Differential patterns of local gene regulation in crush lesions of the rat optic and sciatic nerve: Relevance to posttraumatic regeneration

Cellular Physiology and Biochemistry

Volumn 26, Issue 3, 2010, Pages 483-494

  Zickler, Philipp ^a   Küry, Patrick ^a   Gliem, Michael ^a   Hartung, Hans Peter ^a   Jander, Sebastian ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Aquaporin 4; Axon; Inflammation; Nerve crush; Plasminogen activator

Indexed keywords

AQUAPORIN 4; CATHEPSIN B; CATHEPSIN D; CATHEPSIN L; CD53 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; COMPLEMENT COMPONENT C5A RECEPTOR; CYTOSOLIC PHOSPHOLIPASE A2; DNA TOPOISOMERASE; FATTY ACID BINDING PROTEIN; HEXOKINASE 1; HIGH MOBILITY GROUP PROTEIN; INTERLEUKIN 18; MYELIN BASIC PROTEIN; MYELIN PROTEIN; PLASMINOGEN ACTIVATOR; POTASSIUM CHANNEL KV1.1; PROTEASOME; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DNA DETERMINATION; GENE CONTROL; IMMUNOHISTOCHEMISTRY; MALE; NERVE REGENERATION; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; OPTIC NERVE DISEASE; OPTIC NERVE LESION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCIATIC NERVE; SCIATIC NERVE INJURY;

RATTUS;

EID: 78650001645     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000320571     Document Type: Article

References (72)

