Menu

Transplantation in the nonhuman primate MPTP model of Parkinson’s disease: update and perspectives

Abstract

In order to calibrate stem cell exploitation for cellular therapy in neurodegenerative diseases, fundamental and preclinical research in NHP (nonhuman primate) models is crucial. Indeed, it is consensually recognized that it is not possible to directly extrapolate results obtained in rodent models to human patients. A large diversity of neurological pathologies should benefit from cellular therapy based on neural differentiation of stem cells. In the context of this special issue of Primate Biology on NHP stem cells, we describe past and recent advances on cell replacement in the NHP model of Parkinson’s disease (PD). From the different grafting procedures to the various cell types transplanted, we review here diverse approaches for cell-replacement therapy and their related therapeutic potential on behavior and function in the NHP model of PD.

Authors: Florence Wianny, Julien Vezoli

Affiliations: Univ Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, France; Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany

License: Copyright:
© 2017 Florence Wianny and Julien Vezoli CC BY 4.0 This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/

Article links: DOI: 10.5194/pb-4-185-2017  |  PubMed: 32110706  |  PMC: PMC7041537

Relevance: Moderate: mentioned 3+ times in text

Full text: PDF (285 KB)

References

  1. CH Adler, MJ Thorpy. Sleep issues in Parkinson’s disease. Neurology, 2015
  2. Y Agid. Parkinson’s disease: pathophysiology. Lancet, 1991. [PubMed]
  3. H Almirall, I Pigarev, MD de la Calzada, M Pigareva, MT Herrero, T Sagales. Nocturnal sleep structure and temperature slope in MPTP treated monkeys. J Neural Transm, 1999. [PubMed]
  4. H Almirall, V Bautista, A Sanchez-Bahillo, M Trinidad-Herrero. Ultradian and circadian body temperature and activity rhythms in chronic MPTP treated monkeys. Neurophysiol Clin, 2001. [PubMed]
  5. LE Annett, SB Dunnett, FL Martel, DC Rogers, RM Ridley, HF Baker, CD Marsden. A functional assessment of embryonic dopaminergic grafts in the marmoset. Prog Brain Res, 1990. [PubMed]
  6. LE Annett, FL Martel, DC Rogers, RM Ridley, HF Baker, SB Dunnett. Behavioral assessment of the effects of embryonic nigral grafts in marmosets with unilateral 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol, 1994. [PubMed]
  7. LE Annett, EM Torres, RM Ridley, HF Baker, SB Dunnett. A comparison of the behavioural effects of embryonic nigral grafts in the caudate nucleus and in the putamen of marmosets with unilateral 6-OHDA lesions. Exp Brain Res, 1995. [PubMed]
  8. LE Annett, EM Torres, DJ Clarke, Y Ishida, RA Barker, RM Ridley, SB Dunnett. Survival of nigral grafts within the striatum of marmosets with 6-OHDA lesions depends critically on donor embryo age. Cell Transplant, 1997. [PubMed]
  9. AM Ansari, AK Ahmed, AE Matsangos, F Lay, LJ Born, G Marti, Z Sun. Cellular GFP Toxicity and Immunogenicity: Potential Confounders in in Vivo Cell Tracking Experiments. Stem Cell Rev, 2016
  10. E Arenas, M Denham, JC Villaescusa. How to make a midbrain dopaminergic neuron. Development, 2015. [PubMed]
  11. R Aron Badin, M Vadori, B Vanhove, V Nerriere-Daguin, P Naveilhan, I Neveu, E Cozzi. Cell Therapy for Parkinson’s Disease: A Translational Approach to Assess the Role of Local and Systemic Immunosuppression. Am J Transplant, 2016. [PubMed]
  12. T Asakawa, H Fang, K Sugiyama, T Nozaki, Z Hong, Y Yang, Y Xia. Animal behavioral assessments in current research of Parkinson’s disease. Neurosci Biobehav Rev, 2016. [PubMed]
  13. KS Bankiewicz, RJ Plunkett, I Mefford, IJ Kopin, EH Oldfield. Behavioral recovery from MPTP-induced parkinsonism in monkeys after intracerebral tissue implants is not related to CSF concentrations of dopamine metabolites. Prog Brain Res, 1990. [PubMed]
  14. C Barcia, V Bautista, A Sanchez-Bahillo, E Fernandez-Villalba, JM Navarro-Ruis, AF Barreiro, MT Herrero. Circadian determinations of cortisol, prolactin and melatonin in chronic methyl-phenyl-tetrahydropyridine-treated monkeys. Neuroendocrinology, 2003. [PubMed]
  15. T Ben-Hur, M Idelson, H Khaner, M Pera, E Reinhartz, A Itzik, BE Reubinoff. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells, 2004. [PubMed]
  16. E Bezard, C Imbert, X Deloire, B Bioulac, CE Gross. A chronic MPTP model reproducing the slow evolution of Parkinson’s disease: evolution of motor symptoms in the monkey. Brain Res, 1997. [PubMed]
  17. KB Bjugstad, DE Redmond Jr., YD Teng, JD Elsworth, RH Roth, BC Blanchard, JR Sladek Jr.. Neural stem cells implanted into MPTP-treated monkeys increase the size of endogenous tyrosine hydroxylase-positive cells found in the striatum: a return to control measures. Cell Transplant, 2005. [PubMed]
  18. KB Bjugstad, YD Teng, DE Redmond Jr., JD Elsworth, RH Roth, SK Cornelius, JR Sladek Jr.. Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson’s disease. Exp Neurol, 2008. [PubMed]
  19. J Blesa, C Pifl, MA Sanchez-Gonzalez, C Juri, MA Garcia-Cabezas, R Adanez, JA Obeso. The nigrostriatal system in the presymptomatic and symptomatic stages in the MPTP monkey model: A PET, histological and biochemical study. Neurobiol Dis, 2012. [PubMed]
  20. J Bloch, JF Brunet, CR McEntire, DE Redmond. Primate adult brain cell autotransplantation produces behavioral and biological recovery in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced parkinsonian St. Kitts monkeys. J Comp Neurol, 2014. [PubMed]
  21. H Braak, JR Bohl, CM Muller, U Rub, RA de Vos, K Del Tredici. Stanley Fahn Lecture 2005: The staging procedure for the inclusion body pathology associated with sporadic Parkinson’s disease reconsidered. Mov Disord, 2006. [PubMed]
