Distinctive effects of eicosapentaenoic and docosahexaenoic acids in regulating neural stem cell fate are mediated via endocannabinoid signalling pathways

Neuropharmacology

Volumn 107, Issue , 2016, Pages 387-395

  Dyall, S C ^a,b   Mandhair, H K ^a   Fincham, R E A ^a   Kerr, D M ^c   Roche, M ^c   Molina Holgado, F ^a  

^a UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^b BOURNEMOUTH UNIVERSITY   (United Kingdom)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

CB1 cannabinoid receptor; CB2 cannabinoid receptor; Docosahexaenoic acid; Eicosapentaenoic acid; Endocannabinoids; Neurogenesis

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 ARACHIDONOYLGLYCEROL; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; DOCOSAHEXAENOIC ACID; ENDOCANNABINOID; ICOSAPENTAENOIC ACID; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL CELL; ARTICLE; CELL FATE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; LIQUID CHROMATOGRAPHY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TISSUE REPAIR; WILD TYPE; ANIMAL; BRAIN CORTEX; C57BL MOUSE; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; CELL SURVIVAL; CEREBRAL CORTEX; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; EICOSAPENTAENOIC ACID; ENDOCANNABINOIDS; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; SIGNAL TRANSDUCTION;

EID: 84962783624     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.03.055     Document Type: Article

References (68)

