The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: Convergence on the PI 3-kinase signaling pathway

Journal of Neurochemistry

Volumn 86, Issue 5, 2003, Pages 1116-1128

  Jones, David M ^a   Tucker, Budd A ^a   Rahimtula, Masuma ^a   Mearow, Karen M ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Adult sensory neurons; Glycogen synthase kinase; Insulin like growth factor 1; Mitogen activated protein kinase; Nerve growth factor; Phosphoinositide 3 kinase

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 (3 CARBOXYL 4 CHLOROANILINO) 4 (3 NITROPHENYL)MALEIMIDE; ANTIBODY; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3; GROWTH FACTOR; LITHIUM CHLORIDE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; NEUROTROPHIN; PERIPHERIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IMMUNOBLOTTING; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ANIMALIA;

EID: 0041430783     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01925.x     Document Type: Article

References (56)

1. Ali A., Hoeflich K. P. and Woodgett J. R. (2001) Glycogen synthase kinase-3: properties, functions, and regulation. Chem. Rev. 101, 2527-2540.
2. Atwal J. K., Massie B., Miller F. D. and Kaplan D. R. (2000) The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 27, 265-277.
3. Billingsley M. L. and Kincaid R. L. (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. J. Biochem. 323, 577-591.
4. Bullock B. and Habener J. F. (1998) Phosphorylation of the camp response element binding protein CREB by c-AMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affininty, conformation and increases net charge. Biochem. J. 37, 3795-3809.
5. Cafferty W. B., Gardiner N. J., Gavazzi I., Powell J., McMahon S. B., Heath J. K., Munson J., Cohen J. and Thompson S. W. (2001) Leukemia inhibitory factor determines the growth status of injured adult sensory neurons. J. Neurosci. 21, 7161-7170.
6. Chalecka-Franaszek E. and Chuang D.-M. (1999) 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.
7. Creedon D. J., Johnson E. M. Jr and Lawrence J. C. Jr (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.
8. Dodge M. E., Rahimtula M. and Mearow K. M. (2002) Factors contributing to neurotrophin-independent survival of adult sensory neurons. Brain Res. 953, 144-156.
9. Eickholt B. J., Walsh F. S. and Doherty P. (2002) An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157, 211-217.
10. Fernyhough P., Willars G. B., Lindsay R. M. and Tomlinson D. R. (1993) Insulin and insulin-like growth factor I enhance regeneration in cultured adult rat sensory neurones. Brain Res. 607, 117-124.
11. Fiol C. J., Williams J. S., Chou C. H., Wang Q. M., Roach P. J. and Andrisani O. M. (1994) A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. J. Biol. Chem. 269, 32187-32193.
12. Folli F., Ghidella S., Bonfanti L., Kahn C. and Merighi A. (1996) The early intracellular signaling pathway for the insulin/insulin-like growth factor receptor family in the mammalian central nervous system. Mol. Neurobiol. 13, 155-183.
13. Fu S. Y. and Gordon T. (1997) The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14, 67-116.
14. Ganju P., O'Bryan J. P., Der C., Winter J. and James I. J. (1998) Differential regulation of SHC proteins by nerve growth factor in sensory neurons and PC12 cells. Eur J. Neurosci. 10, 1995-2008.
15. Gavazzi I., Kumar R. D., McMahon S. B. and Cohen J. (1999) Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. Eur. J. Neurosci. 11, 3405-3414.
16. Goold R. G. and Gordon-Weeks P. R. (2001) Microtubule-associated protein aB phosphorylation by glycogen synthase kinase 3b is induced during PC12 cell differentiation. J. Cell Sci. 114, 4273-4284.
17. Goold R. G., Owen R. and Gordon-Weeks P. R. (1999) Glycogen synthase kinase 3b phosphorylation of microtubule-associated protein IB regulates the stability of microtubules in growth cones. J. Cell Sci. 112, 3373-3384.
18. Grimes C. A. and Jope R. S. (2001a) The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog. Neurobiol. 65, 391-426.
19. Grimes C. A. and Jope R. S. (2001b) CREB DNA binding activity is inhibited by glycogen synthase kinase-3β and facilitated by lithium. J. Neurochem. 78, 1219-1232.
20. Jackson T., Blader I., Hammonds-Odie L., Burga C., Cooke F., Hawkins P., WolfA. G., Heldman K. A. and Theibert A. B. (1996) Initiation and maintenance of NGF-stimulated neurite outgrowth required activation of a phosphoinositide 3-kinase. J. Cell Sci. 109, 289-300.
21. Kanje M., Skottner A., Sjoberg J. and Lundborg G. (1989) Insulin-like growth factor I (IGF-1) stimulates regeneration of the rat sciatic nerve. Brain Res. 486, 396-398.
22. Kaplan D. R. and Miller F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
23. Kimpinski K. and Mearow K. (2001) Neurite growth promotion by nerve growth factor and insulin-like growth factor-I in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase. J. Neurosci. Res. 63, 486-499.
24. Kimpinski K., Campenot R. B. and Mearow K. (1997) Effects of neurotrophins NGF, NT3 and BDNF on neurite growth from adult sensory neurons. Neuroscience 93, 253-263.
25. Klein P. S. and Melton D. A. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl Acad. Sci. USA 93, 8455-8459.
26. Klinz F. J., Wolff P. and 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.
