Name: dorsal root ganglion injection and dorsal root crush injury as a model for sensory axon regeneration
Uploaded: 2017-05-03T14:00:00
Description: Watch this Scientific Journal Video about Dorsal Root Ganglion Injection and Dorsal Root Crush Injury as a Model for Sensory Axon Regeneration Video at JoVE.com

This work was supported by grants from the Christopher and Dana Reeve Foundation, the Medical Research Council, the European Research Council ECMneuro, and the Cambridge NHMRC Biomedical Research Center. We would like to express our deepest gratitude to Heleen Merel van &#8217;t Spijker and Justyna Barratt for their technical assistance during the filming. We would like to thank Dr. Elizabeth Moloney and Professor Joost Verhaagen (Netherlands Institute for Neuroscience) for assisting in AAV production.

All the following animal procedures were conducted in accordance with the United Kingdom Animals (Scientific Procedures) Act 1986. If unfamiliar with these procedures, please check with local/national regulations and seek veterinary advice before starting the protocol.
1. Choosing a Suitable Strain of Animals
NOTE: A dorsal root crush injury results in the loss of sensation and paw deafferentation. Common adverse effects of forepaw deafferentation can include over-grooming, self-mutilatio...

<ol>
	<li>Chew, D. J., Fawcett, J. W., Andrews, M. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+challenges+of+long-distance+axon+regeneration+in+the+injured+CNS.">The challenges of long-distance axon regeneration in the injured CNS.</a> Prog Brain Res. 201, 253-294 (2012).</li><li>Wu, A., Lauschke, J. L., Morris, R., Waite, P. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Characterization+of+rat+forepaw+function+in+two+models+of+cervical+dorsal+root+injury.">Characterization of rat forepaw function in two models of cervical dorsal root injury.</a> J Neurotrauma. 26 (1), 17-29 (2009).</li><li>Hocquemiller, M., Giersch, L., Audrain, M., Parker, S., Cartier, N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Adeno-Associated+Virus-Based+Gene+Therapy+for+CNS+Diseases.">Adeno-Associated Virus-Based Gene Therapy for CNS Diseases.</a> Hum Gene Ther. 27 (7), 478-496 (2016).</li><li>Cheah, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Expression+of+an+Activated+Integrin+Promotes+Long-Distance+Sensory+Axon+Regeneration+in+the+Spinal+Cord.">Expression of an Activated Integrin Promotes Long-Distance Sensory Axon Regeneration in the Spinal Cord.</a> J Neurosci. 36 (27), 7283-7297 (2016).</li><li>Andrews, M. 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T., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Purification+of+recombinant+adeno-associated+virus+by+iodixanol+gradient+ultracentrifugation+allows+rapid+and+reproducible+preparation+of+vector+stocks+for+gene+transfer+in+the+nervous+system.">Purification of recombinant adeno-associated virus by iodixanol gradient ultracentrifugation allows rapid and reproducible preparation of vector stocks for gene transfer in the nervous system.</a> Hum Gene Ther. 10 (11), 1885-1891 (1999).</li><li>Kappagantula, S., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Neu3+sialidase-mediated+ganglioside+conversion+is+necessary+for+axon+regeneration+and+is+blocked+in+CNS+axons.">Neu3 sialidase-mediated ganglioside conversion is necessary for axon regeneration and is blocked in CNS axons.</a> J Neurosci. 34 (7), 2477-2492 (2014).</li><li>Alto, L. T., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Chemotropic+guidance+facilitates+axonal+regeneration+and+synapse+formation+after+spinal+cord+injury.">Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury.</a> Nat Neurosci. 12 (9), 1106-1113 (2009).</li><li>Bonner, J. F., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Grafted+neural+progenitors+integrate+and+restore+synaptic+connectivity+across+the+injured+spinal+cord.">Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord.</a> J Neurosci. 31 (12), 4675-4686 (2011).</li><li>Wang, R., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Persistent+restoration+of+sensory+function+by+immediate+or+delayed+systemic+artemin+after+dorsal+root+injury.">Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury.</a> Nat Neurosci. 11 (4), 488-496 (2008).</li><li>Wong, L. E., Gibson, M. E., Arnold, H. M., Pepinsky, B., Frank, E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Artemin+promotes+functional+long-distance+axonal+regeneration+to+the+brainstem+after+dorsal+root+crush.">Artemin promotes functional long-distance axonal regeneration to the brainstem after dorsal root crush.</a> Proc Natl Acad Sci U S A. 112 (19), 6170-6175 (2015).</li><li>Tanguy, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Systemic+AAVrh10+provides+higher+transgene+expression+than+AAV9+in+the+brain+and+the+spinal+cord+of+neonatal+mice.">Systemic AAVrh10 provides higher transgene expression than AAV9 in the brain and the spinal cord of neonatal mice.</a> Front Mol Neurosci. 8, 36 (2015).</li><li>Foust, K. D., Poirier, A., Pacak, C. A., Mandel, R. J., Flotte, T. 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J., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Directed+evolution+of+a+novel+adeno-associated+virus+(AAV)+vector+that+crosses+the+seizure-compromised+blood-brain+barrier+(BBB).">Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood-brain barrier (BBB).</a> Mol Ther. 18 (3), 570-578 (2010).</li><li>Fagoe, N. D., Attwell, C. L., Kouwenhoven, D., Verhaagen, J., Mason, M. 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In this article, we present a step-by-step guide to perform a DRG injection and dorsal root crush injury in the lower cervical spinal cord of an adult rat. As this is an extremely invasive and delicate surgery, we strongly recommend that all potential users obtain sufficient training and practice before advancing to live animal surgery. The users should be familiar not only with spinal cord anatomy, but also with the surrounding muscle tissues, vertebral bone structure, and vasculature. Ideally, a competent user should b...

