Hematopoietic stem cell transplantation for multiple sclerosis: Current status and future challenges

Current Opinion in Neurology

Volumn 16, Issue 3, 2003, Pages 299-305

  Muraro, Paolo A ^b   Ingoni, Riccardo Cassiani ^b   Martin, Roland ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NONE

Author keywords

Hematopoietic stem cell transplantation; Multiple sclerosis; Remyelination; Stem cells

Indexed keywords

BETA INTERFERON; BETA1A INTERFERON; BUSULFAN; CARMUSTINE; CYCLOPHOSPHAMIDE; CYTARABINE; ETOPOSIDE; GADOLINIUM; GLATIRAMER; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON BETA SERINE; MELPHALAN; MITOXANTRONE; MYELIN; THYMOCYTE ANTIBODY;

CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CLINICAL TRIAL; DISEASE ACTIVITY; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; MULTIPLE SCLEROSIS; NERVE REGENERATION; NUCLEAR MAGNETIC RESONANCE IMAGING; REVIEW;

HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MULTIPLE SCLEROSIS;

EID: 0037782258     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/00019052-200306000-00008     Document Type: Review

References (72)

1. McFarlin DE, McFarland HF. Multiple sclerosis (first of two pads). N Engl J Med 1982, 307:1183-1188.
2. Whitaker JN, Mitchell GW. Clinical features of multiple sclerosis. In: Raine CS, McFarland HF, Tourtellotte WW, editors. Multiple sclerosis: clinical and pathogenetic basis. Chapman and Hall, London; 1997. pp. 3-19.
3. National Multiple Sclerosis Society. Research fact sheet. New York: National Multiple Sclerosis Society; 2002.
4. Lublin FD, Reingold SC. Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA), Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 1996; 46:907-911.
5. Trapp BD, Peterson J, Ransohoff RM, et al. Axonal transection in the lesions of multiple sclerosis [see Comments]. N Engl J Med 1998; 338:278-285.
6. Peterson JW, Bo L, Mork S, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50:389-400.
7. Goodin DS, Frohman EM, Garmany GP Jr, et al. Disease modifying therapies in multiple sclerosis: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and the MS Council for Clinical Practice Guidelines. Neurology 2002; 58:169-178.
8. Martin R, Calabresi P, McFarland HF. In: Zhang J, Hafler D, Hohlfeld R. Miller A, editors. Experimental immunotherapies of multiple sclerosis. Chapter 8. Martin Dunitz Ltd., London: 1998. pp. 29-73.
9. McAllister LD, Beatty PG, Rose J. Allogeneic bone marrow transplant for chronic myelogenous leukemia in a patient with multiple sclerosis. Bone Marrow Transplant 1997; 19:395-397.
10. van Gelder M, Kinwel-Bohre EP, van Bekkum DW. Treatment of experimental allergic encephalomyelitis in rats with total body irradiation and syngeneic BMT. Bone Marrow Transplant 1993; 11:233-241.
11. Karussis DM, Vourka-Karussis U, Lehmann D, et al. Prevention and reversal of adoptively transferred, chronic relapsing experimental autoimmune encephalomyelitis with a single high dose cytoreductive treatment followed by syngeneic bone marrow transplantation. J Clin Invest 1993; 92:765-772.
12. Burt RK, Burns W, Ruvoto P, et al. Syngeneic bone marrow transplantation eliminates V beta 8.2 T lymphocytes from the spinal cord of Lewis rats with experimental allergic encephalomyelitis. J Neurosci Res 1995; 41:526-531.
13. Burt RK, Padilla J, Begolka WS, et al. Effect of disease stage on clinical outcome after syngeneic bone marrow transplantation for relapsing experimental autoimmune encephalomyelitis. Blood 1998; 91:2609-2616.
14. Fassas A, Anagnostopoulos A, Kazis A, et al. Peripheral blood stem cell transplantation in the treatment of progressive multiple sclerosis: first results of a pilot study. Bone Marrow Transplant 1997; 20:631-638.
15. Burt RK, Traynor AE, Cohen B, et al. T cell-depleted autologous hematopoietic stem cell transplantation for multiple sclerosis: report on the first three patients. Bone Marrow Transplant 1998; 21:537-541.
16. Burt RK, Traynor AE, Pope R, et al. Treatment of autoimmune disease by intense immunosuppressive conditioning and autologous hematopoietic stem cell transplantation. Blood 1998; 92:3505-3514.
17. Fassas A, Anagnostopoulos A, Kazis A, et al. Autologous stem cell transplantation in progressive multiple sclerosis - an interim analysis of efficacy. J Clin Immunol 2000; 20:24-30.
18. Kozak T, Havrdova E, Pit'ha J, et al. High-dose immunosuppressive therapy with PBPC support in the treatment of poor risk multiple sclerosis. Bone Marrow Transplant 2000; 25:525-531.
19. Mandalfino P, Rice G, Smith A, et al. Bone marrow transplantation in multiple sclerosis. J Neurol 2000; 247:691-695.
20. Nash RA, Bowen JD, McSweeney P, et al. Treatment of severe multiple sclerosis (MS) with high dose immunosuppressive therapy (HDIT) and autologous stem cell transplantation (SCT) [Abstract]. Blood 2000; 96 (Suppl.):842a.
