Cellular repair in the parkinsonian nonhuman primate brain

Rejuvenation Research

Volumn 13, Issue 2-3, 2010, Pages 188-194

  Redmond Jr , Donald Eugene ^a   Weiss, Stephanie ^a   Elsworth, John D ^a   Roth, Robert H ^a   Wakeman, Dustin R ^b   Bjugstad, Kimberly B ^c   Collier, Timothy J ^d   Blanchard, Barbara C ^c   Teng, Yang D ^e   Synder, Evan Y ^f   Sladek Jr , John R ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Children's Hospital Colorado   (United States)

^d UNIVERSITY OF CINCINNATI   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CYTOKINE; DOPAMINE; DOPAMINE RECEPTOR; LEVODOPA; NERVE GROWTH FACTOR; NEURITE PROMOTING FACTOR;

ANATOMY; BRAIN; BRAIN CELL; CADAVER; CELL CULTURE; CELL DIFFERENTIATION; CELL MIGRATION; CELL REGENERATION; CELL TRANSPLANTATION; CLINICAL STUDY; CONTROLLED STUDY; CORPUS STRIATUM; CRYOPRESERVATION; CYTOKINE RELEASE; DISEASE SEVERITY; DONOR; DOPAMINERGIC NERVE CELL; DYSKINESIA; EMBRYONIC STEM CELL; FEASIBILITY STUDY; FETUS CELL; FETUS DEVELOPMENT; GENE THERAPY; GENETIC VARIABILITY; GRAFT PERFUSION; GRAFT SURVIVAL; HOST; HUMAN; IMMUNOHISTOCHEMISTRY; INTERSTITIAL FLUID; LONG TERM CARE; MOTOR DYSFUNCTION; NERVE GRAFT; NERVOUS SYSTEM; NEURAL STEM CELL; NEUROLOGIC DISEASE; NONHUMAN; PARKINSONISM; PATHOLOGY; PHYSIOLOGY; PRIMATE; PRIORITY JOURNAL; PUTAMEN; REDUCTION; REVIEW; SOMATIC CELL; SUBSTANTIA NIGRA; TARGET ORGAN; TREATMENT OUTCOME; VALIDATION PROCESS;

ANIMALS; BRAIN; DOPAMINE; EMBRYONIC STEM CELLS; HUMANS; NERVE REGENERATION; NEURONS; PARKINSONIAN DISORDERS; PRIMATES; STEM CELL TRANSPLANTATION;

PARKINSONIA; PRIMATES;

EID: 77952395905     PISSN: 15491684     EISSN: None     Source Type: Journal    
DOI: 10.1089/rej.2009.0960     Document Type: Review

References (55)

