The role of neurotrophic factors in the pathology and treatment of multiple sclerosis

Immunopharmacology and Immunotoxicology

Volumn 31, Issue 1, 2009, Pages 32-38

  Mirowska Guzel, Dagmara ^a,b  

^a INSTITUTE OF PSYCHIATRY AND NEUROLOGY   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Multiple sclerosis; Neuroprotection; Neurotrophic factors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; DISUFENTON SODIUM; GAMMA INTERFERON; GLATIRAMER; INTERLEUKIN 6; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ALLERGIC ENCEPHALOMYELITIS; B LYMPHOCYTE; BRAIN REGION; CELL PROLIFERATION; CLINICAL FEATURE; DNA POLYMORPHISM; HUMAN; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; OPTIC NEURITIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REVIEW; SEX DIFFERENCE; T LYMPHOCYTE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MULTIPLE SCLEROSIS; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; PEPTIDES;

ANIMALIA;

EID: 60749118353     PISSN: 08923973     EISSN: 15322513     Source Type: Journal    
DOI: 10.1080/08923970802379819     Document Type: Review

References (74)

1. Dhib-Jalbut, S.; Arnold, D.L.; Cleveland, D.W.; Fisher, M.; Friedlander, R.M.; Mouradian, M.; Przedborski, S.; Trapp, B.D.; Wyss-Coray, T.; Yong, V.W. Neurodegeneration and neuroprotection in multiple sclerosis and other neurodegenerative diseases. J. Neuroimmunol. 2006, 176 (1-2):198-215.
2. Trapp, B.D.; Peterson, J.; Ransohoff, R.M.; Rudick, R.; Mork, S.; Bo, L. Axonal transaction in the lesions of multiple sclerosis. N. Engl. J. Med. 1998, 338 (5):278-285.
3. Trapp, B.D.; Ransohoff, R.M.; Rudick, R. Axonal pathology in multiple sclerosis: Relationship to neurologic disability. Curr. Opin. Neurol. 1999, 12 (3):295-302.
4. Bo, L.; Vedeler, C.A.; Nyland, H.; Trapp, B.D.; Mork, S.J. Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult. Scler. 2003, 9 (4):323-331.
5. Hohlfeld, R.; Kerschensteiner, M.; Stadelmann, C.; Lassmann, H.; Wekerle, H. The neuroprotective effect of inflammation: Implications for the therapy of multiple sclerosis. Neurol. Sci. 2006, 27 (suppl. 1):S1-S7.
6. Hohlfeld, R. Neurotrophic cross-talk between the nervous and immune systems: Relevance for repair strategies in multiple sclerosis? J. Neurol. Sci. 2008, 265 (1-2):93-96.
7. Levi-Montalcini, R. The nerve growth factor: Thirty five years later. EMBO J. 1987, 6 (9):1145-1154.
8. Barbacid, M. Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 1995, 7 (2):148-155.
9. Segal, R.A.; Greenberg, M.E. Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 1996, 19:463-489.
10. Hu, Y.; Russek, S.J. BDNF and the diseased nervous system: A delicate balance between adaptive and pathological processes of gene regulation. J. Neurochem. 2008, 105 (1):1-17.
11. Lewin, G.R.; Barde, Y.A. Physiology of the neurotrophins. Annu. Rev. Neurosci. 1996, 19:289-317.
12. Lin, L.; Doherty, D.; Lile, J.D.; Bektesh, S.; Collins, F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260 (5111):1130-1132.
13. Saarma, M. GDNF - A stranger in the TGF-β superfamily? Eur. J. Biochem. 2000, 267 (24):6968-6971.
14. Sariola, H.; Saarma, M. Novel functions and signaling pathways for GDNF. J. Cell Sci. 2003, 116 (19):3855-3862.
15. Klein, R.; Nanduri, V.; Jing, S.A.; Lamballe, F.; Tapley, P.; Bryant, S. The TrkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3.. Cell 1991, 66 (2):395-403.
16. Lu, B.; Pang, P.T.; Woo, N.H. The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 2005, 6 (8):603-614.
17. Barres, B.A.; Raff, M.C.; Gaese, F.; Bartke, I.; Dechant, G.; Barde, Y.A. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 1994, 367 (6461):371-375.
18. Bentley, C.A.; Lee, K.F. p75 is important for axon growth and Schwann cell migration during development. J. Neurosci. 2000, 20 (20):7706-7715.
