Involvement of nitric oxide through endocannabinoids release in microglia activation during the course of CNS regeneration in the medicinal leech

GLIA

Volumn 61, Issue 4, 2013, Pages 636-649

  Arafah, Karim ^a   Croix, Dominique ^a   Vizioli, Jacopo ^a   Desmons, Annie ^a   Fournier, Isabelle ^a   Salzet, Michel ^a  

^a UNIV LILLE   (France)

Author keywords

2 AG; AEA; ATP; Endocannabinoids; Leech; Microglial cells; Nitric oxide; Purinergic receptors; Regeneration; TRPVs

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; ADENOSINE TRIPHOSPHATE; ENDOCANNABINOID; N ARACHIDONYL ETHANOLAMIDE; NITRIC OXIDE; PURINERGIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ASSAY; CELL ISOLATION; CHEMOTAXIS; CONTROLLED STUDY; DEGENERATIVE DISEASE; DILUTION; ELECTROCHEMISTRY; HIRUDO MEDICINALIS; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MASS SPECTROMETRY; MICROGLIA; MOUSE; NERVE INJURY; NERVE REGENERATION; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; ENDOCANNABINOIDS; HIRUDO MEDICINALIS; MICROGLIA; NERVE REGENERATION; NITRIC OXIDE;

EID: 84873718040     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22462     Document Type: Article

References (66)

