Endogenous proBDNF is a negative regulator of migration of cerebellar granule cells in neonatal mice

European Journal of Neuroscience

Volumn 33, Issue 8, 2011, Pages 1376-1384

  Xu, Zhi Qiang ^a,b   Sun, Ying ^a   Li, Hong Yun ^a   Lim, Yoon ^a   Zhong, Jin Hua ^a   Zhou, Xin Fu ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

BrdU; Neurite growth; Neurotrophins; P75NTR; Polarization

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN RECEPTOR P75; SORTILIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CEREBELLUM NUCLEUS; CONTROLLED STUDY; GENE EXPRESSION; GRANULE CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; WESTERN BLOTTING;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL MOVEMENT; CELLS, CULTURED; CEREBELLUM; MICE; MICE, INBRED C57BL; NEURONS; PROTEIN PRECURSORS; RECEPTOR, NERVE GROWTH FACTOR;

EID: 79954459377     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07635.x     Document Type: Article

References (52)

1. Balkowiec, A. & Katz, D.M. (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci., 22, 10399-10407.
2. Barker, P.A. (2009) Whither proBDNF? Nat. Neurosci., 12, 105-106.
3. Beattie, M.S., Harrington, A.W., Lee, R., Kim, J.Y., Boyce, S.L., Longo, F.M., Bresnahan, J.C., Hempstead, B.L. & Yoon, S.O. (2002) ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron, 36, 375-386.
4. Bergami, M., Santi, S., Formaggio, E., Cagnoli, C., Verderio, C., Blum, R., Berninger, B., Matteoli, M. & Canossa, M. (2008) Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J. Cell Biol., 183, 213-221.
5. Borghesani, P.R., Peyrin, J.M., Klein, R., Rubin, J., Carter, A.R., Schwartz, P.M., Luster, A., Corfas, G. & Segal, R.A. (2002) BDNF stimulates migration of cerebellar granule cells. Development, 129, 1435-1442.
6. Chen, Z.Y., Ieraci, A., Tanowitz, M. & Lee, F.S. (2005) A novel endocytic recycling signal distinguishes biological responses of Trk neurotrophin receptors. Mol. Biol. Cell, 16, 5761-5772.
7. Costa, C., Harding, B. & Copp, A.J. (2001) Neuronal migration defects in the Dreher (Lmx1a) mutant mouse: role of disorders of the glial limiting membrane. Cereb. Cortex, 11, 498-505.
8. Davies, A.M. (1994) The role of neurotrophins in the developing nervous system. J. Neurobiol., 25, 1334-1348.
9. Fahnestock, M., Yu, G., Michalski, B., Mathew, S., Colquhoun, A., Ross, G.M. & Coughlin, M.D. (2004) The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J. Neurochem., 89, 581-592.
10. Fan, Y.J., Wu, L.L., Li, H.Y., Wang, Y.J. & Zhou, X.F. (2008) Differential effects of pro-BDNF on sensory neurons after sciatic nerve transection in neonatal rats. Eur. J. Neurosci., 27, 2380-2390.
11. Fujita, S. (1967) Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. J. Cell Biol., 32, 277-287.
12. Fujita, S., Shimada, M. & Nakamura, T. (1966) H3-thymidine autoradiographic studies on the cell proliferation and differentiation in the external and the internal granular layers of the mouse cerebellum. J. Comp. Neurol., 128, 191-208.
13. Gleeson, J.G. (2001) Neuronal migration disorders. Ment. Retard. Dev. Disabil. Res. Rev., 7, 167-171.
14. Guan, C.B., Xu, H.T., Jin, M., Yuan, X.B. & Poo, M.M. (2007) Long-range Ca2+ signaling from growth cone to soma mediates reversal of neuronal migration induced by slit-2. Cell, 129, 385-395.
