N-arachidonoyl-L-serine (AraS) possesses proneurogenic properties in vitro and in vivo after traumatic brain injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 8, 2013, Pages 1242-1250

  Cohen Yeshurun, Ayelet ^a,b   Willner, Dafna ^b   Trembovler, Victoria ^a   Alexandrovich, Alexander ^a   Mechoulam, Raphael ^a   Shohami, Esther ^a   Leker, Ronen R ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

brain trauma; cannabinoids; immunohistochemistry; neural stem cells; neuroregeneration

Indexed keywords

ENDOCANNABINOID; N ARACHIDONOYL L SERINE; NESTIN; NEUROPROTECTIVE AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1 ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TRAUMATIC BRAIN INJURY;

ANIMALS; ARACHIDONIC ACIDS; ASTROCYTES; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN; BRAIN INJURIES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLORING AGENTS; MALE; MICE; NEURAL STEM CELLS; NEUROGENESIS; PROPIDIUM; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; SERINE; TREATMENT OUTCOME; TRPV CATION CHANNELS;

EID: 84881142050     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.75     Document Type: Article

References (42)

1. Merkle FT, Alvarez-Buylla A. Neural stem cells in mammalian development. Curr Opin Cell Biol 2006; 18: 704-709.
2. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C et al. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2003; 2: 175-183.
3. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002; 99: 11946-11950.
4. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997; 17: 5820-5829.
5. Lachyankar MB, Condon PJ, Quesenberry PJ, Litofsky NS, Recht LD, Ross AH. Embryonic precursor cells that express Trk receptors: induction of different cell fates by NGF, BDNF, NT-3, and CNTF. Exp Neurol 1997; 144: 350-360.
6. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C et al. Pregnancystimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003; 299: 117-120.
7. Karishma KK, Herbert J. Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. Eur J Neurosci 2002; 16: 445-453.
8. Palazuelos J, Aguado T, Egia A, Mechoulam R, Guzma?n M, Galve-Roperh I. Nonpsychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 2006; 20: 2405-2407.
9. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B et al. The endocannabinoid system drives neural progenitor proliferation. FASEB J 2005; 19: 1704-1706.
10. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO et al. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 2004; 66: 204-208.
11. Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B et al. The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J Neurosci 2006; 26: 1551-1561.
12. Milman G, Maor Y, Abu-Lafi S, Horowitz M, Gallily R, Batkai S et al. N-arachidonoyl L-serine, an endocannabinoid-like brain constituent with vasodilatory properties. Proc Natl Acad Sci USA 2006; 103: 2428-2433.
13. Cohen-Yeshurun A, Trembovler V, Alexandrovich A, Ryberg E, Greasley PJ, Mechoulam R et al. N-arachidonoyl-L-serine is neuroprotective after traumatic brain injury by reducing apoptosis. J Cereb Blood Flow Metab 2011; 31: 1768-1777.
14. McHugh D, Hu SS, Rimmerman N, Juknat A, Vogel Z, Walker JM et al. N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci 2010; 11: 44.
15. Shohami E, Cohen-Yeshurun A, Magid L, Algali M, Mechoulam R. Endocannabinoids and traumatic brain injury. Br J Pharmacol 2011; 163: 1402-1410.
16. Sun D, Bullock MR, Altememi N, Zhou Z, Hagood S, Rolfe A et al. The effect of epidermal growth factor in the injured brain after trauma in rats. J Neurotrauma 2010; 27: 923-938.
17. Kleindienst A, McGinn MJ, Harvey HB, Colello RJ, Hamm RJ, Bullock MR. Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J Neurotrauma 2005; 22: 645-655.
18. Chen XH, Iwata A, Nonaka M, Browne KD, Smith DH. Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J Neurotrauma 2003; 20: 623-631.
