Retroviral lineage analysis of fibroblast growth factor receptor signaling in FGF2 inhibition of oligodendrocyte progenitor differentiation

GLIA

Volumn 54, Issue 6, 2006, Pages 578-590

  Zhou, Yong Xing ^a   Flint, Nicole C ^a   Murtie, Joshua C ^a,b   Le, Tuan Q ^a   Armstrong, Regina C ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Differentiation; FGF receptor (FGFR); Fibroblast growth factor 2 (FGF2); Oligodendrocyte; siRNA

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR; GREEN FLUORESCENT PROTEIN; PROTEIN P28; RETROVIRUS VECTOR; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL LABELING; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; GENE CONSTRUCT; GENE MUTATION; IN VIVO STUDY; INFECTION; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT; SPINE; STEM CELL; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; GROWTH INHIBITORS; MALE; MICE; MICE, INBRED C57BL; NERVE FIBERS, MYELINATED; NERVE REGENERATION; OLIGODENDROGLIA; RATS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STEM CELLS; TRANSFECTION;

EID: 33748994294     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20410     Document Type: Article

References (68)

1. Alzheimer C, Werner S. 2002. Fibroblast growth factors and neuroprotection. Adv Exp Med Biol 513:335-351.
2. Armstrong RC. 1998. Isolation and characterization of immature oligodendrocyte lineage cells. Methods 16:282-292.
3. Armstrong RC, Dorn HH, Kufta CV, Friedman E, Dubois-Dalcq ME. 1992. Pre-oligodendrocytes from adult human CNS. J Neurosci 12: 1538-1547.
4. Armstrong RC, Kim JG, Hudson LD. 1995. Expression of myelin transcription factor I (MyTI), a "zinc-finger" DNA-binding protein, in developing oligodendrocytes. Glia 14:303-321.
5. Armstrong RC, Le TQ, Frost EE, Borke RC, Vana AC. 2002. Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J Neurosci 22:8574-8585.
6. Armstrong RC, Le TQ, Flint NC, Vana AC, Zhou YX. 2006. Endogenous cell repair of chronic demyelination. J Neuropathol Exp Neurol 65(3): 245-256.
7. Asai T, Wanaka A, Kato H, Masana Y, Seo M, Tohyama M. 1993. Differential expression of two members of FGF receptor gene family, FGFR-1 and FGFR-2 mRNA, in the adult rat central nervous system. Brain Res Mol Brain Res 17:174-178.
8. Ballabriga J, Pozas E, Planas AM, Ferrer I. 1997. bFGF and FGFR-3 immunoreactivity in the rat brain following systemic kainic acid administration at convulsant doses: Localization of bFGF and FGFR-3 in reactive astrocytes, and FGFR-3 in reactive microglia. Brain Res 752:315-318.
9. Bansal R, Kumar M, Murray K, Morrison RS, Pfeiffer SE. 1996. Regulation of FGF receptors in the oligodendrocyte lineage. Mol Cell Neurosci 7:263-275.
10. Bansal R, Lakhina V, Remedies R, Tole S. 2003. Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with Pdgfralpha, Olig2 and Plp/dm20: Implications for oligodendrocyte development. Dev Neurosci 25:83-95.
11. Belluardo N, Wu G, Mudo G, Hansson AC, Pettersson R, Fuxe K. 1997. Comparative localization of fibroblast growth factor receptor-1, -2, and -3 mRNAs in the rat brain: In situ hybridization analysis. J Comp Neurol 379:226-246.
12. Bogler O, Wren D, Barnett SC, Land H, Noble M. 1990. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci USA 87:6368-6372.
13. Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, Richardson WD. 1998. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20:869-882.
14. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. 2000. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20:6404-6412.
15. Chang A, Tourtellotte WW, Rudick R, Trapp BD. 2002. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346:165-173.
16. Decker L, Picard-Riera N, Lachapelle F, Baron-Van Evercooren A. 2002. Growth factor treatment promotes mobilization of young but not aged adult subventricular zone precursors in response to demyelination. J Neurosci Res 69:763-771.
17. Eccleston PA, Silberberg DH. 1984. The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium. Brain Res 318: 1-9.
18. Fortin D, Rom E, Sun H, Yayon A, Bansal R. 2005. Distinct fibroblast growth factor (FGF)/FGF receptor signaling pairs initiate diverse cellular responses in the oligodendrocyte lineage. J Neurosci 25:7470-7479.
