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CDB Seminars
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All Seminars are held in the Gavin De Beer Lecture Theatre, Anatomy Building, Thursday 1-2pm

11 Dec: Marcus Ghosh (Rihel lab)/ (Chubbs lab)

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Prof Patrick Anderson Laboratory

Regeneration in the injured mammalian brain and spinal cord

Patrick Anderson
Bob Lieberman
Greg Campbell

Brain or spinal cord injuries have devastating consequences and cannot yet be repaired. Much of their effect is the result of damage to axons which, unlike their counterparts in peripheral nerves, do not normally regenerate. Unfortunately, although there have been several exciting reports of axonal regeneration in the mammalian spinal cord in recent years, few if any of these apparent breakthroughs have been replicated in different laboratories, and there is still no consensus as to the reasons for the failure of axonal regeneration in the CNS. The aims of our laboratory are to gain an understanding about what normally prevents axonal regeneration in the CNS, and to use this knowledge to develop strategies for improving the repair of CNS lesions such as spinal injuries and stroke.

The expertise in our lab is in experimental surgery, neuroanatomy, electron microscopy, immunohistochemistry, in situ hybridisation and molecular biology. These techniques are essential for careful and accurate investigation of axonal regeneration. With our collaborators in the UK, Holland, Germany and the USA we generate and investigate transgenic mice to identify molecules that are important for axonal regeneration, and use viral vectors for gene therapy experiments to promote regeneration. Overall we seek to gain greater knowledge of the events occurring in the damaged nervous system, while trialing promising approaches to enhancing axonal regeneration.

Ideas behind our research include:

(i) Identifying neuronal genes that control regeneration. The ability of neurons to regenerate axons is determined by their ability to express growth-related genes after injury. Regenerative capacity is correlated with expression of transcription factors such as c-jun and ATF3, growth cone proteins such as GAP-43, CAP-23 and SCG10, and the adhesion molecules L1 and CHL1. Increasing the expression of these genes by injured CNS neurons may be an essential element in repairing the injured brain and spinal cord.

(ii) Identifying inhibitory molecules and their receptors in the injured nervous system. The dominant hypothesis seeking to explain the absence of regeneration in the CNS is that axonal elongation is normally prevented by inhibitory molecules. Many molecules that are capable of blocking neurite elongation in vitro are present in CNS tissue. These include NG2, Nogo and extracellular matrix molecules. We want to establish if any of these are really important in preventing regeneration.

(iii) Prevention of secondary damage. Much of the damage to axons following spinal injury occurs after the initial lesion. This provides a window of opportunity for reducing the effects of injury. This work has immediate clinical relevance and is a developing part of our research programme.

Techniques used and recent results.

Transgenic animals can be used to demonstrate the importance of individual molecules for the regeneration of CNS axons. Overexpressing individual growth-associated molecules, such as GAP-43 and L1, has limited effects on axonal regeneration in the CNS, probably because a whole program of genes must be expressed to regenerate axons vigorously. Transcription factors, which can control the expression of other genes, are now our favoured targets. Knocking out growth-related molecules should enable their importance to be established. Sometimes conventional knockouts are not suitable for regeneration experiments because of their role in development and we are currently generating conditional knockouts for several molecules including GAP-43, SCG10 and CAP-23. ATF3 knockouts are being investigated; if ATF3 is an important switch controlling axonal regeneration, recovery from nerve injury to the mutants should be poor. Knocking out inhibitory molecules should dramatically improve axonal regeneration if such molecules form a significant barrier for regenerating axons. We have tested regeneration in the spinal cord in tenascin-R knockouts and NG2 knockouts, and our results suggest that neither molecule is responsible for preventing axonal regeneration in the spinal cord.

