Localization of the cannabinoid CB1 receptor and the 2-AG synthesizing (DAGLα) and degrading (MAGL, FAAH) enzymes in cells expressing the Ca2+-binding proteins calbindin, calretinin, and parvalbumin in the adult rat hippocampus

Frontiers in Neuroanatomy

Volumn 8, Issue JUN, 2014, Pages

  Rivera, Patricia ^a,b   Arrabal, Sergio ^a,b   Cifuentes, Manuel ^a,b   Grondona, Jesús M ^a   Pérez Martín, Margarita ^a   Rubio, Leticia ^c   Vargas, Antonio ^a   Serrano, Antonia ^a,b   Pavón, Francisco J ^a,b   Suárez, Juan ^a,b   de Fonseca, Fernando Rodríguez ^a,b  

^a Instituto de Investigación Biomédica de Málaga y Plataforma en Nanomedicina IBIMA Plataforma Bionand   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

2 arachidonoylglycerol; Calcium binding protein; Cannabinoid receptor; Confocal microscopy; Hippocampus; Immunohistochemistry; Rat

Indexed keywords

ACYLGLYCEROL LIPASE; CALBINDIN; CALBINDIN 1; CALCIUM BINDING PROTEIN; CALRETININ; CANNABINOID 1 RECEPTOR; DIACYLGLYCEROL LIPASE ALPHA; FATTY ACID AMIDASE; LIPOPROTEIN LIPASE; PARVALBUMIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN REGION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; ENZYME DEGRADATION; ENZYME LOCALIZATION; GRANULAR CELL; HIPPOCAMPAL STRATUM LUCIDUM; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NEUROPIL; NONHUMAN; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; RAT; STRATA RADIATUM; STRATUM PYRAMIDALE; WESTERN BLOTTING;

EID: 84903398533     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00056     Document Type: Article

References (61)

