Intracarotid infusion of mesenchymal stem cells in an animal model of Parkinson’s disease, focusing on cell distribution and neuroprotective and behavioral effects

Stem Cells Translational Medicine

Volumn 4, Issue 9, 2015, Pages 1073-1085

  Cerri, Silvia ^a   Greco, Rosaria ^b   Levandis, Giovanna ^a   Ghezzi, Cristina ^a   Mangione, Antonina Stefania ^b   Fuzzati Armentero, Marie Therese ^a   Bonizzi, Arianna ^a   Avanzini, Maria Antonietta ^c   Maccario, Rita ^c   Blandini, Fabio ^a  

^a Center for Research in Neurodegenerative Diseases   (Italy)

^b C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

Behavioral analyses; Intracarotid infusion; Mannitol; Mesenchymal stem cells; Neuroprotection; Parkinson s disease

Indexed keywords

EVANS BLUE; MANNITOL; OXIDOPAMINE; PROTEIN C FOS; APOMORPHINE; DOPAMINE RECEPTOR STIMULATING AGENT;

AKINESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; CAROTID ARTERY SURGERY; CELL SURVIVAL; CELLULAR DISTRIBUTION; CIRCLING BEHAVIOR; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; EXPERIMENTAL EXTRAVASATION; HEMISPHERE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INFUSION; MALE; MEMBRANE PERMEABILITY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR DYSFUNCTION; NEAR INFRARED IMAGING SYSTEM; NERVE DEGENERATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; RAT; ANIMAL; ANIMAL BEHAVIOR; CAROTID ARTERY; CELL COUNT; CELL TRACKING; CHEMICALLY INDUCED; CORPUS STRIATUM; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; INTRAARTERIAL DRUG ADMINISTRATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MESENCHYMAL STROMA CELL; NERVE CELL; OSMOLARITY; PARKINSON DISEASE, SECONDARY; PATHOLOGY; PATHOPHYSIOLOGY; PERMEABILITY; PHYSIOLOGY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; APOMORPHINE; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; CAROTID ARTERIES; CELL COUNT; CELL TRACKING; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; INJECTIONS, INTRA-ARTERIAL; INJECTIONS, INTRAVENTRICULAR; MALE; MANNITOL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEURONS; OSMOLAR CONCENTRATION; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; PERMEABILITY; RATS; RATS, WISTAR;

EID: 84940099431     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0023     Document Type: Article

References (94)

