Primary progressive multiple sclerosis: Progress and challenges

Journal of Neurology, Neurosurgery and Psychiatry

Volumn 84, Issue 10, 2013, Pages 1100-1106

  Rice, Claire M ^a   Cottrell, David ^b   Wilkins, Alastair ^a   Scolding, Neil J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b FRENCHAY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN; PHENYTOIN; RILUZOLE; SOMATOMEDIN C; TOPIRAMATE;

ALLERGIC ENCEPHALOMYELITIS; BRAIN STEM INJURY; BRUCELLOSIS; CELL PROLIFERATION; CLINICAL FEATURE; DIFFERENTIAL DIAGNOSIS; DISEASE CLASSIFICATION; DISEASE COURSE; EXPANDED DISABILITY STATUS SCALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOMODULATION; LUPUS VULGARIS; MULTIPLE SCLEROSIS; NEUROPROTECTION; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIA; ONSET AGE; OPTIC NEURITIS; OXIDATIVE STRESS; PRION DISEASE; PRIORITY JOURNAL; REMYELINIZATION; REVIEW; SARCOIDOSIS; SCHISTOSOMIASIS; SEX DIFFERENCE; SPASTIC PARAPLEGIA; SPASTICITY; SPINAL CORD DISEASE; STEM CELL TRANSPLANTATION; SYPHILIS; VASCULITIS;

EID: 84884595189     PISSN: 00223050     EISSN: 1468330X     Source Type: Journal    
DOI: 10.1136/jnnp-2012-304140     Document Type: Review

References (107)

1. Bennetto L, Burrow J, Sakai H, et al. The relationship between relapse, impairment and disability in multiple sclerosis. Mult Scler 2011; 17: 1218-24.
2. Muller R. Studies on disseminated sclerosis with special reference to symptomatology, course and prognosis. Acta Med Scand 1949; 133: 1-214.
3. Cottrell DA, Kremenchutzky M, Rice GP, et al. The natural history of multiple sclerosis: a geographically based study. 5. The clinical features and natural history of primary progressive multiple sclerosis. Brain 1999; 122(Pt 4): 625-39. (Pubitemid 29158771)
4. Stevenson VL, Miller DH, Rovaris M, et al. Primary and transitional progressive MS. Neurology 1999; 52: 839.
5. Antel J, Antel S, Caramanos Z, et al. Primary progressive multiple sclerosis: part of the MS disease spectrum or separate disease entity? Acta Neuropathologica 2012; 123: 627-38.
6. Confavreux C, Vukusic S, Moreau T, et al. Relapses and progression of disability in multiple sclerosis. N Engl J Med 2000; 343: 1430-8.
7. Thompson AJ, Toosy AT, Ciccarelli O. Pharmacological management of symptoms in multiple sclerosis: current approaches and future directions. Lancet Neurol 2010; 9: 1182-99.
8. Rice CM, Wilkins A. Symptomatic treatment for progressive multiple sclerosis. In: Wilkins A, ed. Progressive Multiple Sclerosis. A Wilkins, London: Springer, 2012: 147-87.
9. Hauser SL, Johnston SC. 4-aminopyridine: new life for an old drug. Ann Neurol 2010; 68:A8-9.
10. McDonnell GV, Cabrera-Gomez J, Calne DB, et al. Clinical presentation of primary progressive multiple sclerosis 10 years after the incidental finding of typical magnetic resonance imaging brain lesions. Mul Scler 2003; 9: 204-9.
11. Coles AJ, Cox A, Le PE, et al. The window of therapeutic opportunity in multiple sclerosis Evidence from monoclonal antibody therapy. J Neurol 2006; 253: 98-108. (Pubitemid 43157395)
12. Coles AJ, Compston DA, Selmaj KW, et al. Alemtuzumab vs. interferon beta-1a in early multiple sclerosis. N Engl J Med 2008; 359: 1786-801.
13. Polman CH, O'Connor PW, Havrdova E, et al., the A, I. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 2006; 354: 899-910.