1. Baimbridge, K. G., and Miller, J. J. (1982). Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res. 245, 223-229. doi: 10.1016/0006-8993(82) 90804-6
2. Baimbridge, K. G., Miller, J. J., and Parkes, C. O. (1982). Calcium-binding protein distribution in the rat brain. Brain Res. 239, 519-525. doi: 10.1016/0006-8993(82)90526-1
3. Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., et al. (2003). Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163, 463-468. doi: 10.1083/jcb.200305129
4. Blankman, J. L., Simon, G. M., and Cravatt, B. F. (2007). A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol. 14, 1347-1356. doi: 10.1016/j.chembiol.2007.11.006
5. Bouilleret, V., Schwaller, B., Schurmans, S., Celio, M. R., and Fritschy, J. M. (2000). Neurodegenerative and morphogenic changes in a mouse model of temporal lobe epilepsy do not depend on the expression of the calcium-binding proteins parvalbumin, calbindin, or calretinin. Neuroscience 97, 47-58. doi: 10.1016/S0306-4522(00)00017-8
6. Celio, M. R. (1986). Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231, 995-997. doi: 10.1126/sci-ence.3945815
7. Celio, M. R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375-475. doi: 10.1016/0306-4522(90)90091-H
8. Chanda, P. K., Gao, Y., Mark, L., Btesh, J., Strassle, B. W., Lu, P., et al. (2010). Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system. Mol. Pharmacol. 78, 996-1003. doi: 10.1124/mol.110.068304
9. Cravatt, B. F., Demarest, K., Patricelli, M. P., Bracey, M. H., Giang, D. K., Martin, B. R., et al. (2001). Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. U.S.A. 98, 9371-9376. doi: 10.1073/pnas.161191698
10. D'Amico, M., Cannizzaro, C., Preziosi, P., and Martire, M. (2004). Inhibition by anandamide and synthetic cannabimimetics of the release of [3H]D-aspartate and [3H]GABA from synaptosomes isolated from the rat hippocampus. Neurochem. Res. 29, 1553-1561. doi: 10.1023/B:NERE.0000029569.20266.3f
11. Di, S., Malcher-Lopes, R., Marcheselli, V. L., Bazan, N. G., and Tasker, J. G. (2005). Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothala-mic magnocellular neurons. Endocrinology 146, 4292-4301. doi: 10.1210/en. 2005-0610
12. Di Marzo, V., Bisogno, T., De Petrocellis, L., Melck, D., Orlando, P., Wagner, J. A., et al. (1999). Biosynthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in circulating and tumoral macrophages. Eur. J. Biochem. 264, 258-267. doi: 10.1046/j.1432-1327.1999.00631.x
13. Di Marzo, V., Bisogno, T., Sugiura, T., Melck, D., and De Petrocellis, L. (1998). The novel endogenous cannabinoid 2-arachidonoylglycerol is inactivated by neuronal- and basophil-like cells: connections with anandamide. Biochem. J. 331, 15-19.
14. Dinh, T. P., Carpenter, D., Leslie, F. M., Freund, T. F., Katona, I., Sensi, S. L., et al. (2002). Brain monoglyceride lipase participating in endo-cannabinoid inactivation. Proc. Natl. Acad. Sci. U.S.A. 99, 10819-10824. doi: 10.1073/pnas.152334899
15. Egertová, M., Cravatt, B. F., and Elphick, M. R. (2003). Comparative analysis of fatty acid amide hydrolase and cb(1) cannabinoid receptor expression in the mouse brain: evidence of a widespread role for fatty acid amide hydrolase in regulation of endocannabinoid signaling. Neuroscience 119, 481-496. doi: 10.1016/S0306-4522(03)00145-3
16. Egertová, M., and Elphick, M. R. (2000). Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J. Comp. Neurol. 422, 159-171. doi: 10.1002/(SICI)1096-9861(20000626)
17. Gao, Y., Vasilyev, D. V., Goncalves, M. B., Howell, F. V., Hobbs, C., Reisenberg, M., et al. (2010). Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci. 30, 2017-2024. doi: 10.1523/JNEUROSCI.5693-09.2010
18. Garcia-Segura, L. M., Baetens, D., Roth, J., Norman, A. W., and Orci, L. (1984). Immunohistochemical mapping of calcium-binding protein immunoreactivity in the rat central nervous system. Brain Res. 296, 75-86. doi: 10.1016/0006-8993(84)90512-2
19. Goparaju, S. K., Ueda, N., Yamaguchi, H., and Yamamoto, S. (1998). Anandamide amidohydrolase reacting with 2-arachidonoylglycerol, another cannabi-noid receptor ligand. FEBS Lett. 422, 69-73. doi: 10.1016/S0014-5793(97) 01603-7
20. Goparaju, S. K., Ueda, N., Taniguchi, K., and Yamamoto, S. (1999). Enzymes of porcine brain hydrolyzing 2-arachidonoylglycerol, an endogenous ligand of cannabinoid receptors. Biochem. Pharmacol. 57, 417-423. doi: 10.1016/S0006-2952(98)00314-1
21. Gulyás, A. I., Cravatt, B. F., Bracey, M. H., Dinh, T. P., Piomelli, D., Boscia, F., et al. (2004). Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur. J. Neurosci. 20, 441-458. doi: 10.1111/j.1460-9568.2004.03428.x