  22. A Brederlau, AS Correia, SV Anisimov, M Elmi, G Paul, L Roybon, JY Li. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson’s disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells, 2006. [PubMed]
  23. RG Brown, CD Marsden. Cognitive function in Parkinson’s disease: from description to theory. Trends Neurosci, 1990. [PubMed]
  24. B Bruguerolle, N Simon. Biologic rhythms and Parkinson’s disease: a chronopharmacologic approach to considering fluctuations in function. Clin Neuropharmacol, 2002. [PubMed]
  25. P Brundin, OG Nilsson, RE Strecker, O Lindvall, B Astedt, A Bjorklund. Behavioural effects of human fetal dopamine neurons grafted in a rat model of Parkinson’s disease. Exp Brain Res, 1986. [PubMed]
  26. JF Brunet, DE Redmond Jr., J Bloch. Primate adult brain cell autotransplantation, a pilot study in asymptomatic MPTP-treated monkeys. Cell Transplant, 2009. [PubMed]
  27. RS Burns, CC Chiueh, SP Markey, MH Ebert, DM Jacobowitz, IJ Kopin. A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. P Natl Acad Sci USA, 1983
  28. M Caiazzo, MT Dell’Anno, E Dvoretskova, D Lazarevic, S Taverna, D Leo, V Broccoli. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature, 2011. [PubMed]
  29. G Castelo-Branco, J Wagner, FJ Rodriguez, J Kele, K Sousa, N Rawal, E Arenas. Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. P Natl Acad Sci USA, 2003
  30. G Castelo-Branco, N Rawal, E Arenas. GSK-3beta inhibition/beta-catenin stabilization in ventral midbrain precursors increases differentiation into dopamine neurons. J Cell Sci, 2004. [PubMed]
  31. IL Cepeda, J Flores, ML Cornfeldt, JR O’Kusky, DJ Doudet. Human retinal pigment epithelial cell implants ameliorate motor deficits in two rat models of Parkinson disease. J Neuropathol Exp Neurol, 2007. [PubMed]
  32. SM Chambers, CA Fasano, EP Papapetrou, M Tomishima, M Sadelain, L Studer. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol, 2009. [PubMed]
  33. DJ Chang, SH Oh, N Lee, C Choi, I Jeon, HS Kim, J Song. Contralaterally transplanted human embryonic stem cell-derived neural precursor cells (ENStem-A) migrate and improve brain functions in stroke-damaged rats. Exp Mol Med, 2013
  34. Y Chen, M Xiong, Y Dong, A Haberman, J Cao, H Liu, SC Zhang. Chemical Control of Grafted Human PSC-Derived Neurons in a Mouse Model of Parkinson’s Disease. Cell Stem Cells, 2016
  35. LG Chia, LH Liu. Parkinson’s disease in Taiwan: an analysis of 215 patients. Neuroepidemiology, 1992. [PubMed]
  36. F Cicchetti, W Fodor, TW Deacon, C van Horne, S Rollins, W Burton, O Isacson. Immune parameters relevant to neural xenograft survival in the primate brain. Xenotransplantation, 2003. [PubMed]
  37. TJ Collier, DE Redmond Jr., RH Roth, JD Elsworth, JR Taylor, JR Sladek Jr.. Metabolic energy capacity of dopaminergic grafts and the implanted striatum in parkinsonian nonhuman primates as visualized with cytochrome oxidase histochemistry. Cell Transplant, 1997. [PubMed]
  38. TJ Collier, CE Sortwell, JD Elsworth, JR Taylor, RH Roth, JR Sladek Jr., DE Redmond Jr.. Embryonic ventral mesencephalic grafts to the substantia nigra of MPTP-treated monkeys: feasibility relevant to multiple-target grafting as a therapy for Parkinson’s disease. J Comp Neurol, 2002. [PubMed]
  39. L Conti, SM Pollard, T Gorba, E Reitano, M Toselli, G Biella, A Smith. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol, 2005
  40. O Cooper, G Hargus, M Deleidi, A Blak, T Osborn, E Marlow, O Isacson. Differentiation of human ES and Parkinson’s disease iPS cells into ventral midbrain dopaminergic neurons requires a high activity form of SHH, FGF8a and specific regionalization by retinoic acid. Mol Cell Neurosci, 2010. [PubMed]
  41. BJ Cord, J Li, M Works, SK McConnell, T Palmer, MA Hynes. Characterization of axon guidance cue sensitivity of human embryonic stem cell-derived dopaminergic neurons. Mol Cell Neurosci, 2010. [PubMed]
  42. X d’Anglemont de Tassigny, A Pascual, J Lopez-Barneo. GDNF-based therapies, GDNF-producing interneurons, and trophic support of the dopaminergic nigrostriatal pathway, Implications for Parkinson’s disease. Front Neuroanat, 2015. [PubMed]
  43. MM Daadi, BA Grueter, RC Malenka, DE Redmond Jr., GK Steinberg. Dopaminergic neurons from midbrain-specified human embryonic stem cell-derived neural stem cells engrafted in a monkey model of Parkinson’s disease. PLoS ONE, 2012
  44. E Decamp, JS Schneider. Attention and executive function deficits in chronic low-dose MPTP-treated non-human primates. Eur J Neurosci, 2004. [PubMed]
  45. MT Dell’Anno, M Caiazzo, D Leo, E Dvoretskova, L Medrihan, G Colasante, V Broccoli. Remote control of induced dopaminergic neurons in parkinsonian rats. J Clin Invest, 2014. [PubMed]
  46. M DeMattei, AC Levi, RG Fariello. Neuromelanic pigment in substantia nigra neurons of rats and dogs. Neurosci Lett, 1986. [PubMed]
  47. A Destee. Therapeutic strategies for Parkinson’s disease. Rev Prat, 2005. [PubMed]
  48. ER Detrait, WJ Bowers, MW Halterman, RE Giuliano, L Bennice, HJ Federoff, EK Richfield. Reporter gene transfer induces apoptosis in primary cortical neurons. Mol Ther, 2002. [PubMed]
  49. D Doi, A Morizane, T Kikuchi, H Onoe, T Hayashi, T Kawasaki, J Takahashi. Prolonged maturation culture favors a reduction in the tumorigenicity and the dopaminergic function of human ESC-derived neural cells in a primate model of Parkinson’s disease. Stem Cells, 2012. [PubMed]
  50. D Doi, B Samata, M Katsukawa, T Kikuchi, A Morizane, Y Ono, J Takahashi. Isolation of human induced pluripotent stem cell-derived dopaminergic progenitors by cell sorting for successful transplantation. Stem Cell Rep, 2014
  51. DJ Doudet, ML Cornfeldt, CR Honey, AW Schweikert, RC Allen. PET imaging of implanted human retinal pigment epithelial cells in the MPTP-induced primate model of Parkinson’s disease. Exp Neurol, 2004. [PubMed]
