Systemically administered interleukin-10 reduces tumor necrosis factor- alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats

Journal of Neurotrauma

Volumn 16, Issue 10, 1999, Pages 851-863

  Bethea, John R ^a   Nagashima, Hideki ^b   Acosta, Marcia C ^a   Briceno, Carmen ^a   Gomez, Frankie ^a   Marcillo, Alexander E ^a   Loor, Kim ^a   Green, Jeremy ^a   Dietrich, W Dalton ^a  

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

^b TOTTORI UNIVERSITY   (Japan)

Author keywords

Axonal growth; Inflammation; behavioral recovery; Interleukin 10; Spinal cord injury

Indexed keywords

INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; HELPER CELL; MACROPHAGE ACTIVATION; MOTOR PERFORMANCE; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; RAT; SCORING SYSTEM; SPINAL CORD INJURY; WOUND HEALING;

EID: 0032739262     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.1999.16.851     Document Type: Article

References (57)

1. AHUJA, V., MILLER, S.E., and HOWELL, D.N. (1995). Identification of two subpopulations of rat monocytes expressing disparate molecular forms and quantities of CD43. Cell. Immunol. 163, 59-69.
2. BAEUERLE, P.A., and BALTIMORE, D. (1996). NF-κB: ten years after. Cell 87, 13-20.
3. BALASINGHAM, V., and YONG, V.W. (1996). Attenuation of astroglial reactivity by interleukin-10. J. Neurosci. 16, 2945-2955.
4. BARBIERI, I., BRUSA, R., BASUDEV, H., CASATI, C., and GRILLI, M. (1998). Neuroprotective action of interleukin-10 in mouse primary neuronal cultures. J. Neurosci. Abstr., 568.13.
5. 2+ accumulation. Proc. Natl. Acad. Sci. U. S. A. 92, 9328-9332.
6. BARNA, B.P., PETTAY, J., BARNETT, G.H., ZHOU, P., IWASAKI, K., and ESTES, M.L. (1994). Regulation of monocyte chemoattractant protein-1 expression in adult human non-neoplastic astrocytes is sensitive to tumor necrosis factor (TNF) or antibody to the 55-kDa TNF receptor. J. Neuroimmunol. 50, 101-107.
7. BARTHOLDI, D., and SCHWAB, M.E. (1997). Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur. J. Neurosci. 9, 1422-1438.
8. BASSO, M.D., BEATTIE, M.S., and BRESNAHAN J.C. (1996). Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 139, 244-256.
9. BEG A.A., and BALTIMORE, D. (1996). An essential role of NK-κB in preventing TNF-α-induced cell death. Science 274, 272-274.
10. BENVENISTE, E.N. (1992). Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action. Am. J. Physiol. 263, C1-16.
11. BERKMAN, N., JOHN, M., ROESEMS, G., JOSE, P.J., BARNES, P.J., and CHUNG, K.P. (1995). Inhibition of macrophage inflammatory protein-1 α expression by IL-10. J. Immunol. 155, 4412-4418.
12. BERMAN, J.W., GUIDA, M.P., WARREN, J., AMAT, J., and BROSNAN, C.F. (1996). Localization of monocyte chemoattractant peptide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J. Immunol. 156, 3017-3023.
13. BETHEA, J.R., CASTRO, M., KEANE, R.W., DIETRICH, W.D., and YEZEIRSKI, R.P. (1998). Traumatic spinal cord injury induces nuclear factor-κB activation. J Neurosci. 18, 3251-3260.
14. BLIGHT, A.R. (1985). Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. C.N.S. Trauma 2, 299-315.
15. BRACKEN, M.B., SHEPARD, M., COLLINS, W.F., et al. (1990). A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. N. Engl. J. Med. 322, 1405-1411.
16. BRACKEN, M.B., SHEPARD, M., HOLFORD, T.R., et al. (1997). Administration of methylprednisolone for 24 or 48 hours or tirilazaed mesylate for 48 hours in the treatment of acute spinal cord. J.A.M.A. 277, 1597-1604.
17. BRODIE, C. (1996). Differential effects of Th1 and Th2 derived cytokines on NGF synthesis by mouse astrocytes. F.E.B.S. Lett. 394, 117-120.
