Cell-based delivery of brain-derived neurotrophic factor in experimental allergic encephalomyelitis

Journal of Interferon and Cytokine Research

Volumn 34, Issue 8, 2014, Pages 641-647

  Makar, Tapas K ^a,b   Nimmagadda, Vamshi K C ^b   Trisler, David ^a,b   Bever Jr , Christopher T ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DOXYCYCLINE; GLUTAMATE DECARBOXYLASE; CYTOKINE; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BLOOD BRAIN BARRIER; CELL INFILTRATION; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; DRUG DELIVERY SYSTEM; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE TARGETING; GENE THERAPY; GENETIC TRANSFECTION; HEMATOPOIETIC STEM CELL; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; CELL CULTURE; CELL MOTION; CENTRAL NERVOUS SYSTEM; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETIC ENGINEERING; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOLOGY; INBRED MOUSE STRAIN; METABOLISM; PHYSIOLOGY; TRANSGENE; UPREGULATION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL MOVEMENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CYTOKINES; DRUG DELIVERY SYSTEMS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETIC ENGINEERING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED STRAINS; NEUROPROTECTIVE AGENTS; TRANSGENES; UP-REGULATION;

EID: 84905409136     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2013.0160     Document Type: Review

References (68)

1. Aharoni R, Eilam R, Domev H, Labunskay G, Sela M, Arnon R. 2005. The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice. Proc Natl Acad Sci U S A 102(52):19045-19050.
2. Aharoni R, Kayhan B, Eilam R, Sela M, Arnon R. 2003. Gla-tiramer acetate-specific T cells in the brain express T helper 2/3 cytokines and brain-derived neurotrophic factor in situ. Proc Natl Acad Sci U S A 100(24):14157-14162.
3. Azoulay D, Vachapova V, Shihman B, Miler A, Karni A. 2005. Lower brain-derived neurotrophic factor in serum of relapsing remitting MS: reversal by glatiramer acetate. J Neu-roimmunol 167(1-2):215-218.
4. Barde YA. 1997. Help from within for damaged axons. Nature 385(6615):391, 393.
5. Baseri B, Choi JJ, Deffieux T, Samiotaki G, Tung YS, Olu-molade O, Small SA, Morrison B, Konofagou EE. 2012. Activation of signaling pathways following localized delivery of systemically administered neurotrophic factors across the blood-brain barrier using focused ultrasound and micro-bubbles. Phys Med Biol 57(7):N65-N81.
6. Bemelmans AP, Horellou P, Pradier L, Brunet I, Colin P, Mallet J. 1999. Brain-derived neurotrophic factor-mediated protection of striatal neurons in an excitotoxic rat model of Hun-tington's disease, as demonstrated by adenoviral gene transfer. Hum Gene Ther 10(18):2987-2997.
7. Bordignon C, Roncarolo MG. 2002. Therapeutic applications for hematopoietic stem cell gene transfer. Nat Immunol 3(4): 318-321.
8. Bruck W, Wegner C. 2011. Insight into the mechanism of la-quinimod action. J Neurol Sci 306(1-2):173-179.
9. Caggiula M, Batocchi AP, Frisullo G, Angelucci F, Patanella AK, Sancricca C, Nociti V, Tonali PA, Mirabella M. 2006. Neurotrophic factors in relapsing remitting and secondary progressive multiple sclerosis patients during interferon beta therapy. Clin Immunol 118(1):77-82.
10. Canals JM, Pineda JR, Torres-Peraza JF, Bosch M, Martin-Ibanez R, Munoz MT, Mengod G, Ernfors P, Alberch J. 2004. Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J Neurosci 24(35):7727-7739.
11. Chao MV. 2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4(4):299-309.
12. Chen M, Dhib-Jalbut S. 2003. Glatiramer acetate reactive T-cells produce brain derived neurotrophic factor (BDNF). J Neurol Sci 140:37-44.
13. Colombo E, Cordiglieri C, Melli G, Newcombe J, Krumbholz M, Parada LF, Medico E, Hohlfeld R, Meinl E, Farina C. 2012. Stimulation of the neurotrophin receptor TrkB on as-trocytes drives nitric oxide production and neurodegenera-tion. J Exp Med 209(3):521-535.
