The complex modulation of lysosomal degradation pathways by cannabinoid receptors 1 and 2

Life Sciences

Volumn 138, Issue , 2015, Pages 3-7

  Hiebel, Christof ^a   Behl, Christian ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

autophagy; cannabinoid receptor; lysosomal degradation

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR;

APOPTOSIS; AUTOPHAGOSOME; AUTOPHAGY; BIODEGRADATION; CELL DEATH; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CELL VACUOLE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM STRESS; HUMAN; INTRACELLULAR SIGNALING; LYSOSOME; LYSOSOME MEMBRANE; MITOCHONDRION; PROTEIN PHOSPHORYLATION; REVIEW; TUMOR GROWTH; ANIMAL; DRUG EFFECTS; PHYSIOLOGY;

MAMMALIA;

ANIMALS; AUTOPHAGY; HUMANS; LYSOSOMES; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2;

EID: 84940467236     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2015.03.020     Document Type: Review

References (75)

1. B.K. Atwood, J. Wager-Miller, C. Haskins, A. Straiker, and K. Mackie Functional selectivity in CB(2) cannabinoid receptor signaling and regulation: implications for the therapeutic potential of CB(2) ligands Mol. Pharmacol. 81 2012 250 263
2. G. Benard, F. Massa, N. Puente, J. Lourenco, L. Bellocchio, E. Soria-Gomez, and et al. Mitochondrial CB(1) receptors regulate neuronal energy metabolism Nat. Neurosci. 15 2012 558 564
3. L.A. Booth, S. Tavallai, H.A. Hamed, N. Cruickshanks, and P. Dent The role of cell signalling in the crosstalk between autophagy and apoptosis Cell. Signal. 26 2014 549 555
4. G.C. Brailoiu, T.I. Oprea, P. Zhao, M.E. Abood, and E. Brailoiu Intracellular cannabinoid type 1 (CB1R) receptors are activated by anandamide J. Biol. Chem. 286 2011 29166 29174
5. C.S. Breivogel, and S.R. Childers The functional neuroanatomy of brain cannabinoid receptors Neurobiol. Dis. 5 1998 417 431
6. U.T. Brunk, and A. Terman The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis Eur. J. Biochem./FEBS. 269 2002 1996 2002
7. A. Cannich, C.T. Wotjak, K. Kamprath, H. Hermann, B. Lutz, and G. Marsicano CB1R cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice Learn. Mem. 11 2004 625 632
8. A. Carracedo, M. Gironella, M. Lorente, S. Garcia, M. Guzman, G. Velasco, and et al. Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress-related genes Cancer Res. 66 2006 6748 6755
9. G.G. Chiang, and R.T. Abraham Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase J. Biol. Chem. 280 2005 25485 25490
10. A.M. Choi, S.W. Ryter, and B. Levine Autophagy in human health and disease N. Engl. J. Med. 368 2013 651 662
11. I.Y. Choi, C. Ju, A.M. Anthony Jalin, I. Lee da, P.L. Prather, and W.K. Kim Activation of cannabinoid CB2R receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury Am. J. Pathol. 182 2013 928 939
12. R.J. Chorvat, J. Berbaum, K. Seriacki, and J.F. McElroy JD-5006 and JD-5037: peripherally restricted (PR) cannabinoid-1 receptor blockers related to SLV-319 (Ibipinabant) as metabolic disorder therapeutics devoid of CNS liabilities Bioorg. Med. Chem. Lett. 22 2012 6173 6180
13. P. Codogno, M. Mehrpour, and T. Proikas-Cezanne Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat. Rev. Mol. Cell Biol. 13 2012 7 12
14. I. Dando, M. Donadelli, C. Costanzo, E. Dalla Pozza, A. D'Alessandro, L. Zolla, and et al. Cannabinoids inhibit energetic metabolism and induce AMPK-dependent autophagy in pancreatic cancer cells Cell Death Dis. 4 2013 e664