22. Gulyás, A. I., Miettinen, R., Jacobowitz, D. M., and Freund, T. F. (1992). Calretinin is present in non-pyramidal cells of the rat hippocampus-I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48, 1-27. doi: 10.1016/0306-4522(92)90334-X
23. Gulyás, A. I., Tóth, K., Dános, P., and Freund, T. F. (1991). Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecys-tokinin in the rat hippocampus. J. Comp. Neurol. 312, 371-378. doi: 10.1002/ cne.903120305
24. Hashimotodani, Y., Ohno-Shosaku, T., Tsubokawa, H., Ogata, H., Emoto, K., Maejima, T., et al. (2005). Phospholipase Cbeta serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45, 257-268. doi: 10.1016/j.neuron.2005.01.004
25. Karádi, K., Janszky, J., Gyimesi, C., Horváth, Z., Lucza, T., Dóczi, T., et al. (2012). Correlation between calbindin expression in granule cells of the resected hip-pocampal dentate gyrus and verbal memory in temporal lobe epilepsy. Epilepsy Behav. 25, 110-119. doi: 10.1016/j.yebeh.2012.06.007
26. Katona, I., and Freund, T. F. (2008). Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat. Med. 14, 923-930. doi: 10.1038/ nm.f.1869
27. Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E. S., Mackie, K., et al. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19, 4544-4558.
28. Katona, I., Urbán, G. M., Wallace, M., Ledent, C., Jung, K. M., Piomelli, D., et al. (2006). Molecular composition of the endocannabinoid system at gluta-matergic synapses. J. Neurosci. 26, 5628-5637. doi: 10.1523/JNEUROSCI.0309-06.2006
29. Kawamura, Y., Fukaya, M., Maejima, T., Yoshida, T., Miura, E., Watanabe, M., et al. (2006). The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J. Neurosci. 26, 2991-3001. doi: 10.1523/JNEUROSCI.4872-05.2006
30. Kondo, S., Kondo, H., Nakane, S., Kodaka, T., Tokumura, A., Waku, K., et al. (1998). 2-Arachidonoylglycerol, an endogenous cannabinoid receptor agonist: identification as one of the major species of monoacylglycerols in various rat tissues, and evidence for its generation through CA2+-dependent and -independent mechanisms. FEBS Lett. 429, 152-156. doi: 10.1016/S0014-5793(98)00581-X
31. Kosaka, T., Katsumaru, H., Hama, K., Wu, J. Y., and Heizmann, C. W. (1987). GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419, 119-130. doi: 10.1016/0006-8993(87)90575-0
32. Lichtman, A. H., Hawkins, E. G., Griffin, G., and Cravatt, B. F. (2002). Pharmacological activity of fatty acid amides is regulated, but not mediated, by fatty acid amide hydrolase in vivo. J. Pharmacol. Exp. Ther. 302, 73-79. doi: 10.1124/jpet.302.1.73
33. Maejima, T., Hashimoto, K., Yoshida, T., Aiba, A., and Kano, M. (2001). Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabi-noid receptors. Neuron 31, 463-475. doi: 10.1016/S0896-6273(01)00375-0
34. Maejima, T., Oka, S., Hashimotodani, Y., Ohno-Shosaku, T., Aiba, A., Wu, D., et al. (2005). Synaptically driven endocannabinoid release requires Ca2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase Cbeta4 signaling cascade in the cerebellum. J. Neurosci. 25, 6826-6835. doi: 10.1523/JNEUROSCI.0945-05.2005
35. Marsicano, G., and Lutz, B. (1999). Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11, 4213-4225. doi: 10.1046/j.1460-9568.1999.00847.x
36. Miettinen, R., Gulyás, A. I., Baimbridge, K. G., Jacobowitz, D. M., and Freund, T. F. (1992). Calretinin is present in non-pyramidal cells of the rat hippocampus-II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48, 29-43. doi: 10.1016/0306-4522(92)90335-Y
37. Murray, A. J., Sauer, J. F., Riedel, G., McClure, C., Ansel, L., Cheyne, L., et al. (2011). Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nat. Neurosci. 14, 297-299. doi: 10.1038/ nn.2751
38. Nakamura, Y., Nakahama, T., Ushiwata, A., Takeda, M., and Nakaya, K. (1980). Isolation and partial characterization of an acidic calcium-binding protein from synaptic plasma membranes of rat brain. FEBS Lett. 112, 155-158. doi: 10.1016/0014-5793(80)80169-4
39. Nyilas, R., Dudok, B., Urbán, G. M., Mackie, K., Watanabe, M., Cravatt, B. F., et al. (2008). Enzymatic machinery for endocannabinoid biosynthesis associated with calcium stores in glutamatergic axon terminals. J. Neurosci. 28, 1058-1063. doi: 10.1523/JNEUROSCI.5102-07.2008
40. Ohno-Shosaku, T., Hashimotodani, Y., Maejima, T., and Kano, M. (2005). Calcium signaling and synaptic modulation: regulation of endocannabinoid-mediated synaptic modulation by calcium. Cell Calcium 38, 369-374. doi: 10.1016/j.ceca.2005.06.014
41. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. Sixth Edn. Sidney, NSW: Academic Press.
