Amphotericin B, identified from a natural product screen, antagonizes CNS inhibitors to promote axon growth via activation of an Akt pathway in neurons

Journal of Neurochemistry

Volumn 113, Issue 5, 2010, Pages 1331-1342

  Gao, Ying ^a   Deng, Kangwen ^a   Cao, Zixuan ^a   Graziani, Edmund I ^a   Gilbert, Adam M ^a   Koehn, Frank E ^a   Wood, Andrew ^a   Doherty, Patrick ^b   Walsh, Frank S ^b  

^a PFIZER INC   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Akt; Amphotericin B; Axon regeneration; CSPG; GSK 3 ; Myelin

Indexed keywords

AMPHOTERICIN B; ANTIINFECTIVE AGENT; BALANOL; GLYCOGEN SYNTHASE KINASE 3BETA; MADURAHYDROXYLACTONE; MYELIN ASSOCIATED GLYCOPROTEIN; NYSTATIN; PROTEIN KINASE B; PROTEOCHONDROITIN SULFATE; TELEOCIDIN; TELEOCIDIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT;

AMPHOTERICIN B; ANIMALS; ANTIFUNGAL AGENTS; AXONS; BIOLOGICAL PRODUCTS; BLOTTING, WESTERN; CELL PROLIFERATION; DRUG EVALUATION, PRECLINICAL; MYELIN-ASSOCIATED GLYCOPROTEIN; NERVE REGENERATION; NEURITES; NEURONS; ONCOGENE PROTEIN V-AKT; PRINCIPAL COMPONENT ANALYSIS; PROTEOCHONDROITIN SULFATES; RATS; SIGNAL TRANSDUCTION;

EID: 77951903196     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06704.x     Document Type: Article

References (54)