15. P. Derkinderen, E. Valjent, M. Toutant, J.C. Corvol, H. Enslen, C. Ledent, and et al. Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus J. Neurosci. 23 2003 2371 2382
16. W.A. Devane, F.A. Dysarz 3rd, M.R. Johnson, L.S. Melvin, and A.C. Howlett Determination and characterization of a cannabinoid receptor in rat brain Mol. Pharmacol. 34 1988 605 613
17. C.C. Dibble, and B.D. Manning Signal integration by mTORC1 coordinates nutrient input with biosynthetic output Nat. Cell Biol. 15 2013 555 564
18. M. Donadelli, I. Dando, T. Zaniboni, C. Costanzo, E. Dalla Pozza, M.T. Scupoli, and et al. Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism Cell Death Dis. 2 2011 e152
19. R.A. Dunlop, U.T. Brunk, and K.J. Rodgers Oxidized proteins: mechanisms of removal and consequences of accumulation IUBMB life. 61 2009 522 527
20. D. Egan, J. Kim, R.J. Shaw, and K.L. Guan The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR Autophagy 7 2011 643 644
21. G.M. Fimia, A. Stoykova, A. Romagnoli, L. Giunta, S. Di Bartolomeo, R. Nardacci, and et al. Ambra1 regulates autophagy and development of the nervous system Nature 447 2007 1121 1125
22. S. Galiegue, S. Mary, J. Marchand, D. Dussossoy, D. Carriere, P. Carayon, and et al. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations Eur. J. Biochem/FEBS. 232 1995 54 61
23. A. Gohla, K. Klement, and B. Nurnberg The heterotrimeric G protein G(i3) regulates hepatic autophagy downstream of the insulin receptor Autophagy 3 2007 393 395
24. O. Gomez, A. Arevalo-Martin, D. Garcia-Ovejero, S. Ortega-Gutierrez, J.A. Cisneros, G. Almazan, and et al. The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation Glia 58 2010 1913 1927
25. O. Gomez, A. Sanchez-Rodriguez, M. Le, C. Sanchez-Caro, F. Molina-Holgado, and E. Molina-Holgado Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways Br. J. Pharmacol. 163 2011 1520 1532
26. N.L. Grimsey, E.S. Graham, M. Dragunow, and M. Glass Cannabinoid receptor 1 trafficking and the role of the intracellular pool: implications for therapeutics Biochem. Pharmacol. 80 2010 1050 1062
27. C. He, Y. Wei, K. Sun, B. Li, X. Dong, Z. Zou, and et al. Beclin 2 functions in autophagy, degradation of G protein-coupled receptors, and metabolism Cell 154 2013 1085 1099
28. Z. Hegyi, K. Hollo, G. Kis, K. Mackie, and M. Antal Differential distribution of diacylglycerol lipase-alpha and N-acylphosphatidylethanolamine-specific phospholipase d immunoreactivity in the superficial spinal dorsal horn of rats Glia 60 2012 1316 1329
29. C. Hiebel, T. Kromm, M. Stark, and C. Behl Cannabinoid receptor 1 modulates the autophagic flux independent of mTOR- and BECLIN1-complex J. Neurochem. 2014
30. E. Itakura, C. Kishi, K. Inoue, and N. Mizushima Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG Mol. Biol. Cell 19 2008 5360 5372
31. K.A. Jenkin, A.J. McAinch, E. Grinfeld, and D.H. Hryciw Role for cannabinoid receptors in human proximal tubular hypertrophy Cell. Physiol. Biochem. 26 2010 879 886
32. R. Kang, H.J. Zeh, M.T. Lotze, and D. Tang The Beclin 1 network regulates autophagy and apoptosis Cell Death Differ. 18 2011 571 580
33. V. Kirkin, T. Lamark, T. Johansen, and I. Dikic NBR1 cooperates with p62 in selective autophagy of ubiquitinated targets Autophagy 5 2009 732 733
34. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, and et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
35. L.C. Koay, R.J. Rigby, and K.L. Wright Cannabinoid-induced autophagy regulates suppressor of cytokine signaling-3 in intestinal epithelium Am. J. Physiol. Gastrointest. Liver Physiol. 307 2014 G140 G148