19. Mc Tigue, D.M.; Horner, P.J.; Stokes, B.T.; Gage, F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 1998, 18 (14):5354-5365.
20. Du, Y.; Fischer, T.Z.; Lee, L.N.; Lercher, L.D.; Dreyfus, C.F. Regionally specific effects of BDNF on oligodendrocytes. Dev. Neurosci. 2003, 25 (2-4):116-126.
21. Rosenberg, S.S.; Ng, B.K.; Chan, J.R. The quest for remyelination: A new role for neurotrophins and their receptors. Brain Pathol. 2006, 16 (4):288-294.
22. Girard, C.; Bemelmans, A.P.; Dufour, N.; Mallet, J.; Bachelin, C.; Nait-Oumesmar, B.; Baron-VanEvercooren, A.; Lachapelle, F. Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J. Neurosci. 2005, 25 (35):7924-7933.
23. Talbott, J.F.; Cao, Q.; Bertram, J.; Nkansah, M.; Benton, R.L.; Lavik, E.; Whittemore, S.R. CNTF promotes the survival and differentiation of adult spinal cord-derived oligodendrocyte precursor cells in vitro but fails to promote remyelination in vivo. Exp. Neurol. 2007, 204 (1):485-489.
24. Linker, R.; Lee, D.H.; Siglienti, I.; Gold, R. Is there a role for neurotrophins in the pathology of multiple sclerosis? J. Neurol. 2007, 254 (suppl. 1):33-40.
25. Calza, L.; Giardino, L.; Pozza, M.; Bettelli, C.; Micera, A.; Aloe, L. Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: In vivo evidence of a role for nerve growth factor. Proc. Natl. Acad. Sci. 1998, 95 (6):3209-3214.
26. Micera, A.; Properzi, F.; Triaca, V.; Aloe, L. Nerve growth factor antibody exacerbates neuropathological signs of experimental allergic encephalomyelitis in adult Lewis rats. J. Neuroimmunol. 2000, 104 (2):116-123.
27. D'Intino, G.; Paradisi, M.; Fernandez, M.; Giuliani, A.; Aloe, L.; Giardino, L.; Calza, L. Cognitive deficit associated with cholinergic and nerve growth factor down-regulation in experimental allergic encephalomyelitis in rats. PNAS 2005, 102 (8):3070-3075.
28. Maier, K.; Rau, C.; Storch, M.K.; Sattler, M.; Demmer, I.; Weissert, R.; Taherri, N.; Kuhnert, A.; Bahr, M.; Diem, R. Ciliary neurotrophic factor protects retinal ganglion cells from secondary cell death during acute autoimmune optic neuritis in rats. Brain Pathol. 2004, 14 (4):378-387.
29. Kuhlmann, T.; Remington, L.; Cognet, I.; Bourbonniere, L.; Zehnter, S.; Guilhot, F.; Herman, A.; Guay-Giroux, A.; Gauchat, J.-F. Continued administration of ciliary neurotrophic factor protects mice from inflammatory pathology in experimental autoimmune encephalomyelitis. Am. J. Pathol. 2006, 169 (2):584-598.
30. Makar, T.K.; Trisler, D.; Sura, K.T.; Sultana, S.; Patel, N.; Bever, C.T. Brain derived neurotrophic factor treatment reduces inflammation and apoptosis in experimental allergic encephalomyelitis. J. Neurol. Sci. 2008, 270 (1-2):70-76.
31. Makar, T.K.; Trisler, D.; Bever, C.T.; Goolsby, J.E.; Sura, K.T.; Sultana, S.; Patel, N.; Ford, D.; Singh, I.S.; Gupta, A.; Valenzuela, R.M.; Dhib-Jalbut, S. Stem cell based delivery of IFN-beta reduces relapses in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2008, 196 (1-2):67-81.
32. Kerschensteiner, M.; Gallmeier, E.; Behrens, L.; Vargas Leal, V.; Misgeld, T.; Klinkert, E.F.; Kolbeck, R.; Hoppe, E.; Oropeza-Wekerle, R.-L.; Bartke, I.; Stadelmann, Ch.; Lassmann, H.; Wekerle, H.; Hohlfeld, R. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: A neuroprotective role of inflammation? J. Exp. Med. 1999, 189 (5):865-870.
33. Stadelmann, C.; Kerschensteiner, M.; Misgeld, T.; Brück, W.; Hohlfeld, R.; Lassmann, H. BDNF and gd145trkB in multiple sclerosis brain lesions: Neuroprotective interactions between immune and neuronal cells? Brain 2002, 125 (Pt 1):75-85.