1. Defer GL, Geny C, Ricolfi F et al. Long-term outcome of unilaterally transplanted parkinsonian patients. I. Clinicalapproach. Brain1996; 119: 41-50.
2. Freed CR, Breeze RE, Rosenberg NL et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease. N Engl J Med 1992; 327: 1549-1555.
3. Lindvall O, Brundin P, Widner H et al. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 1990; 247: 574-577.
4. Madrazo I, León V, Torres C et al. Transplantation of fetal substantia nigra and adrenal medulla to the caudate nucleus in two patients with Parkinson's disease. N Engl J Med 1988; 318: 51.
5. BjörklundLM, Sánchez-PernauteR, Chung S et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 2002; 99: 2344-2349.
6. Cho YH, Kim DS, Kim PG et al. Dopamine neurons derived from embryonic stem cells efficiently induce behavioral recovery in a Parkinsonian rat model. Biochem Biophys Res Commun 2006; 341: 6-12.
7. Takagi Y, Takahashi J, SaikiHet al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 2005; 115: 102-109.
8. Snyder BJ, Olanow CW. Stem cell treatment for Parkinson's disease: An update for 2005. Curr Opin Neurol 2005; 18: 376-385.
9. Hargus G, Cooper O, DeleidiMet al. Differentiated Parkinson patient-derived induced pluripotent stem cells grow in the adult rodent brain and reduce motor asymmetry in Parkinsonian rats. Proc Natl Acad Sci USA 2010; 107: 15921-15926.
10. Rhee YH, Ko JY, Chang MY et al. Proteinbased human iPS cells efficiently generate functional dopamine neurons and can treat a rat model of Parkinson disease. J Clin Invest 2011; 121: 2326-2335.
11. Wernig M, Zhao JP, Pruszak J et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci USA 2008; 105: 5856-5861.
12. Ahmed H, Salem A, Atta H et al. Do adipose tissue-derived mesenchymal stem cells ameliorate Parkinson's disease in rat model? Hum Exp Toxicol 2014; 33: 1217-1231.
13. Berg J, Roch M, Altschüler J et al. Human adipose-derived mesenchymal stem cells improve motor functions and are neuroprotective in the 6-hydroxydopamine-rat model for Parkinson's disease when cultured in monolayer cultures but suppress hippocampal neurogenesis and hippocampal memory function when cultured in spheroids. Stem Cell Rev 2015; 11: 133-149.
14. Blandini F, Cova L, Armentero MT et al. Transplantation of undifferentiated human mesenchymal stem cells protects against 6-hydroxydopamine neurotoxicity in the rat. Cell Transplant 2010; 19: 203-217.
15. Bouchez G, Sensebé L, Vourc'h P et al. Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease. Neurochem Int 2008; 52: 1332-1342.
16. Capitelli CS, Lopes CS, Alves AC et al. Opposite effects of bone marrow-derived cells transplantation in MPTP-rat model of Parkinson's disease: A comparison study of mononuclear and mesenchymal stem cells. Int J Med Sci 2014; 11: 1049-1064.
17. Chao YX, He BP, Tay SS. Mesenchymal stem cell transplantation attenuates blood brain barrier damage and neuroinflammation and protects dopaminergic neurons against MPTP toxicity in the substantia nigra in a model of Parkinson's disease. J Neuroimmunol 2009; 216: 39-50.
18. Kim YJ, Park HJ, Lee G et al. Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through antiinflammatory action. Glia 2009; 57: 13-23.
19. Park HJ, Lee PH, Bang OYet al. Mesenchymal stem cells therapy exerts neuroprotection in a progressive animal model of Parkinson's disease. J Neurochem 2008; 107: 141-151.
20. Park HJ, Shin JY, Kim HN et al. Neuroprotective effects of mesenchymal stem cells through autophagy modulation in a parkinsonian model. Neurobiol Aging 2014; 35: 1920-1928.
21. Sadan O, Bahat-Stromza M, Barhum Y et al. Protective effects of neurotrophic factor-secreting cells in a 6-OHDA rat model of Parkinson disease. Stem Cells Dev 2009; 18: 1179-1190.
22. Suzuki S, Kawamata J, Iwahara N et al. Intravenous mesenchymal stem cell administration exhibits therapeutic effects against 6-hydroxydopamine-induced dopaminergic neurodegeneration and glial activation in rats. Neurosci Lett 2015; 584: 276-281.
23. Krampera M, Pasini A, Pizzolo G et al. Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr Opin Pharmacol 2006; 6: 435-441.
24. Barkholt L, Flory E, Jekerle V et al. Risk of tumorigenicity in mesenchymal stromal cellbased therapies-bridging scientific observations and regulatory viewpoints. Cytotherapy 2013; 15: 753-759.
25. Bernardo ME, Zaffaroni N, Novara F et al. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 2007; 67: 9142-9149.
26. Choumerianou DM, Dimitriou H, Perdikogianni C et al. Study of oncogenic transformationin exvivoexpandedmesenchymal cells, from paediatric bone marrow. Cell Prolif 2008; 41: 909-922.
27. de Girolamo L, Lucarelli E, Alessandri G et al. Mesenchymal stem/stromal cells: A new "cells as drugs" paradigm. Efficacy and critical aspects in cell therapy. Curr Pharm Des 2013; 19: 2459-2473.
28. von Bahr L, Batsis I, Moll G et al. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. STEM CELLS 2012; 30: 1575-1578.
29. Cova L, Armentero MT, Zennaro E et al. Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson's disease. Brain Res 2010; 1311: 12-27.
30. Crigler L, Robey RC, Asawachaicharn A et al. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 2006; 198: 54-64.