36. J. Kubisch, D. Turei, L. Foldvari-Nagy, Z.A. Dunai, L. Zsakai, M. Varga, and et al. Complex regulation of autophagy in cancer - integrated approaches to discover the networks that hold a double-edged sword Semin. Cancer Biol. 23 2013 252 261
37. C. Leterrier, D. Bonnard, D. Carrel, J. Rossier, and Z. Lenkei Constitutive endocytic cycle of the CB1R cannabinoid receptor J. Biol. Chem. 279 2004 36013 36021
38. C. Leterrier, J. Laine, M. Darmon, H. Boudin, J. Rossier, and Z. Lenkei Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors J. Neurosci. 26 2006 3141 3153
39. M. Li, B. Khambu, H. Zhang, J.H. Kang, X. Chen, D. Chen, and et al. Suppression of lysosome function induces autophagy via a feedback down-regulation of MTOR complex 1 (MTORC1) activity J. Biol. Chem. 288 2013 35769 35780
40. L. Martini, M. Waldhoer, M. Pusch, V. Kharazia, J. Fong, J.H. Lee, and et al. Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1 FASEB J. 21 2007 802 811
41. L.A. Matsuda, S.J. Lolait, M.J. Brownstein, A.C. Young, and T.I. Bonner Structure of a cannabinoid receptor and functional expression of the cloned cDNA Nature 346 1990 561 564
42. R. Mechoulam, and Y. Gaoni A total synthesis of Dl-delta-1-tetrahydrocannabinol, the active constituent of Hashish J. Am. Chem. Soc. 87 1965 3273 3275
43. N. Mizushima, and T. Yoshimori How to interpret LC3 immunoblotting Autophagy 3 2007 542 545
44. N. Mizushima, T. Yoshimori, and Y. Ohsumi The role of Atg proteins in autophagosome formation Annu. Rev. Cell Dev. Biol. 27 2011 107 132
45. T. Morawe, C. Hiebel, A. Kern, and C. Behl Protein homeostasis, aging and Alzheimer's disease Mol. Neurobiol. 46 2012 41 54
46. S. Munro, K.L. Thomas, and M. Abu-Shaar Molecular characterization of a peripheral receptor for cannabinoids Nature 365 1993 61 65
47. J. Noonan, R. Tanveer, A. Klompas, A. Gowran, J. McKiernan, and V.A. Campbell Endocannabinoids prevent beta-amyloid-mediated lysosomal destabilization in cultured neurons J. Biol. Chem. 285 2010 38543 38554
48. L. O'Keefe, A.C. Simcocks, D.H. Hryciw, M.L. Mathai, and A.J. McAinch The cannabinoid receptor 1 and its role in influencing peripheral metabolism Diabetes Obes. Metab. 16 2014 294 304
49. O. Ofek, M. Karsak, N. Leclerc, M. Fogel, B. Frenkel, K. Wright, and et al. Peripheral cannabinoid receptor, CB2R, regulates bone mass Proc. Natl. Acad. Sci. U. S. A. 103 2006 696 701
50. H.A. Oh, S. Kwon, S. Choi, H. Shin, K.H. Yoon, W.J. Kim, and et al. Uncovering a role for endocannabinoid signaling in autophagy in preimplantation mouse embryos Mol. Hum. Reprod. 19 2013 93 101
51. - 3 pathway by cannabinoids in the brain J. Neurochem. 102 2007 1105 1114
52. U. Pagotto, G. Marsicano, D. Cota, B. Lutz, and R. Pasquali The emerging role of the endocannabinoid system in endocrine regulation and energy balance Endocr. Rev. 27 2006 73 100
53. S. Pankiv, T.H. Clausen, T. Lamark, A. Brech, J.A. Bruun, H. Outzen, and et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J. Biol. Chem. 282 2007 24131 24145
54. R.G. Pertwee Pharmacology of cannabinoid CB1R and CB2R receptors Pharmacol. Ther. 74 1997 129 180
55. V.M. Pickel, J. Chan, T.L. Kash, J.J. Rodriguez, and K. MacKie Compartment-specific localization of cannabinoid 1 (CB1R) and mu-opioid receptors in rat nucleus accumbens Neuroscience 127 2004 101 112
56. A. Piyanova, O. Albayram, C.A. Rossi, H. Farwanah, K. Michel, P. Nicotera, and et al. Loss of CB1R receptors leads to decreased cathepsin D levels and accelerated lipofuscin accumulation in the hippocampus Mech. Ageing Dev. 134 2013 391 399