34. Besser, M.; Wank, R. Clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells Th1/Th2 - Polarized expression of their receptors. J. Immunol. 1999, 162 (11):6303-6306.
35. Vargas-Leal, V.; Bruno, R.; Derfuss, T.; Krumbholz, M.; Hohlfeld, R.; Meinl, E. Expression and function of glial cell line-derived neurotrophic factor family ligands and their receptors on human immune cells. J. Immunol. 2005, 175 (4):2301-2308.
36. Schulte-Herbrtggen, O.; Nassenstein, Ch.; Lommatzsch, M.; Quarcoo, D.; Renz, H.; Braun, A. Tumor necrosis factor-α and interleukin-6 regulate secretion of brain-derived neurotrophic factor in human monocytes. J. Neuroimmunol. 2005, 160 (1-2):204-209.
37. Lomen-Hoerth, C.; Shooter, E.M. Widespread neurotrophin receptor expression in the immune system and other nonneuronal rat tissue. J. Neurochem. 1995, 64 (4):1780-1789.
38. Sarchielli, P.; Greco, L.; Stipa, A.; Floridi, A.; Gallai, V. Brain-derived neurotrophic factors in patients with multiple sclerosis. J. Neuroimmunol. 2002, 132 (1-2):180-188.
39. Gielen, A.; Khademi, M.; Muhallab, S.; Olsson, T.; Piehl, F. Increased brain-derived neurotrophic factor expression in white blood cells of relapsing-remitting multiple sclerosis patients. Scand. J. Immunol. 2003, 57 (5):493-497.
40. Azoulay, D.; Urhansky, N.; Karni, A. Low and dysregulated BDNF secretion from immune cells of MS patients is related to reduced neuroprotection. J. Neuroimmunol. 2008, 195 (1-2):186-193.
41. Caggiula, M.; Batocchi, A.P.; Frisullo, G.; Angelucci, F.; Patanella, A.K.; Sancricca, C.; Nociti, V.; Tonali, P.A.; Mirabella, M. Neurotrophic factors and clinical recovery in relapsing-remitting multiple sclerosis. Scand. J. Immunol. 2005, 62 (2):176-182.
42. Hamamcioglu, K.; Reder, A.T. Interferon-β regulates cytokine and BDNF: Greater effect in relapsing than in progressive multiple sclerosis. Mult. Scler. 2007, 13 (4):459-470.
43. Weinstock-Guttman, B.; Zivadinov, R.; Tamano-Blanco, M.; Abdelrahman, N.; Badgett, D.; Durfee, J.; Hussein, S.; Feichter, J.; Patrick, K.; Benedict, R.; Ramanathan, M. Immune cell BDNF secretion is associated with white matter volume in multiple sclerosis. J. Neuroimmunol. 2007, 188 (1-2):167-174.
44. Seidah, N.G.; Benjannet, S.; Pareek, S.; Chrieten, M.; Murphy, R.A. Cellular processing of the neurotrophin precursors of NT 3 and BDNF by the mammalian proprotein convertase. FEBS Lett. 1996, 379 (3):247-250.
45. Shintani, A.; Ono, Y.; Kaisho, Y.; Igarashi, K. Characterization of the 59-flanking region of the human brain-derived neurotrophic factor gene. Biochem. Biophys. Res. Commun. 1992, 182:325-332.
46. Kunugi, H.; Ueki, A.; Otsuka, M.; Isse, K.; Hirasawa, H.; Kato, N.; Nabika, T.; Kobayashi, S.; Nanko, S. A novel polymorphism of the brain-derived neurotrophic factor (BDNF) gene associated with late-onset Alzheimer's disease. Molec. Psychiatry 2001, 6 (1):83-86.
47. Lindquist, S; Schott, BH; Ban, M; Compston, DAS; Sawcer, S; Sailer, M. The BDNF-Val66Met polymorphism: Implication for susceptibility to multiple sclerosis and severity of disease. J. Neuroimmunol. 2005, 167 (1-2):183-185.
48. Blanco, Y.; Gomez-Choco, M.; Arostegui, J.L.; Casanova, B.; Martinez-Rodriguez, J.E.; Bosca, I.; Munteis, E.; Yagüe, J.; Graus, F.; Saiz, A. No association of the Val66Met polymorphism of brainderived neurotrophic factor (BDNF) to multiple sclerosis. Neurosci. Lett. 2006, 396 (3):217-219.