31. Kan I, Barhum Y, Melamed E et al. Mesenchymal stem cells stimulate endogenous neurogenesis in the subventricular zone of adult mice. Stem Cell Rev 2011; 7: 404-412.
32. Paul G, Anisimov SV. The secretome of mesenchymal stem cells: potential implications for neuroregeneration. Biochimie 2013; 95: 2246-2256.
33. Shi Y, Su J, Roberts AI et al. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol 2012; 33: 136-143.
34. Tfilin M, Sudai E, Merenlender A et al. Mesenchymal stem cells increase hippocampal neurogenesis and counteract depressive-like behavior. Mol Psychiatry 2010; 15: 1164-1175.
35. Venkataramana NK, Kumar SK, Balaraju S et al. Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson's disease. Transl Res 2010; 155: 62-70.
36. Venkataramana NK, Pal R, Rao SA et al. Bilateral transplantation of allogenic adult human bone marrow-derived mesenchymal stem cells into the subventricular zone of Parkinson's disease: A pilot clinical study. Stem Cells Int 2012; 2012: 931902.
37. Lee PH, Kim JW, Bang OY et al. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin Pharmacol Ther 2008; 83: 723-730.
38. Lee PH, Lee JE, Kim HSet al. Arandomized trial of mesenchymal stem cells in multiple system atrophy. Ann Neurol 2012; 72: 32-40.
39. Brazzini A, Cantella R, De la Cruz A et al. Intraarterial autologous implantation of adult stem cells for patients with Parkinson disease. J Vasc Interv Radiol 2010; 21: 443-451.
40. Carvey PM, Zhao CH, Hendey B et al. 6-Hydroxydopamine-induced alterations in blood-brain barrier permeability. Eur J Neurosci 2005; 22: 1158-1168.
41. Kortekaas R, Leenders KL, van Oostrom JC et al. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. AnnNeurol 2005; 57: 176-179.
42. Pisani V, Stefani A, Pierantozzi M et al. Increased blood-cerebrospinal fluid transfer of albumin in advanced Parkinson's disease. J Neuroinflammation 2012; 9: 188.
43. Bellavance MA, Blanchette M, Fortin D. Recent advances in blood-brain barrier disruption as a CNS delivery strategy. AAPS J 2008; 10: 166-177.
44. Seyfried DM, Han Y, Yang D et al. Mannitol enhances delivery of marrow stromal cells to the brain after experimental intracerebral hemorrhage. Brain Res 2008; 1224: 12-19.
45. Okuma Y, Wang F, Toyoshima A et al. Mannitol enhances therapeutic effects of intra-arterial transplantation of mesenchymal stem cells into the brain after traumatic brain injury. Neurosci Lett 2013; 554: 156-161.
46. Blandini F, Levandis G, Bazzini E et al. 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 2007; 25: 397-405.
47. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 7th ed. San Diego, CA: Academic Press, 1998.
48. Colaianna M, Tucci P, Zotti M et al. Soluble beta amyloid(1-42): A critical player in producing behavioural and biochemical changes evoking depressive-related state? Br J Pharmacol 2010; 159: 1704-1715.
49. Rapoport SI, Fredericks WR, Ohno K et al. Quantitative aspects of reversible osmotic opening of the blood-brain barrier. AmJ Physiol 1980; 238: R421-R431.
50. Cosolo WC, Martinello P, Louis WJ et al. Blood-brain barrier disruption using mannitol: time course and electron microscopy studies. Am J Physiol 1989; 256: R443-R447.
51. Blanchette M, Fortin D. Blood-brain barrier disruption in the treatment of brain tumors. Methods Mol Biol 2011; 686: 447-463.
52. Al-Mehdi AB, Patel M, Haroon A et al. Increased depth of cellular imaging in the intact lung using far red and near infrared fluorescent probes. Int J Biomed Imag 2006; 2006: 37470.
53. Bossolasco P, Cova L, Levandis G et al. Noninvasive near-infrared live imaging of human adult mesenchymal stem cells transplanted in a rodent model of Parkinson's disease. Int J Nanomedicine 2012; 7: 435-447.
54. Hanabusa K, Nagaya N, Iwase T et al. Adrenomedullin enhances therapeutic potency of mesenchymal stem cells after experimental stroke in rats. Stroke 2005; 36: 853-858.
55. Lehner T, Mitchell E, Bergmeier L et al. The role of gammadelta T cells in generating antiviral factors and beta-chemokines in protection against mucosal simian immunodeficiency virus infection. Eur J Immunol 2000; 30: 2245-2256.
56. Morigi M, Rota C, Montemurro T et al. Life-sparing effect of human cord bloodmesenchymal stem cells in experimental acute kidney injury. STEM CELLS 2010; 28: 513-522.
57. Wallace PK, Muirhead KA. Cell tracking 2007: A proliferation of probes and applications. Immunol Invest 2007; 36: 527-561.
58. Olsson M, Nikkhah G, Bentlage C et al. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 1995; 15: 3863-3875.
59. Tassorelli C, ArmenteroMT, GrecoRet al. Behavioral responses and Fos activation following painful stimuli in a rodent model of Parkinson's disease. Brain Res 2007; 1176: 53-61.
60. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991; 231: 482-497.
61. Kholodenko IV, Konieva AA, Kholodenko RV et al. Molecular mechanisms of migration and homing of intravenously transplanted mesenchymal stem cells. J Regen Med Tissue Eng 2013.
62. Shawkat H, Westwood MM, Mortimer A. Mannitol: a review of its clinical uses. Contin Educ Anaesth Crit Care Pain 2012; 2: 82-85.
