The Cannabinoid Receptor CB1 Interacts with the WAVE1 Complex and Plays a Role in Actin Dynamics and Structural Plasticity in Neurons

PLoS Biology

Volumn 13, Issue 10, 2015, Pages 1-36

  Njoo, Christian ^a   Agarwal, Nitin ^a   Lutz, Beat ^b   Kuner, Rohini ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; CELL PROTEIN; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; WAVE1 PROTEIN; CANNABINOID; CNR1 PROTEIN, MOUSE; HYBRID PROTEIN; NERVE PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOTOPROTEIN; WASL PROTEIN, MOUSE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL MATURATION; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC SPINE; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; AGONISTS; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS CELL LINE; CYTOLOGY; DRUG EFFECTS; FRONTAL LOBE; GENETICS; GROWTH CONE; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PARIETAL LOBE;

ACTIN CYTOSKELETON; ANIMALS; CANNABINOIDS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DENDRITIC SPINES; EMBRYO, MAMMALIAN; FRONTAL LOBE; GROWTH CONES; LUMINESCENT PROTEINS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; PARIETAL LOBE; RECEPTOR, CANNABINOID, CB1; RECOMBINANT FUSION PROTEINS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84946063257     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002286     Document Type: Article

References (66)

1. Mechoulam R, Parker LA, The endocannabinoid system and the brain. Annual review of psychology. 2013;64:21–47. doi: 10.1146/annurev-psych-113011-143739 22804774
2. Pacher P, Batkai S, Kunos G, The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacological reviews. 2006;58(3):389–462. 16968947
3. Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R, The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocrine reviews. 2006;27(1):73–100. doi: 10.1210/er.2005-0009 16306385.
4. Castillo PE, Younts TJ, Chavez AE, Hashimotodani Y, Endocannabinoid signaling and synaptic function. Neuron. 2012;76(1):70–81. doi: 10.1016/j.neuron.2012.09.020 23040807
5. Katona I, Freund TF, Multiple functions of endocannabinoid signaling in the brain. Annual review of neuroscience. 2012;35:529–58. doi: 10.1146/annurev-neuro-062111-150420 22524785
6. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, et al. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nature neuroscience. 2007;10(7):870–9. 17558404
7. Bellocchio L, Lafenetre P, Cannich A, Cota D, Puente N, Grandes P, et al. Bimodal control of stimulated food intake by the endocannabinoid system. Nature neuroscience. 2010;13(3):281–3. doi: 10.1038/nn.2494 20139974
8. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science. 2003;302(5642):84–8. 14526074
9. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, et al. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron. 2006;51(4):455–66. 16908411
10. Ruehle S, Remmers F, Romo-Parra H, Massa F, Wickert M, Wortge S, et al. Cannabinoid CB1 receptor in dorsal telencephalic glutamatergic neurons: distinctive sufficiency for hippocampus-dependent and amygdala-dependent synaptic and behavioral functions. J Neurosci. 2013;33(25):10264–77. doi: 10.1523/JNEUROSCI.4171-12.2013 23785142
11. Argaw A, Duff G, Zabouri N, Cecyre B, Chaine N, Cherif H, et al. Concerted action of CB1 cannabinoid receptor and deleted in colorectal cancer in axon guidance. J Neurosci. 2011;31(4):1489–99. doi: 10.1523/JNEUROSCI.4134-09.2011 21273433
12. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, et al. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science. 2007;316(5828):1212–6. 17525344
13. Harkany T, Guzman M, Galve-Roperh I, Berghuis P, Devi LA, Mackie K, The emerging functions of endocannabinoid signaling during CNS development. Trends in pharmacological sciences. 2007;28(2):83–92. 17222464
14. Pertwee RG, Howlett AC, Abood ME, Alexander SP, Di Marzo V, Elphick MR, et al. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB(1) and CB(2). Pharmacological reviews. 2010;62(4):588–631. doi: 10.1124/pr.110.003004 21079038
15. He JC, Neves SR, Jordan JD, Iyengar R, Role of the Go/i signaling network in the regulation of neurite outgrowth. Canadian journal of physiology and pharmacology. 2006;84(7):687–94. 16998532
16. Ishii I, Chun J, Anandamide-induced neuroblastoma cell rounding via the CB1 cannabinoid receptors. Neuroreport. 2002;13(5):593–6. 11973452.
17. Lauckner JE, Hille B, Mackie K, The cannabinoid agonist WIN55,212–2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(52):19144–9. 16365309
18. Howlett AC, Blume LC, Dalton GD, CB(1) cannabinoid receptors and their associated proteins. Current medicinal chemistry. 2010;17(14):1382–93. 20166926.
