What is the potential of oligodendrocyte progenitor cells to successfully treat human spinal cord injury?

BMC Neurology

Volumn 11, Issue , 2011, Pages

  Watson, Robert A ^a   Yeung, Trevor M ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TACROLIMUS;

ARTICLE; CELL VIABILITY; CLINICAL TRIAL (TOPIC); DEMYELINATION; EMBRYONIC STEM CELL; GRAFT REJECTION; HUMAN; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; OLIGODENDROCYTE STEM CELL TRANSPLANTATION; PATHOGENESIS; PATIENT SAFETY; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; THERAPY EFFECT; UNSPECIFIED SIDE EFFECT; ANIMAL; DISEASE MODEL; METHODOLOGY; OLIGODENDROGLIA; PATHOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); REVIEW; SPINAL CORD; TRANSPLANTATION;

ANIMALS; CLINICAL TRIALS, PHASE I AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; OLIGODENDROGLIA; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION;

EID: 80053172088     PISSN: None     EISSN: 14712377     Source Type: Journal    
DOI: 10.1186/1471-2377-11-113     Document Type: Article

References (94)

1. Spinal Injury Network. Accessed 29th July 2011., http://www.spinal-injury.net/treatment-of-spinal-cord-injury.htm
2. ClinicalTrials.gov. Search for: Trial ID: NCT01217008. Accessed 29th July 2011., http://www.clinicaltrials.gov
3. Geron Corporation Information for patients, clinical trial details. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/patients/clinicaltrials/hESC.aspx
4. Geron Corporation Press Release 23/01/09 - Geron receives FDA clearance to begin World's first human clinical trial of embryonic stem cell-based therapy. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/media/pressview.aspx?id=1148
5. BBC News Online. Accessed 29th July 2011., http://news.bbc.co.uk/1/hi/health/7847450.stm
6. Geron Corporation Press Release 18/08/2009 - Geron's IND for spinal cord injury placed on hold. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/investors/factsheet/pressview.aspx?id=1187
7. Geron Corporation Press Release 28/07/2010 - Geron to proceed with first human clinical trial of embryonic stem cell-based therapy. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/media/pressview.aspx?id=1229
8. Marshall E. Gene therapy: Second child in French trial is found to have leukemia. Science 2003, 299:320-320. 10.1126/science.299.5605.320, 12531981.
9. Sekhon LHS, Fehlings MG. Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 2001, 26:S2-S12. 10.1097/00007632-200112151-00002, 11805601.
10. Bauchet L, Lonjon N, Perrin FE, Gilbert C, Privat A, Fattal C. Strategies for spinal cord repair after injury: a review of the literature and information. Ann Phys Rehabil Med 2009, 52:330-351.
11. National Spinal Cord Injury Statistic Centre Facts and Figures at a Glance 2011. Accessed 29th July 2011, National Spinal Cord Injury Statistic Centre., https://www.nscisc.uab.edu/public_content/pdf/Facts%202011%20Feb%20Final.pdf
12. Potter PJ. Disordered control of the urinary bladder after human spinal cord injury: what are the problems?. Autonomic Dysfunction after Spinal Cord Injury 2006, 152:51-57. Amsterdam: Elsevier Science.
13. Ravenscroft A, Ahmed YS, Burnside IG. Chronic pain after SCI. A patient survey. Spinal Cord 2000, 38:611-614. 10.1038/sj.sc.3101073, 11093322.
14. Kennedy P, Rogers BA. Anxiety and depression after spinal cord injury: A longitudinal analysis. Archives of Physical Medicine and Rehabilitation 2000, 81:932-937. 10.1053/apmr.2000.5580, 10896007.
15. Kennedy P, Evans MJ. Evaluation of post traumatic distress in the first 6 months following SCI. Spinal Cord 2001, 39:381-386. 10.1038/sj.sc.3101172, 11464312.
16. Noreau L, Fougeyrollas P. Long-term consequences of spinal cord injury on social participation: the occurrence of handicap situations. Disabil Rehabil 2000, 22:170-180. 10.1080/096382800296863, 10798305.
17. McDonald JW, Sadowsky C. Spinal-cord injury. Lancet 2002, 359:417-425. 10.1016/S0140-6736(02)07603-1, 11844532.
18. Tator CH. Update on the pathophysiology and pathology of acute spinal-cord injury. Brain Pathology 1995, 5:407-413. 10.1111/j.1750-3639.1995.tb00619.x, 8974623.