49. Liguori, M.; Fera, F.; Gioia, M.C.; Valentino, P.; Manna, I.; Condino, F.; Cerasa, A.; LaRussa, A.; Clodomiro, A.; Paolillo, A.; Nistico, R.; Vercillo, L.; Cittadella, R.; Quattrone, A. Investigating the role of brain-derived neurotrophic factor in relapsing-remitting multiple sclerosis. Genes Brain Behav. 2007, 6 (2):177-183.
50. Mirowska-Guzel, D.; Mach, A.; Gromadzka, G.; Czlonkowski, A.; Czlonkowska, A. G196A and C720T BDNF gene polymorphisms and susceptibility to multiple sclerosis. J. Neuroimmunol. 2008, 193 (1-2):170-172.
51. Ozenci, V.; Kouwenhoven, M.; Teleshova, M.; Pashenkov, M; Fredrikson, S.; Link, H. Multiple sclerosis: Pro- and anti-inflammatory cytokines and metalloproteinases are affected differentially by treatment with IFN-beta. J. Neuroimmunol. 2000, 108 (1-2):236-243.
52. Mirowska, D.; Skierski, J.; Paz, A.; Koronkiewicz, M.; Zaborski, J.; Kruszewska, J.; Członkowski, A.; Członkowska, A. Monitoring of peripheral blood immune phenotype changes, including cytokine producing cells, in multiple sclerosis patients during a two-year IFN-β-1a treatment. J. Neurol. 2003, 250 (10):1229-1236.
53. Petereit, H.F.; Lindemann, H.; Schoppe, S. Effect of immunomodulatory drugs on in vitro production of brain-derived neurotrophic factor. Mult. Scler. 2003, 9 (1):16-20.
54. Caggiula, M.; Batocchi, A.P.; Frisullo, G.; Angelucci, F.; Patanella, A.K.; Sancricca, C.; Nociti, V.; Tonali, P.A.; Mirabella, M. Neurotrophic factors in relapsing remitting and secondary progressive multiple sclerosis patients during interferon therapy. Clin. Immunol. 2006, 118 (1):77-82.
55. Biernacki, K.; Antel, J.; Blain, M.; Narayanan, S.; Arnold, D.L.; Prat, A. Interferon beta promotes nerve growth factor secretion early in the course of multiple sclerosis. Arch. Neurol. 2005, 62 (4):563-568.
56. Ge, Y.; Grossman, R.I.; Udupa, J.K.; Fulton, J.; Constantinescu, C.S.; Gonzales-Scarano, F.; Babb, J.S.; Mannon, L.J.; Kolson, D.L.; Cohen, J.A. Glatiramer acetate (Copaxone) treatment in relapsing-remitting MS: Quantitative MR assessment. Neurology 2000, 54 (4):813-817.
57. Rovaris, M.; Comi, G.; Rocca, M.A.; Wolinsky, J.S.; Filippi, M. Short-term brain volume change in relapsing-remitting multiple sclerosis: Effect of glatiramer acetate and implications. Brain 2001, 124 (Pt 9):1803-1812.
58. Zimmsen, T.; Kümpfel, T.; Klinkert, W.E.F.; Neuhaus, O.; Hohlfeld, R. Glatiramer acetate-specific T-helper 1- and 2-type cell lines produce BDNF: implications for multiple sclerosis therapy. Brain 2002, 125 (Pt 11):2381-2391.
59. Chen, M.; Valenzuela, R.M.; Dhib-Jalbut, S. Glatiramer acetate-reactive T cells produce brain-derived neurotrophic factor. J. Neurol. Sci. 2003, 215 (1-2):37-44.
60. Ziemssen, T.; Kümpfel, T.; Schneider, H.; Klinkert, W.E.F.; Neuhaus, O.; Hohlfeld, R. Secretion of brain-derived neurotrophic factor by glatiramer acetate-reactive T-helper cell lines: implications for multiple sclerosis therapy. J. Neurol. Sci. 2005, 233 (1-2):109-112.
61. Azoulay, D.; Vachapova, V.; Shihman, B.; Miler, A.; Karni, A. Lower brain-derived neurotrophic factor in serum of relapsing remitting MS: reversal by glatiramer acetate. J. Neuroimmunol. 2005, 167 (1-2):215-218.