18. CARLSON, S.L., PARRISH, M.E., SPRINGER, J.E., DOTY, K., and DOSSETT, L. (1998). Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 151, 77-88.
19. CHENG, B., CHRISTAKOS, S., and MATTSON, M.P. (1994). Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12, 139-153.
20. CONSTANTINI, S., and YOUNG, W. (1994). The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. J. Neurosurg. 80, 97-111.
21. CRISI, G.M., SANTAMBROGIO, L., HOCHWALD, G.M., SMITH, S.R., CARLINO, J.A., and THORBECK, G.J. (1995). Staphylococcal enterotoxin B and tumor-necrosis factor-α-induced relapses of experimental allergic encephalomyelitis: protection by transforming growth factor-β and interleukin-10. Eur. J. Immunol. 25, 3035-3040.
22. CUNHA, F.G, MONCADA, S., and LIEW, F.Y. (1992). Interleukin-10 inhibits the induction of nitric oxide synthase by interferon-γ in murine macrophages. Biochem. Biophys. Res. Commun. 183, 1155-1159.
23. DUSART, I., and SCHWAB, M.E. (1994). Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6, 712-724.
24. FREI, K., LINS, H., SCHWERDEL, C., and FONTANA, A. (1994). Antigen presentation in the central nervous system: the inhibitory effect of IL-10 on MHC class II expression and production of cytokines depends on the inducing signals and the type of cell analyzed. J. Immunol. 152, 2720-2728.
25. GHENG, Y., GULBINS, E., ALTMAN, A., and LOTZ, M. (1994). Monocyte deactivation by interleukin 10 via inhibition of tyrosine kinase activity and the Ras signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 91, 8602-8606.
26. GHIRNIKAR, R.S, LEE, Y.L., HE, T.R., and ENG, L.F. (1996). Chemokine expression in rat stab wound brain injury. J. Neurosci. Res. 46, 727-733.
27. GRUNER, J.A. (1992). A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9, 123-128.
28. GUTH, L., ZHANG, Z., and ROBERTS, E. (1995). Key role for pregnenolone in combination therapy that promotes recovery after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 91, 12308-12312.
29. HIRSCHBERG, D.L., YOLES, E., BELKIN, M., and SCHWARTZ, M. (1994). Inflammation after axonal injury has conflicting consequences for recovery of function: rescue of spared axons is impaired but regeneration is supported. J. Neuroimmunol. 50, 9-16.
30. ISSAZASEH, S., LORENTZEN J.C., MUSTAFA, M.I., HOJEBERG, B., MÜSSENER, A., and OLSSON, T. (1996). Cytokines in relapsing experimental autoimmune encephalomyelitis in DA rats: persistent mRNA expression of pro-inflammatory cytokines and absent expression of interleukin-10 and transforming growth factor-β. J Neuroimmunol. 69, 103-115.
31. KLUSMAN, I., and SCHWAB, M.E. (1997). Effects of pro-inflammatory cytokines in experimental spinal cord injury. Brain Res. 762, 173-184.
32. KNOBLACH, S.M., and FADEN, A.I. (1998). Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp. Neurol. 153, 143-151.
33. KOEDEL, U., BERNATOWICZ, A., FREI, K., FONTANA, A., and PFISTER, H.-W. (1996). Systemically (but not intrathecally) administered IL-10 attenuates pathophysiologic alterations in experimental pneumococcal meningitis. J. Immunol. 157, 5185-5191.
34. LAFORTUNE, L., NALBANTOGLU, J., and ANTLE, J.P. (1996). Expression of tumor necrosis factor-α (TNFα) and interleukin 6 (IL-6) mRNA in adult human astrocytes: comparison with adult microglia and fetal astrocytes. J. Neuropathol. Exp. Neurol. 55, 515-521.
35. LAVINE, S.D., HOFMAN, F.M., and ZLOKOVIC, B.V. (1998). Circulating antibody against tumor necrosis factor alpha protects rat brain from reperfusion injury. J. Cereb. Blood Flow Metab. 18, 52-58.
36. LIPTON, S.A. (1997). Janus faces of NF-κB: neurodestruction versus neuroprotection. Nat. Med. 3, 20-22.