14. De Santi L, Annunziata P, Sessa E, Bramanti P. 2009. Brain-derived neurotrophic factor and TrkB receptor in experimental autoimmune encephalomyelitis and multiple sclerosis. J Neurol Sci 287(1-2):17-26.
15. Dhib-Jalbut S. 2002. Mechanisms of action of interferons and glatiramer acetate in multiple sclerosis. Neurology 58 (8 Suppl. 4):S3-S9.
16. Dhib-Jalbut S, Marks S. 2010. Interferon-beta mechanisms of action in multiple sclerosis. Neurology 74 (Suppl. 1):S17-S24.
17. Eglitis MA, Mezey E. 1997. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A 94(8):4080-4085.
18. Felts PA, Smith KJ, Gregson NA, Hughes RA. 2002. Brain-derived neurotrophic factor in experimental autoimmune neuritis. J Neuroimmunol 124(1-2):62-69.
19. Flugel A, Matsumuro K, Neumann H, Klinkert WE, Birnbacher R, Lassmann H, Otten U, Wekerle H. 2001. Anti-inflammatory activity of nerve growth factor in experimental autoimmune encephalomyelitis: inhibition of monocyte transendothelial migration. Eur J Immunol 31(1):11-22.
20. Giralt A, Friedman HC, Caneda-Ferron B, Urban N, Moreno E, Rubio N, Blanco J, Peterson A, Canals JM, Alberch J. 2010. BDNF regulation under GFAP promoter provides engineered astrocytes as a new approach for long-term protection in Huntington's disease. Gene Ther 17(10):1294-1308.
21. Goolsby J, Makar T, Dhib-Jalbut S, Bever CT Jr., Pessac B, Trisler D. 2013. Hematopoietic progenitors express myelin basic protein and ensheath axons in Shiverer brain. J Neu-roimmunol 257(1-2):13-20.
22. Goolsby J, Marty MC, Heletz D, Chiappelli J, Tashko G, Yarnell D, Fishman PS, Dhib-Jalbut S, Bever CT Jr., Pessac B, Trisler D. 2003. Hematopoietic progenitors express neural genes. Proc Natl Acad Sci U S A 100(25):14926-14931.
23. Herrero-Herranz E, Pardo LA, Gold R, Linker RA. 2008. Pattern of axonal injury in murine myelin oligodendrocyte glycoprotein induced experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Neurobiol Dis 30(2):162-173.
24. Hofer MM, Barde YA. 1988. Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature 331(6153):261-262.
25. Jaini R, Hannaman D, Johnson JM, Bernard RM, Altuntas CZ, Delasalas MM, Kesaraju P, Luxembourg A, Evans CF, Tuohy VK. 2006. Gene-based intramuscular interferon-beta therapy for experimental autoimmune encephalomyelitis. Mol Ther 14(3):416-422.
26. Javeri S, Rodi M, Tary-Lehmann M, Lehmann PV, Addicks K, Kuerten S. 2010. Involvement of brain-derived neurotrophic factor (BDNF) in MP4-induced autoimmune encephalomy-elitis. Clin Immunol 137(2):181-189.
27. Kernie SG, Liebl DJ, Parada LF. 2000. BDNF regulates eating behavior and locomotor activity in mice. EMBO J 19(6): 1290-1300.
28. Kerschensteiner M, Gallmeier E, Behrens L, Leal VV, Misgeld T, Klinkert WE, Kolbeck R, Hoppe E, Oropeza-Wekerle RL, Bartke I, Stadelmann C, Lassmann H, Wekerle H, Hohlfeld R. 1999. 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 189(5):865-870.
29. Kipnis J, Yoles E, Porat Z, Cohen A, Mor F, Sela M, Cohen IR, Schwartz M. 2000. T cell immunity to copolymer 1 confers neuroprotection on the damaged optic nerve: possible therapy for optic neuropathies. Proc Natl Acad Sci U S A 97(13): 7446-7451.
30. Kishino A, Katayama N, Ishige Y, Yamamoto Y, Ogo H, Tatsuno T, Mine T, Noguchi H, Nakayama C. 2001. Analysis of effects and pharmacokinetics of subcutaneously administered BDNF. Neuroreport 12(5):1067-1072.
31. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. 1995. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92(19):8856-8860.
32. Kramer R, Zhang Y, Gehrmann J, Gold R, Thoenen H, Wekerle H. 1995. Gene transfer through the blood-nerve barrier: NGF-engineered neuritogenic T lymphocytes attenuate experimental autoimmune neuritis. Nat Med 1(11):1162-1166.