19. Jin W, Brown S, Roche JP, Hsieh C, Celver JP, Kovoor A, et al. Distinct domains of the CB1 cannabinoid receptor mediate desensitization and internalization. J Neurosci. 1999;19(10):3773–80. 10234009.
20. Niehaus JL, Liu Y, Wallis KT, Egertova M, Bhartur SG, Mukhopadhyay S, et al. CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Molecular pharmacology. 2007;72(6):1557–66. 17895407
21. Pierce KL, Lefkowitz RJ, Classical and new roles of beta-arrestins in the regulation of G-protein-coupled receptors. Nat Rev Neurosci. 2001;2(10):727–33. Epub 2001/10/05. 11584310
22. Tappe-Theodor A, Agarwal N, Katona I, Rubino T, Martini L, Swiercz J, et al. A molecular basis of analgesic tolerance to cannabinoids. J Neurosci. 2007;27(15):4165–77. Epub 2007/04/13. 17428994
23. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, Ismail AM, et al. Structure and control of the actin regulatory WAVE complex. Nature. 2010;468(7323):533–8. doi: 10.1038/nature09623 21107423
24. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW, Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature. 2002;418(6899):790–3. 12181570
25. Pickel VM, Chan J, Kash TL, Rodriguez JJ, MacKie K, Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience. 2004;127(1):101–12. 15219673
26. Rothbauer U, Zolghadr K, Muyldermans S, Schepers A, Cardoso MC, Leonhardt H, A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol Cell Proteomics. 2008;7(2):282–9. Epub 2007/10/24. 17951627
27. Mukhopadhyay S, McIntosh HH, Houston DB, Howlett AC, The CB(1) cannabinoid receptor juxtamembrane C-terminal peptide confers activation to specific G proteins in brain. Molecular pharmacology. 2000;57(1):162–70. 10617691. 10617691
28. Howlett AC, Cannabinoid inhibition of adenylate cyclase. Biochemistry of the response in neuroblastoma cell membranes. Molecular pharmacology. 1985;27(4):429–36. 2984538.
29. Hsieh C, Brown S, Derleth C, Mackie K, Internalization and recycling of the CB1 cannabinoid receptor. Journal of neurochemistry. 1999;73(2):493–501. 10428044.
30. Takenawa T, Suetsugu S, The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol. 2007;8(1):37–48. Epub 2006/12/22. 17183359
31. Burianek LE, Soderling SH, Under lock and key: spatiotemporal regulation of WASP family proteins coordinates separate dynamic cellular processes. Seminars in cell & developmental biology. 2013;24(4):258–66. doi: 10.1016/j.semcdb.2012.12.005 23291261
32. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature. 2002;418(6897):530–4. 12152079
33. Pertz O, Spatio-temporal Rho GTPase signaling—where are we now? Journal of cell science. 2010;123(Pt 11):1841–50. doi: 10.1242/jcs.064345 20484664.
34. Komatsu N, Aoki K, Yamada M, Yukinaga H, Fujita Y, Kamioka Y, et al. Development of an optimized backbone of FRET biosensors for kinases and GTPases. Molecular biology of the cell. 2011;22(23):4647–56. doi: 10.1091/mbc.E11-01-0072 21976697
35. Spillane M, Ketschek A, Donnelly CJ, Pacheco A, Twiss JL, Gallo G, . (2012) Nerve growth factor-induced formation of axonal filopodia and collateral branches involves the intra-axonal synthesis of regulators of the actin-nucleating Arp2/3 complex. J Neurosci. 32(49):17671–89. Epub 2012/12/12. doi: 10.1523/JNEUROSCI.1079-12.2012 23223289
36. Ceglia I, Kim Y, Nairn AC, Greengard P, Signaling pathways controlling the phosphorylation state of WAVE1, a regulator of actin polymerization. Journal of neurochemistry. 2010;114(1):182–90. doi: 10.1111/j.1471-4159.2010.06743.x 20403076
37. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, et al. Lifeact: a versatile marker to visualize F-actin. Nature methods. 2008;5(7):605–7. doi: 10.1038/nmeth.1220 18536722.
38. Dent EW, Meiri KF, Distribution of phosphorylated GAP-43 (neuromodulin) in growth cones directly reflects growth cone behavior. Journal of neurobiology. 1998;35(3):287–99. 9622012.
39. Ladarre D, Roland AB, Biedzinski S, Ricobaraza A, Lenkei Z, Polarized cellular patterns of endocannabinoid production and detection shape cannabinoid signaling in neurons. Front Cell Neurosci. 2014;8:426. doi: 10.3389/fncel.2014.00426 25610369
40. Leterrier C, Laine J, Darmon M, Boudin H, Rossier J, Lenkei Z, Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci. 2006;26(12):3141–53. 16554465
41. Roland AB, Ricobaraza A, Carrel D, Jordan BM, Rico F, Simon A, et al. Cannabinoid-induced actomyosin contractility shapes neuronal morphology and growth. Elife. 2014;3:e03159. doi: 10.7554/eLife.03159
42. Rocca DL, Amici M, Antoniou A, Blanco Suarez E, Halemani N, Murk K, et al. The small GTPase Arf1 modulates Arp2/3-mediated actin polymerization via PICK1 to regulate synaptic plasticity. Neuron. 2013;79(2):293–307. doi: 10.1016/j.neuron.2013.05.003 23889934