1. T. Aguado, K. Monory, J. Palazuelos, N. Stella, B. Cravatt, B. Lutz, G. Marsicano, Z. Kokaia, M. Guzman, and I. Galve-Roperh The endocannabinoid system drives neural progenitor proliferation FASEB J. 19 2005 1704 1706
2. A. Artmann, G. Petersen, L.I. Hellgren, J. Boberg, C. Skonberg, C. Nellemann, S.H. Hansen, and H.S. Hansen Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine Biochim. Biophys. Acta 1781 2008 200 212
3. S. Bae, Y. Bessho, M. Hojo, and R. Kageyama The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation Development 127 2000 2933 2943
4. B. Batetta, M. Griinari, G. Carta, E. Murru, A. Ligresti, L. Cordeddu, E. Giordano, F. Sanna, T. Bisogno, S. Uda, M. Collu, I. Bruheim, V. Di Marzo, and S. Banni Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats J. Nutr. 139 2009 1495 1501
5. A. Berger, G. Crozier, T. Bisogno, P. Cavaliere, S.M. Innis, and V. Di Marzo Anandamide and diet: inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets Proc. Natl. Acad. Sci. U. S. A. 98 2001 6402 6406
6. L.S. Campos, D.P. Leone, J.B. Relvas, C. Brakebusch, R. Fassler, U. Suter, and C. ffrench-Constant Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance Development 131 2004 3433 3444
7. C.T. Chen, A.F. Domenichiello, M.O. Trepanier, Z. Liu, M. Masoodi, and R.P. Bazinet The low levels of eicosapentaenoic acid in rat brain phospholipids are maintained via multiple redundant mechanisms J. Lipid Res. 54 2013 2410 2422
8. C.T. Chen, Z. Liu, M. Ouellet, F. Calon, and R.P. Bazinet Rapid beta-oxidation of eicosapentaenoic acid in mouse brain: an in situ study Prostagl. Leukot. Essent. Fat. Acids 80 2009 157 163
9. M.A. Contreras, R.S. Greiner, M.C. Chang, C.S. Myers, N. Salem Jr., and S.I. Rapoport Nutritional deprivation of alpha-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain J. Neurochem. 75 2000 2392 2400
10. V. Darsalia, U. Heldmann, O. Lindvall, and Z. Kokaia Stroke-induced neurogenesis in aged brain Stroke 36 2005 1790 1795
11. A. de la Mano, A. Gato, M.I. Alonso, E. Carnicero, C. Martin, and J.A. Moro Role of interleukin-1beta in the control of neuroepithelial proliferation and differentiation of the spinal cord during development Cytokine 37 2007 128 137
12. P. Derkinderen, C. Ledent, M. Parmentier, and J.A. Girault Cannabinoids activate p38 mitogen-activated protein kinases through CB1 receptors in hippocampus J. Neurochem. 77 2001 957 960
13. S.C. Dyall Methodological issues and inconsistencies in the field of omega-3 fatty acids research Prostagl. Leukot. Essent. Fat. Acids 85 2011 281 285
14. S.C. Dyall The role of omega-3 fatty acids in adult hippocampal neurogenesis Ol. Corps Gras Lipides 18 2011 242 245
15. S.C. Dyall Long-chain omega-3 fatty acids and the brain: a review of the independent and shared effects of EPA, DPA and DHA Front. Aging Neurosci. 7 2015
16. S.C. Dyall, and A.T. Michael-Titus Neurological benefits of omega-3 fatty acids Neuromol. Med. 10 2008 219 235
17. S.C. Dyall, G.J. Michael, and A.T. Michael-Titus Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats J. Neurosci. Res. 88 2010 2091 2102
18. S.C. Dyall, G.J. Michael, R. Whelpton, A.G. Scott, and A.T. Michael-Titus Dietary enrichment with omega-3 polyunsaturated fatty acids reverses age-related decreases in the GluR2 and NR2B glutamate receptor subunits in rat forebrain Neurobiol. Aging 28 2007 424 439
19. D. Ehninger, and G. Kempermann Neurogenesis in the adult hippocampus Cell Tissue Res. 331 2008 243 250
20. J. Folch, M. Lees, and G.H.S. Stanley A simple method for the isolation and purification of total lipid from animal tissues J. Biol. Chem. 226 1957 497 509
21. D. Garcia-Ovejero, A. Arevalo-Martin, B. Navarro-Galve, E. Pinteaux, E. Molina-Holgado, and F. Molina-Holgado Neuroimmmune interactions of cannabinoids in neurogenesis: focus on interleukin-1beta (IL-1beta) signalling Biochem. Soc. Trans. 41 2013 1577 1582
22. M.B. Goncalves, P. Suetterlin, P. Yip, F. Molina-Holgado, D.J. Walker, M.J. Oudin, M.P. Zentar, S. Pollard, R.J. Yanez-Munoz, G. Williams, F.S. Walsh, M.N. Pangalos, and P. Doherty A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner Mol. Cell Neurosci. 38 2008 526 536
23. I. Goshen, T. Kreisel, O. Ben-Menachem-Zidon, T. Licht, J. Weidenfeld, T. Ben-Hur, and R. Yirmiya Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression Mol. Psychiatry 13 2008 717 728
