ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Sun, Ying ^a   Lim, Yoon ^a,b   Li, Fang ^a   Liu, Shen ^a,b   Lu, Jian Jun ^b   Haberberger, Rainer ^a   Zhong, Jin Hua ^b   Zhou, Xin Fu ^b  

^a FLINDERS UNIVERSITY   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; MYELIN ASSOCIATED GLYCOPROTEIN; NEUROTROPHIN RECEPTOR P75; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SORTILIN; ANTIBODY; NERVE GROWTH FACTOR RECEPTOR; PROTEIN PRECURSOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE; TNFRSF16 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; NERVE FIBER; NEURITE; PHYSIOLOGY; PSEUDOPODIUM; TIME LAPSE IMAGING;

MURINAE; MUS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIBODIES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; NERVE FIBERS; NEURITES; PROTEIN PRECURSORS; PSEUDOPODIA; RECEPTORS, NERVE GROWTH FACTOR; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING;

EID: 84860429933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035883     Document Type: Article

References (66)

1. Bradke F, Dotti CG, (2000) Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol 10: 1467-1470.
2. Conde C, Caceres A, (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10: 319-332.
3. Cohen-Cory S, Fraser SE, (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378: 192-196.
4. Gehler S, Gallo G, Veien E, Letourneau PC, (2004) p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci 24: 4363-4372.
5. Lu B, Pang PT, Woo NH, (2005) The yin and yang of neurotrophin action. Nat Rev Neurosci 6: 603-614.
6. Kenchappa RS, Zampieri N, Chao MV, Barker PA, Teng HK, et al. (2006) Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50: 219-232.
7. Yano H, Torkin R, Martin LA, Chao MV, Teng KK, (2009) Proneurotrophin-3 is a neuronal apoptotic ligand: evidence for retrograde-directed cell killing. J Neurosci 29: 14790-14802.
8. Yang F, Je HS, Ji Y, Nagappan G, Hempstead B, et al. (2009) Pro-BDNF-induced synaptic depression and retraction at developing neuromuscular synapses. J Cell Biol 185: 727-741.
9. Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, et al. (2005) Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8: 1069-1077.
10. Koshimizu H, Kiyosue K, Hara T, Hazama S, Suzuki S, et al. (2009) Multiple functions of precursor BDNF to CNS neurons: negative regulation of neurite growth, spine formation and cell survival. Mol Brain 2: 27.
11. Xu ZQ, Sun Y, Li HY, Lim Y, Zhong JH, et al. (2011) Endogenous proBDNF is a negative regulator of migration of cerebellar granule cells in neonatal mice. Eur J Neurosci 33: 1376-1384.
12. Wong I, Liao H, Bai X, Zaknic A, Zhong J, et al. (2010) ProBDNF inhibits infiltration of ED1+macrophages after spinal cord injury. Brain Behav Immun 24: 585-597.
13. Wang KC, Kim JA, 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.
14. Woolf CJ, Bloechlinger S, (2002) Neuroscience. It takes more than two to Nogo. Science 297: 1132-1134.
15. Tang XQ, Tanelian DL, Smith GM, (2004) Semaphorin3A inhibits nerve growth factor-induced sprouting of nociceptive afferents in adult rat spinal cord. J Neurosci 24: 819-827.
16. Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, et al. (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci U S A 102: 10694-10699.
17. Liu X, Hashimoto M, Horii H, Yamaguchi A, Naito K, et al. (2009) Repulsive guidance molecule b inhibits neurite growth and is increased after spinal cord injury. Biochem Biophys Res Commun 382: 795-800.
18. Naska S, Lin DC, Miller FD, Kaplan DR, (2010) p75NTR is an obligate signaling receptor required for cues that cause sympathetic neuron growth cone collapse. Mol Cell Neurosci 45: 108-120.
19. Teng HK, Teng KK, Lee R, Wright S, Tevar S, et al. (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25: 5455-5463.
20. Yamashita T, Tohyama M, (2003) The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 6: 461-467.
21. Gallo G, Letourneau PC, (2000) Neurotrophins and the dynamic regulation of the neuronal cytoskeleton. J Neurobiol 44: 159-173.
22. Marler KJ, Poopalasundaram S, Broom ER, Wentzel C, Drescher U, (2010) Pro-neurotrophins secreted from retinal ganglion cell axons are necessary for ephrinA-p75NTR-mediated axon guidance. Neural Dev 5: 30.
23. Nagappan G, Zaitsev E, Senatorov VV Jr, Yang J, Hempstead BL, et al. (2009) Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc Natl Acad Sci U S A 106: 1267-1272.
24. Yang J, Siao CJ, Nagappan G, Marinic T, Jing D, et al. (2009) Neuronal release of proBDNF. Nat Neurosci 12: 113-115.
25. Wang H, Wu LL, Song XY, Luo XG, Zhong JH, et al. (2006) Axonal transport of BDNF precursor in primary sensory neurons. Eur J Neurosci 24: 2444-2452.
26. Wu LL, Fan Y, Li S, Li XJ, Zhou XF, (2010) Huntingtin-associated protein-1 interacts with pro-brain-derived neurotrophic factor and mediates its transport and release. J Biol Chem 285: 5614-5623.
27. Zhou XF, Song XY, Zhong JH, Barati S, Zhou FH, et al. (2004) Distribution and localization of pro-brain-derived neurotrophic factor-like immunoreactivity in the peripheral and central nervous system of the adult rat. J Neurochem 91: 704-715.
28. Matsumoto T, Rauskolb S, Polack M, Klose J, Kolbeck R, et al. (2008) Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 11: 131-133.
29. Lee R, Kermani P, Teng KK, Hempstead BL, (2001) Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948.