19. Rowland JW, Hawryluk GWJ, Kwon B, Fehlings MG. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurgical Focus 2008, 25.
20. Kakulas BA. A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 1999, 22:119-124.
21. Kakulas BA. Neuropathology: the foundation for new treatments in spinal cord injury. Spinal Cord 2004, 42:549-563. 10.1038/sj.sc.3101670, 15346131.
22. Norenberg MD, Smith J, Marcillo A. The pathology of human spinal cord injury: Defining the problems. Journal of Neurotrauma 2004, 21:429-440. 10.1089/089771504323004575, 15115592.
23. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW, Bethea J, Levi ADO. Apoptosis after traumatic human spinal cord injury. Journal of Neurosurgery 1998, 89:911-920. 10.3171/jns.1998.89.6.0911, 9833815.
24. Beattie MS, Farooqui AA, Bresnahan JC. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 2000, 17:915-925. 10.1089/neu.2000.17.915, 11063057.
25. Geron Corporation GRNOPC1 Background Information. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/GRNOPC1Trial/grnopc1-backgrounder.pdf
26. Faulkner J, Keirstead HS. Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transplant Immunology 2005, 15:131-142. 10.1016/j.trim.2005.09.007, 16412957.
27. Coutts M, Keirstead HS. Stem cells for the treatment of spinal cord injury. Experimental Neurology 2008, 209:368-377. 10.1016/j.expneurol.2007.09.002, 17950280.
28. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
29. Rossi SL, Keirstead HS. Stem cells and spinal cord regeneration. Current Opinion in Biotechnology 2009, 20:552-562. 10.1016/j.copbio.2009.09.008, 19836942.
30. Kan EM, Ling EA, Lu J. Stem cell therapy for spinal cord injury. Curr Med Chem 2010, 17:4492-4510. 10.2174/092986710794182971, 21062255.
31. Mackay-Sim A, St John JA. Olfactory ensheathing cells from the nose: clinical application in human spinal cord injuries. Exp Neurol 2011, 229:174-180. 10.1016/j.expneurol.2010.08.025, 20832402.
32. Uccelli A, Benvenuto F, Laroni A, Giunti D. Neuroprotective features of mesenchymal stem cells. Best Pract Res Clin Haematol 2011, 24:59-64. 10.1016/j.beha.2011.01.004, 21396593.
33. Rossi SL, Nistor G, Wyatt T, Yin HZ, Poole AJ, Weiss JH, Gardener MJ, Dijkstra S, Fischer DF, Keirstead HS. Histological and functional benefit following transplantation of motor neuron progenitors to the injured rat spinal cord. PLoS One 2010, 5(7):e11852. 10.1371/journal.pone.0011852, 2912300, 20686613.
34. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 2005, 49(3):385-396. 10.1002/glia.20127, 15538751.
35. Hatch MN, Nistor G, Keirstead HS. Derivation of High-Purity Oligodendroglial Progenitors. Neural Cell Transplantation 2009, 59-75.
36. Waxman SG. Demyelination in spinal-cord injury. Journal of the Neurological Sciences 1989, 91(12):1-14.
37. Totoiu MO, Keirstead HS. Spinal cord injury is accompanied by chronic progressive demyelination. Journal of Comparative Neurology 2005, 486(4):373-383. 10.1002/cne.20517, 15846782.
38. Guest JD, Hiester ED, Bunge RP. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 2005, 192(2):384-393. 10.1016/j.expneurol.2004.11.033, 15755556.
39. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 1998, 280(5369):1610-1613. 10.1126/science.280.5369.1610, 9616125.
40. Lasiene J, Shupe L, Perlmutter S, Horner P. No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. Journal of Neuroscience 2008, 28(15):3887-3896. 10.1523/JNEUROSCI.4756-07.2008, 2631430, 18400887.
41. Siebert JR, Stelzner DJ, Osterhout DJ. Chondroitinase treatment following spinal contusion injury increases migration of oligodendrocyte progenitor cells. Exp Neurol 2011,
42. Su Z, Yuan Y, Chen J, Zhu Y, Qiu Y, Zhu F, Huang A, He C. Reactive Astrocytes Inhibit the Survival and Differentiation of Oligodendrocyte Precursor Cells by Secreted TNF-alpha. J Neurotrauma 2011, 28(6):1089-1100. 10.1089/neu.2010.1597, 21309692.