62. Blanco, Y.; Saiz, A.; Costa, M.; Torres-Peraza, J.F.; Carreras, E.; Albrecht, J.; Jaraquemada, D.; Graus, F. Evolution of brain-derived neurotrophic factor levels after autologous hematopoetic stem cell transplantation in multiple sclerosis. Neurosci. Lett. 2005, 380 (1-2):122-126.
63. Aebischer, P.; Schluep, M.; Deglon, N.; Joseph, J.M.; Hirt, L.; Heyd, B.; Goddard, M.; Hammang, J.P.; Zurn, A.D.; Kato, A.C.; Regli, F.; Baetge, E.E. Intrarhecal delivery of CNTF using encapsulated genetically modified xenogenic cells in amyotrophic lateral sclerosis patients. Nat. Med. 1996, 2 (6):696-699.
64. ALS CNTF Treatment Study Group: A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. Neurology 1996, 46 (5):1244-1249.
65. Bloch, J.; Bachoud-Levi, A.C.; Eglon, N.; Lefaucheur, J.P.; Winkel, L.; Palfi, S.; Nguyen, J.P.; Bourdet, C.; Gaura, V.; Remy, P.; Brugieres, P.; Boisse, M.F.; Baudic, S.; Cesaro, P.; Hantraye, P.; Aebischer, P.; Peschanski, M. Neuroprotective gene therapy for Huntington's disease, Rusing poylmer-encapsulated cells engineered to secrete human ciliary neurotrophic factor: result of a phase I study. Hum. Gene Ther. 2004, 15 (10):968-975.
66. Borasio, G.D.; Robberecht, W.; Leigh, P.N.; Emile, J.; Guiloff, R.J.; Jerusalem, F.; Silani, V.; Vos, P.E.; Wokke, J.H.; Dobbins, T. A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group. Neurology 1998, 51 (2):583-586.
67. Eriksdotter Jönhagen, M.; Nordberg, A.; Amberla, K.; Bäckman, L.; Ebendal, T.; Meyerson, B.; Olson, L.; Seiger, A.; Shigeta, M.; Theodorsson, E.; Viitanen, M.; Winblad, B.; Wahlund, L.O. Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 1998, 9 (5):246-257.
68. Gill, S.S.; Patel, N.K.; Hotton, G.R.; O'Sullivan, K.; McCarter, R.; Bunnage, M.; Brooks, D.J.; Svendsen, C.N.; Heywood, P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 2003, 9 (5):589-595.
69. Nutt, J.G.; Burchiel, K.J.; Comella, C.L.; Jankovic, J.; Lang, A.E.; Laws, E.R.Jr; Lozano, A.M.; Penn, R.D.; Simpson, R.K.Jr; Stacy, M.; Wooten, G.F. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 2003, 60 (1):69-73.
70. The BDNF Study Group (Phase III): A controlled trial of recombinant methionyl human BDNF in ALS: The BDNF Study Group (Phase III). Neurology 1999, 52 (7):1427-1433.
71. Tuszynski, M.H.; Thal, L.; Pay, M.; Salmon, D.P.; Patel, P.; Blesch, A.; Vahlsing, H.L.; Ho, G.; Tong, G.; Potkin, S.G.; Fallon, J.; Hansen, L.; Mufson, E.J.; Kordower, J.H.; Gall, C.; Conner, J. A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat. Med. 2005, 11 (5):551-555.
72. Czlonkowski, A.; Mirowska-Guzel, D. Therapy of stroke - From experimental to clinical trials. Pharmacol. Rep. 2007, 56 (suppl.1):123-128.
73. Lees, K.R.; Zivin, J.A.; Ashwood, T.; Davalos, A.; Davis, S.M.; Hardemark, H.-Ch.; Grotta, J.; Lyden, P.; Shuaib, A.; Hardemark, H.-G.; Wasiewski, W.W. for the Stroke-Acute Ischemic NXY Treatment (Saint I) Trial Investigators: NXY-059 for acute ischemic stroke. N. Engl. J. Med. 2006, 354 (6):588-600.
74. Shuaib, A.; Lees, K.R.; Lyden, P.; Grotta, J.; Davalos, A.; Davis, S.M.; Diener, H.C.; Ashwood, T.; Wasiewski, W.W.; Emeribe, U., and SAINT II Trial Investigators. NXY-059 for the treatment of acute ischemic stroke. N. Engl. J. Med. 2007, 357 (6):562-571.