Ursocholanic acid rescues mitochondrial function in common forms of familial Parkinson's disease

Brain

Volumn 136, Issue 10, 2013, Pages 3038-3050

  Mortiboys, Heather ^a   Aasly, Jan ^b   Bandmann, Oliver ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

disease modifying therapy; LRRK2; mitochondria; parkin; Parkinson's disease

Indexed keywords

ACETYLCHOLINE; ACIVICIN; ALLOPURINOL; AMLODIPINE BESYLATE; ANTIPARKINSON AGENT; CEFDINIR; CEFTIBUTEN; CHOLANIC ACID; CLOBETASOL PROPIONATE; CLONIDINE; DESIPRAMINE; ENALAPRIL MALEATE; EPHEDRINE; FLUOROMETHOLONE; FRIEDELIN; GATIFLOXACIN; GINKGOLIC ACID; GINKGOLIDE A; HYDROQUINONE; KHELLIN; MENTHONE; OLEANOLIC ACID; PERINDOPRIL TERT BUTYLAMINE; PODOPHYLLOTOXIN; PRAZOSIN; PROBENECID; PROPYLTHIOURACIL; SIMVASTATIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; URSODEOXYCHOLIC ACID;

ADULT; ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN FUNCTION; BRAIN MITOCHONDRION; CONTROLLED STUDY; COST CONTROL; DOSE RESPONSE; DRUG BIOAVAILABILITY; DRUG REPOSITIONING; DRUG SCREENING; EMBRYO; FIBROBLAST; FIBROBLAST CULTURE; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RESPIRATORY CHAIN; WESTERN BLOTTING;

EID: 84884864808     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt224     Document Type: Article

References (54)

