Neurotrophins Elevate cAMP to Reach a Threshold Required to Overcome Inhibition by MAG through Extracellular Signal-Regulated Kinase-Dependent Inhibition of Phosphodiesterase

Journal of Neuroscience

Volumn 23, Issue 37, 2003, Pages 11770-11777

  Gao, Ying ^a   Nikulina, Elena ^a   Mellado, Wilfredo ^a   Filbin, Marie T ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

CAMP; Erk; Myelin associated glycoprotein; Neurotrophin; Phosphodiesterase; Regeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BUCLADESINE; CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; NERVE GROWTH FACTOR; NEUROTROPHIN; PHOSPHODIESTERASE; PHOSPHODIESTERASE IV; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HYDROLYSIS; NERVOUS SYSTEM INJURY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

EID: 0347694856     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-37-11770.2003     Document Type: Article

References (46)

1. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD (2000) Sub-family selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131:811-819.
2. Boniece IR, Wagner JA (1993) Growth factors protect PC12 cells against ischemia by a mechanism that is independent of PKA, PKC, and protein synthesis. J Neurosci 13:4220-4228.
3. Bouschet T, Perez V, Fernandez C, Bockaert J, Eychene A, Journot L (2003) Stimulation of the ERK pathway by GTP-loaded Rap1 requires the concomitant activation of Ras, protein kinase C, and protein kinase A in neuronal cells. J Biol Chem 278:4778-4785.
4. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT (1999) Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22:89-101.
5. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439.
6. Damon DH, D'Amore PA, Wagner JA (1990) Nerve growth factor and fibroblast growth factor regulate neurite outgrowth and gene expression in PC12 cells via both protein kinase C- and cAMP-independent mechanisms. J Cell Biol 110:1333-1339.
7. de Rooij J, Rehmann H, van Triest M, Cool RH, Wittinghofer A, Bos JL (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J Biol Chem 275:20829-20836.
8. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang RC, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin MT (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35:283-290.
9. Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703-713.
10. Fitch MT, Silver J (1999) Beyond the glial scar. In: CNS regeneration (Tuszynski MH, Kordower JH, eds), pp 55-88. San Diego: Academic.
11. Fournier AE, GrandPre T, Strittmatter SM (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341-346.
12. GrandPre T, Nakamura F, Vartanian T, Strittmatter SM (2000) Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 403:439-444.
13. Grewal SS, York RD, Stork PJ (1999) Extracellular signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9:544-553.
14. Hanson Jr MG, Shen S, Wiemelt AP, McMorris FA, Barres BA (1998) cAMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18:7361-7371.
15. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514.
16. Hoffmann R, Baillie GS, MacKenzie SJ, Yarwood SJ, Houslay MD (1999) The MAP kinase ERK2 inhibits the cyclic AMP-specific phosphodiesterase HSPDE4D3 by phosphorylating it at Ser579. EMBO J 18:893-903.
17. Holtzman DM, Li Y, Parada LF, Kinsman S, Chen CK, Valletta JS, Zhou J, Long JB, Mobley WC (1992) p140trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron 9:465-478.
18. Houslay MD, Kolch W (2000) Cell-type specific integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling. Mol Pharmacol 58:659-668.
19. Huber LJ, Chao MV (1995) A potential interaction of p75 and trkA NGF receptors revealed by affinity crosslinking and immunoprecipitation. J Neurosci Res 40:557-563.
20. Jin SL, Richard FJ, Kuo WP, D'Ercole AJ, Conti M (1999) Impaired growth and fertility of cAMP-specific phosphodiesterase PDE4D-deficient mice. Proc Natl Acad Sci USA 96:11998-12003.
21. Johnson PW, Abramow-Newerly W, Seilheimer B, Sadoul R, Tropak MB, Arquint M, Dunn RJ, Schachner M, Roder JC (1989) Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function. Neuron 3:377-385.
22. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
23. Knipper M, Beck A, Rylett J, Breer H (1993a) Neurotrophin induced cAMP and IP3 responses in PC12 cells. Different pathways. FEBS Lett 324:147-152.
24. Knipper M, Beck A, Rylett J, Breer H (1993b) Neurotrophin induced second messenger responses in rat brain synaptosomes. NeuroReport 4:483-486.
25. Lehmann M, Fournier A, Selles-Navarro I, Dergham P, Sebok A, Leclerc N, Tigyi G, McKerracher L (1999) Inactivation of Rho signaling pathway promotes CNS axon regeneration. J Neurosci 19:7537-7547.
26. Liu BP, Fournier A, GrandPre T, Strittmatter SM (2002) Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor., Science 297:1190-1193.
27. MacKenzie SJ, Baillie GS, McPhee I, Bolger GB, Houslay MD (2000) ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. The involvement of COOH-terminal docking sites and NH2-terminal UCR regions. J Biol Chem 275:16609-16617.
28. Martin-Zanca D, Barbacid M, Parada LF (1990) Expression of the trk protooncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev 4:683-694.
29. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811.
30. Meyer-Franke A, Kaplan MR, Pfrieger FW, Barres BA (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15:805-819.
31. Meyer-Franke A, Wilkinson GA, Kruttgen A, Hu M, Munro E, Hanson Jr MG, Reichardt LF, Barres BA (1998) Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21:681-693.
32. Mochizuki N, Ohba Y, Kiyokawa E, Kurata T, Murakami T, Ozaki T, Kitabatake A, Nagashima K, Matsuda M (1999) Activation of the ERK/ MAPK pathway by an isoform of rap1GAP associated with Gα(i). Nature 400:891-894.
33. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
34. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893.
35. Qiu J, Cai D, Filbin MT (2000) Glial inhibition of nerve regeneration in the mature mammalian CNS. Glia 29:166-174.
36. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
37. Robinson MJ, Harkins PC, Zhang J, Baer R, Haycock JW, Cobb MH, Goldsmith EJ (1996) Mutation of position 52 in ERK2 creates a nonproductive binding mode for adenosine 5′-triphosphate. Biochemistry 35:5641-5646.
38. Rydel RE, Greene LA (1988) cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of nerve growth factor. Proc Natl Acad Sci USA 85:1257-1261.
39. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
40. Stork PI, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-266.
41. Vossler MR, Yao H, York RD, Pan MG, Rim CS, Stork PJ (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82.
42. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002a) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG, and OMgp. Nature 420:74-78.
43. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002b) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944.
44. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, Poo MM (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 5:1302-1308.
45. Wu C, Lai CF, Mobley WC (2001) Nerve growth factor activates persistent Rap1 signaling in endosomes. J Neurosci 21:5406-5416.
46. York RD, Yao H, Dillon T, Ellig CL, Eckert SP, McCleskey EW, Stork PJ (1998) Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622-626.