IL-6 promotes regeneration and functional recovery after cortical spinal tract injury by reactivating intrinsic growth program of neurons and enhancing synapse formation

Experimental Neurology

Volumn 236, Issue 1, 2012, Pages 19-27

  Yang, Ping ^a   Wen, Huizhong ^a   Ou, Shan ^a,b   Cui, Jian ^a   Fan, Dehua ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Department of Anesthesiology   (China)

Author keywords

Growth associated genes; IL 6; Intrinsic growth program; Regeneration; SCI; Synapse

Indexed keywords

ARGINASE 1; GROWTH ASSOCIATED PROTEIN; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MYELIN; NEUROMODULIN; PROTEIN SPRR1A; RECOMBINANT INTERLEUKIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REACTIVATION; ENZYME SUBSTRATE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL TRACT; RAT; SPINAL CORD INJURY; SYNAPSE; TREATMENT RESPONSE;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; INTERLEUKIN-6; NERVE GROWTH FACTORS; NERVE REGENERATION; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84861698354     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.03.019     Document Type: Article

References (44)

1. 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.
2. Batchelor P.E., Liberatore G.T., Wong J.Y., Porritt M.J., Frerichs F., Donnan G.A., Howells D.W. Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J. Neurosci. 1999, 19:1708-1716.
3. Bechmann I., Nitsch R. Identification of phagocytic glial cells after lesion-induced anterograde degeneration using double-fluorescence labeling: combination of axonal tracing and lectin or immunostaining. Histochem. Cell Biol. 1997, 107:391-397.
4. Benveniste E.N., Tang L.P., Law R.M. Differential regulation of astrocyte TNF-alpha expression by the cytokines TGF-beta, IL-6 and IL-10. Int. J. Dev. Neurosci. 1995, 13:341-349.
5. Berry M., Ahmed Z., Douglas M.R., Logan A. Epidermal growth factor receptor antagonists and CNS axon regeneration: mechanisms and controversies. Brain Res. Bull. 2011, 84:289-299.
6. Bolin L.M., Verity A.N., Silver J.E., Shooter E.M., Abrams J.S. Interleukin-6 production by Schwann cells and induction in sciatic nerve injury. J. Neurochem. 1995, 64:850-858.
7. Bonilla I.E., Tanabe K., Strittmatter S.M. Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 2002, 22:1303-1315.
8. Cai D., Deng K., Mellado W., Lee J., Ratan R.R., Filbin M.T. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002, 35:711-719.
9. Cao Z., Gao Y., Bryson J.B., Hou J., Chaudhry N., Siddiq M., Martinez J., Spencer T., Carmel J., Hart R.B., Filbin M.T. The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. J. Neurosci. 2006, 26:5565-5573.
10. Codeluppi S., Svensson C., Hefferan M., Valencia F., Silldorff M., Oshiro M., Marsala M., Pasquale E. The Rheb-mTOR pathway is upregulated in reactive astrocytes of the injured spinal cord. J. Neurosci. 2009, 29:1093-1104.
11. Domeniconi M., Filbin M.T. Overcoming inhibitors in myelin to promote axonal regeneration. J. Neurol. Sci. 2005, 233:43-47.
12. Gadient R.A., Otten U. Interleukin-6 and interleukin-6 receptor mRNA expression in rat central nervous system. Ann. N. Y. Acad. Sci. 1995, 762:403-406.
13. Hakkoum D., Stoppini L., Muller D. Interleukin-6 promotes sprouting and functional recovery in lesioned organotypic hippocampal slice cultures. J. Neurochem. 2007, 100:747-757.
14. Heinrich P.C., Behrmann I., Muller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 1998, 334(Pt 2):297-314.
15. Hirano T., Yasukawa K., Harada H., Taga T., Watanabe Y., Matsuda T., Kashiwamura S., Nakajima K., Koyama K., Iwamatsu A., et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1986, 324:73-76.
16. Hirota H., Kiyama H., Kishimoto T., Taga T. Accelerated nerve regeneration in mice by upregulated expression of interleukin (IL) 6 and IL-6 receptor after trauma. J. Exp. Med. 1996, 183:2627-2634.
17. Hoffman P.N. Expression of GAP-43, a rapidly transported growth-associated protein, and class II beta tubulin, a slowly transported cytoskeletal protein, are coordinated in regenerating neurons. J. Neurosci. 1989, 9:893-897.
18. Hoffman P., Cleveland D. Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: induction of a specific beta-tubulin isotype. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:4530-4533.
19. Kiefer R., Lindholm D., Kreutzberg G.W. Interleukin-6 and transforming growth factor-beta 1 mRNAs are induced in rat facial nucleus following motoneuron axotomy. Eur. J. Neurosci. 1993, 5:775-781.