21. Openshaw H, Lund BT, Kashyap A, et al. Peripheral blood stem cell transplantation in multiple sclerosis with busulfan and cyclophosphamide conditioning: report of toxicity and immunological monitoring. Biol Blood Marrow Transplant 2000; 6:563-575.
22. Saiz A, Carreras E, Berenguer J, et al. MRI and CSF oligoclonal bands after autologous hematopoietic stern cell transplantation in MS. Neurology 2001; 56:1084-1089.
23. Mancardi GL, Saccardi R, Filippi M, et al. Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS. Neurology 2001; 57:62-68.
24. Fassas A, Passweg JR, Anagnostopoulos A, et al. Hematopoietic stem cell transplantation for multiple sclerosis. A retrospective multicenter study. J Neurol 2002; 249:1088-1097. A retrospective study of data reported to a European registry providing the largest reported single cohort of MS patients treated with HSCT.
25. Oyama Y, Cohen B, Traynor A, et al. Engraftment syndrome: a common cause for rash and fever following autologous hematopoietic stem cell transplantation for multiple sclerosis. Bone Marrow Transplant 2002; 29:81-85. This study identifies engraftment syndrome as an important and treatable cause of early neurological deterioration in MS patients treated with HSCT.
26. Confavreux C, Vukusic S, Moreau T, Adeleine P. Relapses and progression of disability in multiple sclerosis. N Engl J Med 2000; 343:1430-1438.
27. Kappos L, Polman C, Pozzilli C, et al. Final analysis of the European multicenter trial on IFNbeta-1b in secondary-progressive MS. Neurology 2001; 57:1969-1975.
28. Placebo-controlled multicentre randomised trial of interferon beta-1b in treatment of secondary progressive multiple sclerosis. European Study Group on interferon beta-1b in secondary progressive MS. Lancet 1998; 352:1491-1497.
29. Li DK, Zhao GJ, Paty DW. Randomized controlled trial of interferon-beta-1a in secondary progressive MS: MRI results. Neurology 2001; 56:1505-1513.
30. SPECTRIMS Study Group. Randomized controlled trial of interferon-beta-1a in secondary progressive MS: clinical results. Neurology 2001; 56:1496-1504.
31. Goodkin DE, Group NASS. The north American study of interferon beta-1b in secondary progressive multiple sclerosis. In: 52nd Annual Meeting of the American Academy of Neurology. San Diego, CA, 2000.
32. McDonald WI, Compston A, Edan G, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the Diagnosis of Multiple Sclerosis. Ann Neurol 2001; 50:121-127.
33. McFarland HF. The emerging role of MRI in multiple sclerosis and the new diagnostic criteria. Mult Scler 2002; 8:71-72.
34. Comi G, Kappos L, Clanet M, et al. Guidelines for autologous blood and marrow stem cell transplantation in multiple sclerosis: a consensus report written on behalf of the European Group for Blood and Marrow Transplantation and the European Charcot Foundation. BMT-MS Study Group. J Neurol 2000; 247:376-382.
35. Euler H, Marmont A, Bacigalupo A, et al. Early recurrence or persistence of autoimmune diseases after unmanipulated autologous stem cell transplantation. Blood 1996; 88:3621-3625.
36. Marmont AM. New horizons in the treatment of autoimmune diseases: immunoablation and stem cell transplantation. Annu Rev Med 2000; 51:115-134.
37. Brodsky RA, Petri M, Smith BD, et al. Immunoablative high-dose cyclophosphamide without stem-cell rescue for refractory, severe autoimmune disease. Ann Intern Med 1998; 129:1031-1035.
38. Kozak T, Havrdova E, Pitha J. High dose immunosuppression with hemopoietic stem cell support in the treatment of multiple sclerosis. Israeli Med Assoc J 2000; 2:610-614.
39. Smith PM, Franklin RJ. The effect of immunosuppressive protocols on spontaneous CNS remyelination following toxin-induced demyelination. J Neuroimmunol 2001; 119:261-268.
40. Okamoto R, Yajima T, Yamazaki M, et al. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat Med 2002; 8:1011-1017.
41. Korbling M, Katz RL, Khanna A, et al. Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. N Engl J Med 2002; 346:738-746. Biopsy specimens from patients who received high-dose chemotherapy followed by transplantation of allogeneic peripheral-blood stern cells showed that some donor-derived cells differentiated into hepatocytes and epithelial cells of the gastrointestinal tract and of the skin.
42. Tran SD, Pillemer S, Dutra A, et al. Human bone marrow-derived cells differentiate into buccal epithelial cells in vivo without fusion. Lancet 2003; 361:1084-1088.
43. Mezey E, Key S, Vogelsang G, et al. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci U S A 2003; 100:1364-1369. This study demonstrates for the first time that transplanted adult human bone marrow cells can enter the human brain and generate neurons, as well as other cell types in vivo.
