Co-ultramicronized palmitoylethanolamide/luteolin promotes neuronal regeneration after spinal cord injury

Frontiers in Pharmacology

Volumn 7, Issue MAR, 2016, Pages

  Crupi, Rosalia ^a   Impellizzeri, Daniela ^a   Bruschetta, Giuseppe ^a   Cordaro, Marika ^a   Paterniti, Irene ^a   Siracusa, Rosalba ^a   Cuzzocrea, Salvatore ^a,b   Esposito, Emanuela ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Luteolin; Neurogenesis; Palmitoylethanolamide; Regeneration; Spinal cord injury

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; CO ULTRAPEALUT; DOUBLECORTIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LUTEOLIN; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENT; NEUROTROPHIN 3; PALMIDROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CORRELATIONAL STUDY; DENDRITIC SPINE; DRUG ACTIVITY; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SPINAL CORD INJURY;

EID: 84966330150     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2016.00047     Document Type: Article

References (63)

1. Adhikary, S., Li, H., Heller, J., Skarica, M., Zhang, M., Ganea, D., et al. (2011). Modulation of inflammatory responses by a cannabinoid-2-selective agonist after spinal cord injury. J. Neurotrauma 28, 2417-2427. doi: 10.1089/neu.2011.1853
2. Ahmad, A., Crupi, R., Impellizzeri, D., Campolo, M., Marino, A., Esposito, E., et al. (2012). Administration of palmitoylethanolamide (PEA) protects the neurovascular unit and reduces secondary injury after traumatic brain injury in mice. Brain Behav. Immun. 26, 1310-1321. doi: 10.1016/j.bbi.2012.07.021
3. Alvarez-Buylla, A., and Garcia-Verdugo, J. M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
4. Anderson, D. K., and Hall, E. D. (1993). Pathophysiology of spinal cord trauma. Ann. Emerg. Med. 22, 987-992. doi: 10.1016/S0196-0644(05)82739-8
5. Basso, D. M., Fisher, L. C., Anderson, A. J., Jakeman, L. B., Mctigue, D. M., and Popovich, P. G. (2006). Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23, 635-659. doi: 10.1089/neu.2006.23.635
6. Bauer, S., Hay, M., Amilhon, B., Jean, A., and Moyse, E. (2005). In vivo neurogenesis in the dorsal vagal complex of the adult rat brainstem. Neuroscience 130, 75-90. doi: 10.1016/j.neuroscience.2004.08.047
7. Berdyshev, E., Boichot, E., Corbel, M., Germain, N., and Lagente, V. (1998). Effects of cannabinoid receptor ligands on LPS-induced pulmonary inflammation in mice. Life Sci. 63, PL125-PL129. doi: 10.1016/S0024-3205(98)00324-5
8. Berghuis, P., Rajnicek, A. M., Morozov, Y. M., Ross, R. A., Mulder, J., Urban, G. M., et al. (2007). Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316, 1212-1216. doi: 10.1126/science.1137406
9. Biffo, S., Offenhauser, N., Carter, B. D., and Barde, Y. A. (1995). Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121, 2461-2470.
10. Blight, A. R. (1983). Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line-sampling. Neuroscience 10, 521-543. doi: 10.1016/0306-4522(83)90150-1
11. Bracken, M. B., Shepard, M. J., Holford, T. R., Leo-Summers, L., Aldrich, E. F., Fazl, M., et al. (1998). Methylprednisolone or tirilazad mesylate administration after acute spinal cord injury: 1-year follow up. Results of the third National Acute Spinal Cord Injury randomized controlled trial. J. Neurosurg. 89, 699-706. doi: 10.3171/jns.1998.89.5.0699
12. Butti, E., Bacigaluppi, M., Rossi, S., Cambiaghi, M., Bari, M., Cebrian Silla, A., et al. (2012). Subventricular zone neural progenitors protect striatal neurons from glutamatergic excitotoxicity. Brain 135, 3320-3335. doi: 10.1093/brain/aws194
13. Ceruti, S., Villa, G., Genovese, T., Mazzon, E., Longhi, R., Rosa, P., et al. (2009). The P2Y-like receptor GPR17 as a sensor of damage and a new potential target in spinal cord injury. Brain 132, 2206-2218. doi: 10.1093/brain/awp147
