Val66Met polymorphism of BDNF alters prodomain structure to induce neuronal growth cone retraction

Nature Communications

Volumn 4, Issue , 2013, Pages

  Anastasia, Agustin ^a   Deinhardt, Katrin ^b,c   Chao, Moses V ^b   Will, Nathan E ^a   Irmady, Krithi ^a   Lee, Francis S ^a   Hempstead, Barbara L ^a   Bracken, Clay ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; METHIONINE; NEUROTROPHIN RECEPTOR P75; VALINE;

BRAIN; GENE EXPRESSION; GROWTH; MORPHOLOGY; NEUROLOGY; POLYMORPHISM; RISK FACTOR;

ANXIETY DISORDER; ARTICLE; BIOLOGICAL ACTIVITY; CIRCULAR DICHROISM; CODON; CONTROLLED STUDY; DEPRESSION; GLYCOSYLATION; GROWTH CONE; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR WEIGHT; MORPHOLOGY; MOUSE; NERVE CELL; NERVE CELL GROWTH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EMBRYO, MAMMALIAN; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MEMORY; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROGENESIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR; RECOMBINANT PROTEINS;

EID: 84897930952     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3490     Document Type: Article

References (48)

1. Hajek, T., Kopecek, M. & Hoschl, C. Reduced hippocampal volumes in healthy carriers of brain-derived neurotrophic factor Val66Met polymorphism: meta-analysis. World J. Biol. Psychiatry 13, 178-187 (2012).
2. Egan, M. F. et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-269 (2003).
3. Frielingsdorf, H. et al. Variant brain-derived neurotrophic factor Val66Met endophenotypes: implications for posttraumatic stress disorder. Ann. N.Y. Acad. Sci. 1208, 150-157 (2010).
4. Soliman, F. et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 327, 863-866 (2010).
5. Verhagen, M. et al. Meta-analysis of the BDNF Val66Met polymorphism in major depressive disorder: effects of gender and ethnicity. Mol. Psychiatry 15, 260-271 (2010).
6. Chen, Z. Y. et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143 (2006).
7. Dincheva, I., Glatt, C. E. & Lee, F. S. Impact of the BDNF Val66Met Polymorphism on Cognition: Implications for Behavioral Genetics. Neuroscientist 18, 439-451 (2012).
8. Martinowich, K., Manji, H. & Lu, B. New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10, 1089-1093 (2007).
9. Teng, K. K., Felice, S., Kim, T. & Hempstead, B. L. Understanding proneurotrophin actions: recent advances and challenges. Dev. Neurobiol. 70, 350-359 (2010).
10. Yang, J. et al. Neuronal release of proBDNF. Nat. Neurosci. 12, 113-115 (2009).
11. Nagappan, G. et al. Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc. Natl Acad Sci. USA 106, 1267-1272 (2009).
12. Lee, R., Kermani, P., Teng, K. K. & Hempstead, B. L. Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948 (2001).
13. Mizoguchi, H. et al. Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-BDNF to mature BDNF in the hippocampus. J. Neurosci. 31, 12963-12971 (2011).
14. Teng, H. K. et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci. 25, 5455-5463 (2005).
15. Sun, Y. et al. ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PLoS One 7, e35883 (2012).
16. Deinhardt, K. et al. Neuronal growth cone retraction relies on proneurotrophin receptor signaling through Rac. Sci. Signal. 4, ra82 (2011).
17. Chen, Z. Y. et al. Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway. J. Neurosci. 25, 6156-6166 (2005).
18. Chen, Z. Y. et al. Variant brain-derived neurotrophic factor (BDNF) (Met66) alters the intracellular trafficking and activity-dependent secretion of wild-type BDNF in neurosecretory cells and cortical neurons. J. Neurosci. 24, 4401-4411 (2004).
19. Price, J. L. & Drevets, W. C. Neurocircuitry of mood disorders. Neuropsychopharmacology. 35, 192-216 (2010).
20. Feng, D. et al. Molecular and structural insight into proNGF engagement of p75NTR and sortilin. J. Mol. Biol. 396, 967-984 (2010).