  52. M Drukker, N Benvenisty. The immunogenicity of human embryonic stem-derived cells. Trends Biotechnol, 2004. [PubMed]
  53. M Drukker, G Katz, A Urbach, M Schuldiner, G Markel, J Itskovitz-Eldor, N Benvenisty. Characterization of the expression of MHC proteins in human embryonic stem cells. P Natl Acad Sci USA, 2002
  54. EP Duarte, M Curcio, LM Canzoniero, CB Duarte. Neuroprotection by GDNF in the ischemic brain. Growth Factors, 2012. [PubMed]
  55. JD Elsworth, MS Brittan, JR Taylor, JR Sladek Jr., MS al-Tikriti, Y Zea-Ponce, RH Roth. Restoration of dopamine transporter density in the striatum of fetal ventral mesencephalon-grafted, but not sham-grafted, MPTP-treated parkinsonian monkeys. Cell Transplant, 1996. [PubMed]
  56. JD Elsworth, DE Redmond Jr., C Leranth, KB Bjugstad, JR Sladek Jr., TJ Collier, RH Roth. AAV2-mediated gene transfer of GDNF to the striatum of MPTP monkeys enhances the survival and outgrowth of co-implanted fetal dopamine neurons. Exp Neurol, 2008. [PubMed]
  57. JD Elsworth, JR Sladek Jr., JR Taylor, TJ Collier, DE Redmond Jr., RH Roth. Early gestational mesencephalon grafts, but not later gestational mesencephalon, cerebellum or sham grafts, increase dopamine in caudate nucleus of MPTP-treated monkeys. Neuroscience, 1996. [PubMed]
  58. ME Emborg. Nonhuman primate models of Parkinson’s disease. Ilar J, 2007. [PubMed]
  59. ME Emborg, Y Liu, J Xi, X Zhang, Y Yin, J Lu, SC Zhang. Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep, 2013. [PubMed]
  60. ME Emborg, Z Zhang, V Joers, K Brunner, V Bondarenko, S Ohshima, SC Zhang. Intracerebral transplantation of differentiated human embryonic stem cells to hemiparkinsonian monkeys. Cell Transplant, 2013. [PubMed]
  61. T Falk, NR Congrove, S Zhang, AD McCourt, SJ Sherman, BS McKay. PEDF and VEGF-A output from human retinal pigment epithelial cells grown on novel microcarriers. J Biomed Biotechnol, 2012. [DOI | PubMed]
  62. K Fifel, J Vezoli, K Dzahini, B Claustrat, V Leviel, H Kennedy, HM Cooper. Alteration of daily and circadian rhythms following dopamine depletion in MPTP treated non-human primates. PLoS One, 2014. [DOI | PubMed]
  63. A Fine, SP Hunt, WH Oertel, M Nomoto, PN Chong, A Bond, C Waters, JA Temlett, L Annett, S Dunnett. Transplantation of embryonic marmoset dopaminergic neurons to the corpus striatum of marmosets rendered parkinsonian by 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. Prog Brain Res, 1988. [PubMed]
  64. JD Flax, S Aurora, C Yang, C Simonin, AM Wills, LL Billinghurst, EY Snyder. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol, 1998. [PubMed]
  65. LS Forno, LE DeLanney, I Irwin, JW Langston. Similarities and differences between MPTP-induced parkinsonsim and Parkinson’s disease, Neuropathologic considerations. Adv Neurol, 1993. [PubMed]
  66. SK Franke, RE van Kesteren, S Hofman, JA Wubben, AB Smit, IH Philippens. Individual and Familial Susceptibility to MPTP in a Common Marmoset Model for Parkinson’s Disease. Neurodegener Dis, 2016. [PubMed]
  67. CR Freed, PE Greene, RE Breeze, WY Tsai, W DuMouchel, R Kao, S Fahn. Transplantation of embryonic dopamine neurons for severe Parkinson’s disease. N Engl J Med, 2001. [PubMed]
  68. WJ Freed, JM Morihisa, E Spoor, BJ Hoffer, L Olson, A Seiger, RJ Wyatt. Transplanted adrenal chromaffin cells in rat brain reduce lesion-induced rotational behaviour. Nature, 1981. [PubMed]
  69. RA Fricker, EM Torres, SB Dunnett. The effects of donor stage on the survival and function of embryonic striatal grafts in the adult rat brain. I. Morphological characteristics. Neuroscience, 1997. [PubMed]
  70. RA Fricker, MK Carpenter, C Winkler, C Greco, MA Gates, A Bjorklund. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci, 1999. [PubMed]
  71. WR Gibb, AJ Lees. Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson’s disease. J Neurol Neurosur Ps, 1991
  72. R Gonzalez, I Garitaonandia, A Crain, M Poustovoitov, T Abramihina, A Noskov, R Semechkin. Proof of concept studies exploring the safety and functional activity of human parthenogenetic-derived neural stem cells for the treatment of Parkinson’s disease. Cell Transplant, 2015. [PubMed]
  73. R Gonzalez, I Garitaonandia, M Poustovoitov, T Abramihina, C McEntire, B Culp, RA Kern. Neural Stem Cells Derived From Human Parthenogenetic Stem Cells Engraft and Promote Recovery in a Nonhuman Primate Model of Parkinsons Disease. Cell Transplant, 2016. [PubMed]
  74. PH Gordon, Q Yu, C Qualls, H Winfield, S Dillon, PE Greene, SL Pullman. Reaction time and movement time after embryonic cell implantation in Parkinson disease. Arch Neurol, 2004. [PubMed]
  75. S Grealish, ME Jonsson, M Li, D Kirik, A Bjorklund, LH Thompson. The A9 dopamine neuron component in grafts of ventral mesencephalon is an important determinant for recovery of motor function in a rat model of Parkinson’s disease. Brain, 2010. [PubMed]
  76. S Grealish, E Diguet, A Kirkeby, B Mattsson, A Heuer, Y Bramoulle, M Parmar. Human ESC-derived dopamine neurons show similar preclinical efficacy and potency to fetal neurons when grafted in a rat model of Parkinson’s disease. Cell Stem Cell, 2014. [PubMed]
  77. P Greene, L Cote, S Fahn. Treatment of drug-induced psychosis in Parkinson’s disease with clozapine. Adv Neurol, 1993. [PubMed]
  78. R Grondin, Z Zhang, A Yi, WA Cass, N Maswood, AH Andersen, DM Gash. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain, 2002. [PubMed]
  79. RE Gross, RL Watts, RA Hauser, RA Bakay, H Reichmann, R von Kummer, R Sandbrink. Intrastriatal transplantation of microcarrier-bound human retinal pigment epithelial cells versus sham surgery in patients with advanced Parkinson’s disease: a double-blind, randomised, controlled trial. Lancet Neurol, 2011. [PubMed]
  80. R Guzman, N Uchida, TM Bliss, D He, KK Christopherson, D Stellwagen, GK Steinberg. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. P Natl Acad Sci USA, 2007
