Central but not systemic administration of XPro1595 is therapeutic following moderate spinal cord injury in mice

Journal of Neuroinflammation

Volumn 11, Issue 1, 2014, Pages

  Novrup, Hans G ^b   Bracchi Ricard, Valerie ^a   Ellman, Ditte G ^b   Ricard, Jerome ^a   Jain, Anjana ^a,e   Runko, Erik ^a   Lyck, Lise ^b,c   Yli Karjanmaa, Minna ^b   Szymkowski, David E ^d   Pearse, Damien D ^a   Lambertsen, Kate L ^a,b   Bethea, John R ^a,f  

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

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c Coloplast A/S ^*  (Denmark)

^d Xencor Inc   (United States)

^e Worcester Polytechnic Institute   (United States)

^f DREXEL UNIVERSITY   (United States)

Author keywords

Functional outcome; Spinal cord injury; TLR4; TNFR2; Tumor necrosis factor

Indexed keywords

CALCIUM BINDING PROTEIN; ETANERCEPT; PROTEIN IBA1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; XPRO 1595; TUMOR NECROSIS FACTOR ALPHA; XENP 1595;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BASSO MOUSE SCALE; CATWALK GAIT ANALYSIS TEST; CONTROLLED STUDY; DRUG MECHANISM; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; FEMALE; GRIDWALK TEST; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MACROPHAGE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; REGULATORY MECHANISM; RUNG WALK TEST; SCORING SYSTEM; SPINAL CORD INJURY; THERMAL HYPERALGESIA ANALYSIS; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; EPIDURAL DRUG ADMINISTRATION; INFUSION PUMP; METABOLISM; PATHOLOGY; SPINAL CORD INJURIES; SUBCUTANEOUS DRUG ADMINISTRATION;

ANIMALS; FEMALE; INFUSION PUMPS, IMPLANTABLE; INJECTIONS, EPIDURAL; INJECTIONS, SUBCUTANEOUS; MICE; SPINAL CORD INJURIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84908137998     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0159-6     Document Type: Article

References (59)

