The cannabinoid CB2 receptor agonist AM1241 enhances neurogenesis in GFAP/Gp120 transgenic mice displaying deficits in neurogenesis

British Journal of Pharmacology

Volumn 171, Issue 2, 2014, Pages 468-479

  Avraham, Hava Karsenty ^a   Jiang, Shuxian ^a   Fu, Yigong ^a   Rockenstein, Edward ^b   Makriyannis, Alexandros ^c   Zvonok, Alexander ^c   Masliah, Eliezer ^b   Avraham, Shalom ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

Author keywords

CB2 agonist; GFAP Gp120 transgenic mice; HIV 1 Gp120 protein; neural progenitor cells; neurogenesis

Indexed keywords

3 (2 IODO 5 NITROBENZOYL) 1 (1 METHYL 2 PIPERIDINYLMETHYL)INDOLE; BROXURIDINE; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEIN GP 120;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

CB2 AGONIST; GFAP/GP120 TRANSGENIC MICE; HIV-1 GP120 PROTEIN; NEURAL PROGENITOR CELLS; NEUROGENESIS;

ANIMALS; APOPTOSIS; CANNABINOIDS; CELL DIFFERENTIATION; CELL SURVIVAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HIV ENVELOPE PROTEIN GP120; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; PRIMARY CELL CULTURE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, CANNABINOID, CB2;

EID: 84891277457     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12478     Document Type: Article

References (52)

1. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, et al. (2005). The endocannabinoid system drives neural progenitor proliferation. FASEB J 19: 1704-1706. (Pubitemid 41429536)
2. Albright AV, Martin J, O'Connor M, Gonzalez-Scarano F, (2001). Interactions between HIV-1 gp120, chemokines, and cultured adult microglial cells. J Neurovirol 7: 196-207. (Pubitemid 32685254)
3. Alexander SPH, et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: Overview. Br J Pharmacol 170: 1449-1867.
4. Bari M, Rapino C, Mozetic P, Maccarrone M, (2010). The endocannabinoid system in gp120-mediated insults and HIV-associated dementia. Exp Neurol 224: 74-78.
5. Bunnik EM, Euler Z, Welkers MR, Boeser-Nunnink BD, Grijsen ML, Prins JM, et al. (2010). Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat Med 16: 995-997.
6. Cherner M, Ellis RJ, Lazzaretto D, Young C, Mindt MR, Atkinson JH, et al. (2004). Effects of HIV-1 infection and aging on neurobehavioral functioning: preliminary findings. AIDS 18 (Suppl 1): S27-S34. (Pubitemid 38365903)
7. Corasaniti MT, Maccarrone M, Nistico R, Malorni W, Rotiroti D, Bagetta G, (2001). Exploitation of the HIV-1 coated glycoprotein, gp120, in neurodegenerative Studies in vivo. J Neurochem 79: 1-8. (Pubitemid 32946636)
8. Eljaschewitsch E, Witting A, Mawrin C, Lee T, Schmidt PM, Wolf S, et al. (2006). The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49: 67-79. (Pubitemid 43017186)
9. Fauci AS, (1988). The human immunodeficiency virus: infectivity and mechanisms of pathogenesis. Science 239: 617-622. (Pubitemid 18066223)
10. Galve-Roperh I, Aguado T, Rueda D, Velasco G, Guzmán M, (2006). Endocannabinoids: a new family of lipid mediators involved in the regulation of neural cell development. Curr Pharm 12: 2319-2325. (Pubitemid 43891402)
11. Galve-Roperh I, Aguado T, Palazuelos J, Guzmán M, (2008). Mechanisms of control of neuron survival by the endocannabinoid system. Curr Pharm 14: 2279-2288.
12. Galve-Roperh I, Palazuelos J, Aguado T, Guzmán M, (2009). The endocannabinoid system and the regulation of neural development: potential implications in psychiatric disorders. Eur Arch Psychiatry Clin Neurosci 259: 371-382.
13. Goncalves MB, Suetterlin P, Yip P, Molina-Holgado F, Walker DJ, Oudin MJ, 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.
14. Heifets BD, Castillo PE, (2009). Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71: 283-306.
15. 2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. PNAS 100: 10529-10533. (Pubitemid 37071912)
16. 2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. PNAS 102: 3093-3098. (Pubitemid 40299921)
17. Iskander S, Walsh KA, Hammond RR, (2004). Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J Neuroinflammation 1: 1-9.
18. Katona I, Freund TF, (2008). Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 14: 923-930.
19. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: The ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
20. 2 cannabinoid receptors inhibits HIV-1 envelope glycoprotein Gp120-induced synapse loss. Mol Pharmacol 80: 357-366.
21. Krucker T, Toggas SM, Mucke L, Siggins GR, (1998). Transgenic mice with cerebral expression of human immunodeficiency virus type-1 coat protein gp120 show divergent changes in short- and long-term potentiation in CA1 hippocampus. Neuroscience 83: 691-700. (Pubitemid 28068890)
22. Louboutin JP, Strayer DS, (2012). Blood-brain barrier abnormalities caused by HIV-1/Gp120: mechanistic and therapeutic implications. Sci World J 2012: 482575.
23. McArthur JC, Steiner J, Sacktor N, Nath A, (2010). Human immunodeficiency virus-associated neurocognitive disorders: mind the gap. Ann Neurol 67: 699-714.
24. Maccarrone M, Piccirilli S, Battista N, Del Duca C, Nappi G, Corasaniti MT, et al. (2004). Enhanced anandamide degradation is associated with neuronal apoptosis induced by the HIV-1 coat glycoprotein gp120 in the rat neocortex. J Neurochem 89: 1293-1300. (Pubitemid 38715847)
25. Marchalant Y, Cerbai F, Brothers HM, Wenk GL, (2008). Cannabinoid receptor stimulation is anti-inflammatory and improves memory in old rats. Neurobiol Aging 29: 1894-1901.
26. Marchalant Y, Brother HM, Norman GJ, Karelina K, DeVries AC, Wenk GL, (2009a). Cannabinoids attenuate the effects of aging upon neuroinflammation and neurogenesis. Neurobiol Dis 34: 300-307.
27. Marchalant Y, Brothers HM, Wenk GL, (2009b). Cannabinoid agonist WIN-55, 212-2 partially restores neurogenesis in the aged rat brain. Mol Psychiatry 14: 1068-1069.
