Improving the Survival of Human CNS Precursor-Derived Neurons after Transplantation

Journal of Neuroscience Research

Volumn 76, Issue 2, 2004, Pages 174-183

  Le Belle, J E ^a,c   Caldwell, M A ^a   Svendsen, C N ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Human; Neural; Precursor; Survival; Transplant

Indexed keywords

GLYCOGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL CULTURE; CELL DEATH; CELL METABOLISM; CELL MIGRATION; CELL POPULATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONFERENCE PAPER; CONTROLLED STUDY; DENTATE GYRUS; DISEASE MARKER; EMBRYO; ENERGY METABOLISM; GLIA CELL; GLYCOGEN METABOLISM; GRAFT SURVIVAL; HIPPOCAMPUS; HUMAN; HUMAN NEURAL PRECURSOR CELL; IN VIVO STUDY; METABOLIC STRESS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STARVATION; STEM CELL; STEM CELL TRANSPLANTATION; STRESS;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; EMBRYO; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLYCOGEN; HUMANS; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; L-LACTATE DEHYDROGENASE; MICROSCOPY, CONFOCAL; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RATS; STEM CELL TRANSPLANTATION; STEM CELLS; TIME FACTORS; TUBULIN;

EID: 1842583609     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20035     Document Type: Conference Paper

References (65)

