Mitochondrial dysfunction in Parkinsonian mesenchymal stem cells impairs differentiation

Redox Biology

Volumn 14, Issue , 2018, Pages 474-484

  Angelova, Plamena R ^a   Barilani, Mario ^b,c   Lovejoy, Christopher ^a   Dossena, Marta ^b   Viganò, Mariele ^b   Seresini, Agostino ^b,d   Piga, Daniela ^c,e   Gandhi, Sonia ^a   Pezzoli, Gianni ^d   Abramov, Andrey Y ^a   Lazzari, Lorenza ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d Fondazione Grigioni per il Morbo di Parkinson   (Italy)

^e Service of Clinical Neurophysiology   (Italy)

Author keywords

Mesenchymal stem cells; Parkinsonism; Progressive supranuclear palsy

Indexed keywords

FAT DROPLET; FATTY ACID BINDING PROTEIN 4; GLUTATHIONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; CELL RESPIRATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; OXIDATIVE STRESS; PARKINSONISM; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN EXPRESSION; CELL CULTURE; MESENCHYMAL STROMA CELL; METABOLISM; MITOCHONDRION; MITOPHAGY; PATHOLOGY;

CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MESENCHYMAL STROMAL CELLS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; NAD; OXIDATIVE STRESS; PARKINSONIAN DISORDERS; REACTIVE OXYGEN SPECIES; SUPRANUCLEAR PALSY, PROGRESSIVE;

EID: 85032264354     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.10.016     Document Type: Article

References (47)