19. Frost EE, Nielsen JA, Le TQ, Armstrong RC. 2003. PDGF and FGF2 regulate oligodendrocyte progenitor responses to demyelination. J Neurobiol 54:457-472.
20. Fruttiger M, Karlsson L, Hall AC, Abramsson A, Calver AR, Bostrom H, Willetts K, Bertold CH, Heath JK, Betsholtz C, Richardson WD. 1999. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126:457-467.
21. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB. 2000. Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259-274.
22. Genoud S, Lappe-Siefke C, Goebbels S, Radtke F, Aguet M, Scherer SS, Suter U, Nave KA, Mantei N. 2002. Notch1 control of oligodendrocyte differentiation in the spinal cord. J Cell Biol 158:709-718.
23. Harari D, Finkelstein D, Bernard O. 1997. FGF plays a subtle role in oligodendrocyte maintenance in vivo. J Neurosci Res 49:404-415.
24. Hoch RV, Soriano P. 2006. Context-specific requirements for Fgfr1 signaling through Frs2 and Frs3 during mouse development. Development 133:663-673.
25. Holley JE, Gveric D, Newcombe J, Cuzner ML, Gutowski NJ. 2003. Astrocyte characterization in the multiple sclerosis glial scar. Neuropathol Appl Neurobiol 29:434-444.
26. Hudson LD, Berndt JA, Puckett C, Kozak CA, Lazzarini RA. 1987. Aberrant splicing of proteolipid protein mRNA in the dysmyelinating jimpy mutant mouse. Proc Natl Acad Sci USA 84:1454-1458.
27. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, Brosnan CF. 2002. Multiple sclerosis: Re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 8:1115-1121.
28. Jungnickel J, Claus P, Gransalke K, Timmer M, Grothe C. 2004. Targeted disruption of the FGF-2 gene affects the response to peripheral nerve injury. Mol Cell Neurosci 25:444-452.
29. Jurynczyk M, Jurewicz A, Bielecki B, Raine CS, Selmaj K. 2005. Inhibition of Notch signaling enhances tissue repair in an animal model of multiple sclerosis. J Neuroimmunol 170:3-10.
30. Kakita A, Zerlin M, Takahashi H, Goldman JE. 2003. Some glial progenitors in the neonatal subventricular zone migrate through the corpus callosum to the contralateral cerebral hemisphere. J Comp Neurol 458:381-388.
31. Levison SW, Goldman JE. 1993. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10(2):201-212.
32. Levison SW, Young GM, Goldman JE. 1999. Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. J Neurosci Res 57:435-446.
33. Li X, Chen Y, Scheele S, Arman E, Haffner-Krausz R, Ekblom P, Lonai P. 2001. Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J Cell Biol 153:811-822.
34. Lillien LE, Raff MC. 1990. Differentiation signals in the CNS: Type-2 astrocyte development in vitro as a model system. Neuron 5:111-119.
35. Liu X, Mashour GA, Webster HF, Kurtz A. 1998. Basic FGF, FGF receptor 1 are expressed in microglia during experimental autoimmune encephalomyelitis: Temporally distinct expression of midkine and pleiotrophin. Glia 24:390-397.
36. Logan A, Frautschy SA, Gonzalez AM, Baird A. 1992. A time course for the focal elevation of synthesis of basic fibroblast growth factor and one of its high-affinity receptors (flg) following a localized cortical brain injury. J Neurosci 12:3828-3837.
37. Macklin WB, Gardinier MV, Obeso ZO, King KD, Wight PA. 1991. Mutations in the myelin proteolipid protein gene alter oligodendrocyte gene expression in jimpy and jimpymsd mice. J Neurochem 56:163-171.
38. Mansukhani A, Dell'Era P, Moscatelli D, Kornbluth S, Hanafusa H, Basilico C. 1992. Characterization of the murine BEK fibroblast growth factor (FGF) receptor: Activation by three members of the FGP family and requirement for heparin. Proc Natl Acad Sci USA 89:3305-3309.
39. Masumura M, Murayama N, Inoue T, Ohno T. 1996. Selective induction of fibroblast growth factor receptor-1 mRNA after transient focal ischemia in the cerebral cortex of rats. Neurosci Lett 213:119-122.
40. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA. 1999. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17:969-973.
41. McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA. 1990. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5:603-614.
42. Messersmith DJ, Murtie JC, Le TQ, Frost EE, Armstrong RC. 2000. Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J Neurosci Res 62:241-256.