Mapping the distribution of growth-inhibitory molecules and their receptors
We recently showed that the Nogo-66 receptor (NgR) was only expressed by a minority of neurons and could not explain the general failure of regeneration in the CNS. We are now investigating genes closely related to NgR. Similarly we have shown that NG2, widely believed to be a major inhibitory protein in the damaged spinal cord, is also strongly expressed in injured peripheral nerves where regeneration is vigorous. Gene therapy. In collaboration with Rob Coffin at UCL and J. Verhaagen in Amsterdam we are exploring gene therapy approaches to improving the outcome of spinal cord injury. We have shown that when spinal cord neurons and glia are transfected with the NT-3 gene using an adenovirus vector, regenerating dorsal root axons enter the cord in large numbers and regenerate deep into the grey matter. Unfortunately, delivery of neurotrophins to the CNS is less effective at producing regeneration of axons in ascending and descending tracts within the spinal cord, probably because of inhibitory molecules at lesion sites. We are now developing vectors that can deliver to neurons enzymes that can digest inhibitory molecules (metalloproteases), or deliver antisense (siRNA) sequences to block the expression of receptors for inhibitory molecules. A related approach is the use of conventional antisense oligonucleotides, which we have shown can readily penetrate the spinal cord and knock down gene expression. Increasing axonal sprouting and regeneration by other methods. We are testing various unconventional approaches to produce greater regeneration in the spinal cord. Vaccination with extracts of CNS tissue (myelin, lesion scars) induces the production of antibodies against inhibitory molecules. In our hands this enhances axonal sprouting in the injured spinal cord, but does not lead to long-distance regeneration. Inflammation around neuronal cell bodies has also been shown to increase expression of growth-associated molecules and enhance sprouting of corticospinal axons in the spinal cord. Reducing secondary injury. We have shown that treatment with the immunosuppressant FK506 or antisense connexin 43 are neuroprotective and improve recovery from spinal cord injury.

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A growing sensory axon in culture has the putative inhibitor of axonal growth (Nogo-A, red) in its growth cones. Is neuronal Nogo involved in promoting axonal regeneration?


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Postnatal Day 0 optic disk. Nogo-A (red) is found in growing retinal ganglion cell axons. What is a putative inhibitory molecule (Nogo-A) doing in growing axons? We think that Nogo may be playing a role in axonal growth!

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Sciatic nerve injury site showing regenerating axons (red) and cells expressing another putative inhibitor of axonal regeneration NG2 (green). What is NG2 doing among regenerating axons- could it also play a role in guiding regenerating axons?

Contact Details:

Research Dept of Cell and Developmental Biology
UCL
London
WC1E 6BT
England


e-mail:

a.lieberman at ucl.ac.uk
p.anderson at ucl.ac.uk
g.campbell at ucl.ac.uk

Publications:

  • Cronin,M., Anderson,P., Green,C.R., Becker,D.L. (2006). Antisense delivery and protein knockdown within the intact central nervous system. Frontiers in Bioscience 11, 2967-2975.
  • Fabes,J., Anderson,P., Yanez-Munoz,R.J., Thrasher,A., Brennan,C., Bolsover,S. (2006). Accumulation of the inhibitory receptor EphA4 may prevent regeneration of corticospinal tract axons following lesion. European Journal of Neuroscience 23(7), 1721-1730.
  • Hossain-Ibrahim,M.K., Rezajooi,K., MacNally,J.K., Mason,M.R., Lieberman,A.R., Anderson,P.N. (2006). Effects of lipopolysaccharide-induced inflammation on expression of growth-associated genes by corticospinal neurons. BMC Neuroscience 7, 8.
  • Yanez-Munoz,R.J., Balaggan,K.S., MacNeil,A., Howe,S.J., Schmidt,M., Smith,A.J., Buch,P., MacLaren,R.E., Anderson,P.N., Barker,S.E., Duran,Y., Bartholomae,C., Von Kalle,C., Heckenlively,J.R., Kinnon,C., Ali,R.R., Thrasher,A.J. (2006). Effective gene therapy with non-integrating lentiviral vectors. Nature Medicine 12(3), 348-353.
  • Zhang,X., Bo,X., Anderson,P.N., Lieberman,A.R., Zhang,Y. (2006). Distribution and expression of tissue inhibitors of metalloproteinase in dorsal root entry zone and dorsal column after dorsal root injury. Journal of Neuroscience Research 84(2), 278-290.
  • Campbell,G., Hutchins,K., Winterbottom,J., Grenningloh,G., Lieberman,A.R., Anderson,P.N. (2005). Upregulation of activating transcription factor 3 (ATF3) by intrinsic CNS neurons regenerating axons into peripheral nerve grafts. Experimental Neurology 192, 340-347.
  • Cellek,S., Anderson,P.N., Foxwell,N.A. (2005). Nitrergic neurodegeneration in cerebral arteries of streptozotocin-induced diabetic rats: a new insight into diabetic stroke. Diabetes 54, 212-219.
  • Zhang,Y., Bo,X., Schoepfer,R., Holtmaat,A.J., Verhaagen,J., Emson,P.C., Lieberman,A.R., Anderson,P.N. (2005). Growth-associated protein GAP-43 and L1 act synergistically to promote regenerative growth of Purkinje cell axons in vivo. Proceedings of the National Academy of Sciences of the United States of America 102, 14883-14888.
  • Ahmed,B.Y., Chakravarthy,S., Eggers,R., Hermens,W.T.J.M.C., Zhang,J.Y., Niclou,S.P., Levelt,C., Sablitzky,F., Anderson,P.N., Lieberman,A.R., Verhaagen,J. (2004). Efficient delivery of Cre-recombinase to neurons in vivo and stable transduction of neurons using adeno-associated and lentiviral vectors. BMC Neuroscience 5(4)
  • Anderson,P.N., Campbell,G., Hunt,D., Winterbottom,J.K., Watson,S.D., Lieberman,A.R., Prinjha,R.K. (2004). Nogo-A is expressed in growing and regenerating axons. Society for Neuroscience Online 729.5
  • Campbell,G., Hutchings,K., Winterbottom,J., Grenningloh,G., Lieberman,A.R., Anderson,P.N. (2004). Upregulation of activating transcription factor 3 (ATF3) by intrinsic CNS neurons regenerating axons into peripheral nerve grafts. Experimental Neurology Online
  • Hossain-Ibrahim,K., Rezajooi,K., Stallcup,W.B., Anderson,P.N., Lieberman,A. (2004). Axonal regeneration in NG2-deficient mice. Society for Neuroscience Online 948.12
  • Hunt,D., Hossain-Ibrahim,K., Mason,M.R., Coffin,R.S., Lieberman,A.R., Winterbottom,J., Anderson,P.N. (2004). ATF3 upregulation in glia during Wallerian degeneration: differential expression in peripheral nerves and CNS white matter. BMC Neuroscience 5(9),
  • Mason,M.R.J., Coffin,R.S., Groutsi-Allwright,F., Lieberman,A.R., Anderson,P.N. (2004). Matrix metalloproteinase expression in the injured nervous system and delivery of MT1-MMP to neurons with HSV-1 vectors. Society for Neuroscience Online 43.4
  • Mingorance,A., Fontana,X., Sole,M., Burgaya,F., Urena,J.M., Teng,F.Y.H., Tang,B.L., Hunt,D., Anderson,P.N., Bethea,J.R., Schwab,M.E., Soriano,E., del Rio,J.A. (2004). Regulation of Nogo and Nogo receptor during the development of the entorhino-hippocampal pathway and after adult hippocampal lesions. Molecular and Cellular Neuroscience 26, 34-49.
