Acute delivery of epha4-fc improves functional recovery after contusive spinal cord injury in rats

Journal of Neurotrauma

Volumn 30, Issue 12, 2013, Pages 1023-1024

  Spanevello, Mark Damien ^a,b   Tajouri, Sophie Ines ^a   Mirciov, Cornel ^a   Kurniawan, Nyoman ^a   Pearse, Martin John ^c   Fabri, Louis Jerry ^c   Owczarek, Catherine Mary ^c   Hardy, Matthew Philip ^c   Bradford, Rebecca Anne ^c   Ramunno, Melanie Louise ^c   Turnley, Ann Maree ^d   Ruitenberg, Marc Jan ^a   Boyd, Andrew Wallace ^a,b   Bartlett, Perry Francis ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^c CSL LIMITED   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

EphA4; magnetic resonance imaging; neurotrauma; spinal cord injury

Indexed keywords

EPHRIN RECEPTOR A4; EPHRIN RECEPTOR A4 IMMUNOGLOBULIN G1 FC FRAGMENT FUSION PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CONTUSION; CONVALESCENCE; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; EX VIVO STUDY; FEMALE; LOCOMOTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; OPEN FIELD TEST; RAT; SPINAL CORD INJURY; THORAX INJURY;

ANIMALS; BLOTTING, WESTERN; BRAIN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MAGNETIC RESONANCE IMAGING; RATS; RATS, WISTAR; RECEPTOR, EPHA4; RECOMBINANT FUSION PROTEINS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TRANSFECTION;

EID: 84879330761     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2729     Document Type: Article

References (54)

