Gene therapy in hemiparkinsonian rhesus monkeys: long-term survival and behavioral recovery by transplantation of autologous human tyrosine hydroxylase-expressing neural stem cells

References

• Mendez I, Sanchez-Pernaute R, Cooper O, . Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson’s disease. Brain. 2005;128:1498–510.
   PubMed Web of Science ®Google Scholar
• Freed CR, Breeze RE, Rosenberg NL, . Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson’s disease. N Engl J Med. 1992;327:1549–55.
   PubMed Web of Science ®Google Scholar
• Widner H, Tetrud J, Rehncrona S, Snow B, . Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). N Engl J Med. 1992;327:1556–63.
   PubMed Web of Science ®Google Scholar
• Fisher LJ, Jinnah HA, Kale LC, . Survival and function of intrastriatally grafted primary fibroblasts genetically modified to produce L-dopa. Neuron. 1991;6:371–80.
   PubMed Web of Science ®Google Scholar
• Horellou P, Mallet J. Gene therapy for Parkinson’s disease. Mol Neurobiol. 1997;15:241–56.
   Google Scholar
• During MJ, Samulski RJ, Elsworth JD, . In vivo expression of therapeutic human genes for dopamine production in the caudates of MPTP-treated monkeys using an AAV vector. Gene Ther. 1998;5:820–7.
   PubMed Web of Science ®Google Scholar
• Diduch DR, Coe MR, Joyner C, . Two cell lines from bone marrow that differ in terms of collagen synthesis, osteogenic characteristics, and matrix mineralization. J Bone Joint Surg Am. 1993;75:92–105.
   PubMedGoogle Scholar
• Caplan AI. Mesenchymal stem cells and gene therapy. Clin Orthop Relat Res. 2000;379(Suppl):S67–70.
   Google Scholar
• Bruder SP, Jaiswal N, Haynesworth SE. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem. 1997; 64:278–94.
   PubMed Web of Science ®Google Scholar
• Prockop DJ, Sekiya I, Colter DC. Isolation and characterization of rapidly self-renewing stem cells from cultures of human marrow stromal cells. Cytotherapy. 2001;3:393–6.
   PubMed Web of Science ®Google Scholar
• Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA. 1997;94:4080–5.
   PubMed Web of Science ®Google Scholar
• Pereira RF, O’Hara MD, Laptev AV, . Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci USA. 1998;95:1142–7.
   PubMed Web of Science ®Google Scholar
• Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci USA. 1999;96:10711–16.
   PubMed Web of Science ®Google Scholar
• Levy YS, Bahat-Stroomza M, Barzilay R, . Regenerative effect of neural-induced human mesenchymal stromal cells in rat models of Parkinson’s disease. Cytotherapy. 2008; 10:340–52.
   PubMed Web of Science ®Google Scholar
• Schwarz EJ, Reger RL, Alexander GM, . Rat marrow stromal cells rapidly transduced with a self-inactivating retrovirus synthesize L-DOPA in vitro. Gene Ther. 2001;8: 1214–23
   PubMed Web of Science ®Google Scholar
• Jiang X, Xu R, Yang Z, Jin P, Xu Q. Experimental study on trace marking and oncogenicity of neural stem cells derived from bone marrow. Cell Mol Neurobiol. 2008;28:689–711.
   Google Scholar
• Pitts SM, Markey SP, Murphy DL, . Recommended practices for the safe handling of MPTP. Markey SP, Castagnoli N, Trevor AJ, Kopin IJ. MPTP: A neurotoxin producing a Parkinsonian syndrome. Orlando: Academic Press; 1986. 703–15.
   Google Scholar
• Elsworth JD, Deutch AY, Redmond DE Jr, . Symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates: biochemical changes in striatal regions. Neuroscience. 1989;33:323–31.
   Google Scholar
• Ovadia A, Zhang Z, Gash DM. Increased susceptibility to MPTP toxicity in middle-aged rhesus monkeys. Neurobiol Aging. 1995;6:931–937.
   Google Scholar
• Smeyne RJ, Jackson-Lewis V. The MPTP model of Parkinson’s disease. Brain Res Mol Brain Res. 2005;134:57–66.
   PubMedGoogle Scholar
• O’Malley KL, Anhalt MJ, Martin BM, . Isolation and characterization of the human tyrosine hydroxylase gene: identification of 5′ alternative splice sites responsible for multiple mRNAs. Biochemistry. 1987;26:6910–14.