  81. SN Haber. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat, 2003. [PubMed]
  82. PJ Hallett, M Deleidi, A Astradsson, GA Smith, O Cooper, TM Osborn, O Isacson. Successful function of autologous iPSC-derived dopamine neurons following transplantation in a non-human primate model of Parkinson’s disease. Cell Stem Cell, 2015. [PubMed]
  83. R Hammond, S Blaess, A Abeliovich. Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS One, 2009. [DOI | PubMed]
  84. T Hayashi, S Wakao, M Kitada, T Ose, H Watabe, Y Kuroda, M Dezawa. Autologous mesenchymal stem cell-derived dopaminergic neurons function in parkinsonian macaques. J Clin Invest, 2013. [PubMed]
  85. HL Hernandez-Montiel, E Tamariz, MT Sandoval-Minero, A Varela-Echavarria. Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J Comp Neurol, 2008. [PubMed]
  86. L Iacovitti, AE Donaldson, CE Marshall, S Suon, M Yang. A protocol for the differentiation of human embryonic stem cells into dopaminergic neurons using only chemically defined human additives: Studies in vitro and in vivo. Brain Res, 2007. [PubMed]
  87. J Imitola, K Raddassi, KI Park, FJ Mueller, M Nieto, YD Teng, SJ Khoury. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. P Natl Acad Sci USA, 2004
  88. V Jackson-Lewis, S Przedborski. The MPTP Mouse Model of Parkinson’s Disease: the True, the False, and the Unknown. Parkinson’s Disease. 2008
  89. JN Johannessen, CC Chiueh, RS Burns, SP Markey. Differences in the metabolism of MPTP in the rodent and primate parallel differences in sensitivity to its neurotoxic effects. Life Sci, 1985. [PubMed]
  90. M Joksimovic, BA Yun, R Kittappa, AM Anderegg, WW Chang, MM Taketo, RB Awatramani. Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis. Nat Neurosci, 2009. [PubMed]
  91. SS Jossan, E Sakurai, L Oreland. MPTP toxicity in relation to age, dopamine uptake and MAO-B activity in two rodent species. Pharmacol Toxicol, 1989. [PubMed]
  92. H Kawasaki, K Mizuseki, S Nishikawa, S Kaneko, Y Kuwana, S Nakanishi, Y Sasai. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron, 2000. [PubMed]
  93. H Kawasaki, H Suemori, K Mizuseki, K Watanabe, F Urano, H Ichinose, Y Sasai. Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. P Natl Acad Sci USA, 2002
  94. Z Kefalopoulou, M Politis, P Piccini, N Mencacci, K Bhatia, M Jahanshahi, T Foltynie. Long-term clinical outcome of fetal cell transplantation for Parkinson disease: two case reports. JAMA Neurol, 2014. [PubMed]
  95. S Kelly, TM Bliss, AK Shah, GH Sun, M Ma, WC Foo, GK Steinberg. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. P Natl Acad Sci USA, 2004
  96. H Kennedy, C Dehay. Self-organization and interareal networks in the primate cortex. Prog Brain Res, 2012. [PubMed]
  97. T Kikuchi, A Morizane, D Doi, H Onoe, T Hayashi, T Kawasaki, J Takahashi. Survival of human induced pluripotent stem cell-derived midbrain dopaminergic neurons in the brain of a primate model of Parkinson’s disease. J Parkinsons Dis, 2011. [PubMed]
  98. J Kim, SC Su, H Wang, AW Cheng, JP Cassady, MA Lodato, R Jaenisch. Functional integration of dopaminergic neurons directly converted from mouse fibroblasts. Cell Stem Cell, 2011. [PubMed]
  99. A Kirkeby, J Nelander, M Parmar. Generating regionalized neuronal cells from pluripotency, a step-by-step protocol. Front Cell Neurosci, 2012. [PubMed]
  100. A Kirkeby, S Nolbrant, K Tiklova, A Heuer, N Kee, T Cardoso, M Parmar. Predictive Markers Guide Differentiation to Improve Graft Outcome in Clinical Translation of hESC-Based Therapy for Parkinson’s Disease. Cell Stem Cell, 2017. [PubMed]
  101. A Kirkeby, M Parmar, RA Barker. Strategies for bringing stem cell-derived dopamine neurons to the clinic: A European approach (STEM-PD), Prog Brain Res. Elsevier, 2017
  102. RL Klein, RD Dayton, NJ Leidenheimer, K Jansen, TE Golde, RM Zweig. Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther, 2006. [PubMed]
  103. SM Kolk, RA Gunput, TS Tran, DM van den Heuvel, AA Prasad, AJ Hellemons, RJ Pasterkamp. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J Neurosci, 2009. [PubMed]
  104. JH Kordower, ME Emborg, J Bloch, SY Ma, Y Chu, L Leventhal, P Aebischer. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease. Science, 2000. [PubMed]
  105. JH Kordower, A Vinuela, Y Chu, O Isacson, DE Redmond Jr.. Parkinsonian monkeys with prior levodopa-induced dyskinesias followed by fetal dopamine precursor grafts do not display graft-induced dyskinesias. J Comp Neurol, 2017. [PubMed]
  106. S Kriks, JW Shim, J Piao, YM Ganat, DR Wakeman, Z Xie, L Studer. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature, 2011. [PubMed]
  107. WL Kuan, R Lin, P Tyers, RA Barker. The importance of A9 dopaminergic neurons in mediating the functional benefits of fetal ventral mesencephalon transplants and levodopa-induced dyskinesias. Neurobiol Dis, 2007. [PubMed]
  108. G La Manno, D Gyllborg, S Codeluppi, K Nishimura, C Salto, A Zeisel, S Linnarsson. Molecular Diversity of Midbrain Development in Mouse, Human, and Stem Cells. Cell, 2016. [PubMed]
  109. KW Lange. Behavioural effects and supersensitivity in the rat following intranigral MPTP and MPP + administration. Eur J Pharmacol, 1990. [PubMed]
  110. JW Langston, P Ballard. Parkinsonism induced by 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP): implications for treatment and the pathogenesis of Parkinson’s disease. Can J Neurol Sci, 1984. [PubMed]
  111. SH Lee, N Lumelsky, L Studer, JM Auerbach, RD McKay. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol, 2000. [PubMed]
  112. MJ Lelos, RJ Morgan, CM Kelly, EM Torres, AE Rosser, SB Dunnett. Amelioration of non-motor dysfunctions after transplantation of human dopamine neurons in a model of Parkinson’s disease. Exp Neurol, 2016. [PubMed]
