The biomedical challenge of neurodegenerative disorders: an opportunity for cannabinoid-based therapies to improve on the poor current therapeutic outcomes

British Journal of Pharmacology

Volumn 176, Issue 10, 2019, Pages 1370-1383

  Fernández Ruiz, Javier ^a,b,c  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c INSTITUTO RAMÓN Y CAJAL DE INVESTIGACIÓN SANITARIA IRYCIS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID; CANNABINOID RECEPTOR; ENDOCANNABINOID; CANNABINOID RECEPTOR AGONIST; NEUROPROTECTIVE AGENT;

AGING; BRAIN AGING; CELL REGENERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; DEGENERATIVE DISEASE; EARLY DIAGNOSIS; EXCITOTOXICITY; EXPERIMENTAL ANIMAL; GLIA; HUMAN; MOLECULARLY TARGETED THERAPY; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEURONAL REPLACEMENT; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRESERVATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; AGED; ANIMAL; BRAIN; CLINICAL TRIAL (TOPIC); DISEASE MODEL; DRUG EFFECT; MEDICAL RESEARCH; METABOLISM; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; ANIMALS; BIOMEDICAL RESEARCH; BRAIN; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; TREATMENT OUTCOME;

EID: 85050762924     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.14382     Document Type: Review

References (77)