1. McDonald JW, Sadowsky C. Spinal-cord injury. Lancet 2002, 359(9304):417-425. 10.1016/S0140-6736(02)07603-1, 11844532.
2. Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 2008, 209(2):378-388. 10.1016/j.expneurol.2007.06.009, 17662717.
3. Bracchi-Ricard V, Lambertsen KL, Ricard J, Nathanson L, Karmally S, Johnstone J, Ellman DG, Frydel B, McTigue DM, Bethea JR. Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury. J Neuroinflammation 2013, 10(1):92. 10.1186/1742-2094-10-92, 23880092.
4. Johnstone JT, Morton PD, Jayakumar AR, Johnstone AL, Gao H, Bracchi-Ricard V, Pearse DD, Norenberg MD, Bethea JR. Inhibition of NADPH oxidase activation in oligodendrocytes reduces cytotoxicity following trauma. PLoS One 2013, 8(11):e80975. 10.1371/journal.pone.0080975, 24260524.
5. Benowitz LI, Popovich PG. Inflammation and axon regeneration. Curr Opin Neurol 2011, 24(6):577-583. 10.1097/WCO.0b013e32834c208d, 21968547.
6. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009, 29(43):13435-13444. 10.1523/JNEUROSCI.3257-09.2009, 19864556.
7. Popovich P, McTigue D. Damage control in the nervous system: beware the immune system in spinal cord injury. Nat Med 2009, 15(7):736-737. 10.1038/nm0709-736, 19584863.
8. Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, Karmally S, Green EJ, Bethea JR. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 2005, 202(1):145-156. 10.1084/jem.20041918, 15998793.
9. Brambilla R, Ashbaugh JJ, Magliozzi R, Dellarole A, Karmally S, Szymkowski DE, Bethea JR. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 2011, 134(Pt 9):2736-2754. 10.1093/brain/awr199, 21908877.
10. Bethea JR, Nagashima H, Acosta MC, Briceno C, Gomez F, Marcillo AE, Loor K, Green J, Dietrich WD. 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(10):851-863. 10.1089/neu.1999.16.851, 10547095.
11. Lambertsen KL, Biber K, Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab 2012, 32(9):1677-1698. 10.1038/jcbfm.2012.88, 22739623.
12. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009, 29(5):1319-1330. 10.1523/JNEUROSCI.5505-08.2009, 19193879.
13. Tyring S, Gottlieb A, Papp K, Gordon K, Leonardi C, Wang A, Lalla D, Woolley M, Jahreis A, Zitnik R, Cella D, Krishnan R. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet 2006, 367(9504):29-35. 10.1016/S0140-6736(05)67763-X, 16399150.
14. Taylor PC, Feldmann M. Anti-TNF biologic agents: still the therapy of choice for rheumatoid arthritis. Nat Rev Rheumatol 2009, 5(10):578-582. 10.1038/nrrheum.2009.181, 19798034.
15. McCoy MK, Tansey MG. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation 2008, 5:45. 10.1186/1742-2094-5-45, 18925972.
16. McCoy MK, Ruhn KA, Martinez TN, McAlpine FE, Blesch A, Tansey MG. Intranigral lentiviral delivery of dominant-negative TNF attenuates neurodegeneration and behavioral deficits in hemiparkinsonian rats. Mol Ther 2008, 16(9):1572-1579. 10.1038/mt.2008.146, 18628756.
17. McCoy MK, Martinez TN, Ruhn KA, Szymkowski DE, Smith CG, Botterman BR, Tansey KE, Tansey MG. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci 2006, 26(37):9365-9375. 10.1523/JNEUROSCI.1504-06.2006, 16971520.
18. McAlpine FE, Lee JK, Harms AS, Ruhn KA, Blurton-Jones M, Hong J, Das P, Golde TE, LaFerla FM, Oddo S, Blesch A, Tansey MG. Inhibition of soluble TNF signaling in a mouse model of Alzheimer's disease prevents pre-plaque amyloid-associated neuropathology. Neurobiol Dis 2009, 34(1):163-177. 10.1016/j.nbd.2009.01.006, 19320056.
19. Caminero A, Comabella M, Montalban X. Tumor necrosis factor alpha (TNF-alpha), anti-TNF-alpha and demyelination revisited: an ongoing story. J Neuroimmunol 2011, 234(1-2):1-6. 10.1016/j.jneuroim.2011.03.004, 21474190.
20. Taoufik E, Tseveleki V, Chu SY, Tselios T, Karin M, Lassmann H, Szymkowski DE, Probert L. Transmembrane tumour necrosis factor is neuroprotective and regulates experimental autoimmune encephalomyelitis via neuronal nuclear factor-kappaB. Brain 2011, 134(Pt 9):2722-2735. 10.1093/brain/awr203, 21908876.
21. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 2001, 4(11):1116-1122. 10.1038/nn738, 11600888.
22. Kim GM, Xu J, Xu J, Song SK, Yan P, Ku G, Xu XM, Hsu CY. Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J Neurosci 2001, 21(17):6617-6625. 11517251.