1. Nalls, M.A., Saad, M., Noyce, A.J., Keller, M.F., Schrag, A., Bestwick, J.P., et al. Genetic comorbidities in Parkinson's disease. Hum. Mol. Genet. 23 (2014), 831–841.
2. Klein, C., Westenberger, A., Genetics of Parkinson's disease. Cold Spring Harb. Perspect. Med., 2, 2012, a008888.
3. Jankovic, J., International classification of diseases, tenth revision: neurological adaptation (ICD-10 NA): extrapyramidal and movement disorders. Mov. Disord. 10 (1995), 533–540.
4. Dickson, D.W., Parkinson's disease and parkinsonism: neuropathology. Cold Spring Harb. Perspect. Med., 2012, 2.
5. Karakaya, T., Fusser, F., Prvulovic, D., Hampel, H., Treatment options for tauopathies. Curr. Treat. Options Neurol. 14 (2012), 126–136.
6. Litvan, I., Campbell, G., Mangone, C.A., Verny, M., McKee, A., Chaudhuri, K.R., et al. Which clinical features differentiate progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) from related disorders? A clinicopathological study. Brain 120:Pt 1 (1997), 65–74.
7. Burchell, V.S., Gandhi, S., Deas, E., Wood, N.W., Abramov, A.Y., Plun-Favreau, H., Targeting mitochondrial dysfunction in neurodegenerative disease: Part II. Expert Opin. Ther. Targets 14 (2010), 497–511.
8. Angelova, P.R., Abramov, A.Y., Alpha-synuclein and beta-amyloid - different targets, same players: calcium, free radicals and mitochondria in the mechanism of neurodegeneration. Biochem. Biophys. Res. Commun. 483 (2017), 1110–1115.
9. Tang, C.C., Poston, K.L., Eckert, T., Feigin, A., Frucht, S., Gudesblatt, M., et al. Differential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis. Lancet Neurol. 9 (2010), 149–158.
10. Puig, B., Rey, M.J., Ferrer, I., Individual and regional variations of phospho-tau species in progressive supranuclear palsy. Acta Neuropathol. 110 (2005), 261–268.
11. Kouri, N., Ross, O.A., Dombroski, B., Younkin, C.S., Serie, D.J., Soto-Ortolaza, A., et al. Genome-wide association study of corticobasal degeneration identifies risk variants shared with progressive supranuclear palsy. Nat. Commun., 6, 2015, 7247.
12. Pastor, P., Moreno, F., Clarimon, J., Ruiz, A., Combarros, O., Calero, M., et al. MAPT H1 haplotype is associated with late-onset Alzheimer's disease risk in APOEvarepsilon4 noncarriers: results from the dementia genetics Spanish consortium. J. Alzheimers Dis. 49 (2016), 343–352.
13. Stamelou, M., Reuss, A., Pilatus, U., Magerkurth, J., Niklowitz, P., Eggert, K.M., et al. Short-term effects of coenzyme Q10 in progressive supranuclear palsy: a randomized, placebo-controlled trial. Mov. Disord. 23 (2008), 942–949.
14. Canesi, M., Giordano, R., Lazzari, L., Isalberti, M., Isaias, I.U., Benti, R., et al. Finding a new therapeutic approach for no-option Parkinsonisms: mesenchymal stromal cells for progressive supranuclear palsy. J. Transl. Med., 14, 2016, 127.
15. Angelova, P.R., Abramov, A.Y., Functional role of mitochondrial reactive oxygen species in physiology. Free Radic. Biol. Med. 100 (2016), 81–85.
16. Abramov, A.Y., Smulders-Srinivasan, T.K., Kirby, D.M., Acin-Perez, R., Enriquez, J.A., Lightowlers, R.N., et al. Mechanism of neurodegeneration of neurons with mitochondrial DNA mutations. Brain 133 (2010), 797–807.
17. Berezhnov, A.V., Soutar, M.P., Fedotova, E.I., Frolova, M.S., Plun-Favreau, H., Zinchenko, V.P., et al. Intracellular pH modulates autophagy and mitophagy. J. Biol. Chem. 291 (2016), 8701–8708.
18. Yang, P., Chen, X., Kaushal, S., Reece, E.A., Yang, P., High glucose suppresses embryonic stem cell differentiation into cardiomyocytes: high glucose inhibits ES cell cardiogenesis. Stem Cell Res. Ther., 7, 2016, 187.
19. Takubo, K., Nagamatsu, G., Kobayashi, C.I., Nakamura-Ishizu, A., Kobayashi, H., Ikeda, E., et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12 (2013), 49–61.
20. Katajisto, P., Dohla, J., Chaffer, C.L., Pentinmikko, N., Marjanovic, N., Iqbal, S., et al. Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348 (2015), 340–343.
21. Zhang, Y., Marsboom, G., Toth, P.T., Rehman, J., Mitochondrial respiration regulates adipogenic differentiation of human mesenchymal stem cells. PLoS One, 8, 2013, e77077.
22. Forni, M.F., Peloggia, J., Trudeau, K., Shirihai, O., Kowaltowski, A.J., Murine mesenchymal stem cell commitment to differentiation is regulated by mitochondrial dynamics. Stem Cells 34 (2016), 743–755.
23. Valtieri, M., Sorrentino, A., The mesenchymal stromal cell contribution to homeostasis. J. Cell Physiol. 217 (2008), 296–300.