1. Abbas A, Dargent T, Croix D, Salzet M, Bocquet B. 2009. Ex vivo detection of neural events using THz BioMEMS. Med Sci Monit 15: MT121-MT125.
2. Bao L, Samuels S, Locovei S, Macagno ER, Muller KJ, Dahl G. 2007. Innexins form two types of channels. FEBS Lett 581: 5703-5708.
3. Baylor DA, Nicholls JG. 1971. Patterns of regeneration between individual nerve cells in the central nervous system of the leech. Nature 232: 268-270.
4. Boidin-Wichlacz C, Vergote D, Slomianny C, Jouy N, Salzet M, Tasiemski A. 2012. Morphological and functional characterization of leech circulating blood cells: Role in immunity and neural repair. Cell Mol Life Sci 69: 1717-1731.
5. Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F. 2008. CB2 receptors in the brain: Role in central immune function. Br J Pharmacol 153: 240-251.
6. Carlisle SJ, Marciano-Cabral F, Staab A, Ludwick C, Cabral GA. 2002. Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation. Int Immunopharmacol 2: 69-82.
7. Carrier EJ, Kearn CS, Barkmeier AJ, Breese NM, Yang W, Nithipatikom K, Pfister SL, Campbell WB, Hillard CJ. 2004. Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism. Mol Pharmacol 65: 999-1007.
8. Chen A, Kumar SM, Sahley CL, Muller KJ. 2000. Nitric oxide influences injury-induced microglial migration and accumulation in the leech CNS. J Neurosci 20: 1036-1043.
9. Chen Y, Willcockson HH, Valtschanoff JG. 2009. Influence of the vanilloid receptor TRPV1 on the activation of spinal cord glia in mouse models of pain. Exp Neurol 220: 383-390.
10. Croq F, Vizioli J, Tuzova M, Tahtouh M, Sautiere PE, Van Camp C, Salzet M, Cruikshank WW, Pestel J, Lefebvre C. 2010. A homologous form of human interleukin 16 is implicated in microglia recruitment following nervous system injury in leech Hirudo medicinalis. Glia 58: 1649-1662.
11. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258: 1946-1949.
12. Duan Y, Haugabook SJ, Sahley CL, Muller KJ. 2003. Methylene blue blocks cGMP production and disrupts directed migration of microglia to nerve lesions in the leech CNS. J Neurobiol 57: 183-192.
13. Duan Y, Sahley CL, Muller KJ. 2009. ATP and NO dually control migration of microglia to nerve lesions. Dev Neurobiol 69: 60-72.
14. Dykes IM, Freeman FM, Bacon JP, Davies JA. 2004. Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J Neurosci 24: 886-894.
15. Ehrhart J, Obregon D, Mori T, Hou H, Sun N, Bai Y, Klein T, Fernandez F, Tan J, Shytle RD. 2005. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2: 29.
16. Eljaschewitsch E, Witting A, Mawrin C, Lee T, Schmidt PM, Wolf S, Hoertnagl H, Raine CS, Schneider-Stock R, Nitsch R, Ullrich O. 2006. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49: 67-79.
17. Felder CC, Glass M. 1998. Cannabinoid receptors and their endogenous agonists. Annu Rev Pharmacol Toxicol 38: 179-200.
18. Firme CP III, Natan RG, Yazdani N, Macagno ER, Baker MW. 2012. Ectopic expression of select innexins in individual central neurons couples them to pre-existing neuronal or glial networks that express the same innexin. J Neurosci 32: 14265-14270.
19. Franklin A, Stella N. 2003. Arachidonylcyclopropylamide increases microglial cell migration through cannabinoid CB2 and abnormal-cannabidiol-sensitive receptors. Eur J Pharmacol 474: 195-198.
20. Jansen JK, Nicholls J. 1972. Regeneration and changes in synaptic connections between individual nerve cells in the central nervous system of the leech. Proc Natl Acad Sci USA 69: 636-639.
21. Kandarian B, Sethi J, Wu A, Baker M, Yazdani N, Kym E, Sanchez A, Edsall L, Gaasterland T, Macagno E. 2012. The medicinal leech genome encodes 21 innexin genes: Different combinations are expressed by identified central neurons. Dev Genes Evol 222: 29-44.
22. Kim SR, Chung YC, Chung ES, Park KW, Won SY, Bok E, Park ES, Jin BK. 2007. Roles of transient receptor potential vanilloid subtype 1 and cannabinoid type 1 receptors in the brain: Neuroprotection versus neurotoxicity. Mol Neurobiol 35: 245-254.
23. Kim SR, Kim SU, Oh U, Jin BK. 2006. Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+-mediated mitochondrial damage and cytochrome c release. J Immunol 177: 4322-4329.
24. Kohidai L. 1995. Method for determination of chemoattraction in Tetrahymena pyriformis. Curr Microbiol 30: 251-253.
25. Kumar SM, Porterfield DM, Muller KJ, Smith PJ, Sahley CL. 2001. Nerve injury induces a rapid efflux of nitric oxide (NO) detected with a novel NO microsensor. J Neurosci 21: 215-220.
26. Li Q, Burrell BD. 2009. Two forms of long-term depression in a polysynaptic pathway in the leech CNS: One NMDA receptor-dependent and the other cannabinoid-dependent. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 831-841.
27. Li Q, Burrell BD. 2010. Properties of cannabinoid-dependent long-term depression in the leech. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196: 841-851.
28. Maccarrone M, Lorenzon T, Bari M, Melino G, Finazzi-Agro A. 2000. Anandamide induces apoptosis in human cells via vanilloid receptors. Evidence for a protective role of cannabinoid receptors. J Biol Chem 275: 31938-31945.
29. Maestroni GJ. 2004. The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein. FASEB J 18: 1914-1916.
30. Maresz K, Pryce G, Ponomarev ED, Marsicano G, Croxford JL, Shriver LP, Ledent C, Cheng X, Carrier EJ, Mann MK, Giovannoni G, Pertwee RG, Yamamura T, Buckley NE, Hillard CJ, Lutz B, Baker D, Dittel BN. 2007. Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat Med 13: 492-497.
31. Masuda-Nakagawa LM, Muller KJ, Nicholls JG. 1990. Accumulation of laminin and microglial cells at sites of injury and regeneration in the central nervous system of the leech. Proc Biol Sci 241: 201-206.
32. McCarron RM, Shohami E, Panikashvili D, Chen Y, Golech S, Strasser A, Mechoulam R, Spatz M. 2003. Antioxidant properties of the vasoactive endocannabinoid, 2-arachidonoyl glycerol (2-AG). Acta Neurochir Suppl 86: 271-275.
33. McGlade-McCulloh E, Morrissey AM, Norona F, Muller KJ. 1989. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc Natl Acad Sci USA 86: 1093-1097.
34. Mechoulam R. 2002. Discovery of endocannabinoids and some random thoughts on their possible roles in neuroprotection and aggression. Prostaglandins Leukot Essent Fatty Acids 66: 93-99.