1. Liebscher, T., Schnell, L., Schnell, D., Scholl, J., Schneider, R., Gullo, M., Fouad, K., Mir, A., Rausch, M., Kindler, D., Hamers, F.P., and Schwab, M.E. (2005). Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 58, 706-719. (Pubitemid 41552546)
2. Barritt, A.W., Davies, M., Marchand, F., Hartley, R., Grist, J., Yip, P., McMahon, S.B., and Bradbury, E.J. (2006). Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J. Neurosci. 26, 10,856-10,867.
3. Hata, K., Fujitani, M., Yasuda, Y., Doya, H., Saito, T., Yamagishi, S., Mueller, B.K., and Yamashita, T. (2006). RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J. Cell Biol. 173, 47-58.
4. Goldshmit, Y., McLenachan, S., and Turnley, A. (2006). Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain. Res. Rev. 52, 327-345. (Pubitemid 44291808)
5. Kaneko, S., Iwanami, A., Nakamura, M., Kishino, A., Kikuchi, K., Shibata, S., Okano, H.J., Ikegami, T., Moriya, A., Konishi, O., Nakayama, C., Kumagai, K., Kimura, T., Sato, Y., Goshima, Y., Taniguchi, M., Ito, M., He, Z., Toyama, Y., and Okano, H. (2006). A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 12, 1380-1389. (Pubitemid 44924496)
6. Lau, E., and Margolis, R.U. (2010). Inhibitors of slit protein interactions with the heparan sulphate proteoglycan glypican-1: potential agents for the treatment of spinal cord injury. Clin. Exp. Pharmacol. Physiol. 37, 417-421.
7. Qin, H., Noberini, R., Huan, X., Shi, J., Pasquale, E.B., and Song, J. (2010). Structural characterization of the EphA4-Ephrin-B2 complex reveals new features enabling Eph-ephrin binding promiscuity. J. Biol. Chem. 285, 644-654.
8. Bowden, T.A., Aricescu, A.R., Nettleship, J.E., Siebold, C., Rahman-Huq, N., Owens, R.J., Stuart, D.I., and Jones, E.Y. (2009). Structural plasticity of eph receptor A4 facilitates cross-class ephrin signaling. Structure 17, 1386-1397.
9. Ho, S.K., Kovacevic, N., Henkelman, R.M., Boyd, A., Pawson, T., and Henderson, J.T. (2009). EphB2 and EphA4 receptors regulate formation of the principal inter-hemispheric tracts of the mammalian forebrain. Neuroscience 160, 784-795.
10. Dottori, M., Hartley, L., Galea, M., Paxinos, G., Polizzotto, M., Kilpatrick, T., Bartlett, P.F., Murphy, M., Kontgen, F., and Boyd, A.W. (1998). EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc. Natl. Acad. Sci. U.S.A. 95, 13,248-13,253. (Pubitemid 28509557)
11. Kullander, K., Butt, S.J.B., Lebret, J.M., Lundfald, L., Restrepo, C.E., Rydstrom, A., Klein, R., and Kiehn, O. (2003). Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299, 1889-1892. (Pubitemid 36358203)
12. Fabes, J., Anderson, P., Yanez-Munoz, R.J., Thrasher, A., Brennan, C., and Bolsover, S. (2006). Accumulation of the inhibitory receptor EphA4 may prevent regeneration of corticospinal tract axons following lesion. Eur. J. Neurosci. 23, 1721-1730.
13. Arocho, L.C., Figueroa, J.D., Torrado, A.I., Santiago, J.M., Vera, A.E., and Miranda, J.D. (2011). Expression profile and role of EphrinA1 ligand after spinal cord injury. Cell. Mol. Neurobiol. 31, 1057-1069.
14. Duffy, P., Wang, X., Siegel, C.S., Tu, N., Henkemeyer, M., Cafferty, W.B., and Strittmatter, S.M. (2012). Myelin-derived ephrinB3 restricts axonal regeneration and recovery after adult CNS injury. Proc. Natl. Acad. Sci. U.S.A. 109, 5063-5068.
15. Omoto, S., Ueno, M., Mochio, S., and Yamashita, T. (2011). Corticospinal tract fibers cross the ephrin-B3-negative part of the midline of the spinal cord after brain injury. Neurosci. Res. 69, 187-195.
16. Fabes, J., Anderson, P., Brennan, C., and Bolsover, S. (2007). Regeneration-enhancing effects of EphA4 blocking peptide following corticospinal tract injury in adult rat spinal cord. Eur. J. Neurosci. 26, 2496-2505. (Pubitemid 350064163)
17. Goldshmit, Y., Galea, M.P., Wise, G., Bartlett, P.F., and Turnley, A.M. (2004). Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J. Neurosci. 24, 10,064-10,073. (Pubitemid 39492030)