43. Hotulainen P, Hoogenraad CC, Actin in dendritic spines: connecting dynamics to function. The Journal of cell biology. 2010;189(4):619–29. doi: 10.1083/jcb.201003008 20457765
44. Nimchinsky EA, Sabatini BL, Svoboda K, Structure and function of dendritic spines. Annual review of physiology. 2002;64:313–53. 11826272
45. Simonetti M, Hagenston AM, Vardeh D, Freitag HE, Mauceri D, Lu J, et al. (2013) Nuclear calcium signaling in spinal neurons drives a genomic program required for persistent inflammatory pain. Neuron. 77(1):43–57. Epub 2013/01/15. doi: 10.1016/j.neuron.2012.10.037 23312515
46. D'Mello R, Dickenson AH, Spinal cord mechanisms of pain. Brit J Anaesth. 2008;101(1):8–16. doi: 10.1093/bja/aen088 18417503
47. Dahl JP, Wang-Dunlop J, Gonzales C, Goad ME, Mark RJ, Kwak SP, Characterization of the WAVE1 knock-out mouse: implications for CNS development. J Neurosci. 2003;23(8):3343–52. 12716942.
48. Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature. 2006;442(7104):814–7. 16862120
49. Smith TH, Sim-Selley LJ, Selley DE, . (2012) Cannabinoid CB1 receptor-interacting proteins: novel targets for central nervous system drug discovery? Br J Pharmacol. 160(3):454–66. Epub 2010/07/02.
50. Sarramegn V, Muller I, Milon A, Talmont F, Recombinant G protein-coupled receptors from expression to renaturation: a challenge towards structure. Cellular and molecular life sciences: CMLS. 2006;63(10):1149–64. 16568239
51. Chen B, Brinkmann K, Chen Z, Pak CW, Liao Y, Shi S, et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell. 2014;156(1–2):195–207. doi: 10.1016/j.cell.2013.11.048 24439376
52. Pertwee RG, Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life sciences. 2005;76(12):1307–24. doi: 10.1016/j.lfs.2004.10.025 15670612.
53. Hudson BD, Hebert TE, Kelly ME, Ligand- and heterodimer-directed signaling of the CB(1) cannabinoid receptor. Molecular pharmacology. 2010;77(1):1–9. doi: 10.1124/mol.109.060251 19837905
54. Tortoriello G, Morris CV, Alpar A, Fuzik J, Shirran SL, Calvigioni D, et al. Miswiring the brain: Delta9-tetrahydrocannabinol disrupts cortical development by inducing an SCG10/stathmin-2 degradation pathway. The EMBO journal. 2014;33(7):668–85. doi: 10.1002/embj.201386035 24469251
55. Govek EE, Newey SE, Van Aelst L, The role of the Rho GTPases in neuronal development. Genes & development. 2005;19(1):1–49. 15630019
56. Nakamura T, Aoki K, Matsuda M, FRET imaging in nerve growth cones reveals a high level of RhoA activity within the peripheral domain. Brain research Molecular brain research. 2005;139(2):277–87. 16024133
57. Szebenyi G, Callaway JL, Dent EW, Kalil K, Interstitial branches develop from active regions of the axon demarcated by the primary growth cone during pausing behaviors. J Neurosci. 1998;18(19):7930–40. 9742160.
58. Kuner R, Central mechanisms of pathological pain. Nature medicine. 2010;16(11):1258–66. doi: 10.1038/nm.2231 20948531
59. Katona I, Sperlagh B, Magloczky Z, Santha E, Kofalvi A, Czirjak S, et al. GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience. 2000;100(4):797–804. 11036213.
60. Kawano Y, Yoshimura T, Tsuboi D, Kawabata S, Kaneko-Kawano T, Shirataki H, et al. CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Molecular and cellular biology. 2005;25(22):9920–35. 16260607
61. Ponimaskin E, Harteneck C, Schultz G, Schmidt MF, A cysteine-11 to serine mutant of G alpha12 impairs activation through the thrombin receptor. FEBS letters. 1998;429(3):370–4. 9662451.
62. Barenz F, Inoue D, Yokoyama H, Tegha-Dunghu J, Freiss S, Draeger S, et al. The centriolar satellite protein SSX2IP promotes centrosome maturation. The Journal of cell biology. 2013;202(1):81–95. doi: 10.1083/jcb.201302122 23816619
63. Berkefeld H, Sailer CA, Bildl W, Rohde V, Thumfart JO, Eble S, et al. BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science. 2006;314(5799):615–20. 17068255
64. Inta I, Paxian S, Maegele I, Zhang W, Pizzi M, Spano P, et al. Bim and Noxa are candidates to mediate the deleterious effect of the NF-kappa B subunit RelA in cerebral ischemia. J Neurosci. 2006;26(50):12896–903. 17167080
65. Njoo C, Heinl C, Kuner R, In vivo SiRNA transfection and gene knockdown in spinal cord via rapid noninvasive lumbar intrathecal injections in mice. Journal of visualized experiments: JoVE. 2014;(85).
66. Gangadharan V, Wang R, Ulzhofer B, Luo C, Bardoni R, Bali KK, et al. Peripheral calcium-permeable AMPA receptors regulate chronic inflammatory pain in mice. The Journal of clinical investigation. 2011;121(4):1608–23. doi: 10.1172/JCI44911 21383497