, Summers SA, Birnbaum MJ, Scott PH, Lawrence Jr JC, Roth RA (1998) Construction and characterization of a conditionally active version of the serine/ threonine kinase Akt. J Biol Chem 273:11937-11943.
46. Konishi H, Shinomura T, Kuroda S, Ono Y, Kikkawa U (1994) Molecular cloning of rat RAC protein kinase alpha and beta and their association with protein kinase C zeta. Biochem Biophys Res Commun 205:817-825.
47. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372.
48. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94:325-337.
49. Kurada P, White K (1998) Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319-329.
50. Lindsay RM (1995) Neuron saving schemes. Nature 373:289-290.
51. Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, Fukasawa K, Vande Woude GF, Ahn NG (1994) Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265:966-970.
52. Miyake S, Makimura M, Kanegae Y, Harada S, Sato Y, Takamori K, Tokuda C, Saito I (1996) Efficient generation of recombinant adenoviruses using adenovirus DNA-terminal protein complex and a cosmid bearing the full-length virus genome. Proc Natl Acad Sci USA 93:1320-1324.
53. Morita N, Kiryu S, Kiyama H (1996) p53-independent cyclin G expression in a group of mature neurons and its enhanced expression during nerve regeneration. J Neurosci 16:5961-5966.
54. Morooka T, Nishida E (1998) Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J Biol Chem 273:24285-24288.
55. Namikawa K, Su Q, Kiryu-Seo S, Kiyama H (1998) Enhanced expression of 14-3-3 family members in injured motoneurons. Mol Brain Res 55:315-320.
56. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
57. Oppenheim RW (1996) Neurotrophic survival molecules for motoneurons: an embarrassment of riches. Neuron 17:195-197.
58. Oppenheim RW, Houenou LJ, Johnson JE, Lin LF, Li L, Lo AC, Newsome AL, Prevette DM, Wang S (1995) Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373:344-346.
59. Owada Y, Utsunomiya A, Yoshimoto T, Kondo H (1997) Expression of mRNA for Akt, serine-threonine protein kinase, in the brain during development and its transient enhancement following axotomy of hypoglossal nerve. J Mol Neurosci 9:27-33.
60. Parsadanian AS, Cheng Y, Keller-Peck CR, Holtzman DM, Snider WD (1998) Bcl-xL is an antiapoptotic regulator for postnatal CNS neurons J Neurosci 18:1009-1019.
61. Persson H, Ibán̄ez CF (1993) Role and expression of neurotrophins and the trk family of tyrosine kinase receptors in neural growth and rescue after injury. Curr Opin Neurol Neurosurg 6:11-18.
62. Pettmann B, Henderson CE (1998) Neuronal cell death. Neuron 20: 633-647.
63. Philpott KL, McCarthy MJ, Klippel A, Rubin LL (1997) Activated phosphatidylinositol 3-kinase and Akt kinase promote survival of superior cervical neurons. J Cell Biol 139:809-815.
64. Pong K, Xu RY, Baron WF, Louis JC, Beck KD (1998) Inhibition of phosphatidylinositol 3-kinase activity blocks cellular differentiation mediated by glial cell line-derived neurotrophic factor in dopaminergic neurons. J Neurochem 71:1912-1919.
65. Resh MD (1994) Myristylation and palmitylation of Src family members: the fats of the matter. Cell 76:411-413.
66. Romanes GJ (1946) Motor localization and the effects of nerve injury on the ventral horn cells of the spinal cord. J Anat 80:117-131.
67. Rydell RE, Greene LA (1988) cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of NGF. Proc Natl Acad Sci USA 85:1257-1261.
68. Sato Y, Tanaka K, Lee G, Kanegae Y, Sakai Y, Kaneko S, Nakahayashi H, Tamaoki T, Saito I (1998a) Enhanced and specific gene expression via tissue-specific production of Cre recombinase using adenovirus vector. Biochem Biophys Res Commun 244:455-462.
69. Sato N, Wang S, Li L, Okabe K, Hashimoto M, Yaginuma H, Mikoshiba K, Uchiyama Y, Uetsuki T, Yoshikawa K, Milligan CE, Oppenheim RN (1998b) A novel strategy for introducing exogenous bcl-2 into neuronal cells: the Cre/loxP system-mediated activation of bcl-2 for preventing programmed cell death using recombinant adenoviruses. Mol Cell Neurosci 12:65-78.
70. Shimomura A, Okamoto Y, Hirata Y, Kobayashi M, Kawakami K, Kiuchi K, Wakabayashi T, Hagiwara M (1998) Dominant negative ATF1 blocks cyclic AMP-induced neurite outgrowth in PC12D cells. J Neurochem 70:1029-1034.
71. Snider WD (1994) Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627-638.
72. Snider WD, Elliott JL, Yan Q (1992) Axotomy-induced neuronal death during development. J Neurobiol 23:1231-1246.
73. Su QN, Namikawa K, Toki H, Kiyama H (1997) Differential display reveals transcriptional up-regulation of the motor molecules for both anterograde and retrograde axonal transport during nerve regeneration. Eur J Neurosci 9:1542-1547.
74. Tanabe K, Kiryu-Seo S, Nakamura T, Mori N, Tsujino H, Ochi T, Kiyama H (1998) Alternative expression of She family members in nerve-injured motoneurons. Mol Brain Res 53:291-296.
75. Terashima T, Miwa A, Kanegae Y, Saito I, Okado H (1997) Retrograde and anterograde labeling of cerebellar afferent projection by the injection of recombinant adenoviral vectors into the mouse cerebellar cortex. Anat Embryol 196:363-382.
76. Toki H, Namikawa K, Su Q, Kiryu-Seo S, Sato K, Kiyama H (1998) Enhancement of extracellular glutamate scavenge system in injured motoneurons. J Neurochem 71:913-919.
77. Trupp M, Belluardo N, Funakoshi H, Ibán̄ez CF (1997) Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-α indicates multiple mechanisms of trophic actions in the adult rat CNS. J Neurosci 17:3554-3567.
78. Vejsada R, Sagot Y, Kato AC (1995) Quantitative comparison of the transient rescue effects of neurotrophic factors on axotomized motoneurons in vivo. Eur J Neurosci 7:108-115.
79. Virdee K, Tolkovsky AM (1996) Inhibition of p42 and p44 mitogen-activated protein kinase activity by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurones. J Neurochem 67:1801-1805.
80. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
81. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, Faden AI (1997) Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 17:7415-7424.
82. Yan Q, Matheson C, Lopez OT (1995) In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373:341-344.
83. Yano S, Tokumitsu H, Soderling TR (1998) Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396:584-587.
84. Yao R, Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003-2006.
85. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87:619-628.