43. Wang Y, Cheng X, He Q, Zheng Y, Kim DH, Whittemore SR, Cao QL. Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci 2011, 31(16):6053-6058. 10.1523/JNEUROSCI.5524-09.2011, 3081104, 21508230.
44. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. Journal of Neuroscience 2005, 25(19):4694-4705. 10.1523/JNEUROSCI.0311-05.2005, 15888645.
45. Logan A, Berry M. Transforming growth factor-beta(1) and basic fibroblast growth-factor in the injured cns. Trends in Pharmacological Sciences 1993, 14(9):337-343. 10.1016/0165-6147(93)90007-7, 8249155.
46. Bareyre FM, Schwab ME. Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends in Neurosciences 2003, 26(10):555-563. 10.1016/j.tins.2003.08.004, 14522149.
47. Menei P, Montero-Menei C, Whittemore SR, Bunge RP, Bunge MB. Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. European Journal of Neuroscience 1998, 10(2):607-621. 10.1046/j.1460-9568.1998.00071.x, 9749723.
48. Hagg T, Oudega M. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 2006, 23(34):264-280.
49. McDonald JW, Belegu V. Demyelination and remyelination after spinal cord injury. J Neurotrauma 2006, 23(34):345-359.
50. Barnabe-Heider F, Goritz C, Sabelstrom H, Takebayashi H, Pfrieger FW, Meletis K, Frisen J. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010, 7(4):470-482. 10.1016/j.stem.2010.07.014, 20887953.
51. Zhang YW, Denham J, Thies RS. Oligodendrocyte progenitor cells derived from human embryonic stem cells express neurotrophic factors. Stem Cells Dev 2006, 15(6):943-952. 10.1089/scd.2006.15.943, 17253955.
52. Sharp J, Frame J, Siegenthaler M, Nistor G, Keirstead HS. Human embryonic Stem Cell-Derived Oligodendrocyte Progenitor Cell Transplants Improve Recovery after Cervical Spinal Cord Injury. Stem Cells 2009,
53. Wilkins A, Majed H, Layfield R, Compston A, Chandran S. Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci 2003, 23(12):4967-4974.
54. Schwab JM, Brechtel K, Mueller CA, Failli V, Kaps HP, Tuli SK, Schluesener HJ. Experimental strategies to promote spinal cord regeneration - an integrative perspective. Progress in Neurobiology 2006, 78(2):91-116. 10.1016/j.pneurobio.2005.12.004, 16487649.
55. Thoenen H, Sendtner M. Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nature Neuroscience 2002, 5:1046-1050. 10.1038/nn938, 12403983.
56. McDonald JW, Stefovska VG, Liu XZ, Shin H, Liu S, Choi DW. Neurotrophin potentiation of iron-induced spinal cord injury. Neuroscience 2002, 115(3):931-939. 10.1016/S0306-4522(02)00342-1, 12435430.
57. Finnerup NB, Jensen TS. Spinal cord injury pain - mechanisms and treatment. European Journal of Neurology 2004, 11(2):73-82. 10.1046/j.1351-5101.2003.00725.x, 14748766.
58. Weaver LC, Verghese P, Bruce JC, Fehlings MG, Krenz NR, Marsh DR. Autonomic dysreflexia and primary afferent sprouting after clip-compression injury of the rat spinal cord. J Neurotrauma 2001, 18(10):1107-1119. 10.1089/08977150152693782, 11686496.
59. Almad A, Sahinkaya FR, McTigue DM. Oligodendrocyte fate after spinal cord injury. Neurotherapeutics 2011, 8(2):262-273. 10.1007/s13311-011-0033-5, 21404073.
60. Geron Corporation Press Release 11/11/09 - Geron collaborators publish data on hESC-derived glial progenitor cell therapy in cervical spinal cord injury. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/media/pressview.aspx?id=1196
61. Kerr CL, Letzen BS, Hill CM, Agrawal G, Thakor NV, Sterneckert JL, Gearhart JD, All AH. Efficient differentiation of human embryonic stem cells into oligodendrocyte progenitors for application in a rat contusion model of spinal cord injury. Int J Neurosci 2010, 120(4):305-313. 10.3109/00207450903585290, 20374080.
