3D imaging of axons in transparent spinal cords from rodents and nonhuman primates

eNeuro

Volumn 2, Issue 2, 2015, Pages

  Soderblom, Cynthia ^a   Lee, Do Hun ^a   Dawood, Abdul ^a   Carballosa, Melissa ^a   Santamaria, Andrea Jimena ^a   Benavides, Francisco D ^a   Jergova, Stanislava ^a   Grumbles, Robert M ^a   Thomas, Christine K ^a   Park, Kevin K ^a   Guest, James David ^a   Lemmon, Vance P ^a   Lee, Jae K ^a   Tsoulfas, Pantelis ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

3DISCO; Axon regeneration; Spinal cord injury; Tissue clearing

Indexed keywords

EID: 84943419856     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0001-15.2015     Document Type: Article

References (41)

1. Arenkiel BR, Hasegawa H, Yi JJ, Larsen RS, Wallace ML, Philpot BD, Wang F, Ehlers MD (2011) Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PloS One 6:e29423. CrossRef Medline
2. Ayuso E, Mingozzi F, Montane J, Leon X, Anguela XM, Haurigot V, Edmonson SA, Africa L, Zhou S, High KA, Bosch F, Wright JF (2010) High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene Ther 17:503-510. CrossRef Medline
3. Becker K, Jährling N, Saghafi S, Weiler R, Dodt HU (2012) Chemical clearing and dehydration of GFP expressing mouse brains. PLoS One 7:e33916. CrossRef Medline
4. Belle M, Godefroy D, Dominici C, Heitz-Marchaland C, Zelina P, Hellal F, Bradke F, Chédotal A (2014) A simple method for 3D analysis of immunolabeled axonal tracts in a transparent nervous system. Cell Rep 9:1191-1201. CrossRef Medline
5. Blits B, Derks S, Twisk J, Ehlert E, Prins J, Verhaagen J (2010) Adeno-associated viral vector (AAV)-mediated gene transfer in the red nucleus of the adult rat brain: comparative analysis of the transduction properties of seven AAV serotypes and lentiviral vectors. J Neurosci Methods 185:257-263. CrossRef Medline
6. Cajal SRy (1888) Estructura de los centros nerviosos de las aves. Rev Trimest Histol Norm Patol 1:1-10.
7. Cearley CN, Vandenberghe LH, Parente MK, Carnish ER, Wilson JM, Wolfe JH (2008) Expanded repertoire of AAV vector serotypes mediate unique patterns of transduction in mouse brain. Mol Ther 16:1710-1718. CrossRef Medline
8. Chamberlin NL, Du B, de Lacalle S, Saper CB (1998) Recombinant adeno-associated virus vector: use for transgene expression and anterograde tract tracing in the CNS. Brain Res 793:169-175. Medline
9. Chung K, Wallace J, Kim SY, Kalyanasundaram S, Andalman AS, Davidson TJ, Mirzabekov JJ, Zalocusky KA, Mattis J, Denisin AK, Pak S, Bernstein H, Ramakrishnan C, Grosenick L, Gradinaru V, Deisseroth K (2013) Structural and molecular interrogation of intact biological systems. Nature 497:332-337. CrossRef Medline
10. Chung KH, Hart CC, Al-Bassam S, Avery A, Taylor J, Patel PD, Vojtek AB, Turner DL (2006) Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR-155. Nucleic Acids Res 34:e53. CrossRef Medline
11. Ertürk A, Becker K, Jährling N, Mauch CP, Hojer CD, Egen JG, Hellal F, Bradke F, Sheng M, Dodt HU (2012a) Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat Protoc 7:1983-1995. CrossRef Medline
12. Ertürk A, Mauch CP, Hellal F, Forstner F, Keck T, Becker K, Jahrling N, Steffens H, Richter M, Hubener M, Kramer E, Kirchhoff F, Dodt HU, Bradke F (2012b) Three-dimensional imaging of the unsec-tioned adult spinal cord to assess axon regeneration and glial responses after injury. Nat Med 18:166-171.
13. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51. Medline
14. Fitzsimons HL, Bland RJ, During MJ (2002) Promoters and regulatory elements that improve adeno-associated virus transgene expression in the brain. Methods 28:227-236. Medline
15. Fremeau RT, Jr., Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260. CrossRef
16. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM (2006) Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26:8609-8621. CrossRef Medline
17. Gruner JA (1992) A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 9:123-126. Medline
18. Huisken J, Swoger J, Del Bene F, Wittbrodt J, Stelzer EH (2004) Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305:1007-1009. CrossRef Medline
19. Hutson TH, Verhaagen J, Yañez-Muñoz RJ, Moon LD (2012) Corticospinal tract transduction: a comparison of seven adeno-associated viral vector serotypes and a non-integrating lentiviral vector. Gene Ther 19:49-60. CrossRef
