Neuroprotective effects of human mesenchymal stem cells on neural cultures exposed to 6-hydroxydopamine: Implications for reparative therapy in Parkinson's disease

Apoptosis

Volumn 17, Issue 3, 2012, Pages 289-304

  Cova, Lidia ^a   Bossolasco, Patrizia ^b   Armentero, Marie Therese ^c   Diana, Valentina ^a   Zennaro, Eleonora ^a   Mellone, Manuela ^a   Calzarossa, Cinzia ^a,b   Cerri, Silvia ^c   Lambertenghi Deliliers, Giorgio ^b   Polli, Elio ^b   Blandini, Fabio ^c   Silani, Vincenzo ^a,b  

^a ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

Cell therapy; Cytokines; Dopamine transporter; Neural stem cells; Neurorescue

Indexed keywords

CASPASE 3; CASPASE 7; OXIDOPAMINE; REACTIVE OXYGEN METABOLITE; DOPAMINE TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MESENCHYMAL STEM CELL; MOUSE; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PLASTIC SURGERY; PRIORITY JOURNAL; ANIMAL; CELL DIFFERENTIATION; CELL SURVIVAL; COCULTURE; CYTOLOGY; DRUG EFFECT; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; RAT;

MURINAE;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; NEURAL STEM CELLS; OXIDOPAMINE; PARKINSON DISEASE; RATS;

EID: 84862272787     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-011-0679-9     Document Type: Article

References (58)