14. Chiu, W. T., Lin, H. C., Lam, C., Chu, S. F., Chiang, Y. H., and Tsai, S. H. (2010). Review paper: epidemiology of traumatic spinal cord injury: comparisons between developed and developing countries. Asia Pac. J. Public Health 22, 9-18. doi: 10.1177/1010539509355470
15. Choi, A. Y., Choi, J. H., Lee, J. Y., Yoon, K. S., Choe, W., Ha, J., et al. (2010). Apigenin protects HT22 murine hippocampal neuronal cells against endoplasmic reticulum stress-induced apoptosis. Neurochem. Int. 57, 143-152. doi: 10.1016/j.neuint.2010.05.006
16. Coleman, W. P., and Geisler, F. H. (2004). Injury severity as primary predictor of outcome in acute spinal cord injury: retrospective results from a large multicenter clinical trial. Spine J. 4, 373-378. doi: 10.1016/j.spinee.2003.12.006
17. Crupi, R., Paterniti, I., Ahmad, A., Campolo, M., Esposito, E., and Cuzzocrea, S. (2013). Effects of palmitoylethanolamide and luteolin in an animal model of anxiety/depression. CNS Neurol. Disord. Drug Targets 12, 989-1001. doi: 10.2174/18715273113129990084
18. Cuzzocrea, S., Genovese, T., Mazzon, E., Crisafulli, C., Min, W., Di Paola, R., et al. (2006). Poly(ADP-ribose) glycohydrolase activity mediates post-traumatic inflammatory reaction after experimental spinal cord trauma. J. Pharmacol. Exp. Ther. 319, 127-138. doi: 10.1124/jpet.106.108076
19. Cuzzocrea, S., Riley, D. P., Caputi, A. P., and Salvemini, D. (2001). Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol. Rev. 53, 135-159.
20. Darian-Smith, C. (2009). Synaptic plasticity, neurogenesis, and functional recovery after spinal cord injury. Neuroscientist 15, 149-165. doi: 10.1177/1073858408331372
21. Doetsch, F. (2003). A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 13, 543-550. doi: 10.1016/j.gde.2003.08.012
22. Esposito, E., Paterniti, I., Mazzon, E., Genovese, T., Di Paola, R., Galuppo, M., et al. (2011). Effects of palmitoylethanolamide on release of mast cell peptidases and neurotrophic factors after spinal cord injury. Brain Behav. Immun. 25, 1099-1112. doi: 10.1016/j.bbi.2011.02.006
23. Freund, P., Weiskopf, N., Ward, N. S., Hutton, C., Gall, A., Ciccarelli, O., et al. (2011). Disability, atrophy and cortical reorganization following spinal cord injury. Brain 134, 1610-1622. doi: 10.1093/brain/awr093
24. Furutani, R., and Kibayashi, K. (2012). Morphological alteration and reduction of MAP2-immunoreactivity in pyramidal neurons of cerebral cortex in a rat model of focal cortical compression. J. Neurotrauma 29, 1266-1276. doi: 10.1089/neu.2010.1630
25. Genovese, T., Esposito, E., Mazzon, E., Di Paola, R., Meli, R., Bramanti, P., et al. (2008). Effects of palmitoylethanolamide on signaling pathways implicated in the development of spinal cord injury. J. Pharmacol. Exp. Ther. 326, 12-23. doi: 10.1124/jpet.108.136903
26. Genovese, T., Mazzon, E., Crisafulli, C., Di Paola, R., Muia, C., Bramanti, P., et al. (2006a). Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther. 316, 1006-1016. doi: 10.1124/jpet.105.097188
27. Genovese, T., Mazzon, E., Di Paola, R., Crisafulli, C., Muia, C., Bramanti, P., et al. (2006b). Increased oxidative-related mechanisms in the spinal cord injury in old rats. Neurosci. Lett. 393, 141-146. doi: 10.1016/j.neulet.2005.09.060
28. Goldshmit, Y., Spanevello, M. D., Tajouri, S., Li, L., Rogers, F., Pearse, M., et al. (2011). EphA4 blockers promote axonal regeneration and functional recovery following spinal cord injury in mice. PLoS ONE 6:e24636. doi: 10.1371/journal.pone.0024636
29. Goncalves, M. B., Suetterlin, P., Yip, P., Molina-Holgado, F., Walker, D. J., Oudin, M. J., et al. (2008). A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol. Cell. Neurosci. 38, 526-536. doi: 10.1016/j.mcn.2008.05.001