  • Rezajooi,K., Pavlides,M., Winterbottom,J., Stallcup,W.B., Hamlyn,P.J., Lieberman,A.R., Anderson,P.N. (2004). NG2 proteoglycan expression in the peripheral nervous system: upregulation following injury and comparison with CNS lesions. Molecular and Cellular Neuroscience 25, 572-584.
  • Zhang,X., Bo,X., Anderson,P.N., Lieberman,A.R., Zhang,Y. (2004). Expression and distribution of tissue inhibitors of metalloproteinase in the rat spinal cord following dorsal root injury. Society for Neuroscience Online 107.4
  • Campbell,G., Kitching,J., Anderson,P.N., Lieberman,A.R. (2003). Different effects of astrocytes and Schwann cells on regenerating retinal axons. Neuroreport 14, 2085-2088.
  • Chaisuksunt,V., Campbell,G., Zhang,Y., Schachner,M., Lieberman,A.R., Anderson,P.N. (2003). Expression of regeneration-related molecules in injured and regenerating striatal and nigral neurons. Journal of Neurocytology 32, 161-183.
  • Hunt,D., Coffin,R.S., Anderson,P.N. (2003). The Nogo receptor, its ligands and axonal regeneration in the spinal cord; A review. Journal of Neurocytology 31, 93-120.
  • Hunt,D., Coffin,R.S., Prinjha,R.K., Campbell,G., Anderson,P.N. (2003). Nogo-A expression in the intact and injured nervous system. Molecular and Cellular Neuroscience 24(4), 1083-1102.
  • Mason,M.R.J., Lieberman,A.R., Anderson,P.N. (2003). Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. European Journal of Neuroscience 18, 789-802.
  • Mason,M.R.J., Lieberman,A.R., Latchman,D.S., Anderson,P.N. (2003). FKBP12 mRNA expression is upregulated by intrinsic CNS neurons regenerating axons into peripheral nerve grafts in the brain. Experimental Neurology 181, 181-189.
  • Ahmed,B.Y., Hermens,W.T.J., Niclou,S., Levelt,C., Eggers,R.E., Sablitzky,F., Anderson,P.N., Verhaagen,J., Lieberman,A.R. (2002). Efficient delivery of Cre-recombinase to adult mouse brain using adeno-associated and lentiviral vectors. Society for Neuroscience Abstracts 28
  • Davis,G.R., Dowker,S.E.P., Elliott,J.C., Anderson,P., Wassif,H.S., Boyde,A., Goodship,A.E., Stock,S.R., Ignatiev,K. (2002). 49th Annual Conference on Applications of X-ray Analysis, 31 July-4 August, Denver, CO, Huang,T.C., 8 others (ed.) Newtown Square, PA:International Centre for Diffraction Data, 44, 485-490
  • Elliott,J.C., Davis,G.R., Anderson,P., Dowker,S.E.P., Polly,P.D., Wilson,R.M., Boyde,A., Stock,S.R.,O'Dwyer,J., Cloetens,P. (2002). X-ray microtomographic studies in 3D of bones, teeth and engineering materials. Proceedings of the Royal Microscopical Society 37, 18
  • Hunt,D., Mason,M.R.J., Campbell,G., Coffin,R., Anderson,P.N. (2002). Nogo receptor mRNA expression in intact and regenerating CNS neurons. Molecular and Cellular Neuroscience 20, 537-552.
  • Mason,M.R.J., Lieberman,A.R., Grenningloh,G., Anderson,P.N. (2002). Transcriptional upregulation of SCG10 and CAP-23 is correlated with regeneration of the axons of peripheral and central neurons in vivo. Molecular and Cellular Neuroscience 20, 595-615.
  • Zhang,Y., Holtmaat,A.J.G., Verhaagen,J., Emson,P.C., Winterbottom,J., Campbell,G., Lieberman,A.R., Anderson,P.N. (2002). Overexpression of GAP-43 and L1 fail to promote Purkinje cells to regenerate their axons into peripheral nerve grafts. Society for Neuroscience Abstracts 28
  • Davis,G.R., Dowker,S.E.P., Elliott,J.C., Anderson,P., Wassif,H.S., Boyde,A., Stock,S.R. (2001). Non-destructive 3D structural studies by X-ray microtomography. 50th Annual Denver X-ray Conference 132
  • Lilley,C.E., Groutsi,F., Han,Z., Palmer,J.A., Anderson,P.N., Latchman,D.S., Coffin,R.S. (2001). Multiple immediate-early gene-deficient herpes simplex virus vectors allowing efficient gene delivery to neurons in culture and widespread gene delivery to the central nervous system in vivo. Journal of Virology 75(9), 4343-4356.
  • Pasterkamp,R.J., Anderson,P.N., Verhaagen,J. (2001). Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin 3A. European Journal of Neuroscience 13, 1-16.
  • Smith,M.D., Melton,L.A., Ensor,E.A., Packham,G., Anderson,P.N., Kinloch,R.A., Latchman,D.S. (2001). Brn-3a activates the expression of bcl-xl and promotes neuronal survival in vivo as well as in vitro. Molecular and Cellular Neuroscience 17, 460-470.