1. Bareyre FM, Schwab ME: Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends Neurosci 2003;26:555-563.
2. David S, Lacroix S: Molecular approaches to spinal cord repair. Annu Rev Neurosci 2003;26:411-440.
3. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L: Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338:278-285.
4. Ferguson B, Matyszak MK, Esiri MM, Perry VH: Axonal damage in acute multiple sclerosis lesions. Brain 1997;120:393-399.
5. Harel N Y, Strittmatter SM: Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat Rev Neurosci 2006;7:603-616.
6. David S, Aguayo AJ: Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 1981;214:931-933.
7. Schwab ME: Increasing plasticity and functional recovery of the lesioned spinal cord. Prog Brain Res 2002;137:351-359.
8. Chen ZL, Yu WM, Strickland S: Peripheral regeneration. Annu Rev Neurosci 2007;30:209-233.
9. Vargas ME, Barres BA: Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 2007;30:153-179.
10. Küry P, Schroeter M, Jander S: Transcriptional response to circumscribed cortical brain ischemia: spatiotemporal patterns in ischemic vs. remote non-ischemic cortex. Eur J Neurosci 2004;19:1708-1720.
11. Küry P, Greiner-Petter R, Cornely C, Jurgens T, Müller HW: Mammalian achaete scute homolog 2 is expressed in the adult sciatic nerve and regulates the expression of Krox24, Mob-1, CXCR4, and p57kip2 in Schwann cells. J Neurosci 2002;22:7586-7595.
12. Jander S, Schroeter M, Stoll G: Interleukin-18 expression after focal ischemia of the rat brain: association with the late-stage inflammatory response. J Cereb Blood Flow Metab 2002;22:62-70.
13. Trapp BD, Hauer P, Lemke G: Axonal regulation of myelin protein mRNA levels in actively myelinating Schwann cells. J Neurosci 1988;8:3515-3521.
14. Kim DS, Choi JO, Rim HD, Cho HJ: Downregulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res Mol Brain Res 2002;105:146-152.
15. Carmel JB, Galante A, Soteropoulos P, Tolias P, Recce M, Young W, Hart RP: Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiol Genomics 2001;7:201-213.
16. Fan M, Mi R, Yew DT, Chan WY: Analysis of gene expression following sciatic nerve crush and spinal cord hemisection in the mouse by microarray expression profiling. Cell Mol Neurobiol 2001;21:497-508.
17. Küry P, Abankwa D, Kruse F, Greiner-Petter R, Müller HW: Gene expression profiling reveals multiple novel intrinsic and extrinsic factors associated with axonal regeneration failure. Eur J Neurosci 2004;19:32-42.
18. Szpara ML, Vranizan K, Tai YC, Goodman CS, Speed TP, Ngai J: Analysis of gene expression during neurite outgrowth and regeneration. BMC Neurosci 2007;8:100.
19. Bosse F, Hasenpusch-Theil K, Küry P, Müller HW: Gene expression profiling reveals that peripheral nerve regeneration is a consequence of both novel injury-dependent and reactivated developmental processes. J Neurochem 2006;96:1441-1457.
20. Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke MJ, Misko TP, Shooter E, Thoenen H: Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci USA 1987;84:8735-8739.
21. Perrin FE, Lacroix S, Aviles-Trigueros M, David S: Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration. Brain 2005;128:854-866.
22. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J: Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997;390:680-683.
23. Stoll G, Griffin JW, Li C Y, Trapp BD: Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 1989;18:671-683.
24. Stoll G, Trapp BD, Griffin JW: Macrophage function during Wallerian degeneration of rat optic nerve: clearance of degenerating myelin and Ia expression. J Neurosci 1989;9:2327-2335.
25. Jander S, Lausberg F, Stoll G: Differential recruitment of CD8+ macrophages during Wallerian degeneration in the peripheral and central nervous system. Brain Pathol 2001;11:27-38.
26. Menge T, Jander S, Stoll G: Induction of the proinflammatory cytokine interleukin-18 by axonal injury. J Neurosci Res 2001;65:332-339.
27. Küry P, Zickler P, Stoll G, Hartung H P, Jander S: Osteopontin, a macrophage-derived matricellular glycoprotein, inhibits axon outgrowth. Faseb J 2005;19:398-400.
28. Blaugrund E, Duvdevani R, Lavie V, Solomon A, Schwartz M: Disappearance of astrocytes and invasion of macrophages following crush injury of adult rodent optic nerves: implications for regeneration. Exp Neurol 1992;118:105-115.
29. Frank M, Wolburg H: Cellular reactions at the lesion site after crushing of the rat optic nerve. Glia 1996;16:227-240.
30. Nesic O, Lee J, Ye Z, Unabia GC, Rafati D, Hulsebosch CE, Perez-Polo JR: Acute and chronic changes in aquaporin 4 expression after spinal cord injury. Neuroscience 2006;143:779-792.
31. Saadoun S, Bell BA, Verkman AS, Papadopoulos MC: Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice. Brain. 2008;131:1087-98
32. Warth A, Simon P, Capper D, Goeppert B, Tabatabai G, Herzog H, Dietz K, Stubenvoll F, Ajaaj R, Becker R, Weller M, Meyermann R, Wolburg H, Mittelbronn M: Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood-brain barrier disturbance but not with patient survival. J Neurosci Res 2007;85:1336-1346.
33. Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS: Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. Faseb J 2007;21:108-116.
34. Nicchia GP, Srinivas M, Li W, Brosnan CF, Frigeri A, Spray DC: New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin43. Faseb J 2005;19:1674-1676.
35. Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W, Mandler RN, Weinshenker BG, Pittock SJ, Wingerchuk DM, Lucchinetti CF: Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 2007;130:1194-1205.
36. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR: IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005;202:473-477.
37. Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, Glogowska M, Case D, Antel JP, Owens G P, Gilden D, Nessler S, Stadelmann C, Hemmer B: Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009;66:617-629.
38. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, Adzemovic M, Bauer J, Berger T, Fujihara K, Itoyama Y, Lassmann H: Neuromyelitis optica: pathogenicity of patient immunoglobu-lin in vivo. Ann Neurol 2009;66:630-643.
39. Peterziel H, Unsicker K, Krieglstein K: TGFbeta induces GDNF responsiveness in neurons by recruitment of GFRalpha1 to the plasma membrane. J Cell Biol 2002;159:157-167.