24. J. Guadagno, P. Swan, R. Shaikh, and S.P. Cregan Microglia-derived IL-1beta triggers p53-mediated cell cycle arrest and apoptosis in neural precursor cells Cell Death Dis. 6 2015 e1779
25. R.J. Henry, D.M. Kerr, D.P. Finn, and M. Roche FAAH-mediated modulation of TLR3-induced neuroinflammation in the rat hippocampus J. Neuroimmunol. 276 2014 126 134
26. M. Herkenham Characterization and localization of cannabinoid receptors in brain: an in vitro technique using slide-mounted tissue sections NIDA Res. Monogr. 112 1991 129 145
27. M. Herkenham, A.B. Lynn, M.R. Johnson, L.S. Melvin, B.R. de Costa, and K.C. Rice Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study J. Neurosci. 11 1991 563 583
28. M. Ishibashi, K. Moriyoshi, Y. Sasai, K. Shiota, S. Nakanishi, and R. Kageyama Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system EMBO J. 13 1994 1799 1805
29. W. Jiang, Y. Zhang, L. Xiao, J. Van Cleemput, S.P. Ji, G. Bai, and X. Zhang Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects J. Clin. Investig. 115 2005 3104 3116
30. K. Jin, L. Xie, S.H. Kim, S. Parmentier-Batteur, Y. Sun, X.O. Mao, J. Childs, and D.A. Greenberg Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice Mol. Pharmacol. 66 2004 204 208
31. M. Katakura, M. Hashimoto, T. Okui, H.M. Shahdat, K. Matsuzaki, and O. Shido Omega-3 polyunsaturated Fatty acids enhance neuronal differentiation in cultured rat neural stem cells Stem Cells Int. 2013 2013 490476
32. M. Katakura, M. Hashimoto, H.M. Shahdat, S. Gamoh, T. Okui, K. Matsuzaki, and O. Shido Docosahexaenoic acid promotes neuronal differentiation by regulating basic helix-loop-helix transcription factors and cell cycle in neural stem cells Neuroscience 160 2009 651 660
33. E. Kawakita, M. Hashimoto, and O. Shido Docosahexaenoic acid promotes neurogenesis in vitro and in vivo Neuroscience 139 2006 991 997
34. C.M. Kelly, P. Tyers, M.T. Borg, C.N. Svendsen, S.B. Dunnett, and A.E. Rosser EGF and FGF-2 responsiveness of rat and mouse neural precursors derived from the embryonic CNS Brain Res. Bull. 68 2005 83 94
35. D.M. Kerr, N.N. Burke, G.K. Ford, T.J. Connor, B. Harhen, L.J. Egan, D.P. Finn, and M. Roche Pharmacological inhibition of endocannabinoid degradation modulates the expression of inflammatory mediators in the hypothalamus following an immunological stressor Neuroscience 204 2012 53 63
36. D.M. Kerr, L. Downey, M. Conboy, D.P. Finn, and M. Roche Alterations in the endocannabinoid system in the rat valproic acid model of autism Behav. Brain Res. 249 2013 124 132
37. D.M. Kerr, B. Harhen, B.N. Okine, L.J. Egan, D.P. Finn, and M. Roche The monoacylglycerol lipase inhibitor JZL184 attenuates LPS-induced increases in cytokine expression in the rat frontal cortex and plasma: differential mechanisms of action Br. J. Pharmacol. 169 2013 808 819
38. J.W. Koo, and R.S. Duman IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress Proc. Natl. Acad. Sci. U. S. A. 105 2008 751 756
39. N. Koyano-Nakagawa, J. Kim, D. Anderson, and C. Kintner Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation Development 127 2000 4203 4216
40. H.G. Kuhn, H. Dickinson-Anson, and F.H. Gage Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation J. Neurosci. 16 1996 2027 2033
41. M. Lafourcade, T. Larrieu, S. Mato, A. Duffaud, M. Sepers, I. Matias, V. De Smedt-Peyrusse, V.F. Labrousse, L. Bretillon, C. Matute, R. Rodriguez-Puertas, S. Laye, and O.J. Manzoni Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions Nat. Neurosci. 14 2011 345 350
42. B. Langelier, A. Linard, C. Bordat, M. Lavialle, and C. Heberden Long chain-polyunsaturated fatty acids modulate membrane phospholipid composition and protein localization in lipid rafts of neural stem cell cultures J. Cell Biochem. 110 2010 1356 1364
43. D. Ma, M. Zhang, C.P. Larsen, F. Xu, W. Hua, T. Yamashima, Y. Mao, and L. Zhou DHA promotes the neuronal differentiation of rat neural stem cells transfected with GPR40 gene Brain Res. 1330 2010 1 8
44. H.K. Mandhair, J. Opacka-Juffry, S.C. Dyall, and F. Molina-Holgado An investigation into the effects of pharmacological modulation of omega-3 polyunsaturated fatty acids on endocannabinoid CB1 receptor signalling on regulating microglial cell fate Proc. Br. Pharmacol. Soc. 2012 at http://www.pA2online.org/abstracts/Vol10Issue4abst190P.pdf