1. Bennett DA, Beckett LA, Murray AM, Shannon KM, Goetz CG, Pilgrim DM, Evans DA. Prevalence of parkinsonian signs and associated mortality in a community population of older people. The NewEngland journalofmedicine, 1996;334:71-76.
2. Rajput A. Movement disorders and aging. In: Watts R, Koller W, eds.: Movement Disorders: Neurologic Principles and Practice, New York: McGraw-Hill, 1997, pp 673-686.
3. Nichols ME, Meador KJ, Loring DW, Poon LW, Clayton GM, Martin P. Age-related changes in the neurologic examination of healthy sexagenarians, octogenarians, and centenarians. J Geriatr Psychiatry Neurol 1994;7:1-7.
4. Carlsson A, Winblad B. Influence of age and time interval between death and autopsy on dopamine and 3-methoxytyramine levels in human basal ganglia. J Neur Transmission 1976;38:271-276.
5. McGeer PL, McGeer EG, Suzuki JS. Aging and extrapyra-midal function. Arch Neurol 1977;34:33-35.
6. Adolfsson R, Gottfries CG, Roos BE, Winblad B. Postmortem distribution of dopamine and homovanillic acid in human brain, variations related to age, and a review of the literature. J Neur Transmission, 1979;45:81-105.
7. Hiral S. Ageing of the substantia nigra. Adv Neurol Sci 1968; 7:12845-12849.
8. Mann DM, Yates PO. Possible role of neuromelanin in the pathogenesis of Parkinson's disease. Mech Ageing Dev 1983; 21:193-203.
9. Fearnley JM, Lees AJ. Ageing and Parkinson's disease: Sub-stantia nigra regional selectivity. Brain 1991;114(Pt 5):2283-2301.
10. Bender A, Krishnan KJ, Morris CM, Taylor GA, Reeve AK, Perry RH, Jaros E, Hersheson JS, Betts J, Klopstock T, Taylor RW, Turnbull DM. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat Genet 2006;38:515-517.
11. Biskup S, Moore DJ. Detrimental deletions: Mitochondria, aging and Parkinson's disease. Bioessays 2006;28:963-967.
12. Burton A. mtDNA deletions associated with ageing and PD. Lancet Neurol 2006;5:477.
13. Smigrodzki R, Parks J, Parker WD. High frequency of mi-tochondrial complex I mutations in Parkinson's disease and aging. Neurobiol Aging, 2004;25:1273-1281.
14. Maeda T, Guan JZ, Oyama J, Higuchi Y, Makino N. Aging-associated alteration of subtelomeric methylation in Parkinson's disease. J Gerontol 2009;64:949-955.
15. Villar-Cheda B, Sousa-Ribeiro D, Rodriguez-Pallares J, Rodriguez-Perez AI, Guerra MJ, Labandeira-Garcia JL. Aging and sedentarism decrease vascularization and VEGF levels in the rat substantia nigra. Implications for Parkinson's disease. J Cereb Blood Flow Metab 2009;29:230-234.
16. Chu Y, Kompoliti K, Cochran EJ, Mufson EJ, Kordower JH. Age-related decreases in Nurr1 immunoreactivity in the human substantia nigra. J Comp Neurol 2002;450:203-214.
17. Jellinger KA. Alpha-synuclein lesions in normal aging, Parkinson disease, and Alzheimer disease: evidence from the Baltimore Longitudinal Study of Aging (BLSA). J Neuro-pathol Exp Neurol 2005;64:554.
18. Chu Y, Kordower JH. Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: Is this the target for Parkinson's disease? Neurobiol Dis 2007;25:134-149.
19. Leranth C, Roth RH, Elsworth JD, Naftolin F, Horvath TL, Redmond DE, Jr. Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: Implications for Parkinson's disease and memory. J Neurosci 2000;20:8604-8609.
20. Ragonese P, D'Amelio M, Callari G, Salemi G, Morgante L, Savettieri G. Age at menopause predicts age at onset of Parkinson's disease. Mov Disord 2006;21:2211-2214.
21. Lewitt PA. Levodopa for the treatment of Parkinson's disease. N Engl J Med 2008;359:2468-2476.
22. Hauser RA. Levodopa: Past, present, and future. Eur Neu-rol, 2009;62:1-8.
23. Lang AE. When and how should treatment be started in Parkinson disease? Neurology, 2009;72:S39-43.
24. Alexander T, Sortwell CE, Sladek CD, Roth RH, Steece-Collier K. Comparison of neurotoxicity following repeated administration of l-dopa, d-dopa and dopamine to embryonic mesencephalic dopamine neurons in cultures derived from Fisher 344 and Sprague-Dawley donors. Cell Trans-plantat 1997;6:309-315.
25. Thompson WG. Successful brain grafting. NY Med J 1890;51: 701-702.
26. Dunn EH. Primary and secondary findings in a series of attempts to transplant cerebral cortex in the albino rat. J Comp Neurol 1917;27:565-582.
27. Bjö rklund A, Stenevi U. Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res, 1979. 177. 555-560.
28. Perlow MJ, Freed WJ, Hoffer BJ, Seiger A, Olson L, Wyatt RJ. Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science 1979;204: 643-653.
29. Redmond DE, Jr., Sladek JR, Jr., Roth RH, Collier TJ, Els-worth JD, Deutch AY, Haber S. Fetal neuronal grafts in monkeys given methylphenyltetrahydropyridine. Lancet 1986;1:1125-1127.
30. Elsworth JD, Taylor JR, Redmond DE, Jr., Collier TJ, Sladek JR, Roth RH. Biochemical assessment of reversal of MPTP-induced parkinsonism following intrastriatal transplants of fetal substantia nigra in primates. Restor Neurol Neurosci 1989;1:59.
31. Redmond DE, Jr., Naftolin F, Collier TJ, Leranth C, Robbins RJ, Sladek CD, Roth RH, Sladek JR, Jr. Cryopreservation, culture, and transplantation of human fetal mesencephalic tissue into monkeys. Science 1988;242:768-771.
