Hyperactivated Stat3 boosts axon regeneration in the CNS

Experimental Neurology

Volumn 280, Issue , 2016, Pages 115-120

  Mehta, Saloni T ^a,c   Luo, Xueting ^a,b,c   Park, Kevin K ^a   Bixby, John L ^a,c   Lemmon, Vance P ^a,c  

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

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

Activation domain; Axon regeneration; Neurite outgrowth; Optic nerve; Transcription factor; VP16

Indexed keywords

STAT3 PROTEIN; CHOLERA TOXIN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CENTRAL NERVOUS SYSTEM; CEREBELLUM CELL; CONTROLLED STUDY; DNA BINDING; FEMALE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; AXON; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETIC TRANSDUCTION; GENETICS; METABOLISM; MUTATION; NERVE REGENERATION; NEURITE; NEWBORN; OPTIC NERVE INJURY; PATHOLOGY; PHYSIOLOGY; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AXONS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CEREBRAL CORTEX; CHOLERA TOXIN; FEMALE; HERPES SIMPLEX VIRUS PROTEIN VMW65; MICE; MICE, INBRED C57BL; MUTATION; NERVE REGENERATION; NEURITES; OPTIC NERVE INJURIES; RATS; STAT3 TRANSCRIPTION FACTOR; TRANSDUCTION, GENETIC; UP-REGULATION;

EID: 84963943836     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.03.004     Document Type: Article

References (32)