Achieving axon regeneration after nervous system injury is a challenging task1. To study the failure of axon regeneration in the central nervous system (CNS), researchers have used a plethora of nerve injury models. As regions of the CNS differ, it is important to use an anatomically appropriate model to study axon regeneration. By using the appropriate model, researchers can formulate a specific treatment based on the severity of injury, the neuronal cell type of interest, and the desired spinal tract for assessing regeneration, as opposed to a &#34;one-for-all&#34; treatment strategy.
In spinal cord injury, for example, the most debilitating symptoms stem from the loss of sensation and locomotion. Loss of sensation is caused by damage to the ascending sensory pathways, while the loss of locomotion is caused by damage to the descending motor pathways. Due to cellular and anatomical differences between these two pathways, many targeted axon regeneration studies only focus on one or the other pathway, with the rationale that successful recovery of either would be of tremendous benefit to patients. In this article, we present a protocol that uses a direct dorsal root ganglia (DRG) injection with a viral vector and a concurrent dorsal root crush injury in the lower cervical spinal cord of an adult rat as a model to study sensory axon regeneration.
DRG sensory neurons are responsible for relaying sensory information, such as tactile sensation and pain, from the periphery to the CNS. The long axonal projections of sensory neurons in the spinal cord serve as a good model to study long-distance axon regeneration. In addition, as rodents can survive a sensory pathway lesion such as a dorsal root crush injury with minimal welfare complications, researchers can study CNS axon regeneration without the need to completely lesion the spinal cord. A quadruple C5 - C8 (cervical level 5 - 8) dorsal root crush injury has been shown to be a useful model for forepaw deafferentation2. Additionally, a dorsal root crush injury provides a &#34;cleaner&#34; model to study axon regeneration than a direct spinal cord injury because it is uncomplicated by other factors such as glial scar formation.
The use of viral gene therapy to reprogram neurons into a regenerative state has been increasingly regarded as a promising treatment strategy for many neurological conditions3. Studies have shown the application of an adeno-associated virus (AAV) vector carrying the transgene of a growth-promoting protein can achieve robust axon regeneration with behavioral recovery4,5,6. The apparent low pathogenicity of AAV in eliciting an immune response and the ability to transduce non-dividing cells, such as neurons, make it the optimal vector for gene therapy. Additionally, the recombinant AAV form is used for therapy. In this form, it is incapable of integrating its viral genome into the host genome7, reducing the risk of insertional mutagenesis as compared to other viral vectors, such as lentivirus. This makes AAV a safe choice for gene therapy applications.
As a DRG contains the cell bodies of sensory neurons, it is the most appropriate anatomical target for the administration of virus for gene therapy to study and/or promote sensory axon regeneration. In a study comparing different AAV serotypes and lentivirus, AAV serotype 5 (AAV5) was shown to be the most efficient in transducing DRG neurons over a time course of at least 12 weeks when injected directly into the DRG8. Additionally, AAV can achieve more than 40% transduction efficiency, transducing all DRG neuronal subtypes, such as the large-diameter neurofilament 200 kDa (NF200)-positive neurons and the small-diameter calcitonin gene-related peptide (CGRP)- or isolectin b4 (IB4)-positive neurons4,8.
As the surgical procedure of DRG injection and dorsal root crush injury is extremely invasive and delicate, we believe that this article will help new users to learn the procedure in a very efficient manner. In this article, we show representative results from adult rats four weeks after the injection of a control virus AAV5-GFP (green fluorescent protein) into C6 - C7 DRGs with a concurrent C5 - C8 dorsal root crush injury. This model is especially suitable for researchers who are investigating the use of viral gene therapy to promote sensory axon regeneration.