33. Krishnamoorthy G, Wekerle H. 2009. EAE: an immunologist's magic eye. Eur J Immunol 39(8):2031-2035.
34. Lee DH, Geyer E, Flach AC, Jung K, Gold R, Flugel A, Linker RA, Luhder F. 2012. Central nervous system rather than immune cell-derived BDNF mediates axonal protective effects early in autoimmune demyelination. Acta Neuropathol 123(2):247-258.
35. Lim JY, Jeong CH, Jun JA, Kim SM, Ryu CH, Hou Y, Oh W, Chang JW, Jeun SS. 2011. Therapeutic effects of human umbilical cord blood-derived mesenchymal stem cells after intrathecal administration by lumbar puncture in a rat model of cerebral ischemia. Stem Cell Res Ther 2(5):38.
36. Linker RA, Lee DH, Demir S, Wiese S, Kruse N, Siglienti I, Gerhardt E, Neumann H, Sendtner M, Luhder F, Gold R. 2010. Functional role of brain-derived neurotrophic factor in neuroprotective autoimmunity: therapeutic implications in a model of multiple sclerosis. Brain 133(Pt 8):2248-2263.
37. Lucidi-Phillipi CA, Gage FH, Shults CW, Jones KR, Reichardt LF, Kang UJ. 1995. Brain-derived neurotrophic factor-transduced fibroblasts: production of BDNF and effects of grafting to the adult rat brain. J Comp Neurol 354(3):361-376.
38. Maghzi AH, Minagar A, Waubant E. 2013. Neuroprotection in multiple sclerosis: a therapeutic approach. CNS Drugs 27(10): 799-815.
39. Makar TK, Bever CT, Singh IS, Royal W, Sahu SN, Sura TP, Sultana S, Sura KT, Patel N, Dhib-Jalbut S, Trisler D. 2009. Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle. J Neuroimmunol 210(1-2):40-51.
40. Makar TK, Nimmagadda VK, Patibandla GK, Le T, Judge SI, Trisler D, Bever CT. 2012. Use of engineered bone marrow stem cells to deliver brain derived neurotrophic factor under the control of a tetracycline sensitive response element in experimental allergic encephalomyelitis. J Neuroimmunol 252(1-2):1-15.
41. Makar TK, Trisler D, Bever CT, Goolsby JE, Sura KT, Bala-subramanian S, Sultana S, Patel N, Ford D, Singh IS, Gupta A, Valenzuela RM, Dhib-Jalbut S. 2008a. Stem cell based delivery of IFN-beta reduces relapses in experimental autoimmune encephalomyelitis. J Neuroimmunol 196(1-2):67-81.
42. Makar TK, Trisler D, Eglitis MA, Mouradian MM, Dhib-Jalbut S. 2004. Brain-derived neurotrophic factor (BDNF) gene delivery into the CNS using bone marrow cells as vehicles in mice. Neurosci Lett 356(3):215-219.
43. Makar TK, Trisler D, Sura KT, Sultana S, Patel N, Bever CT. 2008b. Brain derived neurotrophic factor treatment reduces inflammation and apoptosis in experimental allergic en-cephalomyelitis. J Neurol Sci 270(1-2):70-76.
44. Makar TK, Wilt S, Dong Z, Fishman P, Mouradian MM, Dhib-Jalbut S. 2002. IFN-beta gene transfer into the central nervous system using bone marrow cells as a delivery system. J Interferon Cytokine Res 22(7):783-791.
45. Manfredonia F, Pasquali L, Dardano A, Iudice A, Murri L, Monzani F. 2008. Review of the clinical evidence for interferon beta 1a (Rebif) in the treatment of multiple sclerosis. Neuropsychiatr Dis Treat 4(2):321-336.
46. Matsumoto T, Rauskolb S, Polack M, Klose J, Kolbeck R, Korte M, Barde YA. 2008. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 11(2):131-133.
47. McTigue DM, Horner PJ, Stokes BT, Gage FH. 1998. Neuro-trophin-3 and brain-derived neurotrophic factor induce oli-godendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18(14):5354-5365.
48. Mitsumoto H, Ikeda K, Klinkosz B, Cedarbaum JM, Wong V, Lindsay RM. 1994. Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265(5175): 1107-1110.
