PEGylated interferon-β modulates the acute inflammatory response and recovery when combined with forced exercise following cervical spinal contusion injury

Experimental Neurology

Volumn 223, Issue 2, 2010, Pages 439-451

  Sandrow Feinberg, Harra R ^a   Zhukareva, Victoria ^a   Santi, Lauren ^a   Miller, Kassi ^a   Shumsky, Jed S ^a   Baker, Darren P ^b   Houle, John D ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b BIOGEN   (United States)

Author keywords

Cervical contusion; Combination strategy; Forced exercise; Forelimb behavior; Inflammation; Spinal cord injury

Indexed keywords

BETA INTERFERON; HEAT SHOCK PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXERCISE; FEMALE; FORELIMB; GENE EXPRESSION REGULATION; GLIA CELL; IMMUNOMODULATION; LOCOMOTION; NEUROPROTECTION; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; SINGLE DRUG DOSE;

ACUTE DISEASE; ANIMALS; CERVICAL VERTEBRAE; COMBINED MODALITY THERAPY; EXERCISE THERAPY; FEMALE; FORELIMB; INTERFERON-BETA; KERATINS; LOCOMOTION; MYELITIS; NEUROPROTECTIVE AGENTS; POLYETHYLENE GLYCOLS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 77952550253     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.01.009     Document Type: Article

References (52)