18. Goldshmit, Y., Spanevello, M.D., Tajouri, S., Li, L., Rogers, F., Pearse, M., Galea, M., Bartlett, P.F., Boyd, A.W., and Turnley, A.M. (2011). EphA4 blockers promote axonal regeneration and functional recovery following spinal cord injury in mice. PLoS ONE 6, e24636.
19. Bilgen, M., and Rumboldt, Z. (2008). Neuronal and vascular biomarkers in syringomyelia: investigations using longitudinal MRI. Biomark. Med. 2, 113-124. (Pubitemid 351753457)
20. Bozzo, A., Marcoux, J., Radhakrishna, M., Pelletier, J., and Goulet, B. (2011). The role of magnetic resonance imaging in the management of acute spinal cord injury. J. Neurotrauma 28, 1401-1411.
21. Blomster, L.V., Cowin, G.J., Kurniawan, N.D., and Ruitenberg, M.J. (2013). Detection of endogenous iron deposits in the injured mouse spinal cord through high-resolution ex vivo and in vivo MRI. NMR Biomed. 26, 141-150.
22. Ellingson, B.M., Kurpad, S.N., and Schmit, B.D. (2008). Ex vivo diffusion tensor imaging and quantitative tractography of the rat spinal cord during long-term recovery from moderate spinal contusion. J. Magn. Reson. Imaging 28, 1068-1079.
23. Mac Donald, C.L., Dikranian, K., Song, S.K., Bayly, P.V., Holtzman, D.M., and Brody, D.L. (2007). Detection of traumatic axonal injury with diffusion tensor imaging in a mouse model of traumatic brain injury. Exp. Neurol. 205, 116-131. (Pubitemid 46629058)
24. Nishi, R.A., Liu, H., Chu, Y., Hamamura, M., Su, M.Y., Nalcioglu, O., and Anderson, A.J. (2007). Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J. Neurotrauma 24, 674-689. (Pubitemid 46996027)
25. Velardo, M.J., Burger, C., Williams, P.R., Baker, H.V., Lopez, M.C., Mareci, T.H., White, T.E., Muzyczka, N., and Reier, P.J. (2004). Patterns of gene expression reveal a temporally orchestrated wound healing response in the injured spinal cord. J. Neurosci. 24, 8562-8576. (Pubitemid 39313779)
26. Byrnes, K.R., Fricke, S.T., and Faden, A.I. (2010). Neuropathological differences between rats and mice after spinal cord injury. J. Magn. Reson. Imaging 32, 836-846.
27. Day, B.W., Smith, F.M., Chen, K., McCarron, J.K., Herath, N.I., Lackmann, M., and Boyd, A.W. (2006). Eph/Ephrin membrane proteins: a mammalian expression vector pTIg-BOS-Fc allowing rapid protein purification. Protein Pept. Lett. 13, 193-196.
28. Smith, F.M., Vearing, C., Lackmann, M., Treutlein, H., Himanen, J., Chen, K., Saul, A., Nikolov, D., and Boyd, A.W. (2004). Dissecting the EphA3/Ephrin-A5 interactions using a novel functional mutagenesis screen. J. Biol. Chem. 279, 9522-9531. (Pubitemid 38296020)
29. Mizushima, S., and Nagata, S. (1990). pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18, 5322. (Pubitemid 20270119)
30. Scheff, S.W., Rabchevsky, A.G., Fugaccia, I., Main, J.A., and Lumpp, J.E., Jr. (2003). Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20, 179-193. (Pubitemid 36292827)
31. Rossi, S.L., Nistor, G., Wyatt, T., Yin, H.Z., Poole, A.J., Weiss, J.H., Gardener, M.J., Dijkstra, S., Fischer, D.F., and Keirstead, H.S. (2010). Histological and functional benefit following transplantation of motor neuron progenitors to the injured rat spinal cord. PLoS ONE 5, e11852.
32. Schallert, T. (2006). Behavioral tests for preclinical intervention assessment. NeuroRx 3, 497-504. (Pubitemid 44443020)
33. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
34. Rosset, A., Spadola, L., and Ratib, O. (2004). OsiriX: an open-source software for navigating in multidimensional DICOM images. J. Digit. Imaging 17, 205-216. (Pubitemid 40378992)
35. Wang, R., Benner, T., Sorensen, A.G., and Wedeen, V.J. (2007). Diffusion Toolkit: a software package for diffusion imaging data processing and tractography. Proc. Intl. Soc. Mag. Reson. Med. 15, 3720.
36. Anseloni, V.C., Ennis, M., and Lidow, M.S. (2003). Optimization of the mechanical nociceptive threshold testing with the Randall-Selitto assay. J. Neurosci. Methods 131, 93-97. (Pubitemid 37491464)