1. Abou-Sleiman PM, Muqit MM, Wood NW. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 2006; 7: 207-19.
2. Castro-Caldas M, Carvalho AN, Rodrigues E, Henderson CJ, Wolf CR, Rodrigues CM, et al. Tauroursodeoxycholic acid prevents MPTPinduced dopaminergic cell death in a mouse model of Parkinson's disease. Mol Neurobiol 2012; 46: 475-86.
3. Chun HS, Low WC. Ursodeoxycholic acid suppresses mitochondria-dependent programmed cell death induced by sodium nitroprusside in SH-SY5Y cells. Toxicology 2012; 292: 105-12.
4. Chung JY, Lee SJ, Lee SH, Jung YS, Ha NC, Seol W, et al. Direct interaction of alpha-synuclein and AKT regulates IGF-1 signaling: implication of Parkinson disease. Neurosignals 2011; 19: 86-96.
5. Cookson MR, Bandmann O. Parkinson's disease: insights from pathways. Hum Mol Genet 2010; 19: R21-7.
6. Cooper O, Seo H, Andrabi S, Guardia-Laguarta C, Graziotto J, Sundberg M, et al. Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci Transl Med 2012; 4: 141ra190.
7. Dorsey ER, Constantinescu R, Thompson JP, Biglan KM, Holloway RG, Kieburtz K, et al. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 2007; 68: 384-6.
8. Exner N, Lutz AK, Haass C, Winklhofer KF. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J 2012; 31: 3038-62.
9. Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, et al. A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 2006; 8: 834-42.
10. Greene LA, Levy O, Malagelada C. Akt as a victim, villain and potential hero in Parkinson's disease pathophysiology and treatment. Cell Mol Neurobiol 2011; 31: 969-78.
11. Haller J, Mikics E, Makara GB. The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system. A critical evaluation of findings. Front Neuroendocrinol 2008; 29: 273-91.
12. Hardy J. Genetic analysis of pathways to Parkinson disease. Neuron 2010; 68: 201-6.
13. Hashimoto M, Bar-On P, Ho G, Takenouchi T, Rockenstein E, Crews L, et al. Beta-synuclein regulates Akt activity in neuronal cells. A possible mechanism for neuroprotection in Parkinson's disease. J Biol Chem 2004; 279: 23622-9.
14. Hindle S, Afsari F, Stark M, Middleton CA, Evans GJ, Sweeney ST, et al. Dopaminergic expression of the Parkinsonian gene LRRK2-G2019S leads to non-autonomous visual neurodegeneration, accelerated by increased neural demands for energy. Hum Mol Genet 2013; 22: 2129-40.
15. Ho PW, Ho JW, Liu HF, So DH, Tse ZH, Chan KH, et al. Mitochondrial neuronal uncoupling proteins: a target for potential disease-modification in Parkinson's disease. Transl Neurodegener 2012; 1: 3.
16. Kasher PR, De Vos KJ, Wharton SB, Manser C, Bennett EJ, Bingley M, et al. Direct evidence for axonal transport defects in a novel mouse model of mutant spastin-induced hereditary spastic paraplegia (HSP) and human HSP patients. J Neurochem 2009; 110: 34-44.
17. Keene CD, Rodrigues CM, Eich T, Chhabra MS, Steer CJ, Low WC. Tauroursodeoxycholic acid, a bile acid, is neuroprotective in a transgenic animal model of Huntington's disease. Proc Natl Acad Sci USA 2002; 99: 10671-6.
18. Kunkel SD, Suneja M, Ebert SM, Bongers KS, Fox DK, Malmberg SE, et al. mRNA expression signatures of human skeletal muscle atrophy identify a natural compound that increases muscle mass. Cell Metab 2011; 13: 627-38.
19. Lang AE. Neuroprotection in Parkinson's disease: and now for something completely different? Lancet Neurol 2006; 5: 990-1.
20. Lesage S, Durr A, Tazir M, Lohmann E, Leutenegger AL, Janin S, et al. LRRK2 G2019S as a cause of Parkinson's disease in North African Arabs. N Engl J Med 2006; 354: 422-3.
21. Lim L, Jackson-Lewis V, Wong LC, Shui GH, Goh AX, Kesavapany S, et al. Lanosterol induces mitochondrial uncoupling and protects dopaminergic neurons from cell death in a model for Parkinson's disease. Cell Death Differ 2012; 19: 416-27.
22. Liobikas J, Majiene D, Trumbeckaite S, Kursvietiene L, Masteikova R, Kopustinskiene DM, et al. Uncoupling and antioxidant effects of ursolic acid in isolated rat heart mitochondria. J Nat Prod 2011; 74: 1640-4.
23. Loeb V, Yakunin E, Saada A, Sharon R. The transgenic overexpression of alpha-synuclein and not its related pathology associates with complex I inhibition. J Biol Chem 2010; 285: 7334-43.
24. Malagelada C, Jin ZH, Greene LA. RTP801 is induced in Parkinson's disease and mediates neuron death by inhibiting Akt phosphorylation/ activation. J Neurosci 2008; 28: 14363-71.
25. Meissner WG, Frasier M, Gasser T, Goetz CG, Lozano A, Piccini P, et al. Priorities in Parkinson's disease research. Nat Rev Drug Discov 2011; 10: 377-93.
26. Mizuno Y, Ohta S, Tanaka M, Takamiya S, Suzuki K, Sato T, et al. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem Biophys Res Commun 1989; 163: 1450-5.
27. Mortiboys H, Johansen KK, Aasly JO, Bandmann O. Mitochondrial impairment in patients with Parkinson disease with the G2019S mutation in LRRK2. Neurology 2010; 75: 2017-20.