63. Chapel A, Bertho JM, Bensidhoum M et al. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med 2003; 5: 1028-1038.
64. Chavakis E, Urbich C, Dimmeler S. Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 2008; 45: 514-522.
65. Shen LH, Li Y, Chen J et al. Therapeutic benefit of bone marrow stromal cells administered 1. month after stroke. J Cereb Blood Flow Metab 2007; 27: 6-13.
66. Gutiérrez-FernándezM, Rodríguez-Frutos B, Alvarez-Grech J et al. Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience 2011; 175: 394-405.
67. Lu SS, Liu S, Zu QQ et al. In vivo MR imaging of intraarterially delivered magnetically labeled mesenchymal stem cells in a canine stroke model. PLoS One 2013; 8: e54963.
68. Ruan GP, Han YB, WangTH et al. Comparative study among three different methods of bone marrow mesenchymal stem cell transplantation following cerebral infarction in rats. Neurol Res 2013; 35: 212-220.
69. Pavlichenko N, Sokolova I, Vijde S et al. Mesenchymal stem cells transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res 2008; 1233: 203-213.
70. Hoehn M, Küstermann E, Blunk J et al. Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci USA 2002; 99: 16267-16272.
71. Jackson JS, Golding JP, Chapon C et al. Homing of stem cells to sites of inflammatory brain injury after intracerebral and intravenous administration: A longitudinal imaging study. Stem Cell Res Ther 2010; 1: 17.
72. Modo M, Mellodew K, Cash D et al. Mapping transplanted stem cell migration after a stroke: a serial, in vivo magnetic resonance imaging study. Neuroimage 2004; 21: 311-317.
73. Walczak P, Zhang J, Gilad AA et al. Dualmodality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 2008; 39: 1569-1574.
74. SpringerTA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994; 76: 301-314.
75. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003; 108: 863-868.
76. Kraitchman DL, Tatsumi M, Gilson WD et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 2005; 112: 1451-1461.
77. Deak E, Seifried E, Henschler R. Homing pathways of mesenchymal stromal cells (MSCs) and their role in clinical applications. Int Rev Immunol 2010; 29: 514-529.
78. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009; 5: 54-63.
79. Levy YS, Bahat-Stroomza M, Barzilay R et al. Regenerative effect of neural-induced humanmesenchymal stromal cells in rat models of Parkinson's disease. Cytotherapy 2008; 10: 340-352.
80. Lu L, Zhao C, Liu Y et al. Therapeutic benefit of TH-engineered mesenchymal stem cells for Parkinson's disease. Brain Res Brain Res Protoc 2005; 15: 46-51.
81. Yan M, Sun M, Zhou Y et al. Conversion of human umbilical cord mesenchymal stem cells in Wharton's jelly to dopamine neurons mediated by the Lmx1a and neurturin in vitro: potential therapeutic application for Parkinson's disease in a rhesus monkey model. PLoS One 2013; 8: e64000.
82. Park S, Kim E, Koh SE et al. Dopaminergic differentiation of neural progenitors derived from placental mesenchymal stem cells in the brains of Parkinson's disease model rats and alleviation of asymmetric rotational behavior. Brain Res 2012; 1466: 158-166.
83. Schwarting RK, Huston JP. The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog Neurobiol 1996; 50: 275-331.
84. Labandeira-Garcia JL, Rozas G, Lopez-Martin E et al. Time course of striatal changes induced by 6-hydroxydopamine lesion of the nigrostriatal pathway, as studied by combined evaluation of rotational behaviour and striatal Fos expression. Exp Brain Res 1996; 108: 69-84.
85. Harper MM, Grozdanic SD, Blits B et al. Transplantation of BDNF-secreting mesenchymal stem cells provides neuroprotection in chronically hypertensive rat eyes. Invest Ophthalmol Vis Sci 2011; 52: 4506-4515.
86. Zhao HB, Ma H, Ha XQ et al. Salidroside induces rat mesenchymal stem cells to differentiate into dopaminergic neurons. Cell Biol Int 2014; 38: 462-471.
87. Park H, Poo MM. Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 2013; 14: 7-23.
88. McGinty JF, Bache AJ, Coleman NT et al. The role of BDNF/TrkB signaling in acute amphetamine-induced locomotor activity and opioid peptide gene expression in the rat dorsal striatum. Front Syst Neurosci 2011; 5: 60.
89. Klein RL, LewisMH, MuzyczkaN et al. Prevention of 6-hydroxydopamine-induced rotational behavior by BDNF somatic gene transfer. Brain Res 1999; 847: 314-320.
90. SunM, Kong L, WangX et al. Comparisonof the capability of GDNF, BDNF, or both, to protect nigrostriatal neurons in a ratmodel of Parkinson's disease. Brain Res 2005; 1052: 119-129.
91. Lee CS, Sauer H, Bjorklund A. Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by instrastriatal 6-hydroxydopamine in the rat. Neuroscience 1996; 72: 641-653.
92. Löscher W, Richter A, NikkhahG et al. Behavioral and neurochemical dysfunction in the circling (ci) rat: a novel genetic animal model of a movement disorder. Neuroscience 1996; 74: 1135-1142.
93. Metz GA, Whishaw IQ. Drug-induced rotation intensity in unilateral dopaminedepleted rats is not correlated with end point or qualitative measures of forelimb or hindlimb motor performance. Neuroscience 2002; 111: 325-336.
94. Whishaw IQ, O'ConnorWT, Dunnett SB. The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain 1986; 109: 805-843.