  113. C Leranth, JR Sladek Jr., RH Roth, DE Redmond Jr.. Efferent synaptic connections of dopaminergic neurons grafted into the caudate nucleus of experimentally induced parkinsonian monkeys are different from those of control animals. Exp Brain Res, 1998. [PubMed]
  114. J Li, T Duarte, A Kocabas, M Works, SK McConnell, MA Hynes. Evidence for topographic guidance of dopaminergic axons by differential Netrin-1 expression in the striatum. Mol Cell Neurosci, 2014. [PubMed]
  115. T Li, J Zheng, Y Xie, S Wang, X Zhang, J Li, W Ji. Transplantable neural progenitor populations derived from rhesus monkey embryonic stem cells. Stem Cells, 2005. [PubMed]
  116. W Li, E Englund, H Widner, B Mattsson, D van Westen, J Latt, JY Li. Extensive graft-derived dopaminergic innervation is maintained 24 years after transplantation in the degenerating parkinsonian brain. P Natl Acad Sci USA, 2016
  117. L Lin, Y Rao, O Isacson. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol Cell Neurosci, 2005. [PubMed]
  118. LF Lin, DH Doherty, JD Lile, S Bektesh, F Collins. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science, 1993. [PubMed]
  119. O Lindvall. Transplantation into the human brain: present status and future possibilities. J Neurol Neurosur Ps, 1989
  120. O Lindvall. Developing dopaminergic cell therapy for Parkinson’s disease – give up or move forward?. Mov Disord, 2013. [PubMed]
  121. O Lindvall, EO Backlund, L Farde, G Sedvall, R Freedman, B Hoffer, L Olson. Transplantation in Parkinson’s disease: two cases of adrenal medullary grafts to the putamen. Ann Neurol, 1987. [PubMed]
  122. O Lindvall, S Rehncrona, B Gustavii, P Brundin, B Astedt, H Widner, L Olson. Fetal dopamine-rich mesencephalic grafts in Parkinson’s disease. Lancet, 1988. [PubMed]
  123. O Lindvall, P Brundin, H Widner, S Rehncrona, B Gustavii, R Frackowiak, KL Leenders, G Sawle, JC Rothwell, CD Marsden, A Bjorklund. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson’s disease. Science, 1990. [PubMed]
  124. LC Lins, F Wianny, S Livi, C Dehay, J Duchet-Rumeau, JF Gerard. Effect of polyvinylidene fluoride electrospun fiber orientation on neural stem cell differentiation,. J Biomed Mater Res B Appl Biomater, 2016. [DOI]
  125. LC Lins, F Wianny, S Livi, IA Hidalgo, C Dehay, J Duchet-Rumeau, JF Gerard. Development of Bioresorbable Hydrophilic-Hydrophobic Electrospun Scaffolds for Neural Tissue Engineering. Biomacromolecules, 2016. [PubMed]
  126. HS Liu, MS Jan, CK Chou, PH Chen, NJ Ke. Is green fluorescent protein toxic to the living cells?. Biochem Biophys Res Commun, 1999. [PubMed]
  127. X Liu, F Li, EA Stubblefield, B Blanchard, TL Richards, GA Larson, CY Li. Direct reprogramming of human fibroblasts into dopaminergic neuron-like cells. Cell Res, 2012. [PubMed]
  128. A Louveau, TH Harris, J Kipnis. Revisiting the Mechanisms of CNS Immune Privilege. Trends Immunol, 2015. [PubMed]
  129. MR Luquin, M Manrique, J Guillen, J Arbizu, C Ordonez, I Marcilla. Enhanced GDNF expression in dopaminergic cells of monkeys grafted with carotid body cell aggregates. Brain Res, 2011. [PubMed]
  130. I Madrazo, RE Franco-Bourland. Technique of autoadrenal transplantation. J Neurosurg, 1991
  131. I Madrazo, R Drucker-Colin, V Diaz, J Martinez-Mata, C Torres, JJ Becerril. Open microsurgical autograft of adrenal medulla to the right caudate nucleus in two patients with intractable Parkinson’s disease. N Engl J Med, 1987. [PubMed]
  132. DJ Marmion, JH Kordower. alpha-Synuclein nonhuman primate models of Parkinson’s disease. J Neural Transm, 2017. [DOI]
  133. G Martino, S Pluchino. The therapeutic potential of neural stem cells. Nat Rev Neurosci, 2006. [PubMed]
  134. I Mendez, D Sadi, M Hong. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J Neurosci, 1996. [PubMed]
  135. I Mendez, KA Baker, M Hong. Simultaneous intrastriatal and intranigral grafting (double grafts) in the rat model of Parkinson’s disease. Brain Res Rev, 2000. [PubMed]
  136. SF Moore, NV Guzman, SL Mason, CH Williams-Gray, RA Barker. Which patients with Parkinson’s disease participate in clinical trials? One centre’s experiences with a new cell based therapy trial (TRANSEURO). J Parkinsons Dis, 2014. [PubMed]
  137. JM Morihisa, RK Nakamura, WJ Freed, M Mishkin, RJ Wyatt. Adrenal medulla grafts survive and exhibit catecholamine-specific fluorescence in the primate brain. Exp Neurol, 1984. [PubMed]
  138. A Morizane, D Doi, T Kikuchi, K Okita, A Hotta, T Kawasaki, J Takahashi. Direct comparison of autologous and allogeneic transplantation of iPSC-derived neural cells in the brain of a non-human primate. Stem Cell Rep, 2013
  139. LN Nerobkova, NV Markina, TA Voronina, VA Kraineva, TL Garibova, GM Molodavkin, LM Sharkova. Sleep disorders and impaired learning ability in rats with parkinsonian syndrome induced by MPTP. Biull Eksp Biol Med, 1996. [PubMed]
  140. G Nikkhah, MG Cunningham, A Jodicke, U Knappe, A Bjorklund. Improved graft survival and striatal reinnervation by microtransplantation of fetal nigral cell suspensions in the rat Parkinson model. Brain Res, 1994. [PubMed]
  141. K Nishimura, S Murayama, J Takahashi. Identification of Neurexophilin 3 as a Novel Supportive Factor for Survival of Induced Pluripotent Stem Cell-Derived Dopaminergic Progenitors. Stem Cells Transl Med, 2015. [PubMed]
  142. S Ohmachi, Y Watanabe, T Mikami, N Kusu, T Ibi, A Akaike, N Itoh. FGF-20, a novel neurotrophic factor, preferentially expressed in the substantia nigra pars compacta of rat brain. Biochem Biophys Res Commun, 2000. [PubMed]
  143. E Oikonomou, T Paparrigopoulos. Neuropsychiatric manifestations in Parkinson’s disease. Psychiatriki, 2015. [PubMed]
  144. CW Olanow, CG Goetz, JH Kordower, AJ Stoessl, V Sossi, MF Brin, TB Freeman. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson’s disease. Ann Neurol, 2003. [PubMed]