23. Eugster HP, Frei K, Bachmann R, Bluethmann H, Lassmann H, Fontana A. Severity of symptoms and demyelination in MOG-induced EAE depends on TNFR1. Eur J Immunol 1999, 29(2):626-632. 10.1002/(SICI)1521-4141(199902)29:02<626::AID-IMMU626>3.0.CO;2-A, 10064079.
24. Suvannavejh GC, Lee HO, Padilla J, Dal Canto MC, Barrett TA, Miller SD. Divergent roles for p55 and p75 tumor necrosis factor receptors in the pathogenesis of MOG(35-55)-induced experimental autoimmune encephalomyelitis. Cell Immunol 2000, 205(1):24-33. 10.1006/cimm.2000.1706, 11078604.
25. Alexopoulou L, Kranidioti K, Xanthoulea S, Denis M, Kotanidou A, Douni E, Blackshear PJ, Kontoyiannis DL, Kollias G. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur J Immunol 2006, 36(10):2768-2780. 10.1002/eji.200635921, 16983719.
26. Steed PM, Tansey MG, Zalevsky J, Zhukovsky EA, Desjarlais JR, Szymkowski DE, Abbott C, Carmichael D, Chan C, Cherry L, Cheung P, Chirino AJ, Chung HH, Doberstein SK, Eivazi A, Filikov AV, Gao SX, Hubert RS, Hwang M, Hyun L, Kashi S, Kim A, Kim E, Kung J, Martinez SP, Muchhal US, Nguyen DH, O'Brien C, O'Keefe D, Singer K, et al. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science 2003, 301(5641):1895-1898. 10.1126/science.1081297, 14512626.
27. Goffe B, Cather JC. Etanercept: An overview. J Am Acad Dermatol 2003, 49(2 Suppl):S105-111. 10.1016/mjd.2003.554, 12894133.
28. Bedrosian TA, Weil ZM, Nelson RJ. Chronic dim light at night provokes reversible depression-like phenotype: possible role for TNF. Mol Psychiatry 2013, 18(8):930-936. 10.1038/mp.2012.96, 22824811.
29. Wang X, Truong T, Billings PB, Harris JP, Keithley EM. Blockage of immune-mediated inner ear damage by etanercept. Otol Neurotol 2003, 24(1):52-57. 10.1097/00129492-200301000-00012, 12544029.
30. Zalevsky J, Secher T, Ezhevsky SA, Janot L, Steed PM, O'Brien C, Eivazi A, Kung J, Nguyen DH, Doberstein SK, Erard F, Ryffel B, Szymkowski DE. Dominant-negative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J Immunol 2007, 179(3):1872-1883. 10.4049/jimmunol.179.3.1872, 17641054.
31. Pineau I, Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 2007, 500(2):267-285. 10.1002/cne.21149, 17111361.
32. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 2006, 23(5):635-659. 10.1089/neu.2006.23.635, 16689667.
33. Starkey ML, Barritt AW, Yip PK, Davies M, Hamers FP, McMahon SB, Bradbury EJ. Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp Neurol 2005, 195(2):524-539. 10.1016/j.expneurol.2005.06.017, 16051217.
34. Metz GA, Whishaw IQ. 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 2002, 115(2):169-179. 10.1016/S0165-0270(02)00012-2, 11992668.
35. Berrocal Y, Pearse DD, Singh A, Andrade CM, McBroom JS, Puentes R, Eaton MJ. Social and environmental enrichment improves sensory and motor recovery after severe contusive spinal cord injury in the rat. J Neurotrauma 2007, 24(11):1761-1772. 10.1089/neu.2007.0327, 18001204.
36. Lambertsen KL, Gramsbergen JB, Sivasaravanaparan M, Ditzel N, Sevelsted-Møller LM, Oliván-Viguera A, Rabjerg M, Wulff H, Köhler R. Genetic KCa3.1-deficiency produces locomotor hyperactivity and alterations in cerebral monoamine levels. PLoS One 2012, 7(10):e47744. 10.1371/journal.pone.0047744, 23077667.
37. Dissing-Olesen L, Ladeby R, Nielsen HH, Toft-Hansen H, Dalmau I, Finsen B. Axonal lesion-induced microglial proliferation and microglial cluster formation in the mouse. Neuroscience 2007, 149(1):112-122. 10.1016/j.neuroscience.2007.06.037, 17870248.
38. Clausen BH, Lambertsen KL, Babcock AA, Holm TH, Dagnaes-Hansen F, Finsen B. Interleukin-1beta and tumor necrosis factor-alpha are expressed by different subsets of microglia and macrophages after ischemic stroke in mice. J Neuroinflammation 2008, 5:46. 10.1186/1742-2094-5-46, 18947400.
39. Lambertsen KL, Gregersen R, Finsen B. Microglial-macrophage synthesis of tumor necrosis factor after focal cerebral ischemia in mice is strain dependent. J Cereb Blood Flow Metab 2002, 22(7):785-797. 10.1097/00004647-200207000-00004, 12142564.
40. Brambilla R, Morton PD, Ashbaugh JJ, Karmally S, Lambertsen KL, Bethea JR. Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 2014, 62(3):452-467. 10.1002/glia.22616, 24357067.