49. Murer MG, Yan Q, Raisman-Vozari R. 2001. Brain-derived neu-rotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63(1): 71-124.
50. Nikic I, Merkler D, Sorbara C, Brinkoetter M, Kreutzfeldt M, Bareyre FM, Bruck W, Bishop D, Misgeld T, Kerschen-steiner M. 2011. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 17(4):495-499.
51. Nimmagadda VK, Bever CT, Vattikunta NR, Talat S, Ahmad V, Nagalla NK, Trisler D, Judge SI, Royal W 3rd, Chan-drasekaran K, Russell JW, Makar TK. 2013. Overexpression of SIRT1 protein in neurons protects against experimental autoimmune encephalomyelitis through activation of multiple SIRT1 targets. J Immunol 190(9):4595-4607.
52. Park KW, Eglitis MA, Mouradian MM. 2001. Protection of nigral neurons by GDNF-engineered marrow cell transplantation. Neurosci Res 40(4):315-323.
53. Perez-Navarro E, Canudas AM, Akerund P, Alberch J, Arenas E. 2000. Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 prevent the death of striatal projection neurons in a rodent model of Huntington's disease. J Neu-rochem 75(5):2190-2199.
54. Pessac B, Bara MA, Ford D, Patibandla GK, Trisler D. 2011. Hematopoietic progenitors express embryonic stem cell and germ layer genes. C R Biol 334(4):300-306.
55. Pessac B, Nimmagadda VK, Makar T, Fishman PS, Bever CT Jr., Trisler D. 2012. Adult hematopoietic progenitors are multipotent in chimeric mice. C R Biol 335(7):454-462.
56. Prat A, Antel J. 2005. Pathogenesis of multiple sclerosis. Curr Opin Neurol 18(3):225-230.
57. Robinson M, Buj-Bello A, Davies AM. 1996. Paracrine interactions of BDNF involving NGF-dependent embryonic sensory neurons. Mol Cell Neurosci 7(2):143-151.
58. Rubio FJ, Kokaia Z, del Arco A, Garcia-Simon MI, Snyder EY, Lindvall O, Satrustegui J, Martinez-Serrano A. 1999. BDNF gene transfer to the mammalian brain using CNS-derived neural precursors. Gene Ther 6(11):1851-1866.
59. Ryu CH, Park KY, Hou Y, Jeong CH, Kim SM, Jeun SS. 2013. Gene therapy of multiple sclerosis using interferon beta-secreting human bone marrow mesenchymal stem cells. Biomed Res Int 2013:696738.
60. Schaefer C, Hidalgo TR, Cashion L, Petry H, Brooks A, Szy-manski P, Qian HS, Gross C, Wang P, Liu P, Goldman C, Rubanyi GM, Harkins RN. 2006. Gene-based delivery of IFN-beta is efficacious in a murine model of experimental allergic encephalomyelitis. J Interferon Cytokine Res 26(7): 449-454.
61. Schmidt J, Sturzebecher S, Toyka KV, Gold R. 2001. Interferon-beta treatment of experimental autoimmune encepha-lomyelitis leads to rapid nonapoptotic termination of T cell infiltration. J Neurosci Res 65(1):59-67.
62. Sospedra M, Martin R. 2005. Immunology of multiple sclerosis. Annu Rev Immunol 23:683-747.
63. Stadelmann C, Kerschensteiner M, Misgeld T, Bruck W, Hohlfeld R, Lassmann H. 2002. BDNF and gp145trkB in multiple sclerosis brain lesions: neuroprotective interactions between immune and neuronal cells? Brain 125(Pt 1):75-85.
64. Steinman L. 1996. Multiple sclerosis: a coordinated immuno-logical attack against myelin in the central nervous system. Cell 85(3):299-302.
65. VonDran MW, Singh H, Honeywell JZ, Dreyfus CF. 2011. Levels of BDNF impact oligodendrocyte lineage cells following a cuprizone lesion. J Neurosci 31(40):14182-14190.
66. Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M. 2005a. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 195(1):16-26.
67. Zhang J, Li Y, Cui Y, Chen J, Lu M, Elias SB, Chopp M. 2005b. Erythropoietin treatment improves neurological functional recovery in EAE mice. Brain Res 1034(1-2): 34-39.
68. Zuccato C, Cattaneo E. 2009. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5(6):311-322.