14. The North American Study Group on Interferon beta-. Interferon beta-1b in secondary progressive MS. Neurology 2004; 63: 1788-95.
15. Montalban X, Sastre-Garriga J, Tintore M, et al. A single-center, randomized, double-blind, placebo-controlled study of interferon beta-1b on primary progressive and transitional multiple sclerosis. Mult Scler 2009; 15: 1195-205.
16. Hawker K, O'Connor P, Freedman MS, et al. Rituximab in patients with primary progressive multiple sclerosis: results of a randomized double-blind placebo-controlled multicenter trial. Ann Neurol 2009; 66: 460-71.
17. Wolinsky JS, Narayana PA, O'Connor P, et al. Glatiramer acetate in primary progressive multiple sclerosis: results of a multinational, multicenter, double-blind, placebo-controlled trial. Ann Neurol 2007; 61: 14-24. (Pubitemid 46214240)
18. Rojas JI, Romano M, Ciapponi A, et al. Interferon Beta for primary progressive multiple sclerosis. Cochrane Database Syst Rev 2010; 1:(CD006643).
19. Lassmann H. Mechanisms of neurodegeneration shared between multiple sclerosis and Alzheimer ÇÖs disease. J Neural Transm 2011; 118: 747-52.
20. Kapoor R, Furby J, Hayton T, et al. Lamotrigine for neuroprotection in secondary progressive multiple sclerosis: a randomised, double-blind, placebo-controlled, parallel-group trial. Lancet Neurol 2010; 9: 681-8.
21. Bechtold DA, Kapoor R, Smith KJ. Axonal protection using flecainide in experimental autoimmune encephalomyelitis. Ann Neurol 2004; 55: 607-16. (Pubitemid 38544320)
22. Black JA, Liu S, Hains BC, et al. Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 2006; 129: 3196-208. (Pubitemid 44871436)
23. Kapoor R, Davies M, Blaker PA, et al. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 2003; 53: 174-80. (Pubitemid 36163998)
24. Jackson SJ, Baker D, Cuzner ML, et al. Cannabinoid-mediated neuroprotection following interferon-gamma treatment in a three-dimensional mouse brain aggregate cell culture. Eur J Neurosci 2004; 20: 2267-75. (Pubitemid 39472389)
25. Jackson SJ, Diemel LT, Pryce G, et al. Cannabinoids and neuroprotection in CNS inflammatory disease. J Neurol Sci 2005; 233: 21-5. (Pubitemid 40804812)
26. Pryce G, Ahmed Z, Hankey DJ, et al. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003; 126: 2191-202. (Pubitemid 37432364)
27. Zajicek J, Fox P, Sanders H, et al. Cannabinoids for treatment of spasticity and other symptoms related to multiple sclerosis (CAMS study): multicentre randomised placebo-controlled trial. Lancet 2003; 362: 1517-26. (Pubitemid 37410189)
28. Gonsette RE. Oxidative stress and excitotoxicity: a therapeutic issue in multiple sclerosis? Mult Scler 2008; 14: 22-34. (Pubitemid 351541394)
29. Scolding N, Franklin R. Axon loss in multiple sclerosis. Lancet 1998; 352: 340-1. (Pubitemid 28352193)
30. Rodriguez M. A function of myelin is to protect axons from subsequent injury: implications for deficits in multiple sclerosis. Brain 2003; 126: 751-2. (Pubitemid 36372976)
31. Wilkins A, Chandran S, Compston A. A role for oligodendrocyte-derived IGF-1 in trophic support of cortical neurons. Glia 2001; 36: 48-57.
32. Wilkins A, Majed H, Layfield R, et al. 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: 4967-74. (Pubitemid 36793223)
33. Wilkins A, Scolding N. Protecting axons in multiple sclerosis. Mult Scler 2008; 14: 1013-25.
34. Frank JA, Richert N, Lewis B, et al. A pilot study of recombinant insulin-like growth factor-1 in seven multiple sderosis patients. Mult Scler 2002; 8: 24-9. (Pubitemid 34193024)
35. Scolding NJ, Rayner PJ, Sussman J, et al. A proliferative adult human oligodendrocyte progenitor. NeuroReport 1995; 6: 441-5.