41. Yakovlev AG, Faden AI. Sequential expression of c-fos protooncogene, TNF-alpha, and dynorphin genes in spinal cord following experimental traumatic injury. Mol Chem Neuropathol 1994, 23(2-3):179-190. 10.1007/BF02815410, 7702707.
42. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 1999, 158(2):351-365. 10.1006/exnr.1999.7118, 10415142.
43. Kigerl KA, McGaughy VM, Popovich PG. Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J Comp Neurol 2006, 494(4):578-594. 10.1002/cne.20827, 16374800.
44. Schonberg DL, Popovich PG, McTigue DM. Oligodendrocyte generation is differentially influenced by toll-like receptor (TLR) 2 and TLR4-mediated intraspinal macrophage activation. J Neuropathol Exp Neurol 2007, 66(12):1124-1135. 10.1097/nen.0b013e31815c2530, 18090921.
45. Wang CX, Nuttin B, Heremans H, Dom R, Gybels J. Production of tumor necrosis factor in spinal cord following traumatic injury in rats. J Neuroimmunol 1996, 69(1-2):151-156. 10.1016/0165-5728(96)00080-X, 8823387.
46. Hermann GE, Rogers RC, Bresnahan JC, Beattie MS. Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol Dis 2001, 8(4):590-599. 10.1006/nbdi.2001.0414, 11493024.
47. Ferguson AR, Christensen RN, Gensel JC, Miller BA, Sun F, Beattie EC, Bresnahan JC, Beattie MS. Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J Neurosci 2008, 28(44):11391-11400. 10.1523/JNEUROSCI.3708-08.2008, 18971481.
48. Wohleb ES, Patterson JM, Sharma V, Quan N, Godbout JP, Sheridan JF. Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J Neurosci 2014, 34(7):2583-2591. 10.1523/JNEUROSCI.3723-13.2014, 24523548.
49. Naude PJ, Dobos N, van der Meer D, Mulder C, Pawironadi KG, den Boer JA, van der Zee EA, Luiten PG, Eisel UL. Analysis of cognition, motor performance and anxiety in young and aged tumor necrosis factor alpha receptor 1 and 2 deficient mice. Behav Brain Res 2014, 258:43-51. 10.1016/j.bbr.2013.10.006, 24135018.
50. Ertenli I, Ozer S, Kiraz S, Apras SB, Akdogan A, Karadag O, Calguneri M, Kalyoncu U. Infliximab, a TNF-alpha antagonist treatment in patients with ankylosing spondylitis: the impact on depression, anxiety and quality of life level. Rheumatol Int 2012, 32(2):323-330. 10.1007/s00296-010-1616-x, 21079965.
51. Simen BB, Duman CH, Simen AA, Duman RS. TNFalpha signaling in depression and anxiety: behavioral consequences of individual receptor targeting. Biol Psychiatry 2006, 59(9):775-785. 10.1016/j.biopsych.2005.10.013, 16458261.
52. Klaas SJ, Kelly EH, Anderson CJ, Vogel LC. Depression and anxiety in adolescents with pediatric-onset spinal cord injury. Top Spinal Cord Inj Rehabil 2014, 20(1):13-22. 10.1310/sci2001-13, 24574818.
53. January AM, Zebracki K, Chlan KM, Vogel LC. Symptoms of depression over time in adults with pediatric-onset spinal cord injury. Arch Phys Med Rehabil 2014, 95(3):447-454. 10.1016/j.apmr.2013.11.011, 24316327.
54. Slifman NR, Gershon SK, Lee JH, Edwards ET, Braun MM. Listeria monocytogenes infection as a complication of treatment with tumor necrosis factor alpha-neutralizing agents. Arthritis Rheum 2003, 48(2):319-324. 10.1002/art.10758, 12571839.
55. Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis 2004, 38(9):1261-1265. 10.1086/383317, 15127338.
56. Fischer R, Maier O, Siegemund M, Wajant H, Scheurich P, Pfizenmaier K. A TNF receptor 2 selective agonist rescues human neurons from oxidative stress-induced cell death. PLoS One 2011, 6(11):e27621. 10.1371/journal.pone.0027621, 22110694.
57. Fischer R, Wajant H, Kontermann R, Pfizenmaier K, Maier O. Astrocyte-specific activation of TNFR2 promotes oligodendrocyte maturation by secretion of leukemia inhibitory factor. Glia 2014, 62(2):272-283. 10.1002/glia.22605, 24310780.
58. Schonberg DL, McTigue DM. Iron is essential for oligodendrocyte genesis following intraspinal macrophage activation. Exp Neurol 2009, 218(1):64-74. 10.1016/j.expneurol.2009.04.005, 19374902.
59. Wan T, Xu Z, Zhou HJ, Zhang H, Luo Y, Li Y, Min W. Functional analyses of TNFR2 in physiological and pathological retina angiogenesis. Invest Ophthalmol Vis Sci 2013, 54(1):211-221. 10.1167/iovs.12-10364, 23188724.