  145. AM Owen, M James, PN Leigh, BA Summers, CD Marsden, NP Quinn, TW Robbins. Fronto-striatal cognitive deficits at different stages of Parkinson’s disease. Brain, 1992. [PubMed]
  146. CH Park, YK Minn, JY Lee, DH Choi, MY Chang, JW Shim, SH Lee. In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J Neurochem, 2005. [PubMed]
  147. S Peng, Y Ma, J Flores, M Cornfeldt, B Mitrovic, D Eidelberg, DJ Doudet. Modulation of Abnormal Metabolic Brain Networks by Experimental Therapies in a Nonhuman Primate Model of Parkinson Disease: An Application to Human Retinal Pigment Epithelial Cell Implantation. J Nucl Med, 2016. [PubMed]
  148. I Perez-Otano, C Oset, MR Luquin, MT Herrero, JA Obeso, J Del Rio. MPTP-induced parkinsonism in primates: pattern of striatal dopamine loss following acute and chronic administration. Neurosci Lett, 1994. [PubMed]
  149. MJ Perlow, WJ Freed, BJ Hoffer, A Seiger, L Olson, RJ Wyatt. Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science, 1979. [PubMed]
  150. AL Perrier, V Tabar, T Barberi, ME Rubio, J Bruses, N Topf, L Studer. Derivation of midbrain dopamine neurons from human embryonic stem cells. P Natl Acad Sci USA, 2004
  151. U Pfisterer, A Kirkeby, O Torper, J Wood, J Nelander, A Dufour, M Parmar. Direct conversion of human fibroblasts to dopaminergic neurons. P Natl Acad Sci USA, 2011
  152. U Pfisterer, J Wood, K Nihlberg, O Hallgren, L Bjermer, G Westergren-Thorsson, M Parmar. Efficient induction of functional neurons from adult human fibroblasts. Cell Cycle, 2011. [PubMed]
  153. W Poewe. Non-motor symptoms in Parkinson’s disease. Eur J Neurol, 2008. [PubMed]
  154. M Politis, P Piccini. Brain imaging after neural transplantation. Prog Brain Res, 2010. [PubMed]
  155. SM Pollard, R Wallbank, S Tomlinson, L Grotewold, A Smith. Fibroblast growth factor induces a neural stem cell phenotype in foetal forebrain progenitors and during embryonic stem cell differentiation. Mol Cell Neurosci, 2008. [PubMed]
  156. LF Potts, H Wu, A Singh, I Marcilla, MR Luquin, SM Papa. Modeling Parkinson’s disease in monkeys for translational studies, a critical analysis. Exp Neurol, 2014. [PubMed]
  157. MG Purisai, AL McCormack, WJ Langston, LC Johnston, DA Di Monte. Alpha-synuclein expression in the substantia nigra of MPTP-lesioned non-human primates. Neurobiol Dis, 2005. [PubMed]
  158. MA Raghanti, CD Stimpson, JL Marcinkiewicz, JM Erwin, PR Hof, CC Sherwood. Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study. Neuroscience, 2008. [PubMed]
  159. SA Raskin, JC Borod, J Tweedy. Neuropsychological aspects of Parkinson’s disease. Neuropsychol Rev, 1990. [PubMed]
  160. DE Redmond Jr., JR Sladek Jr., RH Roth, TJ Collier, JD Elsworth, AY Deutch, S Haber. Fetal neuronal grafts in monkeys given methylphenyltetrahydropyridine. Lancet, 1986. [PubMed]
  161. DE Redmond Jr., KB Bjugstad, YD Teng, V Ourednik, J Ourednik, DR Wakeman, EY Snyder. Behavioral improvement in a primate Parkinson’s model is associated with multiple homeostatic effects of human neural stem cells. P Natl Acad Sci USA, 2007
  162. DE Redmond Jr., A Vinuela, JH Kordower, O Isacson. Influence of cell preparation and target location on the behavioral recovery after striatal transplantation of fetal dopaminergic neurons in a primate model of Parkinson’s disease. Neurobiol Dis, 2008. [PubMed]
  163. DE Redmond Jr., JD Elsworth, RH Roth, C Leranth, TJ Collier, B Blanchard, JR Sladek Jr.. Embryonic substantia nigra grafts in the mesencephalon send neurites to the host striatum in non-human primate after overexpression of GDNF. J Comp Neurol, 2009. [PubMed]
  164. DE Redmond Jr., CR McEntire, JP Kingsbery, C Leranth, JD Elsworth, KB Bjugstad, JR Sladek Jr.. Comparison of fetal mesencephalic grafts, AAV-delivered GDNF, and both combined in an MPTP-induced nonhuman primate Parkinson’s model. Mol Ther, 2013. [PubMed]
  165. Z Ren, J Wang, S Wang, C Zou, X Li, Y Guan, YA Zhang. Autologous transplantation of GDNF-expressing mesenchymal stem cells protects against MPTP-induced damage in cynomolgus monkeys. Sci Rep, 2013
  166. NJ Riachi, SI Harik, RN Kalaria, LM Sayre. On the mechanisms underlying 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine neurotoxicity. II. Susceptibility among mammalian species correlates with the toxin’s metabolic patterns in brain microvessels and liver. J Pharmacol Exp Ther, 1988. [PubMed]
  167. P Rivetti di Val Cervo, RA Romanov, G Spigolon, D Masini, E Martin-Montanez, EM Toledo, E Arenas. Induction of functional dopamine neurons from human astrocytes in vitro and mouse astrocytes in a Parkinson’s disease model. Nat Biotechnol, 2017. [PubMed]
  168. NS Roy, C Cleren, SK Singh, L Yang, MF Beal, SA Goldman. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med, 2006. [PubMed]
  169. K Russ, J Flores, T Brudek, DJ Doudet. Differential behavioral outcomes following neonatal versus fetal human retinal pigment epithelial cell striatal implants in parkinsonian rats. J Neural Transm, 2017. [PubMed]
  170. H Salmonowicz, JF Passos. Detecting senescence: a new method for an old pigment. Aging Cell, 2017. [PubMed]
  171. R Sanchez-Pernaute, L Studer, D Ferrari, A Perrier, H Lee, A Vinuela, O Isacson. Long-term survival of dopamine neurons derived from parthenogenetic primate embryonic stem cells (cyno-1) after transplantation. Stem Cells, 2005. [PubMed]
  172. J Sautter, JL Tseng, D Braguglia, P Aebischer, C Spenger, RW Seiler, AD Zurn. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic grafts. Exp Neurol, 1998. [PubMed]
  173. D Scherman, C Desnos, F Darchen, P Pollak, F Javoy-Agid, Y Agid. Striatal dopamine deficiency in Parkinson’s disease: role of aging. Ann Neurol, 1989. [PubMed]
  174. JS Schneider, CJ Kovelowski. Chronic exposure to low doses of MPTP. I. Cognitive deficits in motor asymptomatic monkeys. Brain Res, 1990. [PubMed]