  • Zhang,Y., Tohyama,K., Winterbottom,J., Haque,N.S.K., Schachner,M., Lieberman,A.R., Anderson,P.N. (2001). Correlation between putative inhibitory molecules at the dorsal root entry zone and failure of dorsal root axonal regeneration. Molecular and Cellular Neuroscience 17, 444-459. ISSN: 1044-7431
  • Campbell,G., Shotton,H., Sam,S.A.H., Anderson,P.N., Lieberman,A.R. (2000). Spontaneous regeneration of retinal ganglion axons following optic nerve crush in the adult rat-retrograde and anterograde labelling and EM studies. European Journal of Neuroscience 12(11), 336
  • Chaisuksunt,V., Campbell,G., Zhang,Y., Schachner,M., Lieberman,A.R., Anderson,P.N. (2000). The cell recognition molecule CHL1 is strongly upregulated by injured and regenerating thalamic neurons. Journal of Comparative Neurology 425, 382-392.
  • Chaisuksunt,V., Zhang,Y., Anderson,P.N., Campbell,G., Vaudano,E., Schachner,M., Lieberman,A.R. (2000). Axonal regeneration from CNS neurons in the cerebellum and brainstem of adult rats: correlation with the patterns of expression and distribution of messenger RNAs for L1, CHL1, c-jun and growth associated protein-43. Neuroscience 100, 87-108.
  • Lilley,C.E., Groutsi,F., Han,Z.Q., Anderson,P., Latchman,D.S., Coffin,R.S. (2000). Multiply disabled herpes simplex virus vectors for gene delivery to the central nervous system. European Journal of Neuroscience 12, 308-308.
  • Mason,M.R.J., Campbell,G., Caroni,P., Anderson,P.N., Lieberman,A.R. (2000). Overexpression of GAP-43 in thalamic projection neurons of transgenic mice does not enable them to regenerate axons through peripheral nerve grafts. Experimental Neurology 165, 143-152.
  • Zhang,Y., Roslan,R., Lang,D., Schachner,M., Lieberman,A.R., Anderson,P.N. (2000). Expression of CHL1 and L1 by neurons and glia following sciatic nerve and dorsal root injury. Molecular and Cellular Neuroscience 16, 71-86.
  • Anderson,P.N., Lieberman,A.R. (1999). Intrinsic determinants of differential axonal regeneration by adult mammalian CNS neurons. Chapter 3 in Saunders,N.R., Dziegielewska,K.M. (ed.) Degeneration and Regeneration in the Nervous System. Harwood Academic Press, 53-75
  • Bavetta,S., Hamlyn,P.J., Burnstock,G., Lieberman,A.R., Anderson,P.N. (1999). The effects of FK506 on dorsal column axons following spinal cord injury in adult rats: neuroprotection and local regeneration. Experimental Neurology 158(2), 382-393.
  • Campbell,G., Holt,J.K.L., Shotton,H.R., Anderson,P.N., Bavetta,S., Lieberman,A.R. (1999). Spontaneous axonal regeneration after optic nerve injury in adult rat. NeuroReport 10, 3955-3960.
  • Chong,M.S., Woolf,C.J., Haque,N.S.K., Anderson,P.N. (1999). Axonal regeneration from injured dorsal roots into the spinal cord of adult rats. Journal of Comparative Neurology 410, 42-54.
  • Harding,D.I., Greensmith,L., Mason,M., Anderson,P.N., Vrbova,G. (1999). Overexpression of GAP-43 induces prolonged sprouting and causes death of adult motoneurons. European Journal of Neuroscience 11, 2237-2242.
  • Anderson,P.N., Bavetta,S., Haque,N.S.K., Hamlyn,P.J., Lieberman,A.R. (1998). FK506 promotes axonal sparing after spinal cord injury. Society for Neuroscience Abstracts 24(1), 545-545
  • Anderson,P.N., Campbell,G., Zhang,Y., Lieberman,A.R. (1998). Cellular and molecular correlates of the regeneration of adult mammmalian CNS axons into peripheral nerve grafts. in van Leeuwen,F.W., Salehi,A., Giger,R.J., Holtmaat,A.J.G.D., Verhaagen,J. (ed.) Neuronal Degeneration and Regeneration: From Basic Mechanisms to Prospects for Therapy. Progress in Brain Research series. Amsterdam: Elsevier, 211-233
  • Chaisuksunt,V., Schachner,M., Zhang,Y., Anderson,P.N., Lieberman,A.R. (1998). Expression of CHL1, a cell recognition molecule closely related to L1, in adult rat brain following the implantation of a peripheral nerve graft. Journal of Anatomy, 192, 468-468