44. Weimann JM, Charlton CA, Brazelton TR, et al. Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc Natl Acad Sci U S A 2003; 100:2088-2093.
45. Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A 1997; 94:4080-4085.
46. Brazelton TR, Rossi FM, Keshet GI, Blau HM. From marrow to brain: expression of neuronal phenotypes in adult mice. Science 2000; 290:1775-1779.
47. Corti S, Locatelli F, Donadoni C, et al. Neuroectodermal and microglial differentiation of bone marrow cells in the mouse spinal cord and sensory ganglia. J Neurosci Res 2002; 70:721-733.
48. Corti S, Locatelli F, Strazzer S, et al. Modulated generation of neuronal cells from bone marrow by expansion and mobilization of circulating stem cells with in vivo cytokine treatment. Exp Neurol 2002; 177:443-452.
49. Nakano K, Migita M, Mochizuki H, Shimada T. Differentiation of transplanted bone marrow cells in the adult mouse brain. Transplantation 2001; 71:1735-1740.
50. Priller J, Persons DA, Klett FF, et al. Neogenesis of cerebellar Purkinje neurons from gene-marked bone marrow cells in vivo. J Cell Biol 2001; 155:733-738.
51. Sanchez-Ramos JR, Neural cells derived from adult bone marrow and umbilical cord blood. J Neurosci Res 2002; 69:880-893.
52. Song S, Sanchez-Ramos J. Preparation of neural progenitors from bone marrow and umbilical cord blood. Methods Mol Biol 2002; 198:79-88.
53. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418:41-49.
54. Priller J, Flugel A, Wehner T. et al. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 2001; 7:1356-1361.
55. Kabos P, Ehtesham M, Kabosova A, et al. Generation of neural progenitor cells from whole adult bone marrow. Exp Neurol 2002; 178:288-293.
56. Romero-Ramos M, Vourc'h P, Young HE, et al. Neuronal differentiation of stem cells isolated from adult muscle. J Neurosci Res 2002; 69:894-907.
57. Jiang Y, Vaessen B, Lenvik T, et al. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 2002; 30:896-904.
58. Bonilla S, Alarcon P, Villaverde R, et al. Haematopoietic progenitor cells from adult bone marrow differentiate into cells that express oligodendroglial antigens in the neonatal mouse brain. Eur J Neurosci 2002; 15:575-582.
59. Flugel A, Bradl M, Kreutzberg GW, Graeber MB. Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J Neurosci Res 2001; 66:74-82.
60. Mezey E, Chandross KJ, Harta G, et al. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000; 290:1779-1782.
61. Castro RF, Jackson KA, Goodell MA, et al. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 2002; 297:1299.
62. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL, Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002; 297:2256-2259.
63. Sasaki M, Honmou O, Akiyama Y, et al. Transplantation of an acutely isolated bone marrow fraction repairs demyelinated adult rat spinal cord axons. Glia 2001; 35:26-34.
64. Dao MA, Arevalo J, Nolta JA. Reversibility of CD34 expression on human hematopoietic stem cells that retain the capacity for secondary reconstitution. Blood 2003; 101:112-118. These authors demonstrate that the expression of the surface-marker CD34 is reversible on human hematopoietic stem/progenitor cells. Human CD34+/ CD38 - negative stem cells originate CD34-/CD45+ cells upon transplantation in immunodeficient mice, and these cells produce CD34-positive progeny after retransplantation.
65. Akiyama Y, Radtke C, Honmou O, Kocsis JD. Remyerination of the spinal cord following intravenous delivery of bone marrow cells. Glia 2002; 39:229-236.
66. Akiyama Y, Radtke C, Kocsis JD. Remyerination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 2002; 22:6623-6630.
67. Akiyama Y, Honmou O, Kato T, et al. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp Neurol 2001; 167:27-39.
68. Imaizumi T, Lankford KL, Kocsis JD. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res 2000; 854:70-78.
69. Kato T, Honmou O, Uede T, et al. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000; 30:209-218.
70. Windrem MS, Roy NS, Wang J, et al. Progenitor cells derived from the adult human subcortical white matter disperse and differentiate as oligodendrocytes within demyelinated lesions of the rat brain. J Neurosci Res 2002; 69:966-975.
71. Wu YP, McMahon E, Kraine MR, et al. Distribution and characterization of GFP(+) donor hematogenous cells in Twitcher mice after bone marrow transplantation. Am J Pathol 2000; 156:1849-1854.
72. Carreras E, Saiz A, Marin P, et al. CD34+ selected autologous peripheral blood stem cell transplantation for multiple sclerosis: report of toxicity and treatment results at one year of follow-up in 15 patients. Haematologica 2003; 88:306-314.