1. Shulman JM, De Jager PL, Feany MB (2011) Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol 6:193-222
2. Venda LL, Cragg SJ, Buchman VL, Wade-Martins R (2010) alpha-Synuclein and dopamine at the crossroads of Parkinson's disease. Trends Neurosci 33:559-568
3. Allan LE, Petit GH, Brundin P (2010) Cell transplantation in Parkinson's disease: problems and perspectives. Curr Opin Neurol 23:426-432
4. Arenas E (2010) Towards stem cell replacement therapies for Parkinson's disease. Biochem Biophys Res Commun 396:152-156
5. Kim HJ (2011) Stem cell potential in Parkinson's disease and molecular factors for the generation of dopamine neurons. Biochim Biophys Acta 1812:1-11
6. Cova L, Armentero MT, Zennaro E, Calzarossa C, Bossolasco P et al (2010) Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson's disease. Brain Res 1311:12-27
7. Zou Z, Zhang Y, Hao L, Wang F, Liu D et al (2010) More insight into mesenchymal stem cells and their effects inside the body. Expert Opin Biol Ther 10(2):215-230
8. Garcia-Gomez I, Elvira G, Zapata AG, Lamana ML, Ramirez M et al (2010) Mesenchymal stem cells: biological properties and clinical applications. Expert Opin Biol Ther 10:1453-1468
9. Myers TJ, Granero-Molto F, Longobardi L, Li T, Yan Y et al (2010) Mesenchymal stem cells at the intersection of cell and gene therapy. Expert Opin Biol Ther 10:1663-1679
10. Dezawa M (2008) Systematic neuronal and muscle induction systems in bone marrow stromal cells: the potential for tissue reconstruction in neurodegenerative and muscle degenerative diseases. Med Mol Morphol 41:14-19
11. Moloney TC, Rooney GE, Barry FP, Howard L, Dowd E (2010) Potential of rat bone marrow-derived mesenchymal stem cells as vehicles for delivery of neurotrophins to the Parkinsonian rat brain. Brain Res 1359:33-43
12. Blandini F, Cova L, Armentero MT, Zennaro E, Levandis G et al (2010) Transplantation of undifferentiated human mesenchymal stem cells protects against 6-hydroxydopamine neurotoxicity in the rat. Cell Transplant 19:203-217
13. Bouchez G, Sensebe L, Vourc'h P, Garreau L, Bodard S et al (2008) Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease. Neurochem Int 52:1332-1342
14. Danielyan L, Schafer R, von Ameln-Mayerhofer A, Bernhard F, Verleysdonk S et al (2011) Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of Parkinson disease. Rejuvenation Res 14:3-16
15. Delcroix GJ, Garbayo E, Sindji L, Thomas O, Vanpouille-Box C et al (2011) The therapeutic potential of human multipotent mesenchymal stromal cells combined with pharmacologically active microcarriers transplanted in hemi-parkinsonian rats. Biomaterials 32:1560-1573
16. Shetty P, Ravindran G, Sarang S, Thakur AM, Rao HS et al (2009) Clinical grade mesenchymal stem cells transdifferentiated under xenofree conditions alleviates motor deficiencies in a rat model of Parkinson's disease. Cell Biol Int 33:830-838
17. Somoza R, Juri C, Baes M, Wyneken U, Rubio FJ (2010) Intranigral transplantation of epigenetically induced BDNF-secreting human mesenchymal stem cells: implications for cell-based therapies in Parkinson's disease. Biol Blood Marrow Transplant 16:1530-1540
18. Thomas MG, Stone L, Evill L, Ong S, Ziman M et al (2011) Bone marrow stromal cells as replacement cells for Parkinson's disease: generation of an anatomical but not functional neuronal phenotype. Transl Res 157:56-63
19. Wang F, Yasuhara T, Shingo T, Kameda M, Tajiri N et al (2010) Intravenous administration of mesenchymal stem cells exerts therapeutic effects on parkinsonian model of rats: focusing on neuroprotective effects of stromal cell-derived factor-1alpha. BMC Neurosci 11:52
20. Ljungdahl A, Hokfelt T, Jonsson G, Sachs C (1971) Autoradiographic demonstration of uptake and accumulation of 3H-6-hydroxydopamine in adrenergic nerves. Experientia 27:297-299
21. Blum D, Torch S, Nissou MF, Benabid AL, Verna JM (2000) Extracellular toxicity of 6-hydroxydopamine on PC12 cells. Neurosci Lett 283:193-196 (Pubitemid 30168965)
22. Soto-Otero R, Mendez-Alvarez E, Hermida-Ameijeiras A, Munoz-Patino AM, Labandeira-Garcia JL (2000) Autoxidation and neurotoxicity of 6-hydroxydopamine in the presence of some antioxidants: potential implication in relation to the pathogenesis of Parkinson's disease. J Neurochem 74:1605-1612 (Pubitemid 30163982)
23. Blum D, Torch S, Lambeng N, Nissou M, Benabid AL et al (2001) Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 65:135-172 (Pubitemid 32524182)
24. Hanrott K, Gudmunsen L, O'Neill MJ, Wonnacott S (2006) 6-Hydroxydopamine-induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cdelta. J Biol Chem 281:5373-5382 (Pubitemid 43847631)
25. Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L et al (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19:3287-3297 (Pubitemid 29203108)
26. Redman PT, Jefferson BS, Ziegler CB, Mortensen OV, Torres GE et al (2006) A vital role for voltage-dependent potassium channels in dopamine transporter-mediated 6-hydroxydopamine neurotoxicity. Neuroscience 143:1-6 (Pubitemid 44667319)
27. Storch A, Ludolph AC, Schwarz J (2004) Dopamine transporter: involvement in selective dopaminergic neurotoxicity and degeneration. J Neural Transm 111:1267-1286 (Pubitemid 39468390)
28. Bossolasco P, Cova L, Calzarossa C, Servida F, Mencacci NE et al (2010) Metalloproteinase alterations in the bone marrow of ALS patients. J Mol Med 88:553-564
29. Kelly TK, Karsten SL, Geschwind DH, Kornblum HI (2009) Cell lineage and regional identity of cultured spinal cord neural stem cells and comparison to brain-derived neural stemcells. PLoS One 4:e4213