57. R. Rozenfeld, and L.A. Devi Regulation of CB1R cannabinoid receptor trafficking by the adaptor protein AP-3 FASEB J. 22 2008 2311 2322
58. R.C. Russell, Y. Tian, H. Yuan, H.W. Park, Y.Y. Chang, J. Kim, and et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase Nat. Cell Biol. 15 2013 741 750
59. M. Salazar, A. Carracedo, I.J. Salanueva, S. Hernandez-Tiedra, M. Lorente, A. Egia, and et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells J. Clin. Investig. 119 2009 1359 1372
60. D. Sarnataro, C. Grimaldi, S. Pisanti, P. Gazzerro, C. Laezza, C. Zurzolo, and et al. Plasma membrane and lysosomal localization of CB1R cannabinoid receptor are dependent on lipid rafts and regulated by anandamide in human breast cancer cells FEBS Lett. 579 2005 6343 6349
61. J.U. Schweichel, and H.J. Merker The morphology of various types of cell death in prenatal tissues Teratology 7 1973 253 266
62. L.J. Sim-Selley Regulation of cannabinoid CB1R receptors in the central nervous system by chronic cannabinoids Crit. Rev. Neurobiol. 15 2003 91 119
63. N. Stella Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas Glia 58 2010 1017 1030
64. C. Stumm, C. Hiebel, R. Hanstein, M. Purrio, H. Nagel, A. Conrad, and et al. Cannabinoid receptor 1 deficiency in a mouse model of Alzheimer's disease leads to enhanced cognitive impairment despite of a reduction in amyloid deposition Neurobiol. Aging 34 2013 2574 2584
65. I. Tanida Autophagosome formation and molecular mechanism of autophagy Antioxid. Redox Signal. 14 2011 2201 2214
66. L. Tedesco, A. Valerio, M. Dossena, A. Cardile, M. Ragni, C. Pagano, and et al. Cannabinoid receptor stimulation impairs mitochondrial biogenesis in mouse white adipose tissue, muscle, and liver: the role of eNOS, p38 MAPK, and AMPK pathways Diabetes 59 2010 2826 2836
67. A. Terman, and U.T. Brunk Lipofuscin Int. J. Biochem. Cell Biol. 36 2004 1400 1404
68. S. Torres, M. Lorente, F. Rodriguez-Fornes, S. Hernandez-Tiedra, M. Salazar, E. Garcia-Taboada, and et al. A combined preclinical therapy of cannabinoids and temozolomide against glioma Mol. Cancer Ther. 10 2011 90 103
69. M.D. Van Sickle, M. Duncan, P.J. Kingsley, A. Mouihate, P. Urbani, K. Mackie, and et al. Identification and functional characterization of brainstem cannabinoid CB2R receptors Science 310 2005 329 332
70. D. Vara, M. Salazar, N. Olea-Herrero, M. Guzman, G. Velasco, and I. Diaz-Laviada Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy Cell Death Differ. 18 2011 1099 1111
71. M.T. Viscomi, S. Oddi, L. Latini, N. Pasquariello, F. Florenzano, G. Bernardi, and et al. Selective CB2R receptor agonism protects central neurons from remote axotomy-induced apoptosis through the PI3K/Akt pathway J. Neurosci. 29 2009 4564 4570
72. L. Walter, A. Franklin, A. Witting, C. Wade, Y. Xie, G. Kunos, and et al. Nonpsychotropic cannabinoid receptors regulate microglial cell migration J. Neurosci. 23 2003 1398 1405
73. A.M. Wasik, S. Almestrand, X. Wang, K. Hultenby, A.L. Dackland, P. Andersson, and et al. WIN55,212-2 induces cytoplasmic vacuolation in apoptosis-resistant MCL cells Cell Death Dis. 2 2011 e225
74. R.I. Wilson, and R.A. Nicoll Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses Nature 410 2001 588 592
75. Z. Yang, and D.J. Klionsky Mammalian autophagy: core molecular machinery and signaling regulation Curr. Opin. Cell Biol. 22 2010 124 131