1. Alexander SPH, Christopoulos A, Davenport AP, Kelly E, Marrion NV, Peters JA et al. (2017a). The Concise Guide to PHARMACOLOGY 2017/18: G protein-coupled receptors. Br J Pharmacol 174: S17–S129.
2. Alexander SPH, Cidlowski JA, Kelly E, Marrion NV, Peters JA, Faccenda E et al. (2017b). The Concise Guide to PHARMACOLOGY 2017/18: Nuclear hormone receptors. Br J Pharmacol 174: S208–S224.
3. Alexander SPH, Fabbro D, Kelly E, Marrion NV, Peters JA, Faccenda E et al. (2017c). The Concise Guide to PHARMACOLOGY 2017/18: Enzymes. Br J Pharmacol 174: S272–S359.
4. Alexander SPH, Peters JA, Kelly E, Marrion NV, Faccenda E, Harding SD et al. (2017d). The Concise Guide to PHARMACOLOGY 2017/18: Ligand-gated ion channels. Br J Pharmacol 174: S130–S159.
5. Alexander SPH, Striessnig J, Kelly E, Marrion NV, Peters JA, Faccenda E et al. (2017e). The Concise Guide to PHARMACOLOGY 2017/18: Voltage-gated ion channels. Br J Pharmacol 174: S160–S194.
6. Arévalo-Martín A, García-Ovejero D, Gómez O, Rubio-Araiz A, Navarro-Galve B, Guaza C et al. (2008). CB2 cannabinoid receptors as an emerging target for demyelinating diseases: from neuroimmune interactions to cell replacement strategies. Br J Pharmacol 153: 216–225.
7. Athauda D, Foltynie T (2015). The ongoing pursuit of neuroprotective therapies in Parkinson's disease. Nat Rev Neurol 11: 25–40.
8. Baune BT (2015). Inflammation and neurodegenerative disorders: is there still hope for therapeutic intervention? Curr Opin Psychiatry 28: 148–154.
9. 2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J Neurosci 23: 11136–11141.
10. Berk C, Paul G, Sabbagh M (2014). Investigational drugs in Alzheimer's disease: current progress. Expert Opin Investig Drugs 23: 837–846.
11. 2 receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury. Am J Pathol 182: 928–939.
12. Coates JR, Wininger FA (2010). Canine degenerative myelopathy. Vet Clin North Am Small Anim Pract 40: 929–950.
13. Cummings J, Lee G, Mortsdorf T, Ritter A, Zhong K (2017). Alzheimer's disease drug development pipeline: 2017. Alzheimers Dement 3: 367–384.
14. Delenclos M, Jones DR, McLean PJ, Uitti RJ (2016). Biomarkers in Parkinson's disease: advances and strategies. Parkinsonism Relat Disord 22: S106–S110.
15. Demuth HU, Dijkhuizen RM, Farr TD, Gelderblom M, Horsburgh K, Iadecola C et al. (2017). Recent progress in translational research on neurovascular and neurodegenerative disorders. Restor Neurol Neurosci 35: 87–103.
16. Divers TJ, Mohammed HO, Cummings JF (1997). Equine motor neuron disease. Vet Clin North Am Equine Pract 13: 97–105.
17. Dorsey ER, Constantinescu R, Thompson JP, Biglan KM, Holloway RG, Kieburtz K et al. (2007). Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68: 384–386.
18. Duarte JM, Ferreira SG, Carvalho RA, Cunha RA, Köfalvi A (2012). CB₁ receptor activation inhibits neuronal and astrocytic intermediary metabolism in the rat hippocampus. Neurochem Int 60: 1–8.
19. Eaton SL, Wishart TM (2017). Bridging the gap: large animal models in neurodegenerative research. Mamm Genome 28: 324–337.
20. Fagan SG, Campbell VA (2014). The influence of cannabinoids on generic traits of neurodegeneration. Br J Pharmacol 171: 1347–1360.
21. Farzanehfar P (2016). Towards a better treatment option for Parkinson's disease: a review of adult neurogenesis. Neurochem Res 41: 3161–3170.
22. Fernández-Ruiz J, Romero J, Ramos JA (2015a). Endocannabinoids and neurodegenerative disorders: Parkinson's disease, Huntington's chorea, Alzheimer's disease, and others. Handb Exp Pharmacol 231: 233–259.
23. Fernández-Ruiz J, Moro MA, Martínez-Orgado J (2015b). Cannabinoids in neurodegenerative disorders and stroke/brain trauma: from preclinical models to clinical applications. Neurotherapeutics 12: 793–806.
24. Fernández-Ruiz J, Gómez-Ruiz M, García C, Hernández M, Ramos JA (2017). Modeling neurodegenerative disorders for developing cannabinoid-based neuroprotective therapies. Methods Enzymol 593: 175–198.
25. Frisoni GB, Boccardi M, Barkhof F, Blennow K, Cappa S, Chiotis K et al. (2017). Strategic roadmap for an early diagnosis of Alzheimer's disease based on biomarkers. Lancet Neurol 16: 661–676.