37. Fleming, S.M. (2009). Behavioral outcome measures for the assessment of sensorimotor function in animal models of movement disorders. Int. Rev. Neurobiol. 89, 57-65.
38. Cruz-Orengo, L., Figueroa, J.D., Velazquez, I., Torrado, A., Ortiz, C., Hernandez, C., Puig, A., Segarra, A.C., Whittemore, S.R., and Miranda, J.D. (2006). Blocking EphA4 upregulation after spinal cord injury results in enhanced chronic pain. Exp. Neurol. 202, 421-433. (Pubitemid 44692684)
39. Dries, J.L., Kent, S.D., and Virag, J.A. (2011). Intramyocardial administration of chimeric ephrinA1-Fc promotes tissue salvage following myocardial infarction in mice. J. Physiol. 589, 1725-1740.
40. Dobrzanski, P., Hunter, K., Jones-Bolin, S., Chang, H., Robinson, C., Pritchard, S., Zhao, H., and Ruggeri, B. (2004). Antiangiogenic and antitumor efficacy of EphA2 receptor antagonist. Cancer Res. 64, 910-919. (Pubitemid 38176892)
41. Iwasato, T., Katoh, H., Nishimaru, H., Ishikawa, Y., Inoue, H., Saito, Y.M., Ando, R., Iwama, M., Takahashi, R., Negishi, M., and Itohara, S. (2007). Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130, 742-753. (Pubitemid 47268060)
42. Schucht, P., Raineteau, O., Schwab, M.E., and Fouad, K. (2002). Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 176, 143-153. (Pubitemid 34762114)
43. Steeves, J.D., and Jordan, L.M. (1980). Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion. Neurosci. Lett. 20, 283-288. (Pubitemid 11160065)
44. Munro, K.M., Perreau, V.M., and Turnley, A.M. (2012). Differential gene expression in the EphA4 knockout spinal cord and analysis of the inflammatory response following spinal cord injury. PLoS ONE 7, e37635.
45. Murai, K.K., Nguyen, L.N., Irie, F., Yamaguchi, Y., and Pasquale, E.B. (2003). Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6, 153-160. (Pubitemid 36182784)
46. Van Hoecke, A., Schoonaert, L., Lemmens, R., Timmers, M., Staats, K.A., Laird, A.S., Peeters, E., Philips, T., Goris, A., Dubois, B., Anderson, P.M., Al-Chalabi A., Thijs, V., Turnley, A.M., van Vught, P.W., Veldink, J.H., Hardiman, O., Van Den Bosch, L., Gonzalez-Perez, P., Van Damme, P., Brown, R. H. Jr, van den Berg, L.H., and Robberecht, W. (2012) EPHA4 is a disease modifier of amyotrophic lateral sclerosis in animal models and humans. Nat. Med. 18, 1418-1422.
47. Metz, G.A., and Whishaw, I.Q. (2002). Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-And hindlimb stepping, placing, and co-ordination. J. Neurosci. Methods 115, 169-179. (Pubitemid 34461965)
48. Kozlowski, P., Raj, D., Liu, J., Lam, C., Yung, A.C., and Tetzlaff, W. (2008). Characterizing white matter damage in rat spinal cord with quantitative MRI and histology. J. Neurotrauma 25, 653-676. (Pubitemid 351918437)
49. Ellingson, B.M., Schmit, B.D., and Kurpad, S.N. (2010). Lesion growth and degeneration patterns measured using diffusion tensor 9.4-T magnetic resonance imaging in rat spinal cord injury. J. Neurosurg. Spine 13, 181-192.
50. Nielson, J.L., Strong, M.K., and Steward, O. (2011). A reassessment of whether cortical motor neurons die following spinal cord injury. J. Comp. Neurol. 519, 2852-2869.
51. Ghosh, A., Sydekum, E., Haiss, F., Peduzzi, S., Zorner, B., Schneider, R., Baltes, C., Rudin, M., Weber, B., and Schwab, M.E. (2009). Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J Neurosci. 29, 12,210-12,219.
52. Gao, Y.J., and Ji, R.R. (2010). Targeting astrocyte signaling for chronic pain. Neurotherapeutics 7, 482-493.
53. Wen, Y.R., Tan, P.H., Cheng, J.K., Liu, Y.C., and Ji, R.R. (2011). Microglia: a promising target for treating neuropathic and postoperative pain, and morphine tolerance. J. Formos. Med. Assoc. 110, 487-494.
54. Dixon, K.J., Munro, K.M., Boyd, A.W., Bartlett, P.F., and Turnley, A.M. (2012). Partial change in EphA4 knockout mouse phenotype: loss of diminished GFAP upregulation following spinal cord injury. Neurosci. Lett. 525, 66-71