32. Redmond DE, Jr. Cellular replacement therapy for Parkinson's disease\where are we today? Neuroscientist 2002;8: 457-488.
33. Bjorklund A, Dunnett SB. Fifty years of dopamine research. Trends Neurosci 2007;30:185-187.
34. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 2008;14:504-506.
35. Liu X, Huang J, Chen T, Wang Y, Xin S, Li J, Pei G, Kang J. Yamanaka factors critically regulate the developmental signaling network in mouse embryonic stem cells. Cell Res 2008;18:1177-1189.
36. Mendez I, Vinuela A, Astradsson A, Mukhida K, Hallett P, Robertson H, Tierney T, Holness R, Dagher A, Trojanowski JQ, Isacson O. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat Med 2008;14:507-509.
37. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Bill-inghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998;16:1033-1039.
38. Bentlage C, Nikkhah G, Cunningham MG, Bjorklund A. Reformation of the nigrostriatal pathway by fetal dopaminergic micrografts into the substantia nigra is critically dependent on the age of the host. Exp Neurol 1999;159:177-190.
39. Mendez I, Hong M. Reconstruction of the striato-nigro-striatal circuitry by simultaneous double dopaminergic grafts: A tracer study using fluorogold and horseradish peroxidase. Brain Res 1997;778:194-205.
40. Mendez I, Baker KA, Hong M. Simultaneous intrastriatal and intranigral grafting (double grafts) in the rat model of Parkinson's disease. Brain Res Brain Res Rev 2000;32:328-339. (Pubitemid 30177337)
41. Mendez I, Dagher A, Hong M, Gaudet P, Weerasinghe S, McAlister V, King D, Desrosiers J, Darvesh S, Acorn T, Robertson H. Simultaneous intrastriatal and intranigral fetal dopaminergic grafts in patients with Parkinson disease: A pilot study. Report of three cases. J Neurosurg 2002;96:589-596.
42. Collier T, Elsworth J, Taylor J, Sladek J, Jr., Roth R, Redmond D, Jr. Peripheral nerve-dopamine neuron co-grafts in MPTP-treated monkeys: Augmentation of tyrosine hydroxylase-positive fiber staining and dopamine content in host systems. Neuroscience 1994; 61:875-889.
43. Sladek JR, Jr., Bjugstad KB, Collier TJ, Bundock EA, Blan-chard BC, Elsworth JD, Roth RH, Redmond DE, Jr. Embryonic substantia nigra grafts show directional outgrowth to cografted striatal grafts and potential for pathway reconstruction in nonhuman primate. Cell Transplant 2008;17:427-444.
44. Elsworth JD, Redmond DE, Jr., Leranth C, Bjugstad KB, Sla-dek JR, Jr., Collier TJ, Foti SB, Samulski RJ, Vives KP, Roth RH. 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;211: 252-258.
45. Redmond DE, Jr., Elsworth JD, Roth RH, Leranth C, Collier TJ, Blanchard B, Bjugstad KB, Samulski RJ, Aebischer P, Sladek JR, Jr. Embryonic substantia nigra grafts in the mes-encephalon send neurites to the host striatum in non-human primate after overexpression of GDNF. J Comp Neurol 2009; 515:31-40.
46. Redmond DE, Jr., Bjugstad KB, Teng YD, Ourednik V, Ourednik J, Wakeman DR, Parsons XH, Gonzalez R, Blan-chard BC, Kim SU, Gu Z, Lipton SA, Markakis EA, Roth RH, Elsworth JD, Sladek JR, Jr., Sidman RL, Snyder EY. Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc Natl Acad Sci USA 2007;104:12175-12180.
47. Bjugstad KB, Teng YD, Redmond DE, Jr., Elsworth JD, Roth RH, Cornelius SK, Snyder EY, Sladek JR, Jr. Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease. Exp Neurol 2008;211:362-369.
48. Wakeman DR, Hofmann MR, Redmond DE, Jr., Teng YD, Snyder EY. Long-term multilayer adherent network (MAN) expansion, maintenance, and characterization, chemical and genetic manipulation, and transplantation of human fetal forebrain neural stem cells. Curr Prot Stem Cell Biol 2009; Chapter 2:Unit2D 3.
49. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahles-tedt C, Kim KS, Isacson O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 2002;99: 2344-2349.
50. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N. Dopa-minergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 2005;115:102-109.
51. Cho MS, Lee YE, Kim JY, Chung S, Cho YH, Kim DS, Kang SM, Lee H, Kim MH, Kim JH, Leem JW, Oh SK, Choi YM, Hwang DY, Chang JW, Kim DW. Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci USA 2008; 105:3392-3397.
52. O'Keeffe FE, Scott SA, Tyers P, O'Keeffe GW, Dalley JW, Zufferey R, Caldwell MA. Induction of A9 dopaminergic neurons from neural stem cells improves motor function in an animal model of Parkinson's disease. Brain 2008;131:630-641.
53. Yang D, Zhang ZJ, Oldenburg M, Ayala M, Zhang SC. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells (Dayton, Ohio) 2008;26:55-63.
54. Ferrari D, Sanchez-Pernaute R, Lee H, Studer L, Isacson O. Transplanted dopamine neurons derived from primate ES cells preferentially innervate DARPP-32 striatal progenitors within the graft. Eur J Neurosci 2006;24:1885-1896.
55. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, Soldner F, Broccoli V, Constantine-Paton M, Isacson O, Jaenisch R. 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.