43. Miller RH, David S, Patel R, Abney ER, Raff MC. 1985. A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve: In vivo evidence for two distinct astrocyte lineages. Dev Biol 111:35-41.
44. Miyake A, Hattori Y, Ohta M, Itoh N. 1996. Rat oligodendrocytes and astrocytes preferentially express fibroblast growth factor receptor-2 and -3 mRNAs. J Neurosci Res 45:534-441.
45. Murtie JC, Zhou YX, Le TQ, Armstrong RC. 2005a. In vivo analysis of oligodendrocyte lineage development in postnatal FGF2 null mice. Glia 49:542-554.
46. Murtie JC, Zhou YX, Le TQ, Vana AC, Armstrong RC. 2005b. PDGF and FGF2 pathways regulate distinct oligodendrocyte lineage responses in experimental demyelination with spontaneous remyelination. Neurobiol Dis 19:171-182.
47. Nielsen JA, Berndt JA, Hudson LD, Armstrong RC. 2004. Myelin transcription factor 1 (Myt1) modulates the proliferation and differentiation of oligodendrocyte lineage cells. Mol Cell Neurosci 25:111-123
48. Noble M, Murray K, Stroobant P, Waterfield MD, Riddle P. 1988. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333:560-562.
49. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720.
50. Oh LY, Denninger A, Colvin JS, Vyas A, Tole S, Ornitz DM, Bansal R. 2003. Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci 23:883-894.
51. Raff MC, Lillien LE. 1988. Differentiation of a bipotential glial progenitor cell: What controls the timing and the choice of developmental pathway? J Cell Sci Suppl 10:77-83.
52. Raff MC, Miller RH, Noble M. 1983. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303:390-396.
53. Reuss B, von Bohlen und Halbach O. 2003. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313:139-157.
54. Richardson WD, Pringle N, Mosley MJ, Westermark B, Dubois-Dalcq M. 1988. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53:309-319.
55. Ridyard MS, Robbins SM. 2003. Fibroblast growth factor-2-induced signaling through lipid raft-associated fibroblast growth factor receptor substrate 2 (FRS2). J Biol Chem 278:13803-13809.
56. Ruffini F, Furlan R, Poliani PL, Brambilla E, Marconi PC, Bergami A, Desina G, Glorioso JC, Comi G, Martino G. 2001. Fibroblast growth factor-II gene therapy reverts the clinical course and the pathological signs of chronic experimental autoimmune encephalomyelitis in C57BL/6 mice. Gene Ther 8:1207-1213.
57. Shiota C, Ikenaka K, Mikoshiba K. 1991. Developmental expression of myelin protein genes in dysmyelinating mutant mice: Analysis by nuclear run-off transcription assay, in situ hybridization, and immunohistochemistry. J Neurochem 56:818-826.
58. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
59. Small RK, Riddle P, Noble M. 1987. Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328:155-157.
60. Smith C, Berry M, Clarke WE, Logan A. 2001. Differential expression of fibroblast growth factor-2 and fibroblast growth factor receptor 1 in a scarring and nonscarring model of CNS injury in the rat. Eur J Neurosci 13:443-456.
61. Teng YD, Mocchetti I, Taveira-DaSilva AM, Gillis RA, Wrathall JR. 1999. Basic fibroblast growth factor increases long-term survival of spinal motor neurons and improves respiratory function after experimental spinal cord injury. J Neurosci 19:7037-7047.
62. Ueno H, Gunn M, Dell K, Tseng A Jr, Williams L. 1992. A truncated form of fibroblast growth factor receptor 1 inhibits signal transduction by multiple types of fibroblast growth factor receptor. J Biol Chem 267:1470-1476.
63. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
64. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA. 1998. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21:63-75.
65. Wolswijk G. 1998. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 18:601-609.
66. Wolswijk G. 2002. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125:338-349.
67. Wolswijk G, Noble M. 1992. Cooperation between PDGF and FGF converts slowly dividing O-2Aadult progenitor cells to rapidly dividing cells with characteristics of O-2Aperinatal progenitor cells. J Cell Biol 118:889-900.
68. Zhou YX, Xu X, Chen L, Li C, Brodie SG, Deng CX. 2000. A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum Mol Genet 9:2001-2008.