42. Puighermanal, E., Busquets-Garcia, A., Maldonado, R., and Ozaita, A. (2012). Cellular and intracellular mechanisms involved in the cognitive impairment of cannabinoids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 3254-3263. doi: 10.1098/rstb.2011.0384
43. Riedel, G., and Davies, S. N. (2005). Cannabinoid function in learning, memory and plasticity. Handb. Exp. Pharmacol. 168, 445-477. doi: 10.1007/3-540-26573-2_15
44. Rivera, P., Arrabal, S., Vargas, A., Blanco, E., Serrano, A., Pavón, F. J., et al. (2014). Localization of peroxisome proliferator-activated receptor alpha (PPARα) and N-acyl phosphatidylethanolamine phospholipase D (NAPE-PLD) in cells expressing the Ca2+-binding proteins calbindin, calretinin, and parvalbumin in the adult rat hippocampus. Front. Neuroanat. 8:12 doi: 10.3389/fnana.2014.00012
45. Rüttimann, E., Vacher, C. M., Gassmann, M., Kaupmann, K., Van der Putten, H., and Bettler, B. (2004). Altered hippocampal expression of calbindin-D-28k and calretinin in GABA(B(1))-deficient mice. Biochem. Pharmacol. 68, 1613-1620. doi: 10.1016/j.bcp.2004.07.019
46. Schlosburg, J. E., Blankman, J. L., Long, J. Z., Nomura, D. K., Pan, B., Kinsey, S. G., et al. (2010). Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci. 13, 1113-1119. doi: 10.1038/nn.2616
47. Soriano, E., Nitsch, R., and Frotscher, M. (1990). Axo-axonic chandelier cells in the rat fascia dentata: golgi-electron microscopy and immunocytochemical studies. J. Comp. Neurol. 293, 1-25. doi: 10.1002/cne.902930102
48. Stella, N. (2009). Endocannabinoid signaling in microglial cells. Neuropharmacology 56(Suppl. 1), 244-253. doi: 10.1016/j.neuropharm. 2008.07.037
49. Suárez, J., Llorente, R., Romero-Zerbo, S. Y., Mateos, B., Bermúdez-Silva, F. J., de Fonseca, F. R., et al. (2009). Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 19, 623-632. doi: 10.1002/ hipo.20537
50. Suárez, J., Ortíz, O., Puente, N., Bermúdez-Silva, F. J., Blanco, E., Fernández-Llebrez, P., et al. (2011). Distribution of diacylglycerol lipase alpha, an endo-cannabinoid synthesizing enzyme, in the rat forebrain. Neuroscience 192, 112-131. doi: 10.1016/j.neuroscience.2011.06.062
51. Sugiura, T., Kishimoto, S., Oka, S., and Gokoh, M. (2006). Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog. Lipid Res. 45, 405-446. doi: 10.1016/j.plipres.2006.03.003
52. Tanimura, A., Yamazaki, M., Hashimotodani, Y., Uchigashima, M., Kawata, S., Abe, M., et al. (2010). The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65, 320-327. doi: 10.1016/j.neuron.2010.01.021
53. Tsou, K., Brown, S., Sañudo-Peña, M. C., Mackie, K., and Walker, J. M. (1998a). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83, 393-411. doi: 10.1016/S0306-4522(97)00436-3
54. Tsou, K., Mackie, K., Sañudo-Peña, M. C., and Walker, J. M. (1999). Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93, 969-975. doi: 10.1016/S0306-4522(99)00086-X
55. Tsou, K., Nogueron, M. I., Muthian, S., Sañudo-Pena, M. C., Hillard, C. J., Deutsch, D. G., et al. (1998b). Fatty acid amide hydrolase is located preferentially in large neurons in the rat central nervous system as revealed by immuno-histochemistry. Neurosci. Lett. 254, 137-140. doi: 10.1016/S0304-3940(98) 00700-9
56. Uchigashima, M., Narushima, M., Fukaya, M., Katona, I., Kano, M., and Watanabe, M. (2007). Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 27, 3663-3676. doi: 10.1523/ JNEUROSCI.0448-07.2007
57. Uchigashima, M., Yamazaki, M., Yamasaki, M., Tanimura, A., Sakimura, K., Kano, M., et al. (2011). Molecular and morphological configuration for 2-arachidonoylglycerol-mediated retrograde signaling at mossy cell-granule cell synapses in the dentate gyrus. J. Neurosci. 31, 7700-7714. doi: 10.1523/ JNEUROSCI.5665-10.2011
58. Wise, L. E., Thorpe, A. J., and Lichtman, A. H. (2009). Hippocampal CB(1) receptors mediate the memory impairing effects of Delta(9)-tetrahydrocannabinol. Neuropsychopharmacology 34, 2072-2080. doi: 10.1038/npp.2009.31
59. Wouterlood, F. G., Grosche, J., and Härtig, W. (2001). Co-localization of calretinin and calbindin in distinct cells in the hippocampal formation of the rat. Brain Res. 922, 310-314. doi: 10.1016/S0006-8993(01)03220-6
60. Yoshida, T., Fukaya, M., Uchigashima, M., Miura, E., Kamiya, H., Kano, M., et al. (2006). Localization of diacylglycerol lipase-alpha around post-synaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J. Neurosci. 26, 4740-4751. doi: 10.1523/JNEUROSCI.0054-06.2006
61. Zimmermann, L., and Schwaller, B. (2002). Monoclonal antibodies recognizing epitopes of calretinins: dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31, 13-25. doi: 10.1054/ceca.2001.0255