62. Erceg S, Ronaghi M, Oria M, Rosello MG, Arago MA, Lopez MG, Radojevic I, Moreno-Manzano V, Rodriguez-Jimenez FJ, Bhattacharya SS, et al. Transplanted oligodendrocytes and motoneuron progenitors generated from human embryonic stem cells promote locomotor recovery after spinal cord transection. Stem Cells 2010, 28(9):1541-1549. 10.1002/stem.489, 2996083, 20665739.
63. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, et al. Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 2010, 30(8):2989-3001. 10.1523/JNEUROSCI.3174-09.2010, 2836860, 20181596.
64. Precision Systems and Instrumentation LLC Infinite Horizon Impactor. Accessed 29th July 2011, Precision Systems and Instrumentation LLC., http://www.presysin.com/Products/Infinite-Horizon-Impactor.aspx
65. De La Torre JC. Spinal cord injury models. Progress in Neurobiology (Oxford) 1984, 22(4):289-344.
66. Burney RE, Maio RF, Maynard F, Karunas R. Incidence, characteristics, and outcome of spinal-cord injury at trauma centers in North-America. Archives of Surgery 1993, 128(5):596-599.
67. Tator CH, Koyanagi I. Vascular mechanisms in the pathophysiology of human spinal cord injury. Journal of Neurosurgery 1997, 86(3):483-492. 10.3171/jns.1997.86.3.0483, 9046306.
68. Young W. Spinal cord contusion models. Spinal Cord Trauma: Regeneration, Neural Repair and Functional Recovery 2002, 137:231-255.
69. Werner C, Mollenberg O, Kochs E, Schulte J. Sevoflurane improves neurological outcome after incomplete cerebral-ischemia in rats. British Journal of Anaesthesia 1995, 75(6):756-760.
70. Sheng HX, Wang HC, Homi HM, Spasojevic I, Batinic-Haberle I, Pearlstein RD, Warner DS. A no-laminectomy spinal cord compression injury model in mice. J Neurotrauma 2004, 21(5):595-603. 10.1089/089771504774129928, 15165367.
71. Barros TED, Molina A. Analysis of the sensitivity and reproducibility of the Basso, Beattie, Bresnahan (BBB) scale in Wistar rats. Clinics 2008, 63(1):103-108. 10.1590/S1807-59322008000100018, 2664187, 18305873.
72. Akhtar AZ, Pippin JJ, Sandusky CB. Animal models in spinal cord injury: A review. Reviews in the Neurosciences 2008, 19(1):47-60. 10.1515/REVNEURO.2008.19.1.47, 18561820.
73. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nature Reviews Cancer 2011, 11(4):268-277. 10.1038/nrc3034, 21390058.
74. Blum B, Benvenisty N. The tumorigenicity of human embryonic stem cells. Advances in Cancer Research 2008, 100:133-+.
75. Okarma T. Interview with Thomas Okarma, M.D., Ph.D.; CEO, Geron. Rejuvenation Res 2009, 12(4):295-300.
76. Okamura RM, Lebkowski J, Au M, Priest CA, Denham J, Majumdar AS. Immunological properties of human embryonic stem cell-derived oligodendrocyte progenitor cells. Journal of Neuroimmunology 2007, 192(12):134-144.
77. Drukker M, Katz G, Urbach A, Schuldiner M, Markel G, Itskovitz-Eldor J, Reubinoff B, Mandelboim O, Benvenisty N. Characterization of the expression of MHC proteins in human embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(15):9864-9869. 10.1073/pnas.142298299, 125045, 12114532.
78. Li L, Baroja ML, Majumdar A, Chadwick K, Rouleau A, Gallacher L, Ferber I, Lebkowski J, Martin T, Madrenas J, et al. Human embryonic stem cells possess immune-privileged properties. Stem Cells 2004, 22(4):448-456. 10.1634/stemcells.22-4-448, 15277692.
79. Fairchild PJ, Robertson NJ, Minger SL, Waldmann H. Embryonic stem cells: protecting pluripotency from alloreactivity. Current Opinion in Immunology 2007, 19(5):596-602. 10.1016/j.coi.2007.07.010, 17709235.
