The transcription factor Sox11 promotes nerve regeneration through activation of the regeneration-associated gene Sprr1a

Experimental Neurology

Volumn 233, Issue 1, 2012, Pages 221-232

  Jing, Xiaotang ^a   Wang, Ting ^a   Huang, Shaohua ^a   Glorioso, Joseph C ^a   Albers, Kathryn M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

HSV vector; Saphenous nerve injury; Skin delivery; Sry; Transcriptional control

Indexed keywords

HERPESVIRUS VECTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SOX11;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; MALE; MOUSE; MYELINATED NERVE; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE INJURY; PLASMID; PRIORITY JOURNAL; SAPHENOUS NERVE; SKIN SENSITIVITY; SMALL PROLINE RICH PROTEIN 1A GENE; SPINAL GANGLION; TRANSCRIPTION INITIATION; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CORNIFIED ENVELOPE PROLINE-RICH PROTEINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MUTAGENESIS; NERVE CRUSH; NERVE FIBERS; NERVE REGENERATION; NEURITES; PAIN MEASUREMENT; PERIPHERAL NERVE INJURIES; RNA, MESSENGER; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; SIMPLEXVIRUS; SKIN; SOXC TRANSCRIPTION FACTORS; TIME FACTORS; TRANSFECTION;

EID: 84856223608     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.10.005     Document Type: Article

References (50)