<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>Fast Green FCF dye</td>
			<td>Sigma-Aldrich</td>
			<td>F7258</td>
			<td>For visualizing colorless solution. Recommended concentration: 1%</td>
		</tr>
		<tr>
			<td>Cholera Toxin B subunit</td>
			<td>List Biological Laboratories</td>
			<td>104</td>
			<td>For anterograde axonal tracing. Recommended concentration: 1%</td>
		</tr>
		<tr>
			<td>IsoFlo</td>
			<td>Zoetis</td>
			<td>115095</td>
			<td>Inhalation anesthetic (active ingredient: isoflurane)</td>
		</tr>
		<tr>
			<td>Baytril 2.5% injectable</td>
			<td>Bayer</td>
			<td>05032756093017</td>
			<td>Antibiotic (active ingredient: enrofloxacin). Manufacturer&#39;s recommended dosage: 10 mg/kg</td>
		</tr>
		<tr>
			<td>Carprieve 5.0% w/v</td>
			<td>Norbrook</td>
			<td>02000/4229</td>
			<td>Analgesic (active ingredient: carprofen). Manufacturer&#39;s recommended dosage: 4 mg/kg</td>
		</tr>
		<tr>
			<td>Lacri-Lube</td>
			<td>Allergan</td>
			<td>PL 00426/0041</td>
			<td>Eye ointment</td>
		</tr>
		<tr>
			<td>Olsen-Hegar Needle Holder</td>
			<td>Fine Science Tools</td>
			<td>FST 12502-12</td>
			<td></td>
		</tr>
		<tr>
			<td>Friedman Pearson Rongeur Curved 0.7mm Cup</td>
			<td>Fine Science Tools</td>
			<td>FST 16121-14</td>
			<td></td>
		</tr>
		<tr>
			<td>Bonn Micro Forceps</td>
			<td>Fine Science Tools</td>
			<td>FST 11083-07</td>
			<td>For performing dorsal root crush injury</td>
		</tr>
		<tr>
			<td>Tissue Separating Scissors</td>
			<td>Fine Science Tools</td>
			<td>FST 14072-10</td>
			<td></td>
		</tr>
		<tr>
			<td>Fine Scissors</td>
			<td>Fine Science Tools</td>
			<td>FST 14058-11</td>
			<td></td>
		</tr>
		<tr>
			<td>Micro-Adson Forceps</td>
			<td>Fine Science Tools</td>
			<td>FST 11018-12</td>
			<td></td>
		</tr>
		<tr>
			<td>Goldstein Retractor</td>
			<td>Fine Science Tools</td>
			<td>FST 17003-03</td>
			<td></td>
		</tr>
		<tr>
			<td>Vannas Spring Scissors (straight)</td>
			<td>Fine Science Tools</td>
			<td>FST 15018-10</td>
			<td></td>
		</tr>
		<tr>
			<td>SURGIFOAM Absorbable Gelatin Sponge</td>
			<td>Ethicon</td>
			<td>1972</td>
			<td>For bleeding control</td>
		</tr>
		<tr>
			<td>Microliter Syringe RN701 (10 &#956;l)</td>
			<td>Hamilton</td>
			<td>80330</td>
			<td></td>
		</tr>
		<tr>
			<td>Custom-made Removable Needle (for DRG injection)</td>
			<td>Hamilton</td>
			<td>7803-05</td>
			<td>33 gauge, 38 mm, point style 3</td>
		</tr>
		<tr>
			<td>Custom-made Removable Needle (for CTB injection)</td>
			<td>Hamilton</td>
			<td>7803-05</td>
			<td>33 gauge, 10 mm, point style 3</td>
		</tr>
		<tr>
			<td>UltraMicroPump with SYS-Micro4 Controller</td>
			<td>World Precision Instruments</td>
			<td>UMP3-1</td>
			<td></td>
		</tr>
	</tbody>
</table>