37. 2 synthesis by transforming growth factor-β1 and interleukin 10 in activated microglial cultures. J. Neuroimmunol. 82, 31-39.
38. MIZUNO, T., SAWADA, M., MARUNOUCHI, T., and SUZUMURA, A. (1994). Production of interleukin-10 by mouse glial cells in culture. Biochem. Biophys. Res. Commun. 205, 1907-1915.
39. O'FARRELL, A.M. (1998). IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for STAT 3-dependent and independent pathways. EMBO J. 17, 1006-1018.
40. PAN, W., KASTIN, A., BELL, R., and OLSON, R. (1999). Upregulation of tumor necrosis factor-α transport across the blood barrier after acute compressive spinal cord injury. J. Neurosci. 19, 3649-3655.
41. POPOVICH, P.G., WEI, P., and STOKES, B.T. (1997). Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377, 433-464.
42. RANSOHOFF, R.M., and TANI, M. (1998). Do chemokines mediate leukocyte recruitment in post-traumatic CNS inflammation? T.I.N.S. 21, 154-159.
43. ROMANO, M.F, LAMBERTI, A., PETRELLA, A., et al. (1996). IL-10 inhibits nuclear factor-kB/Rel nuclear activity in CD3-stimulated human peripheral T lymphocytes. J. Immunol. 156, 2119-2123.
44. ROSENBERG, G.A. (1995). Matrix metalloproteinases in brain injury. J. Neurotrauma 12, 833-842.
45. ROTHWELL, N.J., ALLAN, S., and TOULMOND, S. (1997). The role of interleukin 1 in acute neurodegeneration and stroke: pathophysiological and therapeutic implications. J. Clin. Invest. 100, 2648-2652.
46. ROTT, O., FLEISHER, B., and CASH, E. (1994). Interleukin-10 prevents experimental allergic encephalomyelitis in rats. Eur. J. Immunol. 24, 1434-1440.
47. SANNA, A., PFLUG, B., COLANGELO, A.M., and MOCCHETTI, I. (1998) Interleukin-10 prevents glutamate-induced apoptosis in cerebellar granule cells. J. Neurosci. Abstr., 704.16.
48. SHRIKANT, P., WEBER, E., JILLING, T., and BENVENISTE, E.N. (1995). Intercellular adhesion molecule-1 gene expression by glial cells. J. Immunol. 155, 1489-1501.
49. SPERA, P.A, ELLISON, J.A, FEUERSTEIN, G.Z., and BARONE, F.C. (1998). IL-10 reduces rat brain injury following focal stroke. Neurosci. Lett. 251, 189-192.
50. STREIT, W.J., SEMPLE-ROWLAND, S., HURLEY, S.D., MILLER, R.C., POPOVICH, P.G, and STOKES, B.T. (1998). Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152, 74-87.
51. TAOKA, Y., OKAJIMA, K., UCHIBA, M., et al. (1998). Activated protein C reduces the severity of compression-induced spinal cord injury in rats by inhibiting activation of leukocytes. J. Neurosci. 18, 1393-1398.
52. TOULMOND, S., PARNET, P., and LINTHORST, A.C.E. (1996). When cytokines get on your nerves: cytokine networks and DNS pathologies. Trends Neurosci. 19, 409-410.
53. TUREEN, J. (1995). Effect of recombinant human tumor necrosis factor-alpha on cerebral oxygen uptake, cerebrospinal fluid lactate, and cerebral blood flow in the rabbit: role of nitric oxide. J. Clin. Invest. 95, 1086-1091.
54. WANG, C.X., NUTTIN, B., HEREMANS, H., DOM, R., and GUYBELS, J. (1996). Production of tumor necrosis factor in spinal cord following traumatic injury in rats. J. Neuroimmunol. 69, 151-156.
55. XU, J., FAN, G., CHEN, S., WU, Y., ZU, X.M., and HSU, C.Y. (1998). Methylprednisolone inhibition of TNF-α expression and NF-kB activation after spinal cord injury in rats. Mol. Brain Res. 59, 135-142.
56. YAKOVLEV, A.G., and FADEN, A.I. (1994). Sequential expression of c-fos protooncogene, TNF-alpha, and dynorphin genes in spinal cord following experimental traumatic injury. Mol. Chem. Neuropathol. 23, 179-190.
57. ZHANG, Z., KREBES, C.J., and GUTH, L. (1997). Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143, 141-152.