1. Abe N., Cavalli V. Nerve injury signaling. Curr. Opin. Neurobiol. 2008, 18:276-283.
2. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., Kuznetsov H., Wang C.F., Coburn D., Newburger D.E., Morris Q., Hughes T.R., Bulyk M.L. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
3. Bergsland M., Werme M., Malewicz M., Perlmann T., Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 2006, 20:3475-3486.
4. Bhattaram P., Penzo-Mendez A., Sock E., Colmenares C., Kaneko K.J., Vassilev A., Depamphilis M.L., Wegner M., Lefebvre V. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat. Commun. 2010, 1:9.
5. 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.
6. Bridge P.M., Ball D.J., Mackinnon S.E., Nakao Y., Brandt K., Hunter D.A., Hertl C. Nerve crush injuries-a model for axonotmesis. Exp. Neurol. 1994, 127:284-290.
7. Carroll J.M., Taichman L.B. Characterization of the human involucrin promoter using a transient beta-galactosidase assay. J. Cell Sci. 1992, 103(Pt 4):925-930.
8. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 2002, 3:16.
9. Fischer D.F., van Drunen C.M., Winkler G.S., van de Putte P., Backendorf C. Involvement of a nuclear matrix association region in the regulation of the SPRR2A keratinocyte terminal differentiation marker. Nucleic Acids Res. 1998, 26:5288-5294.
10. Gladman S.J., Ward R.E., Michael-Titus A.T., Knight M.M., Priestley J.V. The effect of mechanical strain or hypoxia on cell death in subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience 2010, 171:577-587.
11. Goins W.F., Krisky D.M., Wechuck J.B., Huang S., Glorioso J.C. Construction and production of recombinant herpes simplex virus vectors. Methods Mol. Biol. 2008, 433:97-113.
12. Goins W.F., Krisky D.M., Wolfe D.P., Fink D.J., Glorioso J.C. Development of replication-defective herpes simplex virus vectors. Methods Mol. Med. 2002, 69:481-507.
13. Hargrave M., Wright E., Kun J., Emery J., Cooper L., Koopman P. Expression of the Sox11 gene in mouse embryos suggests roles in neuronal maturation and epithelio-mesenchymal induction. Dev. Dyn. 1997, 210:79-86.
14. Harley V.R., Lovell-Badge R., Goodfellow P.N. Definition of a consensus DNA binding site for SRY. Nucleic Acids Res. 1994, 22:1500-1501.
15. Hoffman P.N. A conditioning lesion induces changes in gene expression and axonal transport that enhance regeneration by increasing the intrinsic growth state of axons. Exp. Neurol. 2009, 223:11-18.
16. Hsieh S.T., Chiang H.Y., Lin W.M. Pathology of nerve terminal degeneration in the skin. J. Neuropathol. Exp. Neurol. 2000, 59:297-307.
17. Jankowski M.P., Cornuet P.K., McIlwrath S., Koerber H.R., Albers K.M. SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth. Neuroscience 2006, 143:501-514.
18. Jankowski M.P., Lawson J.J., McIlwrath S.L., Rau K.K., Anderson C.E., Albers K.M., Koerber H.R. Sensitization of cutaneous nociceptors after nerve transection and regeneration: possible role of target-derived neurotrophic factor signaling. J. Neurosci. 2009, 29:1636-1647.
19. Jankowski M.P., McIlwrath S.L., Jing X., Cornuet P.K., Salerno K.M., Koerber H.R., Albers K.M. Sox11 transcription factor modulates peripheral nerve regeneration in adult mice. Brain Res. 2009, 1256:43-54.
20. Jenkins R., Hunt S.P. Long-term increase in the levels of c-jun mRNA and jun protein-like immunoreactivity in motor and sensory neurons following axon damage. Neurosci. Lett. 1991, 129:107-110.
21. Jin H.W., Ichikawa H., Fujita M., Yamaai T., Mukae K., Nomura K., Sugimoto T. Involvement of caspase cascade in capsaicin-induced apoptosis of dorsal root ganglion neurons. Brain Res. 2005, 1056:139-144.
22. Kartasova T., van de Putte P. Isolation, characterization, and UV-stimulated expression of two families of genes encoding polypeptides of related structure in human epidermal keratinocytes. Mol. Cell. Biol. 1988, 8:2195-2203.
23. Kondoh H., Kamachi Y. SOX-partner code for cell specification: Regulatory target selection and underlying molecular mechanisms. Int. J. Biochem. Cell Biol. 2010, 42:391-399.
24. Kuhlbrodt K., Herbarth B., Sock E., Enderich J., Hermans-Borgmeyer I., Wegner M. Cooperative function of POU proteins and SOX proteins in glial cells. J. Biol. Chem. 1998, 273:16050-16057.
25. Lee N., Neitzel K.L., Devlin B.K., MacLennan A.J. STAT3 phosphorylation in injured axons before sensory and motor neuron nuclei: potential role for STAT3 as a retrograde signaling transcription factor. J. Comp. Neurol. 2004, 474:535-545.
26. Lefebvre V., Dumitriu B., Penzo-Mendez A., Han Y., Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int. J. Biochem. Cell Biol. 2007, 39:2195-2214.
27. Levine M., Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151.
28. Lin L., Lee V.M., Wang Y., Lin J.S., Sock E., Wegner M., Lei L. Sox11 regulates survival and axonal growth of embryonic sensory neurons. Dev. Dyn. 2011, 240:52-64.
29. Makwana M., Raivich G. Molecular mechanisms in successful peripheral regeneration. FEBS J. 2005, 272:2628-2638.
30. Marklund N., Fulp C.T., Shimizu S., Puri R., McMillan A., Strittmatter S.M., McIntosh T.K. Selective temporal and regional alterations of Nogo-A and small proline-rich repeat protein 1A (SPRR1A) but not Nogo-66 receptor (NgR) occur following traumatic brain injury in the rat. Exp. Neurol. 2006, 197:70-83.
31. Mata M., Glorioso J.C., Fink D.J. Targeted gene delivery to the nervous system using herpes simplex virus vectors. Physiol. Behav. 2002, 77:483-488.
32. Penzo-Mendez A.I. Critical roles for SoxC transcription factors in development and cancer. Int. J. Biochem. Cell Biol. 2010, 42:425-428.
33. Potzner M.R., Tsarovina K., Binder E., Penzo-Mendez A., Lefebvre V., Rohrer H., Wegner M., Sock E. Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 2010, 137:775-784.
34. Rich K.M., Yip H.K., Osborne P.A., Schmidt R.E., Johnson E.M. Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury. J. Comp. Neurol. 1984, 230:110-118.
35. Schepers G.E., Teasdale R.D., Koopman P. Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev. Cell 2002, 3:167-170.
36. Schmitt A.B., Breuer S., Liman J., Buss A., Schlangen C., Pech K., Hol E.M., Brook G.A., Noth J., Schwaiger F.W. Identification of regeneration-associated genes after central and peripheral nerve injury in the adult rat. BMC Neurosci. 2003, 4:8.
37. Schmutzler B.S., Roy S., Pittman S.K., Meadows R.M., Hingtgen C.M. Ret-dependent and Ret-independent mechanisms of Gfl-induced sensitization. Mol. Pain 2011, 7:22.
38. Seijffers R., Mills C.D., Woolf C.J. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J. Neurosci. 2007, 27:7911-7920.
39. Snider W.D., Zhou F.Q., Zhong J., Markus A. Signaling the pathway to regeneration. Neuron 2002, 35:13-16.
40. Sock E., Rettig S.D., Enderich J., Bosl M.R., Tamm E.R., Wegner M. Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol. Cell. Biol. 2004, 24:6635-6644.
41. Starkey M.L., Davies M., Yip P.K., Carter L.M., Wong D.J., McMahon S.B., Bradbury E.J. Expression of the regeneration-associated protein SPRR1A in primary sensory neurons and spinal cord of the adult mouse following peripheral and central injury. J. Comp. Neurol. 2009, 513:51-68.
42. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr. Opin. Neurobiol. 2010, 20:510-518.
43. Tanabe K., Bonilla I., Winkles J.A., Strittmatter S.M. Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth. J. Neurosci. 2003, 23:9675-9686.
44. Tonge D.A., Golding J.P., Edbladh M., Kroon M., Ekstrom P.E., Edstrom A. Effects of extracellular matrix components on axonal outgrowth from peripheral nerves of adult animals in vitro. Exp. Neurol. 1997, 146:81-90.
45. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 2000, 15:170-182.
46. Vermeij W.P., Backendorf C. Skin cornification proteins provide global link between ROS detoxification and cell migration during wound healing. PLoS One 2010, 5:e11957.
47. Wegner M. All purpose Sox: the many roles of Sox proteins in gene expression. Int. J. Biochem. Cell Biol. 2009.
48. Wiebe M.S., Nowling T.K., Rizzino A. Identification of novel domains within Sox-2 and Sox-11 involved in autoinhibition of DNA binding and partnership specificity. J. Biol. Chem. 2003, 278:17901-17911.
49. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., Yang L., Huang W.J., Fu G., Xu S.H., Cheng X.P., Yan Q., Zhu Z.D., Zhang X., Chen Z., Han Z.G., Zhang X. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8360-8365.
50. Zlatanova J., van Holde K. Binding to four-way junction DNA: a common property of architectural proteins?. FASEB J. 1998, 12:421-431.