1. Atwal J. K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C. Tessier-Lavigne M. (2008) PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967 970.
2. Berry M. (1982) Post-injury myelin-breakdown products inhibit axonal growth: an hypothesis to explain the failure of axonal regeneration in the mammalian central nervous system. Bibl. Anat. 23, 1 11.
3. Bolard J. (1986) How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim. Biophys. Acta 864, 257 304. (Pubitemid 17228111)
4. Brajtburg J., Powderly W. G., Kobayashi G. S. Medoff G. (1990) Amphotericin B: current understanding of mechanisms of action. Antimicrob. Agents Chemother. 34, 183 188. (Pubitemid 20046861)
5. Chen D. F., Jhaveri S. Schneider G. E. (1995) Intrinsic changes in developing retinal neurons result in regenerative failure of their axons. Proc. Natl Acad. Sci. USA 92, 7287 7291.
6. Cross D. A., Alessi D. R., Cohen P., Andjelkovich M. Hemmings B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785 789. (Pubitemid 26004411)
7. Deng K., Gao Y., Cao Z., Graziani E. I., Wood A., Doherty P. Walsh F. S. (2009) Overcoming amino-nogo-induced inhibition on cell spreading and neurite outgrowth by 12-O-tetradecanoylphorbol 13-acetate-type tumor promoters. J. Biol. Chem. 285, 6425 6433.
8. Dergham P., Ellezam B., Essagian C., Avedissian H., Lubell W. D. McKerracher L. (2002) Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 22, 6570 6577. (Pubitemid 35386413)
9. Dill J., Wang H., Zhou F. Li S. (2008) Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J. Neurosci. 28, 8914 8928.
10. Doherty P., Fruns M., Seaton P., Dickson G., Barton C. H., Sears T. A. Walsh F. S. (1990) A threshold effect of the major isoforms of NCAM on neurite outgrowth. Nature 343, 464 466. (Pubitemid 20065233)
11. Eickholt B. J., Walsh F. S. 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. (Pubitemid 34839818)
12. Espada R., Valdespina S., Alfonso C., Rivas G., Ballesteros M. P. Torrado J. J. (2008) Effect of aggregation state on the toxicity of different amphotericin B preparations. Int. J. Pharm. 361, 64 69.
13. Filbin M. T. (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. [Erratum appears in Nat Rev Neurosci. 2003 Dec;4(12):1019]. Nat. Rev. Neurosci. 4, 703 713.
14. Filbin M. T. (2006) Recapitulate development to promote axonal regeneration: good or bad approach? Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1565 1574.
15. Fournier A. E., GrandPre T. Strittmatter S. M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341 346.
16. Fournier A. E., Takizawa B. T. Strittmatter S. M. (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 23, 1416 1423. (Pubitemid 36258920)
17. Fujii G., Chang J. E., Coley T. Steere B. (1997) The formation of amphotericin B ion channels in lipid bilayers. Biochemistry 36, 4959 4968. (Pubitemid 27180978)
18. Fujitani M., Honda A., Hata K., Yamagishi S., Tohyama M. Yamashita T. (2005) Biological activity of neurotrophins is dependent on recruitment of Rac1 to lipid rafts. Biochem. Biophys. Res. Commun. 327, 150 154. (Pubitemid 40051365)
19. Goh E. L., Young J. K., Kuwako K., Tessier-Lavigne M., He Z., Griffin J. W. Ming G. L. (2008) beta1-integrin mediates myelin-associated glycoprotein signaling in neuronal growth cones. Mol. Brain 1, 10.
20. Hannila S. S. Filbin M. T. (2008) The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp. Neurol. 209, 321 332.
21. Hasegawa Y., Fujitani M., Hata K., Tohyama M., Yamagishi S. Yamashita T. (2004) Promotion of axon regeneration by myelin-associated glycoprotein and Nogo through divergent signals downstream of Gi&G. J. Neurosci. 24, 6826 6832. (Pubitemid 38993905)
22. Hiromura M., Okada F., Obata T., Auguin D., Shibata T., Roumestand C. Noguchi M. (2004) Inhibition of Akt kinase activity by a peptide spanning the betaA strand of the proto-oncogene TCL1. J. Biol. Chem. 279, 53407 53418. (Pubitemid 40051845)
23. Hu F. Strittmatter S. M. (2008) The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J. Neurosci. 28, 1262 1269. (Pubitemid 351186346)
24. Huang W., Zhang Z., Han X., Tang J., Wang J., Dong S. Wang E. (2002) Ion channel behavior of amphotericin B in sterol-free and cholesterol- or ergosterol-containing supported phosphatidylcholine bilayer model membranes investigated by electrochemistry and spectroscopy. Biophys. J. 83, 3245 3255. (Pubitemid 36041943)
25. Jiang H., Guo W., Liang X. Rao Y. (2005) Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123 135. (Pubitemid 40094608)
26. Koprivica V., Cho K. S., Park J. B. et al. (2005) EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 310, 106 110. (Pubitemid 41434546)
27. Kubo T., Hata K., Yamaguchi A. Yamashita T. (2007) Rho-ROCK inhibitors as emerging strategies to promote nerve regeneration. Curr. Pharm. Des. 13, 2493 2499. (Pubitemid 47423675)