   PubMedGoogle Scholar
• Jiang X, Xu R, Guo Z, . Neurobiochemistry and neuroelectrophysiology of neuron-like cells differentiated from neural BMSCs-D-NSCs. Conf Proc IEEE Eng Med Biol Soc. 2005;5:5215–18.
   Google Scholar
• Collier TJ, Sortwell CE, Elsworth JD, . 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;442:320–30.
   PubMed Web of Science ®Google Scholar
• Bjugstad KB, Redmond DE Jr, Teng YD, . 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;14:183–92.
   Google Scholar
• Ostenfeld T, Svendsen CN. Recent advances in stem cell neurobiology. Adv Tech Stand Neurosurg. 2003;28:3–89.
   Google Scholar
• Lakatos A, Franklin RJ. Transplant mediated repair of the central nervous system: an imminent solution? Curr Opin Neurol. 2002;15:701–5.
   Google Scholar
• Riess P, Zhang C, Saatman KE, . Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery. 2002;51:1043–54.
   PubMed Web of Science ®Google Scholar
• Beyer Nardi N, da Silva Meirelles L. Mesenchymal stem cells: isolation, in vitro expansion and characterization. Handb Exp Pharmacol. 2006;174:249–82.
   PubMedGoogle Scholar
• Woodbury D, Schwarz EJ, Prochop DJ, . Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61:364–70.
   PubMed Web of Science ®Google Scholar
• Hermann A, Gastl R, Liebau S, . Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci. 2004;117:4411–22.
   PubMed Web of Science ®Google Scholar
• Katarzyna A, Kuzhikandathil EV, Rameshwar P, Trzaska KA, Eldo V, . Specification of a dopaminergic phenotype from adult human mesenchymal stem cells. Stem Cell. 2007;25:2797–808.
   Google Scholar
• Garcia AD, Doan NB, Imura T, . GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci. 2004;7:1233–41.
   PubMed Web of Science ®Google Scholar
• Bonaguidi MA, McGuire T, Hu M, . LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development. 2005;132:5503–14.
   PubMed Web of Science ®Google Scholar
• Coyne TM, Akiva J, Marcus AJ, Woodbury D, Black IB, . Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. Stem Cells. 2006;24:2483–92.
   PubMed Web of Science ®Google Scholar
• Fischman AJ, Babich JW, Elmaleh DR, . SPECT imaging of dopamine transporter sites in normal and MPTP-treated rhesus monkeys. J Nucl Med. 1997;38:144–50.
   Google Scholar
• Huang WS, Chiang YH, Lin JC, Chou YH, Cheng CY, Liu RS, . Crossover study of 99mTc-TRODAT-1 SPECT and 18F-FDOPA PET in Parkinson’s disease patients. J Nucl Med. 2003;44:999–1005.
   Google Scholar
• Kish SJ, Shannak K, Hornykiewicz O. Uneven pattern of dopamine loss in striatum of patients with idiopathic Parkinson’s disease. N Engl J Med. 1988;876:876–80
   Google Scholar
• Chen Y, Teng F, Tang B. Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: progress and uncertainties. Cell Mol Life Sci. 2006;63: 1649–57.
   PubMed Web of Science ®Google Scholar
• Pisati F, Bossolasco P, Meregalli M, . Induction of neurotrophin expression via human adult mesenchymal stem cells: implication for cell therapy in neurodegenerative diseases. Cell Transplant. 2007;16:41–55.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Ringden O. Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr Opin Immunol. 2006;18:586–91.
   PubMed Web of Science ®Google Scholar
• Deng YB, Liu XG, Liu ZG, . Implantation of BM mesenchymal stem cells into injured spinal cord elicits de novo neurogenesis and functional recovery: evidence from a study in rhesus monkeys. Cytotherapy. 2006;8:210–14.
   PubMed Web of Science ®Google Scholar
• Berding G, Odin P, Brooks DJ, . Resting regional cerebral glucose metabolism in advanced Parkinson’s disease studied in the off and on conditions with F-18 FDG-PET. Mov Disord. 2001;16:1014–22.
   PubMedGoogle Scholar
• Eidelberg D, Moeller JR, Ishikawa T, . Early differential diagnosis of Parkinson’s disease with F-18-FDG and PET. Neurology. 1995;45:1995–2004.
   Google Scholar
• Lu L, Zhao C, Liu Y, Sun X, Duan C, Ji M, . Therapeutic benefit of TH-engineered mesenchymal stem cells for Parkinson’s disease. Brain Res Brain Res Protoc. 2005;15:46–51.
   Google Scholar