1. Abercrombie, M. 1946 Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Akerud P, Canals JM, Snyder EY, Arenas E. 2001. Neuroprotection through delivery of glial cell line-derived neurotrophic factor by neural stem cells in a mouse model of Parkinson's disease. J Neurosci 21:8108-8118.
3. Ames A 3rd. 1992. Energy requirements of CNS cells as related to their function and to their vulnerability to ischemia: a commentary based on studies on retina. Can J Physiol Pharmacol 70(Suppl):158-164.
4. Aronowski J, Cho KH, Strong R, Grotta JC. 1999. Neurofilament proteolysis after focal ischemia; when do cells die after experimental stroke? J Cereb Blood Flow Metab 19:652-660.
5. Benzi G, Dagani F, Arrigoni E. 1978. Acute model for the estimation of the cerebral energy state during or after hypoxia and complete or incomplete ischaemia. Eur Neurol 17(Suppl):87-96.
6. Bjorklund A, Lindvall O. 2000. Cell replacement therapies for central nervous system disorders. Nat Neurosci 3:537-544.
7. Bjorklund L, Spenger C, Stromberg 1997. Tirilazad mesylate increases dopaminergic neuronal survival in the in Oculo grafting model. Exp Neurol 148:324-333.
8. Broadwell RD, Charlton HM, Ebert PS, Hickey WF, Shirazi Y, Villegas J, Wolf AL. 1991. Allografts of CNS tissue possess a blood-brain barrier. II. Angiogenesis in solid tissue and cell suspension grafts. Exp Neurol 112: 1-28.
9. Brundin P, Pogarell O, Hagell P, Piccini P, Widner H, Schrag A, Kupsch A, Crabb L, Odin P, Gustavii B, Bjorklund A, Brooks DJ, Marsden CD, Oertel WH, Quinn NP, Rehncrona S, Lindvall O. 2000. Bilateral caudate and putamen grafts of embryonic mesencephalic tissue treated with lazaroids in Parkinson's disease. Brain 123:1380-1390.
10. Caldwell MA, He X, Wilkie N, Pollack S, Marshall G, Wafford KA, Svendsen CN. 2001. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat Biotechnol 19:475-479.
11. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. 2001. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167:48-58.
12. Cavaliere F, D'Ambrosi N, Sancesario G, Bernardi G, Volonte C. 2001. Hypoglycaemia-induced cell death: features of neuroprotection by the P2 receptor antagonist basilen blue. Neurochem Int 38:199-207.
13. Clarkson ED, Zawada WM, Freed CR. 1997. GDNF improves survival and reduces apoptosis in human embryonic dopaminergic neurons in vitro. Cell Tissue Res 289:207-210.
14. Clarkson ED, Zawada WM, Bell KP, Esplen JE, Choi PK, Heidenreich KA, Freed CR. 2001. IGF-I and bFGF improve dopamine neuron survival and behavioral outcome in parkinsonian rats receiving cultured human fetal tissue strands. Exp Neurol 168:183-191.
15. Davoli MA, Fourtounis J, Tam J, Xanthoudakis S, Nicholson D, Robertson GS, Ng GY, Xu D. 2002. Immunohistochemical and biochemical assessment of caspase-3 activation and DNA fragmentation following transient focal ischemia in the rat. Neuroscience 115:125-136.
16. Dringen R, Gebhardt R, Hamprecht B. 1993. Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623: 208-214.
17. Englund U, Bjorklund A, Wictorin K. 2002. Migration patterns and phenotypic differentiation of long-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res Dev Brain Res 134:123-141.
18. Freed WJ. 1985. In: Björklund A, Stenevi U, editors. Neural grafting in the mammalian CNS. Amsterdam: Elsevier. p 32-40.
19. Freed CR, Greene PE, Breeze RE, Tsai WY, DuMouchel W, Kao R, Dillon S, Winfield H, Culver S, Trojanowski JQ, Eidelberg D, Fahn S. 2001. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 344:710-719.
20. Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Bjorklund A. 1999. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 19:5990-6005.
21. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J. 1995. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92:11879-11883.
22. Geny C, Naimi-Sadaoui S, Jeny R, Belkadi AM, Juliano SL, Peschanski M. 1994. Long-term delayed vascularization of human neural transplants to the rat brain. J Neurosci 14:7553-7562.
23. Gideon P, Henriksen O, Sperling B, Christiansen P, Olsen TS, Jorgensen HS, Arlien-Soborg P. 1992. Early time course of N-acetyl aspartate, creatine and phosphocreatine, and compounds containing choline in the brain after acute stroke. A proton magnetic resonance spectroscopy study. Stroke 23:1566-1572.
24. Grasbon-Frodl EM, Nakao N, Brundin P. 1996. The lazaroid U-83836E improves the survival of rat embryonic mesencephalic tissue stored at 4°C and subsequently used for cultures or intracerebral transplantation. Brain Res Bull 39:341-347.
25. Grasbon-Frodl EM, Nakao N, Lindvall O, Brundin P. 1997. Developmental features of human striatal tissue transplanted in a rat model of Huntington's disease. Neurobiol Dis 3:299-311.
26. Gwag BJ, Lobner D, Koh JY, Wie MB, Choi DW. 1995. Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience 68:615-619.
27. Hansson O, Castilho RF, Kaminski Schierle GS, Karlsson J, Nicotera P, Leist M, Brundin P. 2000. Additive effects of caspase inhibitor and lazaroid on the survival of transplanted rat and human embryonic dopamine neurons. Exp Neurol 164:102-111.
28. Herman JP, Abrous ND. 1994. Dopaminergic neural grafts after fifteen years: results and perspectives. Prog Neurobiol 44:1-35.
29. Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol 46:867-877.
30. Jain M, Armstrong RJ, Elneil S, Rosser AE, Barker RA. 2003. Migration and differentiation of transplanted human neural precursor cells. Neuroreport 14:1257-1262.
31. Juurlink BH, Hertz L. 1993. Ischemia-induced death of astrocytes and neurons in primary culture: pitfalls in quantifying neuronal cell death. Brain Res Dev Brain Res 71:239-246.