45. I. Matias, G. Carta, E. Murru, S. Petrosino, S. Banni, and V. Di Marzo Effect of polyunsaturated fatty acids on endocannabinoid and N-acyl-ethanolamine levels in mouse adipocytes Biochim. Biophys. Acta 1781 2008 52 60
46. P.R. Mittelstadt, J.M. Salvador, A.J. Fornace Jr., and J.D. Ashwell Activating p38 MAPK: new tricks for an old kinase Cell Cycle 4 2005 1189 1192
47. G. Moldrich, and T. Wenger Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study Peptides 21 2000 1735 1742
48. E. Molina-Holgado, and F. Molina-Holgado Mending the broken brain: neuroimmune interactions in neurogenesis J. Neurochem. 114 2010 1277 1290
49. F. Molina-Holgado, A. Rubio-Araiz, D. Garcia-Ovejero, R.J. Williams, J.D. Moore, A. Arevalo-Martin, O. Gomez-Torres, and E. Molina-Holgado CB2 cannabinoid receptors promote mouse neural stem cell proliferation Eur. J. Neurosci. 25 2007 629 634
50. W.R. Morrison, and L.M. Smith Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron trifluoride-methanol J. Lipid Res. 5 1964 600 608
51. T. Ohtsuka, M. Sakamoto, F. Guillemot, and R. Kageyama Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain J. Biol. Chem. 276 2001 30467 30474
52. E.S. Onaivi, H. Ishiguro, S. Gu, and Q.R. Liu CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity J. Psychopharmacol. 26 2012 92 103
53. J.M. Parent, T.W. Yu, R.T. Leibowitz, D.H. Geschwind, R.S. Sloviter, and D.H. Lowenstein Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus J. Neurosci. 17 1997 3727 3738
54. A. Piskunov, and C. Rochette-Egly A retinoic acid receptor RARalpha pool present in membrane lipid rafts forms complexes with G protein alphaQ to activate p38MAPK Oncogene 31 2012 3333 3345
55. M.A. Rashid, M. Katakura, G. Kharebava, K. Kevala, and H.Y. Kim N-Docosahexaenoylethanolamine is a potent neurogenic factor for neural stem cell differentiation J. Neurochem. 125 2013 869 884
56. B.A. Reynolds, and S. Weiss Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1992 1707 1710
57. A. Rubio-Araiz, A. Arevalo-Martin, O. Gomez-Torres, B. Navarro-Galve, D. Garcia-Ovejero, P. Suetterlin, E. Sanchez-Heras, E. Molina-Holgado, and F. Molina-Holgado The endocannabinoid system modulates a transient TNF pathway that induces neural stem cell proliferation Mol. Cell Neurosci. 38 2008 374 380
58. D. Rueda, B. Navarro, A. Martinez-Serrano, M. Guzman, and I. Galve-Roperh The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway J. Biol. Chem. 277 2002 46645 46650
59. S.M. Ryan, G.W. O'Keeffe, C. O'Connor, K. Keeshan, and Y.M. Nolan Negative regulation of TLX by IL-1beta correlates with an inhibition of adult hippocampal neural precursor cell proliferation Brain Behav. Immun. 33 2013 7 13
60. N. Sakayori, M. Maekawa, K. Numayama-Tsuruta, T. Katura, T. Moriya, and N. Osumi Distinctive effects of arachidonic acid and docosahexaenoic acid on neural stem/progenitor cells Genes Cells 16 2011 778 790
61. Y. Takagi, K. Nozaki, J. Takahashi, J. Yodoi, M. Ishikawa, and N. Hashimoto Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice Brain Res. 831 1999 283 287
62. V. Tropepe, M. Sibilia, B.G. Ciruna, J. Rossant, E.F. Wagner, and D. van der Kooy Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon Dev. Biol. 208 1999 166 188
63. J.M. Vela, E. Molina-Holgado, A. Arevalo-Martin, G. Almazan, and C. Guaza Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells Mol. Cell Neurosci. 20 2002 489 502
64. S. Watanabe, M. Doshi, and T. Hamazaki n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice Prostaglandins Leukot. Essent. Fat. Acids 69 2003 51 59
65. J.T. Wood, J.S. Williams, L. Pandarinathan, D.R. Janero, C.J. Lammi-Keefe, and A. Makriyannis Dietary docosahexaenoic acid supplementation alters select physiological endocannabinoid-system metabolites in brain and plasma J. Lipid Res. 51 2010 1416 1423
66. F. Xue, L. Liu, J. Fan, S. He, R. Li, Z.W. Peng, and B.R. Wang Interleukin-1beta promotes the neurogenesis of carotid bodies by stimulating the activation of ERK1/2 Respir. Physiol. Neurobiol. 219 2015 78 84
67. D. Zhang, M. Guo, W. Zhang, and X.Y. Lu Adiponectin stimulates proliferation of adult hippocampal neural stem/progenitor cells through activation of p38 mitogen-activated protein kinase (p38MAPK)/glycogen synthase kinase 3beta (GSK-3beta)/beta-catenin signaling cascade J. Biol. Chem. 286 2011 44913 44920
68. C. Zhao, W. Deng, and F.H. Gage Mechanisms and functional implications of adult neurogenesis Cell 132 2008 645 660