35. Meriaux C, Arafah K, Tasiemski A, Wisztorski M, Bruand J, Boidin-Wichlacz C, Desmons A, Debois D, Laprévote O, Brunelle A, Gaasterland T, Macagno E, Fournier I, Salzet M. 2011. Multiple changes in peptide and lipid expression associated with regeneration in the nervous system of the medicinal leech. PLoS One 6: e18359.
36. Morgese VJ, Elliott EJ, Muller KJ. 1983. Microglial movement to sites of nerve lesion in the leech CNS. Brain Res 272: 166-170.
37. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin K, Greenberg DA. 1999. Cannabinoids and neuroprotection in global and focalcerebral ischemia and in neuronal cultures. J Neurosci 19: 2987-2995.
38. Ngu EM, Sahley CL, Muller KJ. 2007. Reduced axon sprouting after treatment that diminishes microglia accumulation at lesions in the leech CNS. J Comp Neurol 503: 101-109.
39. Nicholls JG, Baylor DA. 1968. Specific modalities and receptive fields of sensory neurons in CNS of the leech. J Neurophysiol 31: 740-756.
40. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R, Shohami E. 2001. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413: 527-531.
41. Pryce G, Ahmed Z, Hankey DJ, Jackson SJ, Croxford JL, Pocock JM, Ledent C, Petzold A, Thompson AJ, Giovannoni G, Cuzner ML, Baker D. 2003. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 126 (Part 10): 2191-2202.
42. Salzet M. 2000. Invertebrate molecular neuroimmune processes. Brain Res Brain Res Rev 34: 69-79.
43. Salzet M, Macagno ER. 2009. Recent advances on development, regeneration and immune responses of the leech nervous system. In: Shain D, editor. Annelids as models systems in the biological sciences. Hoboken, NJ: Wiley Blackwell. pp 156-185.
44. Samuels SE, Lipitz JB, Dahl G, Muller KJ. 2010. Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J Gen Physiol 136: 425-442.
45. Schikorski D, Cuvillier-Hot V, Boidin-Wichlacz C, Slomianny C, Salzet M, Tasiemski A. 2009. Deciphering the immune function and regulation by a TLR of the cytokine EMAPII in the lesioned central nervous system using a leech model. J Immunol 183: 7119-7128.
46. Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno E, Salzet M, Tasiemski A. 2008. Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol 181: 1083-1095.
47. Schilling T, Eder C. 2010. Stimulus-dependent requirement of ion channels for microglial NADPH oxidase-mediated production of reactive oxygen species. J Neuroimmunol 225: 190-194.
48. Schilling T, Eder C. 2009. Importance of the non-selective cation channel TRPV1 for microglial reactive oxygen species generation. J Neuroimmunol 216: 118-121.
49. Shafer OT, Chen A, Kumar SM, Muller KJ, Sahley CL. 1998. Injury-induced expression of endothelial nitric oxide synthase by glial and microglial cells in the leech central nervous system within minutes after injury. Proc Biol Sci 265: 2171-2175.
50. Shirakawa H, Nakagawa T, Kaneko S. 2010. [Pathophysiological roles of transient receptor potential channels in glial cells]. Yakugaku Zasshi 130: 281-287.
51. Sinor AD, Irvin SM, Greenberg DA. 2000. Endocannabinoids protect cerebral cortical neurons from in vitro ischemia in rats. Neurosci Lett 278: 157-160.
52. Stefano GB, Rialas CM, Deutsch DG, Salzet M. 1998. Anandamide amidase inhibition enhances anandamide-stimulated nitric oxide release in invertebrate neural tissues. Brain Res 793: 341-345.
53. Stefano GB, Salzet B, Rialas CM, Pope M, Kustka A, Neenan K, Pryor S, Salzet M. 1997a. Morphine- and anandamide-stimulated nitric oxide production inhibits presynaptic dopamine release. Brain Res 763: 63-68.
54. Stefano GB, Salzet B, Salzet M. 1997b. Identification and characterization of the leech CNS cannabinoid receptor: Coupling to nitric oxide release. Brain Res 753: 219-224.
55. Stefano GB, Salzet M, Magazine HI. 2002. Cyclic nitric oxide release by human granulocytes, and invertebrate ganglia and immunocytes: Nano-technological enhancement of amperometric nitric oxide determination. Med Sci Monit 8: BR199-BR204.
56. Stubiger G, Pittenauer E, Allmaier G. 2008. MALDI seamless postsource decay fragment ion analysis of sodiated and lithiated phospholipids. Anal Chem 80: 1664-1678.
57. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K. 1995. 2-Arachidonoylglycerol: A possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215: 89-97.
58. Sugiura T, Waku K. 2000. 2-Arachidonoylglycerol and the cannabinoid receptors. Chem Phys Lipids 108: 89-106.
59. Tahtouh M, Croq F, Vizioli J, Sautiere PE, Van Camp C, Salzet M, Daha MR, Pestel J, Lefebvre C. 2009. Evidence for a novel chemotactic C1q domain-containing factor in the leech nerve cord. Mol Immunol 46: 523-531.
60. Tahtouh M, Garcon-Bocquet A, Croq F, Vizioli J, Sautiere PE, Van Camp C, Salzet M, Nagnan-le Meillour P, Pestel J, Lefebvre C. 2012. Interaction of HmC1q with leech microglial cells: Involvement of C1qBP-related molecule in the induction of cell chemotaxis. J Neuroinflammation 9: 37.
61. Vannacci A, Giannini L, Passani MB, Di Felice A, Pierpaoli S, Zagli G, Fantappie O, Mazzanti R, Masini E, Mannaioni PF. 2004. The endocannabinoid 2-arachidonylglycerol decreases the immunological activation of Guinea pig mast cells: Involvement of nitric oxide and eicosanoids. J Pharmacol Exp Ther 311: 256-264.
62. Veldhuis WB, van der Stelt M, Wadman MW, van Zadelhoff G, Maccarrone M, Fezza F, Veldink GA, Vliegenthart JF, Bär PR, Nicolay K, DiMarzo V. 2003. Neuroprotection by the endogenous cannabinoid anandamide and arvanil against in vivo excitotoxicity in the rat: Role of vanilloid receptors and lipoxygenases. J Neurosci 23: 4127-4133.
63. von Bernhardi R, Muller KJ. 1995. Repair of the central nervous system: Lessons from lesions in leeches. J Neurobiol 27: 353-366.
64. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N. 2003. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 23: 1398-1405.
65. Witting A, Walter L, Wacker J, Moller T, Stella N. 2004. P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc Natl Acad Sci USA 101: 3214-3219.
66. Xian Y, Zhang W, Xue J, Ying X, Jin L, Jin J. 2000. Measurement of nitric oxide released in the rat heart with an amperometric microsensor. Analyst 125: 1435-1439.