20. Kossmann T., Hans V.H., Imhof H.G., Stocker R., Grob P., Trentz O., Morganti-Kossmann C. Intrathecal and serum interleukin-6 and the acute-phase response in patients with severe traumatic brain injuries. Shock 1995, 4:311-317.
21. Kossmann T., Hans V., Imhof H.G., Trentz O., Morganti-Kossmann M.C. Interleukin-6 released in human cerebrospinal fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res. 1996, 713:143-152.
22. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., Xu B., Connolly L., Steward O., Zheng B., He Z. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13:1075-1081.
23. Mogi M., Harada M., Kondo T., Riederer P., Inagaki H., Minami M., Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci. Lett. 1994, 180:147-150.
24. Murphy P.G., Grondin J., Altares M., Richardson P.M. Induction of interleukin-6 in axotomized sensory neurons. J. Neurosci. 1995, 15:5130-5138.
25. Mutlu L.K., Woiciechowsky C., Bechmann I. Inflammatory response after neurosurgery. Best Pract. Res. Clin. Anaesthesiol. 2004, 18:407-424.
26. Neumann H., Schweigreiter R., Yamashita T., Rosenkranz K., Wekerle H., Barde Y.A. Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a rho-dependent mechanism. J. Neurosci. 2002, 22:854-862.
27. Niederost B., Oertle T., Fritsche J., McKinney R.A., Bandtlow C.E. Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J. Neurosci. 2002, 22:10368-10376.
28. Norton W.T., Poduslo S.E. Myelination in rat brain: method of myelin isolation. J. Neurochem. 1973, 21:749-757.
29. Ou S., Zhao Y., Xiao Z., Wen H., Cui J., Ruan H. Effect of lappaconitine on neuropathic pain mediated by P2X3 receptor in rat dorsal root ganglion. Neurochem. Int. 2011, 58:564-573.
30. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult cNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
31. Park K.K., Liu K., Hu Y., Kanter J.L., He Z. PTEN/mTOR and axon regeneration. Exp. Neurol. 2010, 223(1):45-50.
32. Pizzi M., Sarnico I., Boroni F., Benarese M., Dreano M., Garotta G., Valerio A., Spano P. Prevention of neuron and oligodendrocyte degeneration by interleukin-6 (IL-6) and IL-6 receptor/IL-6 fusion protein in organotypic hippocampal slices. Mol. Cell. Neurosci. 2004, 25:301-311.
33. Pradervand S., Yasukawa H., Muller O.G., Kjekshus H., Nakamura T., St Amand T.R., Yajima T., Matsumura K., Duplain H., Iwatate M., Woodard S., Pedrazzini T., Ross J., Firsov D., Rossier B.C., Hoshijima M., Chien K.R. Small proline-rich protein 1A is a gp130 pathway- and stress-inducible cardioprotective protein. EMBO J. 2004, 23:4517-4525.
34. Schobitz B., Voorhuis D.A., De Kloet E.R. Localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Neurosci. Lett. 1992, 136:189-192.
35. Schumann G., Huell M., Machein U., Hocke G., Fiebich B.L. Interleukin-6 activates signal transducer and activator of transcription and mitogen-activated protein kinase signal transduction pathways and induces de novo protein synthesis in human neuronal cells. J. Neurochem. 1999, 73:2009-2017.
36. Schwab M.E. Myelin-associated inhibitors of neurite growth. Exp. Neurol. 1990, 109:2-5.
37. 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.
38. Spooren A., Kolmus K., Laureys G., Clinckers R., De Keyser J., Haegeman G., Gerlo S. Interleukin-6, a mental cytokine. Brain Res. Rev. 2011, 67:157-183.
39. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr. Opin. Neurobiol. 2010, 20:510-518.
40. Swartz K.R., Liu F., Sewell D., Schochet T., Campbell I., Sandor M., Fabry Z. Interleukin-6 promotes post-traumatic healing in the central nervous system. Brain Res. 2001, 896:86-95.
41. Teng F.Y., Tang B.L. Axonal regeneration in adult CNS neurons-signaling molecules and pathways. J. Neurochem. 2006, 96:1501-1508.
42. Wu D., Zhang Y., Bo X., Huang W., Xiao F., Zhang X., Miao T., Magoulas C., Subang M.C., Richardson P.M. Actions of neuropoietic cytokines and cyclic AMP in regenerative conditioning of rat primary sensory neurons. Exp. Neurol. 2007, 204:66-76.
43. Wu D., Yang P., Zhang X., Luo J., Haque M.E., Yeh J., Richardson P.M., Zhang Y., Bo X. Targeting a dominant negative rho kinase to neurons promotes axonal outgrowth and partial functional recovery after rat rubrospinal tract lesion. Mol. Ther. 2009, 17:2020-2030.
44. Yang P., Wen H., Zhang J. Expression of a dominant-negative Rho-kinase promotes neurite outgrowth in a microenvironment mimicking injured central nervous system. Acta Pharmacol. Sin. 2010, 1-9.