27. Kopnisky K. L., Chalecka-Franaszek E., Gonzalez-Zulueta M. and Chuang D. M. (2003) Chronic lithium treatment antagonizes glutamate-induced decrease of phosphorylated CREB in neurons via reducing protein phosphatase 1 and increasing MEK activities. Neuroscience 116, 425-435.
28. Korhonen J., Said F. A., Wong A. and Kaplan D. R. (1999) Gab1 mediates neurite outgrowth, DNA synthesis and survival in PC12 cells. J. Biol. Chem. 274, 37307-37314.
29. Lad S. P., Peterson D. A., Bradshaw R. A. and Neet K. E. (2003) Individual and combined effects of TrkA and p75 nerve growth factor (NGF) receptors: a role for the high-affinity receptor site. J. Biol. Chem. 278, 24808-24817.
30. Li X. and Jope R. S. (1995) Selective inhibition of the expression of signal transduction proteins by lithium in nerve growth factor-differentiated PC12 cells. J. Neurochem. 65, 2500-2508.
31. Lindsay R. M. (1988) Nerve growth factors (NGF, BDNF) enhance axonal regeneration but not required for survival of adult sensory neurons. J. Neurosci. 8, 2394-2405.
32. Liu R. Y. and Snider W. D. (2001) Different signaling pathways mediate regenerative versus developmental sensory axon growth. J. Neurosci. 21, 1-5.
33. Lonze B. E. and Ginty D. D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
34. Lonze B. E., Riccio A., Cohen S. and Ginty D. D. (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34, 371-385.
35. Mandelkow E. M., Biernat J., Drewes G., Gustke B., Trinczek B. and Mandelkow E. (1995) Tau domains, phosphorylation, and interactions with microtubules. Neurobiol. Aging 16, 355-363.
36. Markus A., Zhong J. and Snider W. D. (2002a) Raf and Akt mediate distinct aspects of sensory axon growth. Neuron 35, 65-76.
37. Markus A., Patel T. D. and Snider W. D. (2002b) Neurotrophin factors and axonal growth. Curr Opin. Neurobiol. 12, 523-531.
38. Ming G., Song H., Berninger B., Inagaki N. and Tessier-Lavigne M. and Poo M. (1999) Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidanace. Neuron 23, 139-148.
39. Mora A., Sabio G., Risco A. M., Cuenda A., Alonso J. C., Soler G. and Centeno F. (2002) Lithium blocks the PKB and GSK3 dephosphorylation induced by ceramide through protein phosphatase-2A. Cell Signal. 14, 557-562.
40. Namikawa K., Honma M., Abe K., Takeda M., Mansur K., Obata T., Miwa A., Okado H. and Kiyama H. (2000) Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J. Neurosci. 20, 2875-2886.
41. Oliver C. J. and Shenolikar S. (1998) Physiologic importance of protein phosphatase inhibitors. Front. Biosci. 3, d961-972.
42. Sanchez C., Diaz-Nido J. and Avila J. (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog. Neurobiol. 61, 133-168.
43. Sayas C. L., Moreno-Flores M. T., Avila J. and Wandosell F. (1999) The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like tau phosphorylation. J. Biol. Chem. 27, 37046-37052.
44. Shaw M. and Cohen P. (1999) Role of protein kinase B and MAP kinase cascade in mediating the EGF-dependent inhibition of glycogen synthase kinase 3 in Swiss 3T3 cells. FEBS Lett. 461, 120-124.
45. Sjogren B., Wiklund P. and Ekstrom P. A. R. (2000) Mitogen-activated protein kinase inhibition by PD98059 blocks nerve growth factor stimulated axonal outgrowth from adult mouse dorsal root ganglia in vitro. Neuroscience 100, 407-416.
46. Sondell M., Lundborg G. and Kanje M. (1999) Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J. Neurosci. 19, 5731-5740.
47. Stambolic V., Ruel L. and Woodgett J. R. (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr. Biol. 6, 1664-1668.
48. Takahashi M., Yasutake K. and Tomizawa K. (1999) Lithium inhibits neurite growth and tau protein kinase I/glycogen synthase kinase-3β-dependent phosphorylation of juvenile tau in cultured hippocampal neurons. J. Neurochem. 73, 2073-2083.
49. Wang Q. M., Guan K. L., Roach P. J. and DePaoli-Roach A. (1995) Phosphorylation and activation of the ATP-Mg-dependent protein phosphatase by the mitogen activated protein kinase. J. Biol. Chem. 270, 18532-18358.
50. Wang J. E., Asghari V., Rockel C. and Young L. T. (1999) Cyclic AMP responsive element binding protein phosphorylation and DNA binding is decreased by chronic lithium but not valproate treatment of SH-SY5Y neuroblastoma cells. Neuroscience 91, 771-776.
51. Wiklund P., Ekstrom P. A. R. and Edstrom A. (2002) Mitogen-activated protein kinase inhibition reveals differences in signaling pathways activated by neurotrophin-3 and other growth-stimulating conditions of adult mouse dorsal root ganglia neurons. J. Neurosci. Res. 67, 62-68.
52. Williams R. S. and Harwood A. J. (2000) Lithium therapy and signal transduction. Trends Pharmacol. Sci. 21, 61-64.
53. Xing J., Kornhauser J. M., Xia Z., Thiele E. A. and Greenberg M. E. (1998) Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell Biol. 18, 1946-1955.
54. Yu C. F., Liu Z. X. and Cantley L. G. (2002) ERK negatively regulates the EGF-mediated interaction of Gabl and the PI 3-kinase. J. Biol. Chem. 277, 21382-31388.
55. Zhuang H. X., Snyder C. K., Pu S. F. and Ishii D. N. (1996) Insulin-like growth factors reverse or arrest diabetic neuropathy: effects on hyperalgesia and impaired nerve regeneration in rats. Exp. Neurol. 140, 198-205.
56. Zochodne D. W. and Cheng C. (2000) Neurotrophins and other growth factors in the regenerative milieu of proximal nerve stump tips. J. Anat. 196, 279-283.