26. Fujii M, Sherchan P, Krafft PR, Rolland WB, Soejima Y, Zhang JH (2014). Cannabinoid type 2 receptor stimulation attenuates brain edema by reducing cerebral leukocyte infiltration following subarachnoid hemorrhage in rats. J Neurol Sci 342: 101–106.
27. Galve-Roperh I, Chiurchiù V, Díaz-Alonso J, Bari M, Guzmán M, Maccarrone M (2013). Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog Lipid Res 52: 633–650.
28. Geldenhuys WJ, Van der Schyf CJ (2013). Rationally designed multi-targeted agents against neurodegenerative diseases. Curr Med Chem 20: 1662–1672.
29. Gordon PH, Meininger V (2011). How can we improve clinical trials in amyotrophic lateral sclerosis? Nat Rev Neurol 7: 650–654.
30. Grimm A, Eckert A (2017). Brain aging and neurodegeneration: from a mitochondrial point of view. J Neurochem 143: 418–431.
31. 9-tetrahydrocannabinol are neuroprotective antioxidants. Proc Natl Acad Sci U S A 95: 8268–8273.
32. Harding SD, Sharman JL, Faccenda E, Southan C, Pawson AJ, Ireland S et al. (2018). The IUPHAR/BPS Guide to PHARMACOLOGY in 2018: updates and expansion to encompass the new guide to IMMUNOPHARMACOLOGY. Nucl Acids Res 46: D1091–D1106.
33. Holm IE, Alstrup AK, Luo Y (2016). Genetically modified pig models for neurodegenerative disorders. J Pathol 238: 267–287.
34. Hoque A, Hossain MI, Ameen SS, Ang CS, Williamson N, Ng DC et al. (2016). A beacon of hope in stroke therapy – blockade of pathologically activated cellular events in excitotoxic neuronal death as potential neuroprotective strategies. Pharmacol Ther 160: 159–179.
35. Hwang J, Adamson C, Butler D, Janero DR, Makriyannis A, Bahr BA (2010). Enhancement of endocannabinoid signaling by fatty acid amide hydrolase inhibition: a neuroprotective therapeutic modality. Life Sci 86: 615–623.
36. Iuvone T, Esposito G, De Filippis D, Scuderi C, Steardo L (2009). Cannabidiol: a promising drug for neurodegenerative disorders? CNS Neurosci Ther 15: 65–75.
37. Jones EG, Mendell LM (1999). Assessing the decade of the brain. Science 284: 739.
38. Khan TA, Hassan I, Ahmad A, Perveen A, Aman S, Quddusi S et al. (2016). Recent updates on the dynamic association between oxidative stress and neurodegenerative disorders. CNS Neurol Disord Drug Targets 15: 310–320.
39. Koprich JB, Kalia LV, Brotchie JM (2017). Animal models of α-synucleinopathy for Parkinson disease drug development. Nat Rev Neurosci 18: 515–529.
40. Kowal SL, Dall TM, Chakrabarti R, Storm MV, Jain A (2013). The current and projected economic burden of Parkinson's disease in the United States. Mov Disord 28: 311–318.
41. Kudelova J, Fleischmannova J, Adamova E, Matalova E (2015). Pharmacological caspase inhibitors: research towards therapeutic perspectives. J Physiol Pharmacol 66: 473–482.
42. Maas AI, Murray G, Henney H 3rd, Kassem N, Legrand V, Mangelus M et al. (2006). Efficacy and safety of dexanabinol in severe traumatic brain injury: results of a phase III randomised, placebo-controlled, clinical trial. Lancet Neurol 5: 38–45.
43. Mancuso R, Navarro X (2015). Amyotrophic lateral sclerosis: current perspectives from basic research to the clinic. Prog Neurobiol 133: 1–26.
44. Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M (2010). Alzheimer's disease: clinical trials and drug development. Lancet Neurol 9: 702–716.
45. 1. J Neurochem 80: 448–456.
46. Mazucanti CH, Cabral-Costa JV, Vasconcelos AR, Andreotti DZ, Scavone C, Kawamoto EM (2015). Longevity pathways (mTOR, SIRT, insulin/IGF-1) as key modulatory targets on aging and neurodegeneration. Curr Top Med Chem 15: 2116–2138.
47. McLellan MA, Rosenthal NA, Pinto AR (2017). Cre-loxP-mediated recombination: general principles and experimental considerations. Curr Protoc Mouse Biol 7: 1–12.
48. Mechoulam R, Shohami E (2007). Endocannabinoids and traumatic brain injury. Mol Neurobiol 36: 68–74.
49. Meldolesi J (2017). Neurotrophin receptors in the pathogenesis, diagnosis and therapy of neurodegenerative diseases. Pharmacol Res 121: 129–137.
50. Menalled L, Brunner D (2014). Animal models of Huntington's disease for translation to the clinic: best practices. Mov Disord 29: 1375–1390.