20. Lacroix S, Havton LA, McKay H, Yang H, Brant A, Roberts J, Tuszynski MH (2004) Bilateral corticospinal projections arise from each motor cortex in the macaque monkey: a quantitative study. J Comp Neurol 473:147-161. CrossRef
21. Lee JK, Johnson CS, Wrathall JR (2007) Up-regulation of 5-HT2 receptors is involved in the increased H-reflex amplitude after contusive spinal cord injury. Exp Neurol 203:502-511. CrossRef Medline
22. Lemmon VP, Ferguson AR, Popovich PG, Xu XM, Snow DM, Igarashi M, Beattie CE, Bixby JL, Consortium M (2014) Minimum information about a spinal cord injury expriment: a proposed reporting standard for spinal cord injury expriements. J Neurotrauma 31: 1354-1361. CrossRef Medline
23. Liang H, Paxinos G, Watson C (2012) The red nucleus and the rubrospinal projection in the mouse. Brain Struct Funct 217:221-232. CrossRef Medline
24. Luo X, Salgueiro Y, Beckerman SR, Lemmon VP, Tsoulfas P, Park KK (2013) Three-dimensional evaluation of retinal ganglion cell axon regeneration and pathfinding in whole mouse tissue after injury. Exp Neurol 247:653-662. CrossRef Medline
25. Mason MR, Ehlert EM, Eggers R, Pool CW, Hermening S, Huseinovic A, Timmermans E, Blits B, Verhaagen J (2010) Comparison of AAV serotypes for gene delivery to dorsal root ganglion neurons. Mol Ther 18:715-724. CrossRef Medline
26. Papadakis ED, Nicklin SA, Baker AH, White SJ (2004) Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther 4:89-113. Medline
27. Paterna JC, Büeler H (2002) Recombinant adeno-associated virus vector design and gene expression in the mammalian brain. Methods 28:208-218. Medline
28. Paterna JC, Moccetti T, Mura A, Feldon J, Büeler H (2000) Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther 7:1304-1311. CrossRef Medline
29. Persson S, Boulland JL, Aspling M, Larsson M, Fremeau RT, Jr., Edwards RH, Storm-Mathisen J, Chaudhry FA, Broman J (2006) Distribution of vesicular glutamate transporters 1 and 2 in the rat spinal cord, with a note on the spinocervical tract. J Comp Neurol 497:683-701. CrossRef Medline
30. Petrs-Silva H, Dinculescu A, Li Q, Min SH, Chiodo V, Pang JJ, Zhong L, Zolotukhin S, Srivastava A, Lewin AS, Hauswirth WW (2009) High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 17:463-471. CrossRef Medline
31. Renier N, Wu Z, Simon DJ, Yang J, Ariel P, Tessier-Lavigne M (2014) iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:896-910. CrossRef Medline
32. Rotterman TM, Nardelli P, Cope TC, Alvarez FJ (2014) Normal distribution of VGLUT1 synapses on spinal motoneuron dendrites and their reorganization after nerve injury. J Neurosci 34:3475-3492. CrossRef Medline
33. Steward O, Zheng B, Tessier-Lavigne M (2003) False resurrections: distinguishing regenerated from spared axons in the injured central nervous system. J Comp Neurol 459:1-8. CrossRef Medline
34. Swett JE, Wikholm RP, Blanks RH, Swett AL, Conley LC (1986) Mo-toneurons of the rat sciatic nerve. Exp Neurol 93:227-252. Medline
35. Takao D, Taniguchi A, Takeda T, Sonobe S, Nonaka S (2012) High-speed imaging of amoeboid movements using light-sheet microscopy. PLoS One 7:e50846. CrossRef Medline
36. Taymans JM, Vandenberghe LH, Haute CV, Thiry I, Deroose CM, Mortelmans L, Wilson JM, Debyser Z, Baekelandt V (2007) Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther 18:195-206. CrossRef Medline
37. Tenenbaum L, Chtarto A, Lehtonen E, Velu T, Brotchi J, Levivier M (2004) Recombinant AAV-mediated gene delivery to the central nervous system. J Gene Med 6 Suppl 1:S212-222. CrossRef Medline
38. Tomer R, Ye L, Hsueh B, Deisseroth K (2014) Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nat Protoc 9:1682-1697. CrossRef Medline
39. Tuszynski MH, Steward O (2012) Concepts and methods for the study of axonal regeneration in the CNS. Neuron 74:777-791. CrossRef Medline
40. Yata Y, Scanga A, Gillan A, Yang L, Reif S, Breindl M, Brenner DA, Rippe RA (2003) DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 37:267-276. CrossRef Medline
41. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO (2002) Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28:158-167. Medline