28. Marchalant Y, Brothers HM, Wenk GL, (2009c). New neuron production can be increased in the hippocampus of aged rats following cannabinoid treatment. Mol Psychiatry 14: 1067.
29. Marchalant Y, Baranger K, Wenk GL, Khrestchatisky M, Rivera S, (2012). Can the benefits of cannabinoid receptor stimulation on neuroinflammation, neurogenesis and memory during normal aging be useful in AD prevention. J Neuroinflammation 9: 10.
30. 1 cannabinoid receptors and on demand defense against excitotoxicity. Science 302: 84-88. (Pubitemid 37210691)
31. Mattson MP, Haughey NJ, Nath A, (2005). Cell death in HIV dementia. Cell Death Differ 12: 893-904. (Pubitemid 41030604)
32. Maurin JC, Couble ML, Staquet MJ, Carrouel F, About I, Avila J, et al. (2009). Microtubule-associated protein 1b, a neuronal marker involved in odontoblast differentiation. J Endod 35: 992-996.
33. McGrath J, Drummond G, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. Mucke L, Abraham CR, Ruppe MD, Rockenstein EM, Toggas SM, Mallory M, et al. (1995). Protection against HIV-1/Gp120-induced brain damage by neuronal expression of human amyloid precursor protein. J Exp Med 181: 1551-1556.
35. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin K, et al. (1999). Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 19: 2987-2995. (Pubitemid 29173995)
36. Okamoto S, Kang YJ, Brechtel CW, Siviglia E, Russo R, Clemente A, et al. (2007). HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint Kinase-Mediated Cell-Cycle withdrawal and G1 arrest. Cell Stem Cell 1: 230-236. (Pubitemid 47215594)
37. 2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 20: 2405-2407.
38. Palazuelos J, Ortega Z, Díaz-Alonso J, Guzmán N, Galve-Roperh I, (2012). CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signalling. J Biol Chem 287: 1198-1209.
39. Panikashvili D, Shein NA, Mechoulam R, Trembovler V, Kohen R, Alexandrovich A, et al. (2006). The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol Dis 22: 257-264.
40. Price RW, Spudich S, (2008). Antiretroviral therapy and central nervous system HIV type 1 infection. J Infect Dis 197 (Suppl 3): S294-S306. (Pubitemid 351717319)
41. Ramírez BG, Blázquez C, Gõmez del Pulgar T, Guzmán M, de Ceballos ML, (2005). Prevention of Alzheimer's disease by cannabinoids: neuroprotection mediated by blockade of microglial activation. J Neurosci 25: 1904-1913. (Pubitemid 40289395)
42. Rockenstein E, Mante M, Adame A, Crews L, Moessler H, Masliah E, (2007). Effects of Cerebrolysin on neurogenesis in an APP transgenic model of Alzheimer's disease. Acta Neuropathol 113: 265-275. (Pubitemid 46443562)
43. Sarne Y, Mechoulam R, (2005). Cannabinoids: between neuroprotection and neurotoxicity. Curr Drug Targets CNS Neurol Disord 4: 677-684. (Pubitemid 41782629)
44. Scott JC, Woods SP, Carey CL, Weber E, Bondi MW, Grant I, (2011). HIV Neurobehavioral Research Center (HNRC) Group: neurocognitive consequences of HIV infection in older adults: an evaluation of the 'cortical' hypothesis. AIDS and Behav 15: 1187-1196.
45. Shah A, Kumar A, (2010). HIV-1/Gp120-mediated increases in IL-8 production in astrocytes are mediated through the NF-κB pathway and can be silenced by gp120-specific siRNA. J Neuroinflammation 29: 96.
46. van der Stelt M, Veldhuis WB, Bär PR, Veldink GA, Vliegenthart JF, Nicolay K, (2001). Neuroprotection by Δ9-tetrahydrocannabinol, the main active compound of marijuana, against ouabain-induced in vivo excitotoxicity. J Neurosci 21: 6475-6479. (Pubitemid 32781091)
47. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L, (1994). Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367: 188-193. (Pubitemid 24031702)
48. Toggas SM, Masliah E, Mucke L, (1996). Prevention of HIV-1/Gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res 706: 303-307. (Pubitemid 26046728)
49. Tran PB, Ren D, Miller RJ, (2005). The HIV-1 coat protein gp120 regulates CXCR4- mediated signaling in neural progenitor cells. J Neuroimmunol 160: 68-76. (Pubitemid 40248595)
50. Walsh KA, Megyesi JF, Wilson JX, Crukley J, Laubach VE, Hammond RR, (2004). Antioxidant protection from HIV-1 gp120-induced neuroglial toxicity. J Neuroinflammation 1: 8.
51. Wiley CA, Achim CL, Christopherson C, Kidane Y, Kwok S, Masliah E, et al. (1999). HIV mediates a productive infection of the brain. AIDS 13: 2055-2059. (Pubitemid 29509581)
52. Wyss-Coray T, Masliah E, Toggas SM, Rockenstein EM, Brooker MJ, Lee HS, et al. (1996). Dysregulation of signal transduction pathways as a potential mechanism of nervous system alterations in HIV-1/Gp120 transgenic mice and humans with HIV-1 encephalitis. J Clin Invest 97: 789-798. (Pubitemid 26057098)