  • Chaisuksunt,V., Zhang,Y., Schachner,M., Anderson,P.N., Lieberman,A.R. (1998). Expression of the cell recognition molecule CHL1 (close homologue of L1) in adult rat brain following peripheral nerve graft implantation. Society for Neuroscience Abstracts 24(2), 2009-2009
  • Dijkhuizen,P.A., Zhang,Y., Anderson,P.N., Hermens,W.T.J.M.C., Teunis,M.A.T., Lieberman,A.R., Verhaagen,J. (1998). Regrowth of injured dorsal root axons into the spinal cord by adenoviral vector-mediated NT-3 delivery. Society of Neuroscience Abstracts 24(1), 38-38
  • Harding,D.I., Greensmith,L., Anderson,P.N., Vrbová,G. (1998). Motoneurones induced to sprout remain susceptible to nerve injury in adult transgenic mice overexpressing GAP-43. Journal of Anatomy 192, 468-468
  • Harding,D.I., Greensmith,L., Anderson,P.N., Vrbová,G. (1998). Motoneurons innervating partially denervated rat hindlimb muscles remain susceptible to axotomy-induced cell death. Neuroscience 86, 291-299.
  • Howard,M.K., Kershaw,T., Gibb,B., Storey,N., Maclean,A.R., Zeng,B., Tel,B.C., Jenner,P., Brown,S.M., Woolf,C.J., Anderson,P.N., Coffin,R.S., Latchman,D.S. (1998). High efficiency gene transfer to the central nervous system of rodents and primates using herpes virus vectors lacking functional ICP27 and ICP34.5. Gene Therapy 5, 1137-1147.
  • Roslan,R., Haque,N., Schachner,M., Anderson,P.N. (1998). CHL1, a cell recognition molecule closely related to L1, is expressed in motor neurons following sciatic nerve crush in the rat. Journal of Anatomy 192, 458-459.
  • Roslan,R.J., Schachner,M., Vaudano,E., Anderson,P.N. (1998). The cell recognition molecule, close homologue of L1, is expressed in motor neurons in the lumbar spinal cord following axotomy. Society for Neuroscience Abstracts 24, 1053-1053 [Detail] Tew,E.M.M., Anderson,P.N., Saffrey,M.J., Burnstock,G. (1998). Intrastriatal grafts of rat colonic smooth muscle lacking myenteric ganglia stimulate axonal sprouting and regeneration. Journal of Anatomy 192(1), 25-35.
  • Woolhead,C., Zhang,Y., Lieberman,A.R., Schachner,M., Emson,P.C., Anderson,P.N. (1998). Differential effects of autologous peripheral nerve grafts to the corpus striatum of adult rats on the regeneration of axons of striatal and nigral neurons and on the expression of GAP-43 and the cell adhesion molecules N-CAM and L1. Journal of Comparative Neurology 391, 259-273.
  • Zhang,Y., Dijkhuizen,P.A., Anderson,P.N., Lieberman,A.R., Verhaagen,J. (1998). NT-3 delivered by an adenoviral vector induces injured dorsal root axons to regenerate into the spinal cord of adult rats. Journal of Neuroscience Research 54, 554-562.
  • Zhang,Y., Vaudano,E., Campbell,G., Anderson,P.N., Lieberman,A.R. (1998). Differential regenerative capacities and molecular responses of adult rat cerebellar neurons following axonal injury and the implantation of a peripheral nerve graft, Journal of Anatomy, 192, 142-142 [Detail] Davis,G.R., Elliott,J.C., Anderson,P., Wouters,K., Procter,P., Boyde,A. (1997). Rapid prototyping of a high resolution x-ray microtomographic image data set showing trabecular bone within a human vertebral body. Scanning 19, 175-177.
  • Elliott,J.C., Anderson,P., Davis,G.R., Wong,F.S.L., Dowker,S.E., Kozul,N., Boyde,A. (1997). Microtomography in Medicine and related fields. Developments in Tomography, Proceedings of Society of Photo-Optic Instrumentation Engineers 3149, 2-12
  • Howard,M.K., Coffin,R.S., Maclean,A.R., Brown,S.M., Bailey,D., Anderson,P.N., Burnstock,G., Latchman,D.S. (1997). Gene delivery to rat enteric neurons using herpes simplex virus based vectors. Journal of Molecular Neuroscience 9, 65-74.
  • Zhang,Y., Anderson,P.N., Campbell,G., Schachner,M., Lieberman,A.R. (1997). Upregulation of L1 mRNA in adult rat cerebellar neurons is correlated with their ability to regenerate axons. Society for Neuroscience Abstracts 23, 1721-1721
  • Zhang,Y., Winterbottom,J., Schachner,M., Lieberman,A.R., Anderson,P.N. (1997). Tenascin-C expression and axonal sprouting following injury to the spinal dorsal columns in the adult rat. Journal of Neuroscience Research 49, 433-450.
   

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