1. Akbar M.T., Lundberg A.M., Liu K., Vidyadaran S., Wells K.E., Dolatshad H., Wynn S., Wells D.J., Latchman D.S., de Belleroche J. The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J. Biol. Chem. 2003, 278:19956-19965.
2. Arduini R.M., Li Z., Rapoza A., Gronke R., Hess D.M., Wen D., Miatkowski K., Coots C., Kaffashan A., Viseux N., Delaney J., Domon B., Young C.N., Boynton R., Chen L.L., Chen L., Betzenhauser M., Miller S., Gill A., Pepinsky R.B., Hochman P.S., Baker D.P. Expression, purification, and characterization of rat interferon-beta, and preparation of an N-terminally PEGylated form with improved pharmacokinetic parameters. Protein Expr. Purif. 2004, 34:229-242.
3. Baker D.P., Lin E.Y., Lin K., Pellegrini M., Petter R.C., Chen L.L., Arduini R.M., Brickelmaier M., Wen D., Hess D.M., Chen L., Grant D., Whitty A., Gill A., Lindner D.J., Pepinsky R.B. N-terminally PEGylated human interferon-beta-1a with improved pharmacokinetic properties and in vivo efficacy in a melanoma angiogenesis model. Bioconjug. Chem. 2006, 17:179-188.
4. Baptiste D.C., Fehlings M.G. Update on the treatment of spinal cord injury. Prog. Brain Res. 2007, 161:217-233.
5. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 2004, 7:269-277.
6. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
7. Basu A., Yang K., Wang M., Liu S., Chintala R., Palm T., Zhao H., Peng P., Wu D., Zhang Z., Hua J., Hsieh M.C., Zhou J., Petti G., Li X., Janjua A., Mendez M., Liu J., Longley C., Mehlig M., Borowski V., Viswanathan M., Filpula D. Structure-function engineering of interferon-beta-1b for improving stability, solubility, potency, immunogenicity, and pharmacokinetic properties by site-selective mono-PEGylation. Bioconjug. Chem. 2006, 17:618-630.
8. Beattie M.S. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol. Med. 2004, 10:580-583.
9. Beckman J.S., Chen J., Crow J.P., Ye Y.Z. Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog. Brain Res. 1994, 103:371-380.
10. Bethea J.R. Spinal cord injury-induced inflammation: a dual-edged sword. Prog. Brain Res. 2000, 128:33-42.
11. Bethea J.R., Nagashima H., Acosta M.C., Briceno C., Gomez F., Marcillo A.E., Loor K., Green J., Dietrich W.D. Systemically administered interleukin-10 reduces tumor necrosis factor-alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats. J. Neurotrauma 1999, 16:851-863.
12. Brewer K.L., Bethea J.R., Yezierski R.P. Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp. Neurol. 1999, 159:484-493.
13. Brown I.R. Heat shock proteins and protection of the nervous system. Ann. N.Y. Acad. Sci. 2007, 1113:147-158.
14. Bunge M.B. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal Cord Med. 2008, 31:262-269.
15. Cao Y., Shumsky J.S., Sabol M.A., Kushner R.A., Strittmatter S., Hamers F.P., Lee D.H., Rabacchi S.A., Murray M. Nogo-66 receptor antagonist peptide (NEP1-40) administration promotes functional recovery and axonal growth after lateral funiculus injury in the adult rat. Neurorehabil. Neural Repair 2008, 22:262-278.
16. Chabot S., Yong V.W. Interferon beta-1b increases interleukin-10 in a model of T cell-microglia interaction: relevance to MS. Neurology 2000, 55:1497-1505.
17. Chen Y., Arrigo A.P., Currie R.W. Heat shock treatment suppresses angiotensin II-induced activation of NF-kappaB pathway and heart inflammation: a role for IKK depletion by heat shock?. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H1104-1114.
18. Conti A., Miscusi M., Cardali S., Germano A., Suzuki H., Cuzzocrea S., Tomasello F. Nitric oxide in the injured spinal cord: synthases cross-talk, oxidative stress and inflammation. Brain Res. Rev. 2007, 54:205-218.
19. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 2008, 14:69-74.
20. DeMeester S.L., Buchman T., Cobb J.P. The heat shock paradox: does NF-kappaB determine cell fate?. FASEB J. 2001, 15:270-274.
21. Donnelly D.J., Popovich P.G. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 2008, 209:378-388.
22. Dupont-Versteegden E.E., Houle J.D., Dennis R.A., Zhang J., Knox M., Wagoner G., Peterson C.A. Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve 2004, 29:73-81.
23. Dwyer B.E., Nishimura R.N., Lu S.Y., Alcaraz A. Transient induction of heme oxygenase after cortical stab wound injury. Brain Res. Mol. Brain Res. 1996, 38:251-259.
24. Ersoy E., Kus C.N., Sener U., Coker I., Zorlu Y. The effects of interferon-beta on interleukin-10 in multiple sclerosis patients. Eur. J. Neurol. 2005, 12:208-211.
25. Felderhoff-Mueser U., Schmidt O.I., Oberholzer A., Buhrer C., Stahel P.F. IL-18: a key player in neuroinflammation and neurodegeneration?. Trends Neurosci. 2005, 28:487-493.