32. Karlsson J, Love RM, Clarke DJ, Brundin P. 1999. Effects of anaesthetics and lazaroid U-83836E on survival of transplanted rat dopaminergic neurones. Brain Res 821:546-550.
33. Knusel B, Michel PP, Schwaber JS, Hefti F. 1990. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and the insulin-like growth factors I and II. J Neurosci 10:558-570.
34. Kordower JH, Freeman TB, Chen EY, Mufson EJ, Sanberg PR, Hauser RA, Snow B, Olanow CW. 1998. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Mov Disord 13:383-393.
35. Krum JM, Rosenstein JM. 1988. Patterns of angiogenesis in neural transplant models: II. Fetal neocortical transplants. J Comp Neurol 271:331-345.
36. Lindvall O. 1999. Cerebral implantation in movement disorders: state of the art. Mov Disord 14:201-205.
37. Lindvall O, Sawle G, Widner H, Rothwell JC, Bjorklund A, Brooks D, Brundin P, Frackowiak R, Marsden CD, Odin P. 1994. Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson's disease. Ann Neurol 35:172-180.
38. Lowry OH. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
39. Lowry OH, Passonneau JV, Hasselberger FX, Schulz DW. 1964. Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J Biol Chem 239:18-30.
40. Lundberg C, Martinez-Serrano A, Cattaneo E, McKay RD, Bjorklund A. 1997. Survival, integration, and differentiation of neural stem cell lines after transplantation to the adult rat striatum. Exp Neurol 145:342-360.
41. Magistretti FJ, Sorg O, Yu N, Martin JL, Pellerin L. 1993. Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev Neurosci 15:306-312.
42. Olanow CW, Kordower JH, Freeman TB. 1996. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci 19:102-109.
43. Ostenfeld T, Caldwell MA, Prowse KR, Linskens MH, Jauniaux E, Svendsen CN. 2000. Human neural precursor cells express low levels of telomerase in vitro and show diminishing cell proliferation with extensive axonal outgrowth following transplantation. Exp Neurol 164:215-226.
44. Ouyang YB, He QP, Li PA, Janelidze S, Wang GX, Siesjo BK. 2000. Is neuronal injury caused by hypoglycemic coma of the necrotic or apoptotic type? Neurochem Res 25:661-667.
45. Pauwels PJ, Opperdoes FR, Trouet A. 1985. Effects of antimycin, glucose deprivation, and serum on cultures of neurons, astrocytes, and neuroblastoma cells. J Neurochem 44:143-148.
46. Passonneau JV, Lauderdale VR. 1974. A comparison of three methods of glycogen measurement in tissues. Anal Biochem 60:405-412.
47. Pellerin L, Stolz M, Sorg O, Martin JL, Deschepper CF, Magistretti PJ. 1997. Regulation of energy metabolism by neurotransmitters in astrocytes in primary culture and in an immortalized cell line. Glia 21:74-83.
48. Reinhart PH, Pfeiffer B, Spengler S, Hamprecht B. 1990. Purification of glycogen phosphorylase from bovine brain and immunocytochemical examination of rat glial primary cultures using monoclonal antibodies raised against this enzyme. J Neurochem 54:1474-1483.
49. Rosenstein JM. 1995. Why do neural transplants survive? An examination of some metabolic and pathophysiological considerations in neural transplantation. Exp Neurol 133:1-6.
50. Rosenstein JM, Brightman MW. 1978. Intact cerebral ventricle as a site for tissue transplantation. Nature 276:83-85.
51. Rosser AE, Tyers P, Dunnett SB. 2000. The morphological development of neurons derived from EGF- and FGF-2-driven human CNS precursors depends on their site of integration in the neonatal rat brain. Eur J Neurosci 12:2405-2413.
52. Shetty AK, Gopinath G, Tandon PN. 1991. Fetal nigral transplants in the lateral ventricle of adult rats. A long-term morphological study. Dev Neurosci 13:1-10.
53. Suhonen JO, Peterson DA, Ray J, Gage FH. 1996. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383:624-627.
54. Swanson RA, Choi DW. 1993. Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 13:162-169.
55. Swanson RA, Yu AC, Sharp FR, Chan PH. 1989a. Regulation of glycogen content in primary astrocyte culture: effects of glucose analogues, phenobarbital, and methionine sulfoximine. J Neurochem 52:1359-1365.
56. Swanson RA, Sagar SM, Sharp FR. 1989b. Regional brain glycogen stores and metabolism during complete global ischaemia. Neurol Res 11:24-28.
57. Svendsen CN, Caldwell MA, Shen J, ter Borg MG, Rosser AE, Tyers P, Karmiol S, Dunnett SB. 1997. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp Neurol 148:135-146.
58. Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, Caldwell MA. 1998. A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 85: 141-152.
59. Vibulsreth S, Hefti F, Ginsberg MD, Dietrich WD, Busto R. 1987. Astrocytes protect cultured neurons from degeneration induced by anoxia. Brain Res 422:303-311.
60. Vicario-Abejon C, Cunningham MG, McKay RD. 1995. Cerebellar precursors transplanted to the neonatal dentate gyrus express features characteristic of hippocampal neurons. J Neurosci 15:6351-6363.
61. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
62. Winkler C, Fricker RA, Gates MA, Olsson M, Hammang JP, Carpenter MK, Bjorklund A. 1998. Incorporation and glial differentiation of mouse EGF-responsive neural progenitor cells after transplantation into the embryonic rat brain. Mol Cell Neurosci 11:99-116.
63. Wright LS, Li J, Caldwell MA, Wallace K, Johnson JA, Svendsen CN. 2003. Gene expression in human neural stem cells: effects of leukemia inhibitory factor. J Neurochem 86:179-195.
64. Yager JY, Kala G, Hertz L, Juurlink BH. 1994. Correlation between content of high-energy phosphates and hypoxic-ischemic damage in immature and mature astrocytes. Brain Res Dev Brain Res 82:62-68.
65. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA. 2001. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19:1129-1133.