Looking downstream: The role of cyclic AMP-regulated genes in axonal regeneration

Frontiers in Molecular Neuroscience

Volumn 8, Issue JUNE, 2015, Pages

  Siddiq, Mustafa M ^a   Hannila, Sari S ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Arginase I; Cyclic AMP; Interleukin 6; Metallothionein; Regeneration; SLPI; Spinal cord injury; Transcription

Indexed keywords

ARGINASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP; INTERLEUKIN 6; METALLOTHIONEIN I; METALLOTHIONEIN II; METALLOTHIONEIN III; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SMAD2 PROTEIN; STAT3 PROTEIN;

ARTICLE; GENE CONTROL; MICROARRAY ANALYSIS; NERVE FIBER REGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SPINAL GANGLION;

EID: 84941009365     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2015.00026     Document Type: Article

References (39)

1. Boucher, J. L., Custot, J., Vadon, S., Delaforge, M., Lepoivre, M., Tenu, J. P., et al. (1994). N omega-hydroxyl-L-arginine, an intermediate in the L-arginine to nitric oxide pathway, is a strong inhibitor of liver and macrophage arginase. Biochem. Biophys. Res. Commun. 203, 1614-1621. doi: 10.1006/bbrc.1994.2371
2. Cafferty, W. B. J., Gardiner, N. J., Das, P., Qiu, J., McMahon, S. B., and Thompson, S. W. N. (2004). Conditioning injury-induced spinal axon regeneration fails in interleukin-6 knock-out mice. J. Neurosci. 24, 4432-4443. doi: 10.1523/jneurosci.2245-02.2004
3. Cafferty, W. B. J., Gardiner, N. J., Gavazzi, I., Powell, J., McMahon, S. B., Heath, J. K., et al. (2001). Leukemia inhibitory factor determines the growth status of injured adult sensory neurons. J. Neurosci. 21, 7161-7170. doi: 10.3410/f.1001073.15264
4. Cai, D., Deng, K., Mellado, W., Lee, J., Ratan, R. R., and Filbin, M. T. (2002). Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35, 711-719. doi: 10.1016/s0896-6273(02)00826-7
5. Cai, D., Shen, Y., De Bellard, M., Tang, S., and Filbin, M. T. (1999). Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22, 89-101. doi: 10.1016/s0896-6273(00)80681-9
6. Cao, Z., Gao, Y., Bryson, J. B., Hou, J., Chaudhry, N., Siddiq, M., et al. (2006). The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. J. Neurosci. 26, 5565-5573. doi: 10.1523/jneurosci.0815-06.2006
7. Carrasco, J., Penkowa, M., Hadberg, H., Molinero, A., and Hidalgo, J. (2000). Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I+II-deficient mice. Eur. J. Neurosci. 12, 2311-2322. doi: 10.1046/j.1460-9568.2000.00128.x
8. Chung, R. S., Hidalgo, J., and West, A. K. (2008). New insight into the molecular pathways of metallothionein-mediated neuroprotection and regeneration. J. Neurochem. 104, 14-20. doi: 10.1111/j.1471-4159.2007.05026.x
9. Deng, K., He, H., Qiu, J., Lorber, B., Bryson, J. B., and Filbin, M. T. (2009). Increased synthesis of spermidine as a result of upregulation of arginase I promotes axonal regeneration in culture and in vivo. J. Neurosci. 29, 9545-9552. doi: 10.1523/jneurosci.1175-09.2009
10. Di Giovanni, S., Knights, C. D., Rao, M., Yakovlev, A., Beers, J., Catania, J., et al. (2006). The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J. 25, 4084-4096. doi: 10.1038/sj.emboj.7601292
11. Finkbeiner, S., Tavazoie, S. F., Maloratsky, A., Jacobs, K. M., Harris, K. M., and Greenberg, M. E. (1997). CREB: a major mediator of neuronal neurotrophin responses.Neuron 19, 1031-1047. doi: 10.1016/s0896-6273(00)80395-5
12. Gao, Y., Deng, K., Hou, J., Bryson, J. B., Barco, A., Nikulina, E., et al. (2004). Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44, 609-621. doi: 10.1016/j.neuron.2004.10.030
13. Gaub, P., Tedeschi, A., Puttagunta, R., Nguyen, T., Schmandke, A., and Di Giovanni, S. (2010). HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ.17, 1392-1408. doi: 10.1038/cdd.2009.216
14. Ghasemlou, N., Bouhy, D., Yang, J., López-Vales, R., Haber, M., Thuraisingam, T., et al. (2010). Beneficial effects of secretory leukocyte protease inhibitor after spinal cord injury. Brain 133, 126-138. doi: 10.1093/brain/awp304
15. Hannila, S. S., Siddiq, M. M., Carmel, J. B., Hou, J., Chaudhry, N., Bradley, P. M. J., et al. (2013). Secretory leukocyte protease inhibitor reverses inhibition by CNS myelin, promotes regeneration in the optic nerve and suppresses expression of the TGFβ signaling protein Smad2. J. Neurosci. 33, 5138-5151. doi: 10.1523/jneurosci.5321-12.2013
16. Ihara, S., Nakajima, K., Fukada, T., Hibi, M., Nagata, S., Hirano, T., et al. (1997). Dual control of neurite outgrowth by STAT3 and MAP kinase in PC12 cells stimulated with interleukin-6. EMBO J. 16, 5345-5352. doi: 10.1093/emboj/16.17.5345
17. Kobayashi, N. R., Fan, D. P., Giehl, K. M., Bedard, A. M., Wiegand, S. J., and Tetzlaff, W. (1997). BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Talpha1-tubulin mRNA expression and promote axonal regeneration. J. Neurosci. 17, 9583-9595.