1. Bareyre F.M., Garzorz N., Lang C., Misgeld T., Büning H., Kerschensteiner M. In vivo imaging reveals a phase-specific role of STAT3 during central and peripheral nervous system axon regeneration. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:6282-6287. 10.1073/pnas.1015239108.
2. Beerli R.R., Segal D.J., Dreier B., Barbas C.F. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc. Natl. Acad. Sci. 1998, 95:14628-14633. 10.1073/pnas.95.25.14628.
3. Benowitz L.I., Yin Y. Optic nerve regeneration. Arch. Ophthalmol. 2010, 128:1059-1064. (Chicago, Ill. 1960). 10.1001/archophthalmol.2010.152.
4. Blackmore M.G., Moore D.L., Smith R.P., Goldberg J.L., Bixby J.L., Lemmon V.P. High content screening of cortical neurons identifies novel regulators of axon growth. Mol. Cell. Neurosci. 2010, 44:43-54. 10.1016/j.mcn.2010.02.002.
5. Blackmore M.G., Wang Z., Lerch J.K., Motti D., Zhang Y.P., Shields C.B., Lee J.K., Goldberg J.L., Lemmon V.P., Bixby J.L. Krüppel-like factor 7 engineered for transcriptional activation promotes axon regeneration in the adult corticospinal tract. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7517-7522. 10.1073/pnas.1120684109.
6. 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.
7. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., Darnell J.E. Stat3 as an oncogene. Cell 1999, 98:295-303.
8. Dauer D.J., Ferraro B., Song L., Yu B., Mora L., Buettner R., Enkemann S., Jove R., Haura E.B. Stat3 regulates genes common to both wound healing and cancer. Oncogene 2005, 24:3397-3408. 10.1038/sj.onc.1208469.
9. Dominguez E., Mauborgne A., Mallet J., Desclaux M., Pohl M. SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. J. Neurosci. 2010, 30:5754-5766. 10.1523/JNEUROSCI.5007-09.2010.
10. Gao Y., Deng K., Hou J., Bryson J.B., Barco A., Nikulina E., Spencer T., Mellado W., Kandel E.R., Filbin M.T. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 2004, 44:609-621. 10.1016/j.neuron.2004.10.030.
11. Hirai H., Tani T., Kikyo N. Structure and functions of powerful transactivators: VP16, MyoD and FoxA. Int. J. Dev. Biol. 2010, 54:1589-1596. 10.1387/ijdb.103194hh.
12. Huebner E.A., Strittmatter S.M. Axon regeneration in the peripheral and central nervous systems. Results Probl. Cell Differ. 2009, 48:339-351. 10.1007/400_2009_19.
13. Kobayashi N., Horn P.J., Sullivan S.M., Triezenberg S.J., Boyer T.G., Berk A.J. DA-complex assembly activity required for VP16C transcriptional activation. Mol. Cell. Biol. 1998, 18:4023-4031. 10.1128/MCB.18.7.4023.
14. Konermann S., Brigham M.D., Trevino A.E., Hsu P.D., Heidenreich M., Cong L., Platt R.J., Scott D.A., Church G.M., Zhang F. Optical control of mammalian endogenous transcription and epigenetic states. Nature 2013, 500:472-476. 10.1038/nature12466.
15. Lang C., Bradley P.M., Jacobi A., Kerschensteiner M., Bareyre F.M. STAT3 promotes corticospinal remodelling and functional recovery after spinal cord injury. EMBO Rep. 2013, 14:931-937. 10.1038/embor.2013.117.
16. Lerch J.K., Kuo F., Motti D., Morris R., Bixby J.L., Lemmon V.P. Isoform diversity and regulation in peripheral and central neurons revealed through RNA-Seq. PLoS One 2012, 7. 10.1371/journal.pone.0030417.
17. Lerch J.K., Martínez-Ondaro Y.R., Bixby J.L., Lemmon V.P. cJun promotes CNS axon growth. Mol. Cell. Neurosci. 2014, 59:97-105. 10.1016/j.mcn.2014.02.002.
18. Luo X., Salgueiro Y., Beckerman S.R., Lemmon V.P., Tsoulfas P., Park K.K. Three-dimensional evaluation of retinal ganglion cell axon regeneration and pathfinding in whole mouse tissue after injury. Exp. Neurol. 2013, 247:653-662. 10.1016/j.expneurol.2013.03.001.
19. Milbradt A.G., Kulkarni M., Yi T., Takeuchi K., Sun Z.-Y.J., Luna R.E., Selenko P., Näär A.M., Wagner G. Structure of the VP16 transactivator target in the mediator. Nat. Struct. Mol. Biol. 2011, 18:410-415. 10.1038/nsmb.1999.
20. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., Goldberg J.L. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301. 10.1126/science.1175737.
21. 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. 10.1126/science.1161566.
22. Pernet V., Joly S., Jordi N., Dalkara D., Guzik-Kornacka a, Flannery J.G., Schwab M.E. Misguidance and modulation of axonal regeneration by Stat3 and Rho/ROCK signaling in the transparent optic nerve. Cell Death Dis. 2013, 4. 10.1038/cddis.2013.266.
23. Qiu J., Cafferty W.B.J., McMahon S.B., Thompson S.W.N. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. J. Neurosci. 2005, 25:1645-1653. 10.1523/JNEUROSCI.3269-04.2005.
24. Sanchez J.-P. Regulation of gene expression in Arabidopsis thaliana by artificial zinc finger chimeras. Plant Cell Physiol. 2002, 43:1465-1472. 10.1093/pcp/pcf186.
25. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3:1101-1108. 10.1038/nprot.2008.73.
26. Schwaiger F.-W., Schmitt G.H., andreas B., Horvat A., Hager G., Streif R., Spitzer C., Gamal S., Breuer S., Brook G.A., Nacimiento W., Kreutzberg G.W. Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). Eur. J. Neurosci. 2000, 12:1165-1176. 10.1046/j.1460-9568.2000.00005.x.
27. Shi W., Inoue M., Minami M., Takeda K., Matsumoto M., Matsuda Y., Kishimoto T., Akira S. The genomic structure and chromosomal localization of the mouse STAT3 gene. Int. Immunol. 1996, 8:1205-1211.
28. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., Martinez-Carrasco I., Connolly L., He Z. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623. 10.1016/j.neuron.2009.11.021.
29. Smith R.P., Lerch-Haner J.K., Pardinas J.R., Buchser W.J., Bixby J.L., Lemmon V.P. Transcriptional profiling of intrinsic PNS factors in the postnatal mouse. Mol. Cell. Neurosci. 2011, 46:32-44. 10.1016/j.mcn.2010.07.015.
30. Tedeschi A. Tuning the orchestra: transcriptional pathways controlling axon regeneration. Front. Mol. Neurosci. 2011, 4:60. 10.3389/fnmol.2011.00060.
31. Wang X., Hasan O., Arzeno A., Benowitz L.I., Cafferty W.B.J., Strittmatter S.M. Axonal regeneration induced by blockade of glial inhibitors coupled with activation of intrinsic neuronal growth pathways. Exp. Neurol. 2012, 237:55-69. 10.1016/j.expneurol.2012.06.009.
32. Yungher B.J., Luo X., Salgueiro Y., Blackmore M.G., Park K.K. Viral vector-based improvement of optic nerve regeneration: characterization of individual axons' growth patterns and synaptogenesis in a visual target. Gene Ther. 2015, 22:811-821. 10.1038/gt.2015.51.