dorsal root ganglion injection and dorsal root crush injury as a model for sensory axon regeneration

Achieving axon regeneration after nervous system injury is a challenging task. As different parts of the central nervous system (CNS) differ from each other anatomically, it is important to identify an appropriate model to use for the study of axon regeneration. By using a suitable model, we can formulate a specific treatment based on the severity of injury, the neuronal cell type of interest, and the desired spinal tract for assessing regeneration. Within the sensory pathway, DRG neurons are responsible for relaying sensory information from the periphery to the CNS. We present here a protocol that uses a DRG injection with a viral vector and a concurrent dorsal root crush injury in the lower cervical spinal cord of an adult rat as a model to study sensory axon regeneration. As demonstrated using a control virus, AAV5-GFP, we show the effectiveness of a direct DRG injection in transducing DRG neurons and tracing sensory axons into the spinal cord. We also show the effectiveness of the dorsal root crush injury in denervating the forepaw as an injury model for evaluating axon regeneration. Despite the requirement for specialized training to perform this invasive surgical procedure, the protocol is flexible, and potential users can modify many parts to accommodate their experimental requirements. Importantly, it can serve as a foundation for those in search of a suitable animal model for their studies. We believe that this article will help new users to learn the procedure in a very efficient and effective manner.

As a representation, a transverse spinal cord section with the attached DRG is presented to show the effectiveness of this protocol in transducing DRG neurons and tracing sensory axons in the spinal cord four weeks after injecting a control virus, AAV5-GFP, directly into the C7 DRG without a dorsal root crush injury (Figure 1A). Axons in both the dorsal column and the dorsal horn of the spinal cord express GFP (Figure 1B), as well as the cell bodies and a...

Watch this Scientific Journal Video about Dorsal Root Ganglion Injection and Dorsal Root Crush Injury as a Model for Sensory Axon Regeneration Video at JoVE.com

Dorsal Root Ganglion Injection and Dorsal Root Crush Injury as a Model for Sensory Axon Regeneration Video (Video) | JoVE

This protocol presents the use of a dorsal root ganglion (DRG) injection with a viral vector and a concurrent dorsal root crush injury in an adult rat as a model to study sensory axon regeneration. This model is suitable for investigating the use of gene therapy to promote sensory axon regeneration.

Dorsal Root Ganglion Injection and Dorsal Root Crush Injury as a Model for Sensory Axon Regeneration

Achieving axon regeneration after nervous system injury is a challenging task. As different parts of the central nervous system (CNS) differ from each ...

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Neuroscience

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There are growing interests to study the molecular and cellular interactions among immune cells and sensory neurons in the dorsal root ganglia after ...