  175. P Sensharma, G Madhumathi, RD Jayant, AK Jaiswal. Biomaterials and cells for neural tissue engineering: Current choices. Mater Sci Eng C Mater Biol Appl, 2017. [PubMed]
  176. BA Sieber, A Kuzmin, JM Canals, A Danielsson, G Paratcha, E Arenas, CF Ibanez. Disruption of EphA/ephrin-a signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine. Mol Cell Neurosci, 2004. [PubMed]
  177. T Simuni, K Sethi. Nonmotor manifestations of Parkinson’s disease. Ann Neurol, 2008
  178. SR Sinclair, CN Svendsen, EM Torres, D Martin, JW Fawcett, SB Dunnett. GDNF enhances dopaminergic cell survival and fibre outgrowth in embryonic nigral grafts. Neuroreport, 1996. [PubMed]
  179. JR Sladek Jr., I Shoulson. Neural transplantation: a call for patience rather than patients. Science, 1988. [PubMed]
  180. JR Sladek Jr., DE Redmond Jr., TJ Collier, JP Blount, JD Elsworth, JR Taylor, RH Roth. Fetal dopamine neural grafts: extended reversal of methylphenyltetrahydropyridine-induced parkinsonism in monkeys. Prog Brain Res, 1988. [PubMed]
  181. JR Sladek Jr., TJ Collier, JD Elsworth, RH Roth, JR Taylor, DE Redmond Jr.. Intrastriatal grafts from multiple donors do not result in a proportional increase in survival of dopamine neurons in nonhuman primates. Cell Transplant, 1998. [PubMed]
  182. JR Sladek Jr., TJ Collier, JD Elsworth, JR Taylor, RH Roth, DE Redmond Jr.. Can graft-derived neurotrophic activity be used to direct axonal outgrowth of grafted dopamine neurons for circuit reconstruction in primates?. Exp Neurol, 1993. [PubMed]
  183. JR Sladek Jr., JD Elsworth, RH Roth, LE Evans, TJ Collier, SJ Cooper, DE Redmond Jr.. Fetal dopamine cell survival after transplantation is dramatically improved at a critical donor gestational age in nonhuman primates. Exp Neurol, 1993. [PubMed]
  184. JR Sladek Jr., KB Bjugstad, TJ Collier, EA Bundock, BC Blanchard, JD Elsworth, DE Redmond Jr.. Embryonic substantia nigra grafts show directional outgrowth to cografted striatal grafts and potential for pathway reconstruction in nonhuman primate. Cell Transplant, 2008. [PubMed]
  185. CE Sortwell, BC Blanchard, TJ Collier, JD Elsworth, JR Taylor, RH Roth, JR Sladek Jr.. Pattern of synaptophysin immunoreactivity within mesencephalic grafts following transplantation in a parkinsonian primate model. Brain Res, 1998. [PubMed]
  186. N Spitzer, GS Sammons, EM Price. Autofluorescent cells in rat brain can be convincing impostors in green fluorescent reporter studies. J Neurosci Meth, 2011
  187. PA Starr, T Wichmann, C van Horne, RA Bakay. Intranigral transplantation of fetal substantia nigra allograft in the hemiparkinsonian rhesus monkey. Cell Transplant, 1999. [PubMed]
  188. DT Stephenson, MD Meglasson, MA Connell, MA Childs, E Hajos-Korcsok, ME Emborg. The effects of a selective dopamine D2 receptor agonist on behavioral and pathological outcome in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated squirrel monkeys. J Pharmacol Exp Ther, 2005. [PubMed]
  189. I Stromberg, S Johnson, B Hoffer, L Olson. Reinnervation of dopamine-denervated striatum by substantia nigra transplants: immunohistochemical and electrophysiological correlates. Neuroscience, 1985. [PubMed]
  190. T Subramanian, D Marchionini, EM Potter, ML Cornfeldt. Striatal xenotransplantation of human retinal pigment epithelial cells attached to microcarriers in hemiparkinsonian rats ameliorates behavioral deficits without provoking a host immune response. Cell Transplant, 2002. [PubMed]
  191. AM Sullivan, A Toulouse. Neurotrophic factors for the treatment of Parkinson’s disease. Cytokine Growth Factor Rev, 2011. [PubMed]
  192. Y Sun, S Pollard, L Conti, M Toselli, G Biella, G Parkin, A Smith. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci, 2008. [PubMed]
  193. M Sundberg, H Bogetofte, T Lawson, J Jansson, G Smith, A Astradsson, O Isacson. Improved cell therapy protocols for Parkinson’s disease based on differentiation efficiency and safety of hESC-, hiPSC-, and non-human primate iPSC-derived dopaminergic neurons. Stem Cells, 2013. [PubMed]
  194. E Sundstrom, EB Samuelsson. Comparison of key steps in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) neurotoxicity in rodents. Pharmacol Toxicol, 1997. [PubMed]
  195. DM Swallow, MA Lawton, KA Grosset, N Malek, CR Smith, NP Bajaj, DG Grosset. Variation in Recent Onset Parkinson’s Disease: Implications for Prodromal Detection. J Parkinsons Dis, 2016. [PubMed]
  196. Y Takagi, J Takahashi, H Saiki, A Morizane, T Hayashi, Y Kishi, N Hashimoto. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest, 2005. [PubMed]
  197. JR Taylor, JD Elsworth, RH Roth, JR Sladek Jr., DE Redmond Jr.. Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain, 1990. [PubMed]
  198. JR Taylor, JD Elsworth, RH Roth, JR Sladek Jr., TJ Collier, DE Redmond Jr.. Grafting of fetal substantia nigra to striatum reverses behavioral deficits induced by MPTP in primates: a comparison with other types of grafts as controls. Exp Brain Res, 1991. [PubMed]
  199. L Thompson, P Barraud, E Andersson, D Kirik, A Bjorklund. Identification of dopaminergic neurons of nigral and ventral tegmental area subtypes in grafts of fetal ventral mesencephalon based on cell morphology, protein expression, and efferent projections. J Neurosci, 2005. [PubMed]
  200. LH Thompson, S Grealish, D Kirik, A Bjorklund. Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur J Neurosci, 2009. [PubMed]
  201. ER Torre, CA Gutekunst, RE Gross. Expression by midbrain dopamine neurons of Sema3A and 3F receptors is associated with chemorepulsion in vitro but a mild in vivo phenotype. Mol Cell Neurosci, 2010. [PubMed]
  202. EM Torres, C Monville, MA Gates, V Bagga, SB Dunnett. Improved survival of young donor age dopamine grafts in a rat model of Parkinson’s disease. Neuroscience, 2007. [PubMed]