15. Jansen, P., Giehl, K., Nyengaard, J.R., Teng, K., Lioubinski, O., Sjoegaard, S.S., Breiderhoff, T., Gotthardt, M., Lin, F., Eilers, A., Petersen, C.M., Lewin, G.R., Hempstead, B.L., Willnow, T.E. & Nykjaer, A. (2007) Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat. Neurosci., 10, 1449-1457.
16. Jiang, Y., Kumada, T., Cameron, D.B. & Komuro, H. (2008) Cerebellar granule cell migration and the effects of alcohol. Dev. Neurosci., 30, 7-23.
17. Kenchappa, R.S., Zampieri, N., Chao, M.V., Barker, P.A., Teng, H.K., Hempstead, B.L. & Carter, B.D. (2006) Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron, 50, 219-232.
18. 2+ fluctuations. J. Neurobiol., 37, 110-130.
19. Komuro, H. & Yacubova, E. (2003) Recent advances in cerebellar granule cell migration. Cell. Mol. Life Sci., 60, 1084-1098.
20. Komuro, H., Yacubova, E. & Rakic, P. (2001) Mode and tempo of tangential cell migration in the cerebellar external granular layer. J. Neurosci., 21, 527-540.
21. Koshimizu, H., Hazama, S., Hara, T., Ogura, A. & Kojima, M. (2010) Distinct signaling pathways of precursor BDNF and mature BDNF in cultured cerebellar granule neurons. Neurosci. Lett., 473, 229-232.
22. Lee, R., Kermani, P., Teng, K.K. & Hempstead, B.L. (2001) Regulation of cell survival by secreted proneurotrophins. Science, 294, 1945-1948.
23. Liao, H., Bu, W.Y., Wang, T.H., Ahmed, S. & Xiao, Z.C. (2005) Tenascin-R plays a role in neuroprotection via its distinct domains that coordinate to modulate the microglia function. J. Biol. Chem., 280, 8316-8323.
24. Lu, B. (2003) Pro-region of neurotrophins: role in synaptic modulation. Neuron, 39, 735-738.
25. Lu, B., Pang, P.T. & Woo, N.H. (2005) The yin and yang of neurotrophin action. Nat. Rev. Neurosci., 6, 603-614.
26. Matsumoto, T., Rauskolb, S., Polack, M., Klose, J., Kolbeck, R., Korte, M. & Barde, Y.A. (2008) Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat. Neurosci., 11, 131-133.
27. Mowla, S.J., Farhadi, H.F., Pareek, S., Atwal, J.K., Morris, S.J., Seidah, N.G. & Murphy, R.A. (2001) Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J. Biol. Chem., 276, 12660-12666.
28. Murphy, R.A., Acheson, A., Hodges, R., Haskins, J., Richards, C., Reklow, E., Chlumecky, V., Barker, P.A., Alderson, R.F. & Lindsay, R.M. (1993) Immunological relationships of NGF, BDNF, and NT-3: recognition and functional inhibition by antibodies to NGF. J. Neurosci., 13, 2853-2862.
29. Nagappan, G., Zaitsev, E., Senatorov, V.V. Jr, Yang, J., Hempstead, B.L. & Lu, B. (2009) Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc. Natl. Acad. Sci. U S A, 106, 1267-1272.
30. Nykjaer, A., Lee, R., Teng, K.K., Jansen, P., Madsen, P., Nielsen, M.S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T.E., Hempstead, B.L. & Petersen, C.M. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature, 427, 843-848.
31. Pedraza, C.E., Podlesniy, P., Vidal, N., Arevalo, J.C., Lee, R., Hempstead, B., Ferrer, I., Iglesias, M. & Espinet, C. (2005) Pro-NGF isolated from the human brain affected by Alzheimer's disease induces neuronal apoptosis mediated by p75NTR. Am. J. Pathol., 166, 533-543.
32. Phinney, D.G., Baddoo, M., Dutreil, M., Gaupp, D., Lai, W.T. & Isakova, I.A. (2006) Murine mesenchymal stem cells transplanted to the central nervous system of neonatal versus adult mice exhibit distinct engraftment kinetics and express receptors that guide neuronal cell migration. Stem Cells Dev., 15, 437-447.
33. Rieger, S., Senghaas, N., Walch, A. & Koster, R.W. (2009) Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol., 7, e1000240.