80. Hatch MN, Nistor GI, Keirstead HS. Oligodendrocyte Differentiation from Human Embryonic Stem Cells. Human Stem Cell Manual: A Laboratory Guide 2007, 210-226. New York: Elsevier, Loring J, Wesselschmidt RL, Schwartz PH, 1.
81. Sundberg M, Hyysalo A, Skottman H, Shin S, Vemuri M, Suuronen R, Narkilahti S. A xeno-free culturing protocol for pluripotent stem cell-derived oligodendrocyte precursor cell production. Regen Med 2011, 6(4):449-460. 10.2217/rme.11.36, 21749203.
82. Cloutier F, Siegenthaler MM, Nistor G, Keirstead HS. Transplantation of human embryonic stem cell-derived oligodendrocyte progenitors into rat spinal cord injuries does not cause harm. Regen Med 2006, 1(4):469-479. 10.2217/17460751.1.4.469, 17465839.
83. McLaren A. Ethical and social considerations of stem cell research. Nature 2001, 414(6859):129-131. 10.1038/35102194, 11689959.
84. Zarzeczny A, Caulfield T. Emerging Ethical, Legal and Social Issues Associated with Stem Cell Research & and the Current Role of the Moral Status of the Embryo. Stem Cell Reviews and Reports 2009, 5(2):96-101. 10.1007/s12015-009-9062-4, 19521800.
85. Lo B, Parham L. Ethical Issues in Stem Cell Research. Endocrine Reviews 2009, 30(3):204-213. 10.1210/er.2008-0031, 2726839, 19366754.
86. Bretzner F, Gilbert F, Baylis F, Brownstone RM. Target populations for first-in-human embryonic stem cell research in spinal cord injury. Cell Stem Cell 2011, 8(5):468-475. 10.1016/j.stem.2011.04.012, 21549321.
87. Wirth E, Lebkowski JS, Lebacqz K. Response to Frederic Bretzner et al. "Target populations for first-in-human embryonic stem cell research in spinal cord injury". Cell Stem Cell 2011, 8(5):476-478. 10.1016/j.stem.2011.04.008, 21549322.
88. Solbakk JH, Zoloth L. The tragedy of translation: the case of "first use" in human embryonic stem cell research. Cell Stem Cell 2011, 8(5):479-481. 10.1016/j.stem.2011.04.009, 21549323.
89. Geron Corporation Press release 07/06/2011 - Geron Presents Data From GRNOPC1 Trial at International Conferences on Spinal Cord Medicine and Rehabilitation. Accessed 29th July 2011, Geron Corporation., http://www.geron.com/media/pressview.aspx?id=1271
90. Wirth E, Priest C, Davies A, Cullen S, Denham J, Owens N, Sugianto A, Bacolini L, Reddy A, Okamura R, Lebkowski J. Update on a Phase 1 Safety Trial of Human Embryonic Stem Cell- Derived Oligodendrocyte Progenitor Cells (GRNOPC1) in Subjects with Neurologically Complete, Subacute Spinal Cord Injuries. Abstract from 2011 ISCoS Meeting Accessed 29th July 2011., http://www.iscos.org.uk/files/Oral Presentation Abstracts from the 2011 International Congress on Spinal Cord Medicine and Rehabilitation.pdf
91. Geron Corporation Geron Corporation presentation at Jefferies 2011 global healthcare conference. Accessed 29th July 2011, Geron Corporation., http://www.wsw.com/webcast/jeff60/gern/
92. Dobkin BH, Curt A, Guest J. Cellular transplants in China: Observational study from the largest human experiment in chronic spinal cord injury. Neurorehabilitation and Neural Repair 2006, 20(1):5-13. 10.1177/1545968305284675, 16467274.
93. Cohen CB, Cohen PJ. International stem cell tourism and the need for effective regulation. Part I: Stem cell tourism in Russia and India: clinical research, innovative treatment, or unproven hype?. Kennedy Inst Ethics J 2010, 20(1):27-49. 10.1353/ken.0.0305, 20506693.
94. Cohen CB, Cohen PJ. International stem cell tourism and the need for effective regulation. Part II: Developing sound oversight measures and effective patient support. Kennedy Inst Ethics J 2010, 20(3):207-230. 10.1353/ken.2010.0001, 21133333.