36. Scolding N, Franklin R, Stevens S, et al. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 1998; 121: 2221-8. (Pubitemid 28552461)
37. Wolswijk G. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 2002; 125: 338-49. (Pubitemid 34127436)
38. Chang A, Nishiyama A, Peterson J, et al. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000; 20: 6404-12.
39. Snethen H, Love S, Scolding N. Disease-responsive neural precursor cells are present in multiple sclerosis lesions. Regen Med 2008; 3: 835-47.
40. Patrikios P, Stadelmann C, Kutzelnigg A, et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006; 129: 3165-72. (Pubitemid 44871433)
41. Fancy SPJ, Kotter MR, Harrington EP, et al. Overcoming remyelination failure in multiple sclerosis and other myelin disorders. Exp Neurol 2010; 225: 18-23.
42. Fancy SP, Baranzini SE, Zhao C, et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009; 23: 1571-85.
43. Mi S, Hu B, Hahm K, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007; 13: 1228-33. (Pubitemid 47530642)
44. Manrique-Hoyos N, Jurgens T, Gronborg M, et al. Late motor decline after accomplished remyelination: impact for progressive MS. Ann Neurol 2012; 71: 227-44.
45. Fox JM, Chamberlain G, Ashton BA, et al. Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 2007; 137: 491-502. (Pubitemid 46817339)
46. Karp JM, Leng Teo GS. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009; 4: 206-16.
47. Korbling M, Estrov Z. Adult stem cells for tissue repair. N Engl J Med 2003; 349: 570-82.
48. Gordon D, Pavlovska G, Uney JB, et al. Human mesenchymal stem cells infiltrate the spinal cord, reduce demyelination, and localize to white matter lesions in experimental autoimmune encephalomyelitis. J Neuropathol Exp Neurol 2010; 69: 1087-95.
49. Rice CM, Scolding N. Adult human mesenchymal cells proliferate and migrate in response to chemokines expressed in demyelination. Cell Adhes Migration 2010; 4: 235-40.
50. Phinney DG. Biochemical heterogeneity of mesenchymal stem cell populations: clues to their therapeutic efficacy. Cell Cycle 2007; 6: 2884-9.
51. Rice CM, Scolding NJ. Adult stem cells-reprogramming neurological repair? Lancet 2004; 364: 193-9. (Pubitemid 38891691)
52. Zhang J, Li Y, Chen J, et al. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 2005; 195: 16-26. (Pubitemid 41116810)
53. Gerdoni E, Gallo B, Casazza S, et al. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 2007; 61: 219-27. (Pubitemid 46557346)
54. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106: 1755-61. (Pubitemid 41208591)
55. Gordon D, Pavlovska G, Glover CP, et al. Human mesenchymal stem cells abrogate experimental allergic encephalomyelitis after intraperitoneal injection and with sparse CNS infiltration. Neurosci Lett 2008; 448: 71-3.
56. Akiyama Y, Radtke C, Honmou O, et al. Remyelination of the spinal cord following intravenous delivery of bone marrow cells. Glia 2002; 39: 229-36.
57. Akiyama Y, Radtke C, Kocsis JD. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 2002; 22: 6623-30. (Pubitemid 35386418)
58. Munoz JR, Stoutenger BR, Robinson AP, et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA 2005; 102: 18171-6. (Pubitemid 41798520)
