An assay to image neuronal microtubule dynamics in mice

Nature Communications

Volumn 5, Issue , 2014, Pages

  Kleele, Tatjana ^a   Marinković, Petar ^b,c   Williams, Philip R ^a   Stern, Sina ^c   Weigand, Emily E ^d   Engerer, Peter ^a   Naumann, Ronald ^e   Hartmann, Jana ^a   Karl, Rosa M ^a   Bradke, Frank ^c   Bishop, Derron ^d   Herms, Jochen ^b,c,f   Konnerth, Arthur ^a,f,g   Kerschensteiner, Martin ^b,f   Godinho, Leanne ^a   Misgeld, Thomas ^a,c,f,g  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d BALL STATE UNIVERSITY   (United States)

^e MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^f Germany 3 Munich Cluster for Systems Neurology   (Germany)

^g Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; END BINDING PROTEIN 3; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; EB3 PROTEIN, MOUSE; HYBRID PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PHOTOPROTEIN; THY 1 ANTIGEN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ASSAY; CYTOLOGY; DRUG; FLUORESCENCE; GENE EXPRESSION; NERVOUS SYSTEM; NEUROLOGY; PROTEIN; RODENT;

ARTICLE; ASSAY; CENTRAL NERVOUS SYSTEM; DEGENERATIVE DISEASE; MICROTUBULE; MICROTUBULE DYNAMICS; MOUSE; NERVE DEGENERATION; NERVE FIBER; NEURITE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; BIOASSAY; CELL POLARITY; CYTOLOGY; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENETICS; HIPPOCAMPUS; MALE; METABOLISM; MOLECULAR IMAGING; NERVE CELL; PATHOLOGY; PRIMARY CELL CULTURE; PROCEDURES; PROMOTER REGION; SPINAL GANGLION; TRANSGENIC MOUSE; ULTRASTRUCTURE; VIDEORECORDING;

MAMMALIA; MUS; MUS MUSCULUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIGENS, THY-1; BACTERIAL PROTEINS; BIOLOGICAL ASSAY; CELL POLARITY; DISEASE MODELS, ANIMAL; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION; HIPPOCAMPUS; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR IMAGING; NEURONS; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; VIDEO RECORDING;

EID: 84908256346     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5827     Document Type: Article

References (58)