28. Lee D. H., Strittmatter S. M. Sah D. W. (2003) Targeting the Nogo receptor to treat central nervous system injuries. Nat. Rev. Drug Discov. 2, 872 878. (Pubitemid 37407793)
29. Liu B. P., Cafferty W. B., Budel S. O. Strittmatter S. M. (2006) Extracellular regulators of axonal growth in the adult central nervous system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1593 1610. (Pubitemid 44450213)
30. Manning B. D. Cantley L. C. (2007) AKT&PKB signaling: navigating downstream. Cell 129, 1261 1274.
31. McDunn J. E., Muenzer J. T., Rachdi L., Chang K. C., Davis C. G., Dunne W. M., Piwnica-Worms D., Bernal-Mizrachi E. Hotchkiss R. S. (2008) Peptide-mediated activation of Akt and extracellular regulated kinase signaling prevents lymphocyte apoptosis. FASEB J. 22, 561 568. (Pubitemid 351225592)
32. McKeon R. J., Hoke A. Silver J. (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 136, 32 43.
33. Mi S., Lee X., Shao Z. et al. (2004) LINGO-1 is a component of the Nogo-66 receptor&p75 signaling complex. Nat. Neurosci. 7, 221 228. (Pubitemid 38280445)
34. Morgenstern D. A., Asher R. A. Fawcett J. W. (2002) Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137, 313 332.
35. Niederost B., Oertle T., Fritsche J., McKinney R. A. Bandtlow C. E. (2002) Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J. Neurosci. 22, 10368 10376. (Pubitemid 35416874)
36. Nishi K. K., Antony M., Mohanan P. V., Anilkumar T. V., Loiseau P. M. Jayakrishnan A. (2007) Amphotericin B-gum arabic conjugates: synthesis, toxicity, bioavailability, and activities against Leishmania and fungi. Pharm. Res. 24, 971 980. (Pubitemid 46675399)
37. Norton W. T. Poduslo S. E. (1973) Myelination in rat brain: method of myelin isolation. J. Neurochem. 21, 749 757.
38. Riese U., Ziegler E. Hamburger M. (2004) Militarinone A induces differentiation in PC12 cells via MAP and Akt kinase signal transduction pathways. FEBS Lett. 577, 455 459. (Pubitemid 39535330)
39. Rudge J. S. Silver J. (1990) Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 10, 3594 3603.
40. Schwab M. E. (2004) Nogo and axon regeneration. Curr. Opin. Neurobiol. 14, 118 124.
41. Shen Y., Tenney A. P., Busch S. A., Horn K. P., Cuascut F. X., Liu K., He Z., Silver J. Flanagan J. G. (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326, 592 596.
42. Silver J. Miller J. H. (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146 156. (Pubitemid 38160289)
43. Sivasankaran R., Pei J., Wang K. C., Zhang Y. P., Shields C. B., Xu X. M. He Z. (2004) PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat. Neurosci. 7, 261 268. (Pubitemid 38280450)
44. Smith-Thomas L. C., Fok-Seang J., Stevens J., Du J. S., Muir E., Faissner A., Geller H. M., Rogers J. H. Fawcett J. W. (1994) An inhibitor of neurite outgrowth produced by astrocytes. J. Cell Sci. 107 (Pt 6), 1687 1695. (Pubitemid 24198487)
45. Vinson M., Strijbos P. J., Rowles A., Facci L., Moore S. E., Simmons D. L. Walsh F. S. (2001) Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J. Biol. Chem. 276, 20280 20285. (Pubitemid 37411105)
46. Vinson M., Rausch O., Maycox P. R. et al. (2003) Lipid rafts mediate the interaction between myelin-associated glycoprotein (MAG) on myelin and MAG-receptors on neurons. Mol. Cell. Neurosci. 22, 344 352. (Pubitemid 36407597)
47. Vives E., Brodin P. Lebleu B. (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272, 16010 16017. (Pubitemid 27265584)
48. Vyas A. A., Patel H. V., Fromholt S. E., Heffer-Lauc M., Vyas K. A., Dang J., Schachner M. Schnaar R. L. (2002) Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc. Natl Acad. Sci. USA 99, 8412 8417. (Pubitemid 34651066)
49. Wang K. C., Kim J. A., Sivasankaran R., Segal R. He Z. (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74 78. (Pubitemid 35291442)
50. Wong S. T., Henley J. R., Kanning K. C., Huang K. H., Bothwell M. Poo M. M. (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5, 1302 1308. (Pubitemid 35417765)
51. Yiu G. He Z. (2003) Signaling mechanisms of the myelin inhibitors of axon regeneration. Curr. Opin. Neurobiol. 13, 545 551. (Pubitemid 37441273)
52. Yoshimura T., Arimura N., Kawano Y., Kawabata S., Wang S. Kaibuchi K. (2006) Ras regulates neuronal polarity via the PI3-kinase&Akt&GSK- 3beta&CRMP-2 pathway. Biochem. Biophys. Res. Commun. 340, 62 68. (Pubitemid 41827648)
53. Yu W., Guo W. Feng L. (2004) Segregation of Nogo66 receptors into lipid rafts in rat brain and inhibition of Nogo66 signaling by cholesterol depletion. FEBS Lett. 577, 87 92. (Pubitemid 39452365)
54. Zhou F. Q., Zhou J., Dedhar S., Wu Y. H. Snider W. D. (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42, 897 912. (Pubitemid 38798229)