59. Bai L, Lennon DP, Eaton V, et al. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 2009; 57: 1192-203.
60. Li Y, Chen J, Zhang CL, et al. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 2005; 49: 407-17. (Pubitemid 40222918)
61. Chen Q, Long Y, Yuan X, et al. Protective effects of bone marrow stromal cell transplantation in injured rodent brain: synthesis of neurotrophic factors. J Neurosci Res 2005; 80: 611-19. (Pubitemid 40896182)
62. Garcia R, Aguiar J, Alberti E, et al. Bone marrow stromal cells produce nerve growth factor and glial cell line-derived neurotrophic factors. Biochem Biophys Res Commun 2004; 316: 753-4. (Pubitemid 38368017)
63. Li Y, Chen J, Chen XG, et al. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 2002; 59: 514-23. (Pubitemid 34919983)
64. Ye M, Chen S, Wang X, et al. Glial cell line-derived neurotrophic factor in bone marrow stromal cells of rat. NeuroReport 2005; 16: 581-4. (Pubitemid 40586087)
65. Wilkins A, Kemp K, Ginty M, et al. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res 2009; 3: 67-70.
66. Kemp K, Hares K, Mallam E, et al. Mesenchymal stem cell-secreted superoxide dismutase promotes cerebellar neuronal survival. J Neurochem 2009; 114: 1569-80.
67. Kemp K, Gray E, Mallam E, et al. Inflammatory cytokine induced regulation of superoxide dismutase 3 expression by human mesenchymal stem cells. Stem Cell Rev 2010; 6: 548-59.
68. Johansson CB, Youssef S, Koleckar K, et al. Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat Cell Biol 2008; 10: 575-83. (Pubitemid 351627377)
69. Nygren JM, Liuba K, Breitbach M, et al. Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat Cell Biol 2008; 10: 584-92. (Pubitemid 351627378)
70. Kemp K, Gordon D, Wraith DC, et al. Fusion between human mesenchymal stem cells and rodent cerebellar Purkinje cells. Neuropathol Appl Neurobiol 2010; 37: 166-78.
71. da Silva ML, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006; 119: 2204-13. (Pubitemid 43960310)
72. Mosna F, Sensebe L, Krampera M. Human bone marrow and adipose tissue mesenchymal stem cells: a user's guide. Stem Cells Dev 2010; 19: 1449-70.
73. Zuba-Surma EK, Kucia M, Ratajczak J, et al. 'Small stem cells' in adult tissues: very small embryonic-like stem cells stand up! Cytometry A 2009; 75: 4-13.
74. Koshizuka S, Okada S, Okawa A, et al. Transplanted hematopoietic stem cells from bone marrow differentiate into neural lineage cells and promote functional recovery after spinal cord injury in mice. J Neuropathol Exp Neurol 2004; 63: 64-72. (Pubitemid 38030234)
75. Takakura N, Watanabe T, Suenobu S, et al. A role for hematopoietic stem cells in promoting angiogenesis. Cell 2000; 102: 199-209.
76. Burt RK, Traynor AE, Oyama Y, et al. Plasticity of hematopoietic stem cells: enough to induce tolerance and repair tissue? Arthritis Rheum 2002; 46: 855-8. (Pubitemid 34303794)
77. Fu X, Sun X. Can hematopoietic stem cells be an alternative source for skin regeneration? Ageing Res Rev 2009; 8: 244-9.
78. Zhou P, Wirthlin L, McGee J, et al. Contribution of human hematopoietic stem cells to liver repair. Semin Immunopathol 2009; 31: 411-19.
79. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991; 78: 55-62.
80. Psaltis PJ, Paton S, See F, et al. Enrichment for STRO-1 expression enhances the cardiovascular paracrine activity of human bone marrow-derived mesenchymal cell populations. J Cell Physiol 2010; 223: 530-40.
81. Stewart K, Monk P, Walsh S, et al. STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res 2003; 313: 281-90. (Pubitemid 37260435)
82. Dennis JE, Carbillet JP, Caplan AI, et al. The STRO-1+ marrow cell population is multipotential. Cells Tissues Organs 2002; 170: 73-82.
83. Nasef A, Zhang YZ, Mazurier C, et al. Selected Stro-1-enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation. Int J Lab Hematol 2009; 31: 9-19.
84. Bakondi B, Shimada IS, Perry A, et al. CD133 identifies a human bone marrow stem/progenitor cell sub-population with a repertoire of secreted factors that protect against stroke. Mol Ther 2009; 17: 1938-47.