18. Kondoh, M., Inoue, Y., Atagi, S., Futakawa, N., Higashimoto, M., and Sato, M. (2001). Specific induction of metallothionein synthesis by mitochondrial oxidative stress. Life Sci. 69, 2137-2146. doi: 10.1016/s0024-3205(01)01294-2
19. Kwon, B. K., Liu, J., Messerer, C., Kobayashi, N. R., McGraw, J., Oschipok, L., et al. (2002). Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc. Natl. Acad. Sci. U S A 99, 3246-3251. doi: 10.1073/pnas.052308899
20. Leibinger, M., Andreadaki, A., Diekmann, H., and Fischer, D. (2013). Neuronal STAT3 activation is essential for CNTF- and inflammatory stimulation-induced CNS axon regeneration. Cell Death Dis. 4:e805. doi: 10.1038/cddis.2013.310
21. Mayr, B., and Montminy, M. (2001). Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609. doi: 10.1038/35085068
22. Miyazaki, I., Asanuma, M., Kikkawa, Y., Takeshima, M., Murakami, S., Miyoshi, K., et al. (2011). Astrocyte-derived metallothionein protects dopaminergic neurons from dopamine quinone toxicity. Glia 59, 435-451. doi: 10.1002/glia.21112
23. Müller, A., Hauk, T. G., and Fischer, D. (2007). Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 130, 3308-3320. doi: 10.1093/brain/awm257
24. Munder, M. (2009). Arginase: an emerging key player in the mammalian immune system. Br. J. Pharmacol. 158, 638-651. doi: 10.1111/j.1476-5381.2009.00291.x
25. Neumann, S., Bradke, F., Tessier-Lavigne, M., and Basbaum, A. I. (2002). Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893. doi: 10.1016/s0896-6273(02)00702-x
26. Neumann, S., and Woolf, C. J. (1999). Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23, 83-91. doi: 10.1016/s0896-6273(00)80755-2
27. Penkowa, M., Espejo, C., Martinez-Cáceres, E. M., Poulsen, C. B., Montalban, X., and Hidalgo, J. (2001). Altered inflammatory response and increased neurodegeneration in metallothionein I+II deficient mice during experimental autoimmune encephalomyelitis. J. Neuroimmunol. 119, 248-260. doi: 10.1016/s0165-5728(01)00357-5
28. Penkowa, M., Giralt, M., Carrasco, J., Hadberg, H., and Hidalgo, J. (2000). Impaired inflammatory response and increased oxidative stress and neurodegeneration after brain injury in interleukin-6-deficient mice. Glia 32, 271-285. doi: 10.1002/1098-1136(200012)32:3<271::aid-glia70>3.0.co;2-5
29. Qiu, J., Cai, D., Dai, H., McAtee, M., Hoffman, P. N., Bregman, B. S., et al. (2002). Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895-903. doi: 10.1016/s0896-6273(02)00730-4
30. Siddiq, M. M., Hannila, S. S., Carmel, J. B., Bryson, J. B., Hou, J., Nikulina, E., et al. (2015). Metallothionein-I/II promotes axonal regeneration in the central nervous system. J. Biol. Chem. pii:jbc.M114.630574. doi: 10.1074/jbc.m114.630574
31. Slotkin, T. A., Seidler, F. J., Trepanier, P. A., Whitmore, W. L., Lerea, L., Barnes, G. A., et al. (1982). Ornithine decarboxylase and polyamines in tissues of the neonatal rat: effects of alpha-difluoromethylornithine, a specific, irreversible inhibitor of ornithine decarboxylase. J. Pharmacol. Exp. Ther. 222, 741-745.
32. Tedeschi, A., Nguyen, T., Puttagunta, R., Gaub, P., and Di Giovanni, S. (2009). A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth and regeneration. Cell Death Differ. 16, 543-554. doi: 10.1038/cdd.2008.175
33. Trendelenburg, G., Prass, K., Priller, J., Kapinya, K., Polley, A., Muselmann, C., et al. (2002). Serial analysis of gene expression identifies metallothionein-II as major neuroprotective gene in mouse focal cerebral ischemia. J. Neurosci. 22, 5879-5888.
34. Uchida, Y., Takio, K., Titani, K., Ihara, Y., and Tomonaga, M. (1991). The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Neuron 7, 337-347. doi: 10.1016/0896-6273(91)90272-2
35. Vo, N., and Goodman, R. H. (2001). CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 276, 13505-13508. doi: 10.1074/jbc.r000025200
36. Wang, X., Li, X., Xu, L., Zhan, Y., Yaish-Ohad, S., Erhardt, J. A., et al. (2003). Up-regulation of secretory leukocyte protease inhibitor (SLPI) in the brain after ischemic stroke: adenoviral expression of SLPI protects brain from ischemic injury. Mol. Pharmacol. 64, 833-840. doi: 10.1124/mol.64.4.833
37. West, A. K., Hidalgo, J., Eddins, D., Levin, E. D., and Aschner, M. (2008). Metallothionein in the central nervous system: roles in protection, regeneration and cognition. Neurotoxicology 29, 489-503. doi: 10.1016/j.neuro.2007.12.006
38. Zeng, J., Vallee, B. L., and Kägi, J. H. R. (1991). Zinc transfer from transcription factors IIIA fingers to thionein clusters. Proc. Natl. Acad. Sci. U S A 88, 9984-9988. doi: 10.1073/pnas.88.22.9984
39. Zorina, Y., Iyengar, R., and Bromberg, K. D. (2010). Cannabinoid 1 receptor and interleukin-6 receptor together induce integration of protein kinase and transcription factor signaling to trigger neurite outgrowth. J. Biol. Chem. 285, 1358-1370. doi: 10.1074/jbc.m109.049841