24. Bossolasco, P., Cova, L., Calzarossa, C., Servida, F., Mencacci, N.E., Onida, F., et al. Metalloproteinase alterations in the bone marrow of ALS patients. J. Mol. Med. (Berl.) 88 (2010), 553–564.
25. Koh, S.H., Baik, W., Noh, M.Y., Cho, G.W., Kim, H.Y., Kim, K.S., et al. The functional deficiency of bone marrow mesenchymal stromal cells in ALS patients is proportional to disease progression rate. Exp. Neurol. 233 (2012), 472–480.
26. Cho, G.W., Noh, M.Y., Kim, H.Y., Koh, S.H., Kim, K.S., Kim, S.H., Bone marrow-derived stromal cells from amyotrophic lateral sclerosis patients have diminished stem cell capacity. Stem Cells Dev. 19 (2010), 1035–1042.
27. Sarkar, P., Cole, A., Scolding, N.J., Rice, C.M., Percutaneous endoscopic gastrostomy tube insertion in neurodegenerative disease: a retrospective study and literature review. Clin. Endosc. 50 (2017), 270–278.
28. Moon, H.E., Yoon, S.H., Hur, Y.S., Park, H.W., Ha, J.Y., Kim, K.H., et al. Mitochondrial dysfunction of immortalized human adipose tissue-derived mesenchymal stromal cells from patients with Parkinson's disease. Exp. Neurobiol. 22 (2013), 283–300.
29. Giordano, R., Canesi, M., Isalberti, M., Isaias, I.U., Montemurro, T., Vigano, M., et al. Autologous mesenchymal stem cell therapy for progressive supranuclear palsy: translation into a phase I controlled, randomized clinical study. J. Transl. Med., 12, 2014, 14.
30. Swerdlow, R.H., Golbe, L.I., Parks, J.K., Cassarino, D.S., Binder, D.R., Grawey, A.E., et al. Mitochondrial dysfunction in cybrid lines expressing mitochondrial genes from patients with progressive supranuclear palsy. J. Neurochem. 75 (2000), 1681–1684.
31. Acin-Perez, R., Carrascoso, I., Baixauli, F., Roche-Molina, M., Latorre-Pellicer, A., Fernandez-Silva, P., et al. ROS-triggered phosphorylation of complex II by Fgr kinase regulates cellular adaptation to fuel use. Cell Metab. 19 (2014), 1020–1033.
32. Cardol, P., Matagne, R.F., Remacle, C., Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J. Mol. Biol. 319 (2002), 1211–1221.
33. Fan, W., Waymire, K.G., Narula, N., Li, P., Rocher, C., Coskun, P.E., et al. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319 (2008), 958–962.
34. Kruse, S.E., Watt, W.C., Marcinek, D.J., Kapur, R.P., Schenkman, K.A., Palmiter, R.D., Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 7 (2008), 312–320.
35. Pitkanen, S., Robinson, B.H., Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Investig. 98 (1996), 345–351.
36. Murphy, M.P., Modulating mitochondrial intracellular location as a redox signal. Sci. Signal., 5, 2012, e39.
37. Angelova, P.R., Kasymov, V., Christie, I., Sheikhbahaei, S., Turovsky, E., Marina, N., Korsak, A., Zwicker, J., Teschemacher, A.G., et al. Functional oxygen sensitivity of astrocytes. J. Neurosci. 22 (2015), 10460–10473.
38. Hu, L., Wang, H., Huang, L., Zhao, Y., Wang, J., The protective roles of ROS-mediated mitophagy on 125I seeds radiation induced cell death in HCT116 cells. Oxid Med. Cell Longev., 2016, 2016, 9460462.
39. Rubinstein, A.D., Kimchi, A., Life in the balance - a mechanistic view of the crosstalk between autophagy and apoptosis. J. Cell Sci. 125 (2012), 5259–5268.
40. Frank, M., Duvezin-Caubet, S., Koob, S., Occhipinti, A., Jagasia, R., Petcherski, A., et al. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim. Biophys. Acta 1823 (2012), 2297–2310.
41. Scherz-Shouval, R., Elazar, Z., Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 36 (2011), 30–38.
42. Wei, X., Qi, Y., Zhang, X., Qiu, Q., Gu, X., Tao, C., et al. Cadmium induces mitophagy through ROS-mediated PINK1/Parkin pathway. Toxicol. Mech. Methods 24 (2014), 504–511.
43. Li, B., Duan, P., Li, C., Jing, Y., Han, X., Yan, W., et al. Role of autophagy on bone marrow mesenchymal stemcell proliferation and differentiation into neurons. Mol. Med. Rep. 13 (2016), 1413–1419.
44. Albers, D.S., Swerdlow, R.H., Manfredi, G., Gajewski, C., Yang, L., Parker, W.D. Jr., et al. Further evidence for mitochondrial dysfunction in progressive supranuclear palsy. Exp. Neurol. 168 (2001), 196–198.
45. Chirichigno, J.W., Manfredi, G., Beal, M.F., Albers, D.S., Stress-induced mitochondrial depolarization and oxidative damage in PSP cybrids. Brain Res. 951 (2002), 31–35.
46. Bartolome, F., Abramov, A.Y., Measurement of mitochondrial NADH and FAD autofluorescence in live cells. Methods Mol. Biol. 1264 (2015), 263–270.
47. Deas, E., Cremades, N., Angelova, P.R., Ludtmann, M.H., Yao, Z., Chen, S., et al. Alpha-synuclein oligomers interact with metal ions to induce oxidative stress and neuronal death in parkinson's disease. Antioxid. Redox Signal. 24 (2016), 376–391.