  203. EM Torres, E Dowd, SB Dunnett. Recovery of functional deficits following early donor age ventral mesencephalic grafts in a rat model of Parkinson’s disease. Neuroscience, 2008. [PubMed]
  204. B Vagaska, SE New, C Alvarez-Gonzalez, F D’Acquisto, SG Gomez, NW Bulstrode, P Ferretti. MHC-class-II are expressed in a subpopulation of human neural stem cells in vitro in an IFNgamma-independent fashion and during development. Sci Rep, 2016. [DOI | PubMed]
  205. T Vazin, J Chen, CT Lee, R Amable, WJ Freed. Assessment of stromal-derived inducing activity in the generation of dopaminergic neurons from human embryonic stem cells. Stem Cells, 2008. [PubMed]
  206. J Vezoli, K Fifel, V Leviel, C Dehay, H Kennedy, HM Cooper, E Procyk. Early presymptomatic and long-term changes of rest activity cycles and cognitive behavior in a MPTP-monkey model of Parkinson’s disease. PLoS ONE, 2011. [DOI | PubMed]
  207. J Vezoli, K Dzahini, N Costes, CR Wilson, K Fifel, HM Cooper, E Procyk. Increased DAT binding in the early stage of the dopaminergic lesion: a longitudinal [11C]PE2I binding study in the MPTP-monkey. Neuroimage, 2014. [PubMed]
  208. DR Wakeman, MR Hofmann, DE Redmond Jr., YD Teng, EY Snyder. Long-term multilayer adherent network (MAN) expansion, maintenance, and characterization, chemical and genetic manipulation, and transplantation of human fetal forebrain neural stem cells. Curr Protoc Stem Cell Biol, 2009. [DOI]
  209. DR Wakeman, DE Redmond Jr., HB Dodiya, JR Sladek Jr., C Leranth, YD Teng, EY Snyder. Human neural stem cells survive long term in the midbrain of dopamine-depleted monkeys after GDNF overexpression and project neurites toward an appropriate target. Stem Cells Transl Med, 2014. [PubMed]
  210. S Wang, C Zou, L Fu, B Wang, J An, G Song, Z Chen. Autologous iPSC-derived dopamine neuron transplantation in a nonhuman primate Parkinson’s disease model. Cell Discov, 2015. [DOI | PubMed]
  211. K Watanabe, D Kamiya, A Nishiyama, T Katayama, S Nozaki, H Kawasaki, Y Sasai. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci, 2005. [PubMed]
  212. RL Watts, CD Raiser, NP Stover, ML Cornfeldt, AW Schweikert, RC Allen, RA Bakay. Stereotaxic intrastriatal implantation of human retinal pigment epithelial (hRPE) cells attached to gelatin microcarriers: a potential new cell therapy for Parkinson’s disease. J Neural Transm Suppl, 2003
  213. F Wianny, PY Bourillot, C Dehay. Embryonic stem cells in non-human primates: An overview of neural differentiation potential. Differentiation, 2011. [PubMed]
  214. H Widner, P Brundin, A Bjorklund, E Moller. Survival and immunogenicity of dissociated allogeneic fetal neural dopamine-rich grafts when implanted into the brains of adult mice. Exp Brain Res, 1989. [PubMed]
  215. MJ Wilby, SR Sinclair, EM Muir, R Zietlow, KH Adcock, P Horellou, JW Fawcett. A glial cell line-derived neurotrophic factor-secreting clone of the Schwann cell line SCTM41 enhances survival and fiber outgrowth from embryonic nigral neurons grafted to the striatum and to the lesioned substantia nigra. J Neurosci, 1999. [PubMed]
  216. SM Williams, PS Goldman-Rakic. Widespread origin of the primate mesofrontal dopamine system. Cereb Cortex, 1998. [PubMed]
  217. EF Wolff, L Mutlu, EE Massasa, JD Elsworth, D Eugene Redmond Jr., HS Taylor. Endometrial stem cell transplantation in MPTP-exposed primates: an alternative cell source for treatment of Parkinson’s disease. J Cell Mol Med, 2015. [PubMed]
  218. J Xi, Y Liu, H Liu, H Chen, ME Emborg, SC Zhang. Specification of midbrain dopamine neurons from primate pluripotent stem cells. Stem Cells, 2012. [PubMed]
  219. D Xiao, GM Miller, A Jassen, SV Westmoreland, D Pauley, BK Madras. Ephrin/Eph receptor expression in brain of adult nonhuman primates: implications for neuroadaptation. Brain Res, 2006. [PubMed]
  220. Q Xu, X Jiang, Y Ke, S Zhang, R Xu, Y Zeng. Gene therapy in hemiparkinsonian rhesus monkeys: long-term survival and behavioral recovery by transplantation of autologous human tyrosine hydroxylase-expressing neural stem cells. Cytotherapy, 2010. [PubMed]
  221. Y Yan, D Yang, ED Zarnowska, Z Du, B Werbel, C Valliere, SC Zhang. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells, 2005. [PubMed]
  222. D Yang, ZJ Zhang, M Oldenburg, M Ayala, SC Zhang. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells, 2008. [PubMed]
  223. Y Yang, BS Tang, JF Guo. Parkinson’s Disease and Cognitive Impairment. Parkinsons Dis, 2016. [DOI | PubMed]
  224. D Yin, FE Valles, MS Fiandaca, J Forsayeth, P Larson, P Starr, KS Bankiewicz. Striatal volume differences between non-human and human primates. J Neurosci Meth, 2009
  225. Y Yue, DA Widmer, AK Halladay, DP Cerretti, GC Wagner, JL Dreyer, R Zhou. Specification of distinct dopaminergic neural pathways: roles of the Eph family receptor EphB1 and ligand ephrin-B2. J Neurosci, 1999. [PubMed]
  226. JW Yun, JB Ahn, BC Kang. Modeling Parkinson’s disease in the common marmoset (Callithrix jacchus): overview of models, methods, and animal care. Lab Anim Res, 2015. [PubMed]
  227. X Zeng, J Cai, J Chen, Y Luo, ZB You, E Fotter, WJ Freed. Dopaminergic differentiation of human embryonic stem cells. Stem Cells, 2004. [PubMed]
  228. C Zhang, Y Jin, KS Ziemba, AM Fletcher, B Ghosh, E Truit, GM Smith. Long distance directional growth of dopaminergic axons along pathways of netrin-1 and GDNF. Exp Neurol, 2013. [PubMed]
  229. Y Zhou, M Sun, H Li, M Yan, Z He, W Wang, S Lu. Recovery of behavioral symptoms in hemi-parkinsonian rhesus monkeys through combined gene and stem cell therapy. Cytotherapy, 2013. [PubMed]

Related Posts

The content on this platform is provided for informational and educational purposes only and does not constitute medical advice, diagnosis, or treatment. Always consult a qualified healthcare professional before making any health-related decisions.