30. Manakova S, Puttonen KA, Raasmaja A, Mannisto PT (2004) The roles of dopamine transporter and Bcl-2 protein in the protection of CV1-P cells from 6-OHDA-induced toxicity. Toxicol Lett 154:117-123 (Pubitemid 39314595)
31. Lan F, Xu J, Zhang X, Wong VW, Li X et al (2008) Hepatocyte growth factor promotes proliferation and migration in immortalized progenitor cells. Neuroreport 19:765-769 (Pubitemid 351555987)
32. Yasuhara T, Shingo T, Muraoka K, Kameda M, Agari T et al (2005) Neurorescue effects of VEGF on a rat model of Parkinson's disease. Brain Res 1053:10-18 (Pubitemid 41116785)
33. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317 (Pubitemid 44269669)
34. Al-Jarrah M, Jamous M, Al Zailaey K, Bweir SO (2010) Endurance exercise training promotes angiogenesis in the brain of chronic/progressive mouse model of Parkinson's Disease. NeuroRehabilitation 26:369-373
35. Tian YY, Tang CJ, Wang JN, Feng Y, Chen XW et al (2007) Favorable effects of VEGF gene transfer on a rat model of Parkinson disease using adeno-associated viral vectors. Neurosci Lett 421:239-244 (Pubitemid 46935363)
36. Blandini F, Levandis G, Bazzini E, Nappi G, Armentero MT (2007) Time-course of nigrostriatal damage, basal ganglia metabolic changes and behavioural alterations following intrastriatal injection of 6-hydroxydopamine in the rat: new clues from an old model. Eur J Neurosci 25:397-405
37. Mignini F, Traini E, Tomassoni D, Amenta F (2006) Dopamine plasma membrane transporter (DAT) in rat thymus and spleen: an immunochemical and immunohistochemical study. Auton Autacoid Pharmacol 26:183-189
38. Moe MC, Westerlund U, Varghese M, Berg-Johnsen J, Svensson M et al (2005) Development of neuronal networks from single stem cells harvested from the adult human brain. Neurosurgery 56:1182-1188 discussion 1188-1190
39. Salim K, Guest PC, Skynner HA, Bilsland JG, Bonnert TP et al (2007) Identification of proteomic changes during differentiation of adult mouse subventricular zone progenitor cells. Stem Cells Dev 16:143-165 (Pubitemid 46362599)
40. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH et al (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726-735 (Pubitemid 38859057)
41. Saito Y, Nishio K, Ogawa Y, Kinumi T, Yoshida Y et al (2007) Molecular mechanisms of 6-hydroxydopamine-induced cytotoxicity in PC12 cells: involvement of hydrogen peroxide-dependent and -independent action. Free Radic Biol Med 42:675-685 (Pubitemid 46205147)
42. Jiang Y, Pei L, Li S, Wang M, Liu F (2008) Extracellular dopamine induces the oxidative toxicity of SH-SY5Y cells. Synapse 62:797-803
43. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J et al (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8:59-71
44. Hardy SA, Maltman DJ, Przyborski SA (2008) Mesenchymal stem cells as mediators of neural differentiation. Curr Stem Cell Res Ther 3:43-52 (Pubitemid 352024866)
45. Nagatsu T, Mogi M, Ichinose H, Togari A (2000) Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm Suppl 277-290 (Pubitemid 32037200)
46. Nagatsu T, Sawada M (2007) Biochemistry of postmortem brains in Parkinson's disease: historical overview and future prospects. J Neural Transm Suppl 113-120
47. Chalovich EM, Zhu JH, Caltagarone J, Bowser R, Chu CT (2006) Functional repression of cAMP response element in 6-hydroxydopamine- treated neuronal cells. J Biol Chem 281:17870-17881 (Pubitemid 44035586)
48. Nandhu MS, Paul J, Kuruvilla KP, Malat A, Romeo C et al (2011) Enhanced glutamate, IP3 and cAMP activity in the cerebral cortex of unilateral 6-hydroxydopamine induced Parkinson's rats: effect of 5-HT, GABA and bone marrow cell supplementation. J Biomed Sci 18:5
49. Takeuchi H, Natsume A, Wakabayashi T, Aoshima C, Shimato S et al (2007) Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci Lett 426:69-74 (Pubitemid 47464707)
50. Koike H, Ishida A, Shimamura M, Mizuno S, Nakamura T et al (2006) Prevention of onset of Parkinson's disease by in vivo gene transfer of human hepatocyte growth factor in rodent model: a model of gene therapy for Parkinson's disease. Gene Ther 13:1639-1644 (Pubitemid 44774208)
51. Hu ZX, Geng JM, Liang DM, Luo M, Li ML (2010) Hepatocyte growth factor protects human embryonic stem cell derived-neural progenitors from hydrogen peroxide-induced apoptosis. Eur J Pharmacol 645:23-31
52. Yasuhara T, Shingo T, Muraoka K, wen Ji Y, Kameda M et al (2005) The differences between high and low-dose administration of VEGF to dopaminergic neurons of in vitro and in vivo Parkinson's disease model. Brain Res 1038:1-10 (Pubitemid 40340955)
53. Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98:1076-1084 (Pubitemid 44128350)
54. Bai L, Caplan A, Lennon D, Miller RH (2007) Human mesenchymal stem cells signals regulate neural stem cell fate. Neurochem Res 32:353-362 (Pubitemid 46238881)
55. Rodriguez-Pallares J, Parga JA, Munoz A, Rey P, Guerra MJ et al (2007) Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine- induced degeneration of dopaminergic neurons. J Neurochem 103:145-156 (Pubitemid 47404195)
56. Isele NB, Lee HS, Landshamer S, Straube A, Padovan CS et al (2006) Bone marrow stromal cells mediate protection through stimulation of PI3-K/Akt and MAPK signaling in neurons. Neurochem Int 50:243-250
57. Habisch HJ, Liebau S, Lenk T, Ludolph AC, Brenner R et al (2010) Neuroectodermally converted human mesenchymal stromal cells provide cytoprotective effects on neural stem cells and inhibit their glial differentiation. Cytotherapy 12:491-504
58. Adler MW, Geller EB, Chen X, Rogers TJ (2005) Viewing chemokines as a third major system of communication in the brain. Aaps J 7:E865-E870