30. Gould, E. (2007). How widespread is adult neurogenesis in mammals? Nat. Rev. Neurosci. 8, 481-488. doi: 10.1038/nrn2147
31. Iijima, K., Igawa, Y., Wyndaele, J. J., and De Wachter, S. (2009). Mechanosensitive primary bladder afferent activity in rats with and without spinal cord transection. J. Urol. 182, 2504-2510. doi: 10.1016/j.juro.2009.07.012
32. Kazanis, I. (2009). The subependymal zone neurogenic niche: a beating heart in the centre of the brain: how plastic is adult neurogenesis? Opportunities for therapy and questions to be addressed. Brain 132, 2909-2921. doi: 10.1093/brain/awp237
33. Kernie, S. G., and Parent, J. M. (2010). Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol. Dis. 37, 267-274. doi: 10.1016/j.nbd.2009.11.002
34. King, V. R., Huang, W. L., Dyall, S. C., Curran, O. E., Priestley, J. V., and Michael-Titus, A. T. (2006). Omega-3 fatty acids improve recovery, whereas omega-6 fatty acids worsen outcome, after spinal cord injury in the adult rat. J. Neurosci. 26, 4672-4680. doi: 10.1523/JNEUROSCI.5539-05.2006
35. Kozlova, E. N. (2003). Differentiation and migration of astrocytes in the spinal cord following dorsal root injury in the adult rat. Eur. J. Neurosci. 17, 782-790. doi: 10.1046/j.1460-9568.2003.02518.x
36. Lambert, D. M., Vandevoorde, S., Jonsson, K. O., and Fowler, C. J. (2002). The palmitoylethanolamide family: a new class of anti-inflammatory agents? Curr. Med. Chem. 9, 663-674. doi: 10.2174/0929867023370707
37. Leker, R. R., and Shohami, E. (2002). Cerebral ischemia and trauma-different etiologies yet similar mechanisms: neuroprotective opportunities. Brain Res. Brain Res. Rev. 39, 55-73. doi: 10.1016/S0165-0173(02)00157-1
38. Lin, L. Z., Lu, S., and Harnly, J. M. (2007). Detection and quantification of glycosylated flavonoid malonates in celery, Chinese celery, and celery seed by LC-DAD-ESI/MS. J. Agric. Food Chem. 55, 1321-1326. doi: 10.1021/jf0624796
39. Loverme, J., La Rana, G., Russo, R., Calignano, A., and Piomelli, D. (2005). The search for the palmitoylethanolamide receptor. Life Sci. 77, 1685-1698. doi: 10.1016/j.lfs.2005.05.012
40. Malberg, J. E., Eisch, A. J., Nestler, E. J., and Duman, R. S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110.
41. Meletis, K., Barnabe-Heider, F., Carlen, M., Evergren, E., Tomilin, N., Shupliakov, O., et al. (2008). Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 6:e182. doi: 10.1371/journal.pbio.0060182
42. Moyse, E., Bauer, S., Charrier, C., Coronas, V., Krantic, S., and Jean, A. (2006). Neurogenesis and neural stem cells in the dorsal vagal complex of adult rat brain: new vistas about autonomic regulations-a review. Auton. Neurosci. 126-127:50-58. doi: 10.1016/j.autneu.2006.03.006
43. Nakagawara, A., Azar, C. G., Scavarda, N. J., and Brodeur, G. M. (1994). Expression and function of TRK-B and BDNF in human neuroblastomas. Mol. Cell. Biol. 14, 759-767. doi: 10.1128/MCB.14.1.759
44. Nishimura, Y., and Isa, T. (2009). Compensatory changes at the cerebral cortical level after spinal cord injury. Neuroscientist 15, 436-444. doi: 10.1177/1073858408331375
45. Okabe, S., and Hirokawa, N. (1989). Rapid turnover of microtubule-associated protein MAP2 in the axon revealed by microinjection of biotinylated MAP2 into cultured neurons. Proc. Natl. Acad. Sci. U.S.A. 86, 4127-4131. doi: 10.1073/pnas.86.11.4127
46. Paterniti, I., Esposito, E., Mazzon, E., Bramanti, P., and Cuzzocrea, S. (2011). Evidence for the role of PI(3)-kinase-AKT-eNOS signalling pathway in secondary inflammatory process after spinal cord compression injury in mice. Eur. J. Neurosci. 33, 1411-1420. doi: 10.1111/j.1460-9568.2011.07646.x