21. Sattlera, M., Schleucherb, J. & Griesinger, C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc. 34, 93-158 (1999).
22. Marsh, J. A., Singh, V. K., Jia, Z. & Forman-Kay, J. D. Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein: implications for fibrillation. Protein Sci. 15, 2795-2804 (2006).
23. Shen, Y., Delaglio, F., Cornilescu, G. & Bax, A. TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223 (2009).
24. Bassett, D. S. & Bullmore, E. T. Human brain networks in health and disease. Curr. Opin. Neurol. 22, 340-347 (2009).
25. Nykjaer, A. et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848 (2004).
26. Quistgaard, E. M. et al. Ligands bind to Sortilin in the tunnel of a ten-bladed beta-propeller domain. Nat. Struct. Mol. Biol. 16, 96-98 (2009).
27. Gonzalez-Billault, C. et al. The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton (Hoboken.) 69, 464-485 (2012).
28. Kurien, B. T. & Scofield, R. H. A brief review of other notable protein detection methods on blots. Methods Mol. Biol. 536, 557-571 (2009).
29. Karey, K. P. & Sirbasku, D. A. Glutaraldehyde fixation increases retention of low molecular weight proteins (growth factors) transferred to nylon membranes for western blot analysis. Anal. Biochem. 178, 255-259 (1989).
30. Baquet, Z. C., Gorski, J. A. & Jones, K. R. Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci. 24, 4250-4258 (2004).
31. Kolbeck, R., Bartke, I., Eberle, W. & Barde, Y. A. Brain-derived neurotrophic factor levels in the nervous system of wild-type and neurotrophin gene mutant mice. J. Neurochem. 72, 1930-1938 (1999).
32. Bath, K. G. et al. BDNF Val66Met impairs fluoxetine-induced enhancement of adult hippocampus plasticity. Neuropsychopharmacology 37, 1297-1304 (2012).
33. Chiaruttini, C. et al. Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation. Proc. Natl Acad. Sci. USA 106, 16481-16486 (2009).
34. Goodman, L. J. et al. Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol. Cell Neurosci. 7, 222-238 (1996).
35. Uversky, V. N., Oldfield, C. J. & Dunker, A. K. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys. 37, 215-246 (2008).
36. Tompa, P. Intrinsically disordered proteins: a 10-year recap. Trends Biochem. Sci. 37, 509-516 (2012).
37. Bussell, Jr. R. & Eliezer, D. Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein. J. Biol. Chem. 276, 45996-46003 (2001).
38. Dwivedi, Y. Brain-Derived Neurotrophic Factor in Suicide Pathophysiology (2012). The Neurobiological Basis of Suicide. Chapter 8. CRC Press; Boca Raton (FL).
39. Shi, M. et al. Latent TGF-beta structure and activation. Nature 474, 343-349 (2011).
40. Mossessova, E. & Lima, C. D. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876 (2000).
41. Marley, J., Lu, M. & Bracken, C. A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75 (2001).
42. Gill, S. C. & von Hippel, P. H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326 (1989).
43. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
44. Goddard, T. D. & Kneller, D. G. SPARKY 3 (University of Californina, San Francisco, 2002).
45. Cao, W., Bracken, C., Kallenbach, N. R. & Lu, M. Helix formation and the unfolded state of a 52-residue helical protein. Protein Sci. 13, 177-189 (2004).
46. Wu, D. H. Chen., A. D. & Johnson, C. S. An improved diffusion-ordered spectroscopy experiment incorporating bipolar-gradient pulses. J. Magn. Reson. 115, 260-264 (1995).
47. Jones, J. A. Wilkins,D. K., Smith, L. J. & Dobson, C. M. Characterization of protein unfolding by NMR diffusion measurements. J. Biomol. NMR 10, 199-203 (1997).
48. Neubrand, V. E., Thomas, C., Schmidt, S., Debant, A. & Schiavo, G. Kidins220/ARMS regulates Rac1-dependent neurite outgrowth by direct interaction with the RhoGEF Trio. J. Cell Sci. 123, 2111-2123 (2010).