34. Rocamora, N., Garcia-Ladona, F.J., Palacios, J.M. & Mengod, G. (1993) Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Brain Res. Mol. Brain Res., 17, 1-8.
35. Rogers, M.L., Atmosukarto, I., Berhanu, D.A., Matusica, D., Macardle, P. & Rush, R.A. (2006) Functional monoclonal antibodies to p75 neurotrophin receptor raised in knockout mice. J. Neurosci. Methods, 158, 109-120.
36. -/- mice reveals a role for neurotrophins in CNS patterning. Neuron, 19, 269-281.
37. Segal, R.A., Pomeroy, S.L. & Stiles, C.D. (1995) Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J. Neurosci., 15, 4970-4981.
38. Shen, J.S., Watabe, K., Ohashi, T. & Eto, Y. (2001) Intraventricular administration of recombinant adenovirus to neonatal twitcher mouse leads to clinicopathological improvements. Gene Ther., 8, 1081-1087.
39. Sobeih, M.M. & Corfas, G. (2002) Extracellular factors that regulate neuronal migration in the central nervous system. Int. J. Dev. Neurosci., 20, 349-357.
40. Teng, H.K., Teng, K.K., Lee, R., Wright, S., Tevar, S., Almeida, R.D., Kermani, P., Torkin, R., Chen, Z.Y., Lee, F.S., Kraemer, R.T., Nykjaer, A. & Hempstead, B.L. (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci., 25, 5455-5463.
41. Walsh, C.A. (2000) Genetics of neuronal migration in the cerebral cortex. Ment. Retard. Dev. Disabil. Res. Rev., 6, 34-40.
42. Wang, H., Wu, L.L., Song, X.Y., Luo, X.G., Zhong, J.H., Rush, R.A. & Zhou, X.F. (2006) Axonal transport of BDNF precursor in primary sensory neurons. Eur. J. Neurosci., 24, 2444-2452.
43. Wang, Y.J., Valadares, D., Sun, Y., Wang, X., Zhong, J.H., Liu, X.H., Majd, S., Chen, L., Gao, C.Y., Chen, S., Lim, Y., Pollard, A., Aguilar, E., Gai, W.P., Yang, M. & Zhou, X.F. (2010) Effects of proNGF on neuronal viability, neurite growth and amyloid-beta metabolism. Neurotox. Res., 17, 257-267.
44. Ward, M.E. & Rao, Y. (2005) Investigations of neuronal migration in the central nervous system. Methods Mol. Biol., 294, 137-156.
45. Wong, I., Liao, H., Bai, X., Zaknic, A., Zhong, J., Guan, Y., Li, H.Y., Wang, Y.J. & Zhou, X.F. (2010) ProBDNF inhibits infiltration of ED1+ macrophages after spinal cord injury. Brain Behav. Immun., 24, 585-597.
46. Woo, N.H., Teng, H.K., Siao, C.J., Chiaruttini, C., Pang, P.T., Milner, T.A., Hempstead, B.L. & Lu, B. (2005) Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci., 8, 1069-1077.
47. Wu, L.L., Fan, Y., Li, S., Li, X.J. & Zhou, X.F. (2010) Huntingtin-associated protein-1 interacts with pro-brain-derived neurotrophic factor and mediates its transport and release. J. Biol. Chem., 285, 5614-5623.
48. Yacubova, E. & Komuro, H. (2003) Cellular and molecular mechanisms of cerebellar granule cell migration. Cell Biochem. Biophys., 37, 213-234.
49. Yang, J., Siao, C.J., Nagappan, G., Marinic, T., Jing, D., McGrath, K., Chen, Z.Y., Mark, W., Tessarollo, L., Lee, F.S., Lu, B. & Hempstead, B.L. (2009) Neuronal release of proBDNF. Nat. Neurosci., 12, 113-115.
50. Yano, H., Torkin, R., Martin, L.A., Chao, M.V. & Teng, K.K. (2009) Proneurotrophin-3 is a neuronal apoptotic ligand: evidence for retrograde-directed cell killing. J. Neurosci., 29, 14790-14802.
51. Zhou, X.F., Song, X.Y., Zhong, J.H., Barati, S., Zhou, F.H. & Johnson, S.M. (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.
52. Zhou, P., Porcionatto, M., Pilapil, M., Chen, Y., Choi, Y., Tolias, K.F., Bikoff, J.B., Hong, E.J., Greenberg, M.E. & Segal, R.A. (2007) Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron, 55, 53-68.