85. Harris JR, Fisher R, Jorgensen M, et al. CD133 progenitor cells from the bone marrow contribute to retinal pigment epithelium repair. Stem Cells 2009; 27: 457-66.
86. Sasaki H, Ishikawa M, Tanaka N, et al. Administration of human peripheral blood-derived CD133+ cells accelerates functional recovery in a rat spinal cord injury model. Spine (Phila Pa 1976.) 2009; 34: 249-54.
87. Morikawa S, Mabuchi Y, Niibe K, et al. Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun 2009; 379: 1114-19.
88. Nagoshi N, Shibata S, Kubota Y, et al. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2008; 2: 392-403. (Pubitemid 351455244)
89. Rice CM, Clavel C, Mazo M, et al. Multipotent adult progenitor cell isolation and proliferation in cytokine and serum free medium conditioned by rat B104 cells. Br J Haematol 2010; 148: 441-4.
90. Ruckh JM, Zhao JW, Shadrach JL, et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 2012; 10: 96-103.
91. Prockop DJ, Brenner M, Fibbe WE, et al. Defining the risks of mesenchymal stromal cell therapy. Cytotherapy 2010; 12: 576-8.
92. Miura M, Miura Y, Padilla-Nash HM, et al. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 2006; 24: 1095-103. (Pubitemid 44464742)
93. Dahl JA, Duggal S, Coulston N, et al. Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int J Dev Biol 2008; 52: 1033-42.
94. Tonti GA, Mannello F. From bone marrow to therapeutic applications: different behaviour and genetic/epigenetic stability during mesenchymal stem cell expansion in autologous and foetal bovine sera? Int J Dev Biol 2008; 52: 1023-32.
95. Alves H, Munoz-Najar U, de WJ, et al. A link between the accumulation of DNA damage and loss of multipotency of human mesenchymal stromal cells. J Cell Mol Med 2009.
96. Kretlow JD, Jin YQ, Liu W, et al. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 2008; 9: 60.
97. Crisostomo PR, Wang M, Wairiuko GM, et al. High passage number of stem cells adversely affects stem cell activation and myocardial protection. Shock 2006; 26: 575-80. (Pubitemid 44789631)
98. Dominici M, Le BK, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-17. (Pubitemid 44269669)
99. Dominici M, Paolucci P, Conte P, et al. Heterogeneity of multipotent mesenchymal stromal cells: from stromal cells to stem cells and vice versa. Transplantation 2009; 87:S36-42.
100. Burt RK, Loh Y, Pearce W, et al. Clinical applications of blood-derived and marrow-derived stem cells for nonmalignant diseases. JAMA 2008; 299: 925-36. (Pubitemid 351397068)
101. Grigoriadis N, Lourbopoulos A, Lagoudaki R, et al. Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis. Exp Neurol 2011; 230: 78-89.
102. Murphy MP, Lawson JH, Rapp BM, et al. Autologous bone marrow mononuclear cell therapy is safe and promotes amputation-free survival in patients with critical limb ischemia. J Vasc Surg 2011; 53: 1565-74.
103. Siqueira RC, Messias A, Voltarelli JC, et al. Intravitreal injection of autologous bone marrow-derived mononuclear cells for hereditary retinal dystrophy: a Phase I Trial. RETINA 2011; 31: 1207-14.
104. Savitz SI, Misra V, Kasam M, et al. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann Neurol 2011; 70: 59-69.
105. Rice CM, Mallam EA, Whone AL, et al. Safety and feasibility of autologous bone marrow cellular therapy in relapsing-progressive multiple sclerosis. Clin Pharmacol Ther 2010; 87: 679-85.
106. Cottrell DA, Kremenchutzky M, Rice GP, et al. The natural history of multiple sclerosis: a geographically based study. 6. Applications to planning and interpretation of clinical therapeutic trials in primary progressive multiple sclerosis. Brain 1999; 122(Pt 4): 641-7. (Pubitemid 29158772)
107. Tremlett H, Paty D, Devonshire V. The natural history of primary progressive MS in British Columbia, Canada. Neurology 2005; 65: 1919-23. (Pubitemid 43970111)