1. Conde, C., & Caceres, A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10, 319-332 (2009).
2. Mitchison, T., & Kirschner, M. Dynamic instability of microtubule growth. Nature 312, 237-242 (1984).
3. Neukirchen, D., & Bradke, F. Neuronal polarization and the cytoskeleton. Dev. Biol. 22, 825-833 (2011).
4. Bishop, D. L., Misgeld, T., Walsh, M. K., Gan, W. B., & Lichtman, J. W. Axon branch removal at developing synapses by axosome shedding. Neuron 44, 651-661 (2004).
5. Chevalier-Larsen, E., & Holzbaur, E. L. Axonal transport and neurodegenerative disease. Biochim. Biophys. Acta 1762, 1094-1108 (2006).
6. Fanara, P. et al. Stabilization of hyperdynamic microtubules is neuroprotective in amyotrophic lateral sclerosis. J. Biol. Chem. 282, 23465-23472 (2007).
7. d'Ydewalle, C. et al. HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease. Nat. Med. 17, 968-974 (2011).
8. Galjart, N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 20, R528-R537 (2010).
9. Akhmanova, A., & Hoogenraad, C. C. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17, 47-54 (2005).
10. Stepanova, T. et al. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655-2664 (2003).
11. Erez, H. et al. Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J. Cell Biol. 176, 497-507 (2007).
12. Stone, M. C., Roegiers, F., & Rolls, M. M. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol. Biol. Cell 19, 4122-4129 (2008).
13. Norden, C., Young, S., Link, B. A., & Harris, W. A. Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138, 1195-1208 (2009).
14. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).
15. Misgeld, T., Kerschensteiner, M., Bareyre, F. M., Burgess, R. W., & Lichtman, J. W. Imaging axonal transport of mitochondria in vivo. Nat. Methods 4, 559-561 (2007).
16. De Paola, V., Arber, S., & Caroni, P. AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks. Nat. Neurosci. 6, 491-500 (2003).
17. Wyatt, R. M., & Balice-Gordon, R. J. Heterogeneity in synaptic vesicle release at neuromuscular synapses of mice expressing synaptopHluorin. J. Neurosci. 28, 325-335 (2008).
18. Komarova, Y. et al. EB1 and EB3 control CLIP dissociation from the ends of growing microtubules. Mol. Biol. Cell 16, 5334-5345 (2005).
19. Kerschensteiner, M., Reuter, M. S., Lichtman, J. W., & Misgeld, T. Ex vivo imaging of motor axon dynamics in murine triangularis sterni explants. Nat. Protoc. 3, 1645-1653 (2008).
20. Applegate, K. T. et al. plusTipTracker: quantitative image analysis software for the measurement of microtubule dynamics. J. Struct. Biol. 176, 168-184 (2011).
21. Nicovich, P. R., & Zhou, F. Q. Acquisition frame rate affects microtubule plusend tracking analysis. Nat. Methods 11, 219-220 (2014).
22. Baas, P. W., Deitch, J. S., Black, M. M., & Banker, G. A. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl Acad. Sci. USA 85, 8335-8339 (1988).
23. Fuhrmann, M., Mitteregger, G., Kretzschmar, H., & Herms, J. Dendritic pathology in prion disease starts at the synaptic spine. J. Neurosci. 27, 6224-6233 (2007).
24. Holtmaat, A. et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144 (2009).
25. Schiff, P. B., & Horwitz, S. B. Taxol stabilizes microtubules in mouse fibroblast cells. Proc. Natl Acad. Sci. USA 77, 1561-1565 (1980).
26. Jordan, M. A., & Wilson, L. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer 4, 253-265 (2004).
27. Erturk, A., Hellal, F., Enes, J., & Bradke, F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J. Neurosci. 27, 9169-9180 (2007).
28. Hellal, F. et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331, 928-931 (2011).
29. Barten, D. M. et al. Hyperdynamic microtubules, cognitive deficits, and pathology are improved in tau transgenic mice with low doses of the microtubule-stabilizing agent BMS-241027. J. Neurosci. 32, 7137-7145 (2012).
30. Kerschensteiner, M., Schwab, M. E., Lichtman, J. W., & Misgeld, T. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 11, 572-577 (2005).
31. Chen, L., Stone, M. C., Tao, J., & Rolls, M. M. Axon injury and stress trigger a microtubule-based neuroprotective pathway. Proc. Natl Acad. Sci. USA 109, 11842-11847 (2012).
32. El Bejjani, R., & Hammarlund, M. Neural regeneration in Caenorhabditis elegans. Annu. Rev. Genet. 46, 499-513 (2012).
33. Tanaka, E. M., & Ferretti, P. Considering the evolution of regeneration in the central nervous system. Nat. Rev. Neurosci. 10, 713-723 (2009).
34. Galbraith, J. A., & Terasaki, M. Controlled damage in thick specimens by multiphoton excitation. Mol. Biol. Cell 14, 1808-1817 (2003).
35. Stone, M. C., Nguyen, M. M., Tao, J., Allender, D. L., & Rolls, M. M. Global upregulation of microtubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol. Biol. Cell 21, 767-777 (2010).
36. Nguyen, Q. T., Sanes, J. R., & Lichtman, J. W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5, 861-867 (2002).
37. Coleman, M. P., & Freeman, M. R. Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 33, 245-267 (2010).
38. Beirowski, B. et al. Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J. Neurosci. 29, 653-668 (2009).
39. Marinkovic, P. et al. Axonal transport deficits and degeneration can evolve independently in mouse models of amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 109, 4296-4301 (2012).
40. Jaworski, J. et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100 (2009).
41. Holtmaat, A., & Svoboda, K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10, 647-658 (2009).
42. Lichtman, J. W., & Colman, H. Synapse elimination and indelible memory. Neuron 25, 269-278 (2000).
43. Bridge, K. E. et al. Late onset distal axonal swelling in YFP-H transgenic mice. Neurobiol. Aging 30, 309-321 (2009).
44. Baas, P. W., & Lin, S. Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev. Neurobiol. 71, 403-418 (2011).
45. Marinkovic, P., Godinho, L., & Misgeld, T. in Imaging In Neuroscience And Development. (eds Yuste, R., & Konnerth, A.) Chapter 22 (CSH Press, 2011).
46. Caroni, P. Overexpression of growth-Associated proteins in the neurons of adult transgenic mice. J. Neurosci. Methods 71, 3-9 (1997).
47. Gurney, M. E. et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775 (1994).
48. Bruijn, L. I. et al. Elevated free nitrotyrosine levels, but not protein-bound nitrotyrosine or hydroxyl radicals, throughout amyotrophic lateral sclerosis (ALS)-like disease implicate tyrosine nitration as an aberrant in vivo property of one familial ALS-linked superoxide dismutase 1 mutant. Proc. Natl Acad. Sci. USA 94, 7606-7611 (1997).
49. Durand, G. M., Marandi, N., Herberger, S. D., Blum, R., & Konnerth, A. Quantitative single-cell RT-PCR and Ca2+ imaging in brain slices. Pflugers Arch. 451, 716-726 (2006).
50. Enes, J. et al. Electrical activity suppresses axon growth through Ca(v)1.2 channels in adult primary sensory neurons. Curr. Biol. 20, 1154-1164 (2010).
51. Witte, H., Neukirchen, D., & Bradke, F. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180, 619-632 (2008).
52. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., & Stuurman, N. Computer control of microscopes using microManager. Curr. Protoc. Mol. Biol Chapter 14, 20 (2010).
53. Angaut-Petit, D., & Faille, L. Inability of regenerating mouse motor axons to innervate a denervated target. Neurosci. Lett. 75, 163-168 (1987).
54. Nikic, I. et al. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat. Med. 17, 495-499 (2011).
55. Romanelli, E. et al. Cellular, subcellular and functional in vivo labeling of the spinal cord using vital dyes. Nat. Protoc. 8, 481-490 (2013).
56. Davalos, D. et al. Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J. Neurosci. Methods 169, 1-7 (2008).
57. Thevenaz, P., Ruttimann, U. E., & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process 7, 27-41 (1998).
58. Coupe, P., Munz, M., Manjon, J. V., Ruthazer, E. S., & Collins, D. L. A CANDLE for a deeper in vivo insight. Med. Image Anal. 16, 849-864 (2012).