28. Mortiboys H, Thomas KJ, Koopman WJ, Klaffke S, Abou-Sleiman P, Olpin S, et al. Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts. Ann Neurol 2008; 64: 555-65.
29. Murata H, Sakaguchi M, Jin Y, Sakaguchi Y, Futami J, Yamada H, et al. A new cytosolic pathway from a Parkinson disease-associated kinase, BRPK/PINK1: activation of AKT via mTORC2. J Biol Chem 2011; 286: 7182-9.
30. Ohta E, Kawakami F, Kubo M, Obata F. LRRK2 directly phosphorylates Akt1 as a possible physiological substrate: impairment of the kinase activity by Parkinson's disease-associated mutations. FEBS Lett 2011; 585: 2165-70.
31. Ozelius LJ, Senthil G, Saunders-Pullman R, Ohmann E, Deligtisch A, Tagliati M, et al. LRRK2 G2019S as a cause of Parkinson's disease in Ashkenazi Jews. N Engl J Med 2006; 354: 424-5.
32. Papkovskaia TD, Chau KY, Inesta-Vaquera F, Papkovsky DB, Healy DG, Nishio K, et al. G2019S leucine-rich repeat kinase 2 causes uncoupling protein-mediated mitochondrial depolarization. Hum Mol Genet 2012; 21: 4201-13.
33. Parker WD Jr, Boyson SJ, Parks JK. Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann Neurol 1989; 26: 719-23.
34. Parry GJ, Rodrigues CM, Aranha MM, Hilbert SJ, Davey C, Kelkar P, et al. Safety, tolerability, and cerebrospinal fluid penetration of ursodeoxycholic acid in patients with amyotrophic lateral sclerosis. Clin Neuropharmacol 2010; 33: 17-21.
35. Ramalho RM, Viana RJ, Low WC, Steer CJ, Rodrigues CM. Bile acids and apoptosis modulation: an emerging role in experimental Alzheimer's disease. Trends Mol Med 2008; 14: 54-62.
36. Rodrigues CM, Sola S, Nan Z, Castro RE, Ribeiro PS, Low WC, et al. Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc Natl Acad Sci USA 2003; 100: 6087-92.
37. Rodriguez-Navarro JA, Rodriguez L, Casarejos MJ, Solano RM, Gomez A, Perucho J, et al. Trehalose ameliorates dopaminergic and tau pathology in parkin deleted/tau overexpressing mice through autophagy activation. Neurobiol Dis 2010; 39: 423-38.
38. Schapira AH. Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol 2008; 7: 97-109.
39. Schapira AH. Targeting mitochondria for neuroprotection in Parkinson's disease. Antioxid Redox Signal 2012; 16: 965-73.
40. Schapira AH, Cooper JM, Dexter D, Jenner P, Clark JB, Marsden CD. Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1989; 1: 1269.
41. Sharma R, Prichard D, Majer F, Byrne AM, Kelleher D, Long A, et al. Ursodeoxycholic acid amides as novel glucocorticoid receptor modulators. J Med Chem 2011; 54: 122-30.
42. Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, Whitworth AJ. Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 2009; 12: 1129-35.
43. Tanaka H, Makino I. Ursodeoxycholic acid-dependent activation of the glucocorticoid receptor. Biochem Biophys Res Commun 1992; 188: 942-8.
44. Timmons S, Coakley MF, Moloney AM, O'Neill C. Akt signal transduction dysfunction in Parkinson's disease. Neurosci Lett 2009; 467: 30-5.
45. Trempe JF, Sauve V, Grenier K, Seirafi M, Tang MY, Menade M, et al. Structure of Parkin reveals mechanisms for ubiquitin ligase activation. Science 2013; 340: 1451-5.
46. Umeda-Kameyama Y, Tsuda M, Ohkura C, Matsuo T, Namba Y, Ohuchi Y, et al. Thioredoxin suppresses Parkin-associated endothelin receptor-like receptor-induced neurotoxicity and extends longevity in Drosophila. J Biol Chem 2007; 282: 11180-7.
47. Ved R, Saha S, Westlund B, Perier C, Burnam L, Sluder A, et al. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J Biol Chem 2005; 280: 42655-68.
48. Vilain S, Esposito G, Haddad D, Schaap O, Dobreva MP, Vos M, et al. The yeast complex I equivalent NADH dehydrogenase rescues pink1 mutants. PLoS Genet 2012; 8: e1002456.
49. Vos M, Esposito G, Edirisinghe JN, Vilain S, Haddad DM, Slabbaert JR, et al. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science 2012; 336: 1306-10.
50. Ward A, Brogden RN, Heel RC, Speight TM, Avery GS. Ursodeoxycholic acid: a review of its pharmacological properties and therapeutic efficacy. Drugs 1984; 27: 95-131.
51. Wilkinson K, Boyd JD, Glicksman M, Moore KJ, El Khoury J. A high content drug screen identifies ursolic acid as an inhibitor of amyloid beta protein interactions with its receptor CD36. J Biol Chem 2011; 286: 34914-22.
52. Yang Y, Gehrke S, Haque ME, Imai Y, Kosek J, Yang L, et al. Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc Natl Acad Sci USA 2005; 102: 13670-5.
53. Yasuda T, Hayakawa H, Nihira T, Ren YR, Nakata Y, Nagai M, et al. Parkin-mediated protection of dopaminergic neurons in a chronic MPTP-minipump mouse model of Parkinson disease. J Neuropathol Exp Neurol 2011; 70: 686-97.
54. Yin MC, Lin MC, Mong MC, Lin CY. Bioavailability, distribution, and antioxidative effects of selected triterpenes in mice. J Agric Food Chem 2012; 60: 7697-701.