26. Garg M.S., Marcillo A.E., Diaz P., Sipski M.L., Baker D.P., Pearse D.D. Interferon-β improves histopathological outcome after moderate thoracic spinal cord contusion. J. Spinal Cord Med. 2006, 29:277-278.
27. Girgis J., Merrett D., Kirkland S., Metz G.A., Verge V., Fouad K. Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 2007, 130:2993-3003.
28. Gok B., Okutan O., Beskonakli E., Palaoglu S., Erdamar H., Sargon M.F. Effect of immunomodulation with human interferon-beta on early functional recovery from experimental spinal cord injury. Spine (Phila Pa 1976) 2007, 32:873-880.
29. Gomez-Pinilla F., Ying Z., Roy R.R., Molteni R., Edgerton V.R. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J. Neurophysiol. 2002, 88:2187-2195.
30. Grill R., Murai K., Blesch A., Gage F.H., Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 1997, 17:5560-5572.
31. Javed A., Reder A.T. Therapeutic role of beta-interferons in multiple sclerosis. Pharmacol. Ther. 2006, 110:35-56.
32. Katori M., Buelow R., Ke B., Ma J., Coito A.J., Iyer S., Southard D., Busuttil R.W., Kupiec-Weglinski J.W. Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway. Transplantation 2002, 73:287-292.
33. Latchman D.S. HSP27 and cell survival in neurones. Int. J. Hyperthermia 2005, 21:393-402.
34. Liu Y., Tachibana T., Dai Y., Kondo E., Fukuoka T., Yamanaka H., Noguchi K. Heme oxygenase-1 expression after spinal cord injury: the induction in activated neutrophils. J. Neurotrauma 2002, 19:479-490.
35. Mehindate K., Sahlas D.J., Frankel D., Mawal Y., Liberman A., Corcos J., Dion S., Schipper H.M. Proinflammatory cytokines promote glial heme oxygenase-1 expression and mitochondrial iron deposition: implications for multiple sclerosis. J. Neurochem. 2001, 77:1386-1395.
36. Moseley P.L. Heat shock proteins and the inflammatory response. Ann. N.Y. Acad. Sci. 1998, 856:206-213.
37. Noronha A., Toscas A., Jensen M.A. Interferon beta decreases T cell activation and interferon gamma production in multiple sclerosis. J. Neuroimmunol. 1993, 46:145-153.
38. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
39. Sandrow H.R., Shumsky J.S., Amin A., Houle J.D. Aspiration of a cervical spinal contusion injury in preparation for delayed peripheral nerve grafting does not impair forelimb behavior or axon regeneration. Exp. Neurol. 2008, 210:489-500.
40. Sandrow-Feinberg H.R., Izzi J., Shumsky J.S., Zhukareva V., Houle J.D. Forced exercise as a rehabilitation strategy after unilateral cervical spinal cord contusion injury. J. Neurotrauma 2009, 26:721-731.
41. Schwab J.M., Brechtel K., Mueller C.A., Failli V., Kaps H.P., Tuli S.K., Schluesener H.J. Experimental strategies to promote spinal cord regeneration-an integrative perspective. Prog. Neurobiol. 2006, 78:91-116.
42. Schwab M.E., Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 1996, 76:319-370.
43. Schwartz M., Yoles E. Immune-based therapy for spinal cord repair: autologous macrophages and beyond. J. Neurotrauma 2006, 23:360-370.
44. Sharma H.S., Gordh T., Wiklund L., Mohanty S., Sjoquist P.O. Spinal cord injury induced heat shock protein expression is reduced by an antioxidant compound H-290/51. An experimental study using light and electron microscopy in the rat. J. Neural. Transm. 2006, 113:521-536.
45. Smith R.R., Shum-Siu A., Baltzley R., Bunger M., Baldini A., Burke D.A., Magnuson D.S. Effects of swimming on functional recovery after incomplete spinal cord injury in rats. J. Neurotrauma 2006, 23:908-919.
46. Tator C.H. Review of treatment trials in human spinal cord injury: issues, difficulties, and recommendations. Neurosurgery 2006, 59:957-982. discussion 982-957.
47. van Noort J. Stress proteins in CNS inflammation. J. Pathol. 2008, 214:267-275.
48. Vaynman S., Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil. Neural Repair 2005, 19:283-295.
49. Vaynman S., Ying Z., Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 2003, 122:647-657.
50. Xu J., Kim G.M., Chen S., Yan P., Ahmed S.H., Ku G., Beckman J.S., Xu X.M., Hsu C.Y. iNOS and nitrotyrosine expression after spinal cord injury. J. Neurotrauma 2001, 18:523-532.
51. Yong V.W., Agrawal S.M., Stirling D.P. Targeting MMPs in acute and chronic neurological conditions. Neurotherapeutics 2007, 4:580-589.
52. Yushchenko M., Mader M., Elitok E., Bitsch A., Dressel A., Tumani H., Bogumil T., Kitze B., Poser S., Weber F. Interferon-beta-1 b decreased matrix metalloproteinase-9 serum levels in primary progressive multiple sclerosis. J. Neurol. 2003, 250:1224-1228.