40. Kveiborg M, Flyvbjerg A, Eriksen EF, Kassem M: Transforming growth factor-beta1 stimulates the production of insulin-like growth factor-I and insulinlike growth factor-binding protein-3 in human bone marrow stromal osteoblast progenitors. J Endocrinol 2001;169:549-561.
41. Mohan S, Baylink DJ: IGF-binding proteins are multifunctional and act via IGF-dependent and -independent mechanisms. J Endocrinol 2002;175:19-31.
42. Oh SH, Lee OH, Schroeder CP, Oh YW, Ke S, Cha HJ, Park RW, Onn A, Herbst RS, Li C, Lee HY: Antimetastatic activity of insulin-like growth factor binding protein-3 in lung cancer is mediated by insulin-like growth factor-independent urokinase-type plasminogen activator inhibition. Mol Cancer Ther 2006;5:2685-2695.
43. Dunn SE, Torres J V, Oh JS, Cykert DM, Barrett JC: Up-regulation of urokinase-type plasminogen activator by insulinlike growth factor-I depends upon phosphatidylinositol-3 kinase and mitogen-activated protein kinase kinase. Cancer Res 2001;61:1367-1374.
44. Pizzi MA, Crowe MJ: Matrix metalloproteinases and proteoglycans in axonal regeneration. Exp Neurol 2007;204:496-511.
45. Siconolfi LB, Seeds NW: Mice lacking tPA, uPA, or plasminogen genes showed delayed functional recovery after sciatic nerve crush. J Neurosci 2001;21:4348-4355.
46. Siconolfi LB, Seeds NW: Induction of the plasminogen activator system accompanies peripheral nerve regeneration after sciatic nerve crush. J Neurosci 2001;21:4336-4347.
47. Akassoglou K, Kombrinck KW, Degen JL, Strickland S: Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol 2000;149:1157-1166.
48. Moalem G, Gdalyahu A, Shani Y, Otten U, Lazarovici P, Cohen IR, Schwartz M: Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J Autoimmun 2000;15:331-345.
49. Starkey GD, Petratos S, Shipham KA, Butzkueven H, Bucci T, Lowry K, Cheema SS, Kilpatrick TJ: Neurotrophin receptor expression and responsiveness by postnatal cerebral oligodendroglia. Neuroreport 2001;12:4081-4086.
50. Sachs BD, Baillie GS, McCall JR, Passino MA, Schachtrup C, Wallace DA, Dunlop AJ, MacKenzie KF, Klussmann E, Lynch MJ, Sikorski SL, Nuriel T, Tsigelny I, Zhang J, Houslay MD, Chao MV, Akassoglou K: p75 neurotrophin receptor regulates tissue fibrosis through inhibition of plasminogen activation via a PDE4/ cAMP/PKA pathway. J Cell Biol 2007;177:1119-1132.
51. Nakajima K, Reddington M, Kohsaka S, Kreutzberg GW: Induction of urokinase-type plasminogen activator in rat facial nucleus by axotomy of the facial nerve. J Neurochem 1996;66:2500-2505.
52. Moriwaki H, Stempien-Otero A, Kremen M, Cozen AE, Dichek DA: Overexpression of urokinase by macrophages or deficiency of plasminogen activator inhibitor type 1 causes cardiac fibrosis in mice. Circ Res 2004;95:637-644.
53. Parfyonova Y, Plekhanova O, Solomatina M, Naumov V, Bobik A, Berk B, Tkachuk V: Contrasting effects of urokinase and tissue-type plasminogen activators on neointima formation and vessel remodelling after arterial injury. J Vasc Res 2004;41:268-276.
54. Schäfer BM, Maier K, Eickhoff U, Todd RF, Kramer MD: Plasminogen activation in healing human wounds. Am J Pathol 1994;144:1269-1280.
55. Bugge TH, Flick MJ, Danton MJ, Daugherty CC, Romer J, Dano K, Carmeliet P, Collen D, Degen JL: Urokinase-type plasminogen activator is effective in fibrin clearance in the absence of its receptor or tissue-type plasminogen activator. Proc Natl Acad Sci USA 1996;93:5899-5904.
56. Zhu M, Gokhale VM, Szabo L, Munoz RM, Baek H, Bashyam S, Hurley LH, Von Hoff DD, Han H: Identification of a novel inhibitor of urokinase-type plasminogen activator. Mol Cancer Ther 2007;6:1348-1356.
57. Lin AC, Holt CE: Local translation and directional steering in axons. Embo J 2007;26:3729-3736.
58. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M: Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 2003;40:1095-1104.
59. Willis DE, Twiss JL: The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 2006;16:111-118.
60. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW: Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 2005;25:331-342.
61. Sun W, Kim H: Neurotrophic roles of the beta-thymosins in the development and regeneration of the nervous system. Ann N Y Acad Sci 2007;1112:210-218.
62. Kim Y, Kim EH, Hong S, Rhyu IJ, Choe J, Sun W, Kim H: Expression of thymosin beta in the rat brain following transient global ischemia. Brain Res 2006;1085:177-182.
63. Roth LW, Bormann P, Wiederkehr C, Reinhard E: Beta-thymosin, a modulator of the actin cytoskeleton is increased in regenerating retinal ganglion cells. Eur J Neurosci 1999;11:3488-3498.
64. Colby GP, Sung YJ, Ambron RT: mRNAs encoding the Aplysia homologues of fasciclin-I and beta-thymosin are expressed only in the second phase of nerve injury and are differentially segregated in axons regenerating in vitro and in vivo. J Neurosci Res 2005;82:484-498.
65. Choe J, Sun W, Yoon SY, Rhyu IJ, Kim EH, Kim H: Effect of thymosin beta15 on the branching of developing neurons. Biochem Biophys Res Commun 2005;331:43-49.
66. Roth LW, Bormann P, Bonnet A, Reinhard E: beta-thymosin is required for axonal tract formation in developing zebrafish brain. Development 1999;126:1365-1374.
67. Van Kesteren RE, Carter C, Dissel HM, van Minnen J, Gouwenberg Y, Syed NI, Spencer GE, Smit AB: Local synthesis of actin-binding protein beta-thymosin regulates neurite outgrowth. J Neurosci 2006;26:152-157.
68. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL: Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 2007;178:965-980.
69. Faden AI, Movsesyan VA, Knoblach SM, Ahmed F, Cernak I: Neuroprotective effects of novel small peptides in vitro and after brain injury. Neuropharmacology 2005;49:410-424.
70. Anadon R, Luz Diaz M, Becerra M, Jesus Manso M: Presence of thyrotropin-releasing-hormone-immunoreactive (TRHir) amacrine cells in the retina of anuran and urodele amphibians. Brain Res 2002;926:86-93.
71. Fernandez-Agullo T: Thyrotropin-releasing hormone and its receptor in glia. Glia 2001;33:267-276.
72. Murashov AK, Chintalgattu V, Islamov RR, Lever TE, Pak ES, Sierpinski PL, Katwa LC, Van Scott MR: RNAi pathway is functional in peripheral nerve axons. Faseb J 2007;21:656-670.