19. Lu D, Mahmood A, Zhang R, Copp M. Upregulation of neurogenesis and reduction in functional deficits following administration of DEtA/NONOate, a nitric oxide donor, after traumatic brain injury in rats. J Neurosurg 2003; 99: 351-361.
20. Chirumamilla S, Sun D, Bullock MR, Colello RJ. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J Neurotrauma 2002; 19: 693-703.
21. Urrea C, Castellanos DA, Sagen J, Tsoulfas P, Bramlett HM, Dietrich WD. Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor Neurol Neurosci 2007; 25: 65-76.
22. Ramaswamy S, Goings GE, Soderstrom KE, Szele FG, Kozlowski DA. Cellular proliferation and migration following a controlled cortical impact in the mouse. Brain Res 2005; 1053: 38-53.
23. Goings G, Sahni V, Szele F. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res 2004; 996: 213-226.
24. Kernie SG, Erwin TM, Parada LF. Brain remodeling due to neuronal and astrocytic proliferation after controlled cortical injury in mice. J Neurosci Res 2001; 66: 317-326.
25. Thau-Zuchman O, Shohami E, Alexandrovich AG, Leker RR. Vascular endothelial growth factor increases neurogenesis after traumatic brain injury. J Cereb Blood Flow Metab 2010; 30: 1008-1016.
26. Mechoulam R, Spatz M, Shohami E. Endocannabinoids and neuroprotection. Sci STKE. 2002; 23: RE5.
27. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-1710.
28. Yatsiv I, Grigoriadis N, Simeonidou C, Stahel PF, Schmidt OI, Alexandrovitch AG et al. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J 2005; 19: 1701-1703.
29. Shapira Y, Shohami E, Sidi A, Soffer D, Freeman S, Cotev S. Experimental closed head injury in rats: mechanical, pathophysiologic, and neurologic properties. Crit Care Med. 1988; 16: 258-265.
30. Shapira Y, Setton D, Artru AA, Shohami E. Blood-brain barrier permeability, cerebral edema, and neurologic function after closed head injury in rats. Anesth Analg 1993; 77: 141-148.
31. Beni-Adani L, Gozes I, Cohen Y, Assaf Y, Steingart RA, Brenneman DE et al. A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice. J Pharmacol Exp Ther 2001; 296: 57-63.
32. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 1990; 10: 290-293.
33. Chen Y, Constantini S, Trembovler V, Weinstock M, Shohami E. An experimental model of closed head injury in mice: pathophysiology, histopathology, and cognitive deficits. J Neurotrauma 1996; 13: 557-568.
34. Palazuelos J, Ortega Z, Daz-Alonso J, Guzman M, Galve-Roperh I. CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J Biol Chem 2012; 287: 1198-1209.
35. Madhavan L, Ourednik V, Ourednik J. Neural stem/progenitor cells initiate the formation of cellular networks that provide neuroprotection by growth factormodulated antioxidant expression. Stem Cells 2008; 26: 254-265.
36. Su H, Zhang W, Guo J, Guo A, Yuan Q, Wu W. Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J Neurotrauma 2009; 26: 67-80.
37. Ben-Hur T. Immunomodulation by neural stem cells. J Neurol Sci 2008; 265: 102-104.
38. Leker RR, Lasri V, Chernoguz D. Growth factors improve neurogenesis and outcome after focal cerebral ischemia. J Neural Transm 2009; 116: 1397-1402.
39. Werner C, Engelhard K. Pathophysiology of traumatic brain injury. Br J Anaesth 2007; 99: 4-9.
40. Oertel M, Boscardin WJ, Obrist WD, Glenn TC, McArthur DL, Gravori T et al. Posttraumatic vasospasm: the epidemiology, severity, and time course of an underestimated phenomenon: a prospective study performed in 229 patients. J Neurosurg 2005; 103: 812-824.
41. Golech SA, McCarron RM, Chen Y, Bembry J, Lenz F, Mechoulam R et al. Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. Brain Res Mol Brain Res 2004; 132: 87-92.
42. Chen Y, McCarron RM, Ohara Y, Bembry J, Azzam N, Lenz FA et al. Human brain capillary endothelium: 2-arachidonoglycerol (endocannabinoid) interacts with endothelin-1. Circ Res 2000; 87: 323-327.