47. Paterniti, I., Impellizzeri, D., Crupi, R., Morabito, R., Campolo, M., Esposito, E., et al. (2013a). Molecular evidence for the involvement of PPAR-delta and PPAR-gamma in anti-inflammatory and neuroprotective activities of palmitoylethanolamide after spinal cord trauma. J. Neuroinflammation 10:20. doi: 10.1186/1742-2094-10-20
48. Paterniti, I., Impellizzeri, D., Di Paola, R., Navarra, M., Cuzzocrea, S., and Esposito, E. (2013b). A new co-ultramicronized composite including palmitoylethanolamide and luteolin to prevent neuroinflammation in spinal cord injury. J. Neuroinflammation 10:91. doi: 10.1186/1742-2094-10-91
49. Pezet, S., and Malcangio, M. (2004). Brain-derived neurotrophic factor as a drug target for CNS disorders. Expert Opin. Ther. Targets 8, 391-399. doi: 10.1517/14728222.8.5.391
50. Rioux, L., Nissanov, J., Lauber, K., Bilker, W. B., and Arnold, S. E. (2003). Distribution of microtubule-associated protein MAP2-immunoreactive interstitial neurons in the parahippocampal white matter in subjects with schizophrenia. Am. J. Psychiatry 160, 149-155. doi: 10.1176/appi.ajp.160.1.149
51. Seaberg, R. M., and Van Der Kooy, D. (2002). Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784-1793.
52. Shea, T. B. (1994). Technical report. An inexpensive densitometric analysis system using a Macintosh computer and a desktop scanner. Biotechniques 16, 1126-1128.
53. Snapyan, M., Lemasson, M., Brill, M. S., Blais, M., Massouh, M., Ninkovic, J., et al. (2009). Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 29, 4172-4188. doi: 10.1523/JNEUROSCI.4956-08.2009
54. Song, X. Y., Li, F., Zhang, F. H., Zhong, J. H., and Zhou, X. F. (2008). Peripherally-derived BDNF promotes regeneration of ascending sensory neurons after spinal cord injury. PLoS ONE 3:e1707. doi: 10.1371/journal.pone.0001707
55. Thored, P., Arvidsson, A., Cacci, E., Ahlenius, H., Kallur, T., Darsalia, V., et al. (2006). Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24, 739-747. doi: 10.1634/stemcells.2005-0281
56. Thored, P., Wood, J., Arvidsson, A., Cammenga, J., Kokaia, Z., and Lindvall, O. (2007). Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38, 3032-3039. doi: 10.1161/STROKEAHA.107.488445
57. Uchida, K., Nakajima, H., Hirai, T., Yayama, T., Chen, K., Guerrero, A. R., et al. (2012). The retrograde delivery of adenovirus vector carrying the gene for brain-derived neurotrophic factor protects neurons and oligodendrocytes from apoptosis in the chronically compressed spinal cord of twy/twy mice. Spine 37, 2125-2135. doi: 10.1097/BRS.0b013e3182600ef7
58. Velayudhan, L., Van Diepen, E., Marudkar, M., Hands, O., Suribhatla, S., Prettyman, R., et al. (2014). Therapeutic potential of cannabinoids in neurodegenerative disorders: a selective review. Curr. Pharm. Des. 20, 2218-2230. doi: 10.2174/13816128113199990434
59. Vessal, M., and Darian-Smith, C. (2010). Adult neurogenesis occurs in primate sensorimotor cortex following cervical dorsal rhizotomy. J. Neurosci. 30, 8613-8623. doi: 10.1523/JNEUROSCI.5272-09.2010
60. Wallace, M., Luine, V., Arellanos, A., and Frankfurt, M. (2006). Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res. 1126, 176-182. doi: 10.1016/j.brainres.2006.07.064
61. Xu, B., Li, X. X., He, G. R., Hu, J. J., Mu, X., Tian, S., et al. (2010). Luteolin promotes long-term potentiation and improves cognitive functions in chronic cerebral hypoperfused rats. Eur. J. Pharmacol. 627, 99-105. doi: 10.1016/j.ejphar.2009.10.038
62. Yuan, Q., Su, H., Chiu, K., Wu, W., and Lin, Z. X. (2013). Contrasting neuropathology and functional recovery after spinal cord injury in developing and adult rats. Neurosci. Bull. 29, 509-516. doi: 10.1007/s12264-013-1356-5
63. Zai, L. J., and Wrathall, J. R. (2005). Cell proliferation and replacement following contusive spinal cord injury. Glia 50, 247-257. doi: 10.1002/glia.20176