51. Molina-Holgado F, Pinteaux E, Moore JD, Molina-Holgado E, Guaza C, Gibson RM et al. (2003). Endogenous interleukin-1 receptor antagonist mediates anti-inflammatory and neuroprotective actions of cannabinoids in neurons and glia. J Neurosci 23: 6470–6474.
52. Morton AJ, Howland DS (2013). Large genetic animal models of Huntington's disease. J Huntingtons Dis 2: 3–19.
53. OECD (2017). Health at a glance. OECD.
54. Olanow CW, Kieburtz K, Katz R (2017). Clinical approaches to the development of a neuroprotective therapy for PD. Exp Neurol 298: 246–251.
55. Pacher P, Mechoulam R (2011). Is lipid signaling through cannabinoid 2 receptors part of a protective system? Prog Lipid Res 50: 193–211.
56. Petrov D, Mansfield C, Moussy A, Hermine O (2017). ALS clinical trials review: 20 years of failure. Are we any closer to registering a new treatment? Front Aging Neurosci 9: 68.
57. Pop E (2000). Dexanabinol Pharmos. Curr Opin Investig Drugs 1: 494–503.
58. Rodrigues FB, Wild EJ (2018). Huntington's disease clinical trials corner: February 2018. J Huntingtons Dis 7: 89–98.
59. Rodríguez-Cueto C, Benito C, Romero J, Hernández-Gálvez M, Gómez-Ruiz M, Fernández-Ruiz J (2014). Endocannabinoid-hydrolysing enzymes in the post-mortem cerebellum of humans affected by hereditary autosomal dominant ataxias. Pathobiology 81: 149–159.
60. Rodríguez-Cueto C, Hernández-Gálvez M, Hillard CJ, Maciel P, García-García L, Valdeolivas S et al. (2016). Dysregulation of the endocannabinoid signaling system in the cerebellum and brainstem in a transgenic mouse model of spinocerebellar ataxia type-3. Neuroscience 339: 191–209.
61. Rosser A, Svendsen CN (2014). Stem cells for cell replacement therapy: a therapeutic strategy for HD? Mov Disord 29: 1446–1454.
62. Saba L (2015). Imaging in Neurodegenerative Disorders. Oxford University Press: Oxford, UK.
63. Salat DH (2011). The declining infrastructure of the aging brain. Brain Connect 1: 279–293.
64. Sampaio C, Borowsky B, Reilmann R (2014). Clinical trials in Huntington's disease: interventions in early clinical development and newer methodological approaches. Mov Disord 29: 1419–1428.
65. Sardi SP, Cedarbaum JM, Brundin P (2018). Targeted therapies for Parkinson's disease: from genetics to the clinic. Mov Disord, in press 33: 684–696. https://doi.org/10.1002/mds.27414.
66. Sarkar S (2013). Regulation of autophagy by mTOR-dependent and mTOR-independent pathways: autophagy dysfunction in neurodegenerative diseases and therapeutic application of autophagy enhancers. Biochem Soc Trans 41: 1103–1130.
67. Sasaguri H, Nilsson P, Hashimoto S, Nagata K, Saito T, De Strooper B et al. (2017). APP mouse models for Alzheimer's disease preclinical studies. EMBO J 36: 2473–2487.
68. Stella N (2010). Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 58: 1017–1030.
69. Stoker TB, Blair NF, Barker RA (2017). Neural grafting for Parkinson's disease: challenges and prospects. Neural Regen Res 12: 389–392.
70. Stranahan AM, Mattson MP (2012). Recruiting adaptive cellular stress responses for successful brain ageing. Nat Rev Neurosci 13: 209–216.
71. United Nations (2015). World population prospects: the 2015 revision. UN
72. 2 receptors in neuroprotection at the level of the blood–brain barrier. Neuromolecular Med 16: 620–642.
73. Whitelaw CB, Sheets TP, Lillico SG, Telugu BP (2016). Engineering large animal models of human disease. J Pathol 238: 247–256.
74. World Health Organization (2016). Life expectancy increased by 5 years since 2000, but health inequalities persist. WHO.
75. Yang W, Tu Z, Sun Q, Li XJ (2016). CRISPR/Cas9: implications for modeling and therapy of neurodegenerative diseases. Front Mol Neurosci 9: 30.
76. Youssef SA, Capucchio MT, Rofina JE, Chambers JK, Uchida K, Nakayama H et al. (2016). Pathology of the aging brain in domestic and laboratory animals, and animal models of human neurodegenerative diseases. Vet Pathol 53: 327–348.
77. Ziemka-Nałęcz M, Zalewska T (2012). Endogenous neurogenesis induced by ischemic brain injury or neurodegenerative diseases in adults. Acta Neurobiol Exp 72: 309–324.