30. Fahnestock M, Yu G, Michalski B, Mathew S, Colquhoun A, et al. (2004) The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J Neurochem 89: 581-592.
31. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, et al. (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 5: 1302-1308.
32. Bentley CA, Lee KF, (2000) p75 is important for axon growth and schwann cell migration during development. J Neurosci 20: 7706-7715.
33. Walsh GS, Krol KM, Crutcher KA, Kawaja MD, (1999) Enhanced neurotrophin-induced axon growth in myelinated portions of the CNS in mice lacking the p75 neurotrophin receptor. J Neurosci 19: 4155-4168.
34. Singh KK, Park KJ, Hong EJ, Kramer BM, Greenberg ME, et al. (2008) Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 11: 649-658.
35. Ahmed Z, Mazibrada G, Seabright RJ, Dent RG, Berry M, et al. (2006) TACE-induced cleavage of NgR and p75NTR in dorsal root ganglion cultures disinhibits outgrowth and promotes branching of neurites in the presence of inhibitory CNS myelin. FASEB J 20: 1939-1941.
36. Jansen P, Giehl K, Nyengaard JR, Teng K, Lioubinski O, et al. (2007) Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 10: 1449-1457.
37. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, et al. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13: 805-811.
38. 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.
39. Lee JK, Zheng B, (2011) Role of myelin-associated inhibitors in axonal repair after spinal cord injury. Exp Neurol.
40. Lee JK, Kim JE, Sivula M, Strittmatter SM, (2004) Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J Neurosci 24: 6209-6217.
41. Zheng B, Ho C, Li S, Keirstead H, Steward O, et al. (2003) Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38: 213-224.
42. Lee JK, Chow R, Xie F, Chow SY, Tolentino KE, et al. (2010) Combined genetic attenuation of myelin and semaphorin-mediated growth inhibition is insufficient to promote serotonergic axon regeneration. J Neurosci 30: 10899-10904.
43. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, et al. (2010) Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 66: 663-670.
44. Kater SB, Rehder V, (1995) The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 5: 68-74.
45. Wang GX, Poo MM, (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434: 898-904.
46. Kuhn TB, Meberg PJ, Brown MD, Bernstein BW, Minamide LS, et al. (2000) Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J Neurobiol 44: 126-144.
47. Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, et al. (2000) A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26: 431-441.
48. Yamashita T, Tucker KL, Barde YA, (1999) Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 24: 585-593.
49. Park KJ, Grosso CA, Aubert I, Kaplan DR, Miller FD, (2010) p75NTR-dependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat Neurosci 13: 559-566.
50. Grados-Munro EM, Fournier AE, (2003) Myelin-associated inhibitors of axon regeneration. J Neurosci Res 74: 479-485.
51. McGee AW, Strittmatter SM, (2003) The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci 26: 193-198.
52. Zhang G, Lehmann HC, Manoharan S, Hashmi M, Shim S, et al. (2011) Anti-ganglioside antibody-mediated activation of RhoA induces inhibition of neurite outgrowth. J Neurosci 31: 1664-1675.
53. Fujita Y, Endo S, Takai T, Yamashita T, (2011) Myelin suppresses axon regeneration by PIR-B/SHP-mediated inhibition of Trk activity. EMBO J 30: 1389-1401.
54. Kaplan DR, Miller FD, (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10: 381-391.
55. Nguyen N, Lee SB, Lee YS, Lee KH, Ahn JY, (2009) Neuroprotection by NGF and BDNF against neurotoxin-exerted apoptotic death in neural stem cells are mediated through Trk receptors, activating PI3-kinase and MAPK pathways. Neurochem Res 34: 942-951.
56. Huang EJ, Reichardt LF, (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642.
57. Song XY, Zhong JH, Wang X, Zhou XF, (2004) Suppression of p75NTR does not promote regeneration of injured spinal cord in mice. J Neurosci 24: 542-546.
58. Zhou XF, Li HY, (2007) Roles of glial p75NTR in axonal regeneration. J Neurosci Res 85: 1601-1605.
59. Fry EJ, Ho C, David S, (2007) A role for Nogo receptor in macrophage clearance from injured peripheral nerve. Neuron 53: 649-662.
60. Tomita K, Kubo T, Matsuda K, Fujiwara T, Yano K, et al. (2007) The neurotrophin receptor p75NTR in Schwann cells is implicated in remyelination and motor recovery after peripheral nerve injury. Glia 55: 1199-1208.
61. Song XY, Zhang FH, Zhou FH, Zhong J, Zhou XF, (2009) Deletion of p75NTR impairs regeneration of peripheral nerves in mice. Life Sci 84: 61-68.
62. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, et al. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69: 737-749.
63. Fan YJ, Wu LL, Li HY, Wang YJ, Zhou XF, (2008) Differential effects of pro-BDNF on sensory neurons after sciatic nerve transection in neonatal rats. Eur J Neurosci 27: 2380-2390.
64. Bastian I, Tam Tam S, Zhou XF, Kazenwadel J, Van der Hoek M, et al. (2011) Differential expression of microRNA-1 in dorsal root ganglion neurons. Histochem Cell Biol 135: 37-45.
65. Wang YJ, Valadares D, Sun Y, Wang X, Zhong JH, et al. (2010) Effects of proNGF on neuronal viability, neurite growth and amyloid-beta metabolism. Neurotox Res 17: 257-267.
66. Wu D, Huang W, Richardson PM, Priestley JV, Liu M, (2008) TRPC4 in rat dorsal root ganglion neurons is increased after nerve injury and is necessary for neurite outgrowth. J Biol Chem 283: 416-426.