Full Access
In situ expression of fibroblast growth factor receptors by oligodendrocyte progenitors and oligodendrocytes in adult mouse central nervous system
Jeffrey M. Redwine,
Karen L. Blinder,
Regina C. Armstrong,
Jeffrey M. Redwine
Neurosciences Program, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Search for more papers by this authorKaren L. Blinder
Department of Anatomy and Cell Biology, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Search for more papers by this authorCorresponding Author
Regina C. Armstrong
Neurosciences Program, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Department of Anatomy and Cell Biology, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Department of Anatomy and Cell Biology, 4301 Jones Bridge Rd., Uniformed Services University of the Health Sciences, Bethesda, MD 20814-4799Search for more papers by this authorJeffrey M. Redwine,
Karen L. Blinder,
Regina C. Armstrong,
Jeffrey M. Redwine
Neurosciences Program, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Search for more papers by this authorKaren L. Blinder
Department of Anatomy and Cell Biology, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Search for more papers by this authorCorresponding Author
Regina C. Armstrong
Neurosciences Program, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Department of Anatomy and Cell Biology, Uniformed Services University of the Health Sciences, Bethesda, Maryland
Department of Anatomy and Cell Biology, 4301 Jones Bridge Rd., Uniformed Services University of the Health Sciences, Bethesda, MD 20814-4799Search for more papers by this authorFirst published: 07 December 1998
Citations: 50
Abstract
Basic fibroblast growth factor (bFGF) induces proliferation and alters differentiation of cultured oligodendrocyte lineage cells. In situ, bFGF is present in normal adult central nervous system (CNS) and upregulated during an early stage of various pathological conditions. We examined the expression of receptors for bFGF (FGFRs) by oligodendrocyte progenitors and oligodendrocytes in situ in normal adult mouse CNS to further understand the potential in situ response to bFGF. We found FGFR immunoreactivity in oligodendrocyte progenitors, identified by expression of NG2 or platelet-derived growth factor α receptor (PDGFαR), and in oligodendrocytes expressing 2′,3′-cyclic nucleotide 3′ phosphodiesterase. Particularly interesting is the demonstration that oligodendrocyte progenitors simultaneously expressing receptors for both bFGF and PDGF-AA are present in normal adult CNS. Since in vitro bFGF and PDGF-AA in combination induce oligodendrocyte progenitors from normal adult CNS to undergo rapid proliferation and migration, the in situ coexpression of FGFRs and PDGFαR supports the hypothesis that oligodendrocyte progenitors can respond to bFGF and PDGF-AA in situ, and that both growth factors may be critical for repopulation of demyelinated lesions during remyelination. J. Neurosci. Res. 50:229–237, 1997. © 1997 Wiley-Liss, Inc.
References
- Armstrong RC, Dorn HH, Kufta CV, Friedman E, Dubois-Dalcq ME (1992): Pre-oligodendrocytes from adult human CNS. J Neurosci 12: 1538–1547.
- Armstrong RC, Kim JG, Hudson LD (1995): Expression of myelin transcription factor 1 (MyT1), a “zinc-finger” DNA-binding protein, in developing oligodendrocytes. Glia 14: 303–321.
-
Armstrong RC,
Migneault A,
Shegog ML,
Kim JG,
Hudson LD,
Hessler RB
(1997):
High grade human brain tumors exhibit increased expression of myelin transcription factor 1 (Myt1), a zinc finger DNA-binding protein.
J Neuropath Exp Neurol
57:
772–781.
10.1097/00005072-199756070-00003 Google Scholar
- 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. Mol Brain Res 17: 174–178.
- Bansal R, Kumar M, Murray K, Morrison R, Pfeiffer SE (1996a) : Regulation of FGF receptors in the oligodendrocyte lineage. Mol Cell Neurosci 7: 263–275.
- Bansal R, Kumar M, Murray K, Pfeiffer SE (1996b) : Developmental and FGF-2-mediated regulation of syndecans (1–4) and glypican in oligodendrocytes. Mol Cell Neurosci 7: 276–288.
-
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.
10.1002/(SICI)1096-9861(19970310)379:2<226::AID-CNE5>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- Bögler O, Wren D, Barnett SC, Land H, Noble M (1990): Cooperation between two growth factors promotes extended self-renewal, and inhibits differentiation, of O-2A progenitor cells. Proc Natl Acad Sci USA 87: 6368–6372.
- Carrington WA, Fogarty KE, Fay FS (1990): 3D fluorescence imaging of single cells using image restoration. In K Foster (ed): “ Non-Invasive Techniques in Cell Biology.” New York: Wiley-Liss, pp. 53–72.
- Cohen RI, Chandross KJ, Hudson LD (1997): FGF-9 and FGF-2 regulate the expression of fibroblast growth factor receptors and myelin proteins during oligodendrocyte development. J Neurochem 69(supplement): S89B.
- Eckenstein, FP (1994): Fibroblast growth factors in the nervous system. J Neurobiol 25: 1467–1480.
- Ellison JA, deVellis J (1994): Platelet-derived growth factor receptor is expressed by cells in the early oligodendrocyte lineage. J Neurosci Res 37: 116–128.
-
Engel U,
Wolswijk G
(1996):
Oligodendrocyte-type-2 astrocyte progenitor cells derived from adult rat spinal cord: In vitro characteristics and response to PDGF, bFGF, and NT-3.
Glia
16:
16–26.
10.1002/(SICI)1098-1136(199601)16:1<16::AID-GLIA3>3.0.CO;2-9 CAS PubMed Web of Science® Google Scholar
- Fressinaud C, Laeng P, Labourdette G, Durand J, Vallat JM (1993): The proliferation of mature oligodendrocytes in vitro is stimulated by basic fibroblast growth factor and inhibited by oligodendrocyte type 2 astrocyte precursors. Dev Biol 158: 317–329.
-
Gensert JM,
Goldman JE
(1996):
In vivo characterization of endogenous proliferating cells in the adult rat subcortical white matter.
Glia
17:
39–51.
10.1002/(SICI)1098-1136(199605)17:1<39::AID-GLIA4>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- Gogate N, Verma L, Zhou JM, Milward E, Rusten R, O'Conner M, Kufta C, Kim J, Hudson L, Dubois-Dalcq M (1994): Plasticity in the adult human oligodendrocyte lineage. J Neurosci 14: 4571–4587.
- Gomez-Pinila F, Lee JW, Cotman CW (1992): Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J Neurosci 12: 345–355.
- Gonzales AM, Berry M, Maher PA, Logan A, Baird A (1995): A comprehensive analysis of the distribution of FGF-2 and FGFR1 in the rat brain. Brain Res 701: 201–226.
-
Grinspan JB,
Reeves MF,
Coulaloglou MJ,
Nathanson D,
Pleasure D
(1996):
Re-entry into the cell cycle is required for bFGF-induced oligodendroglial dedifferentiation and survival.
J Neurosci Res
46:
456–464.
10.1002/(SICI)1097-4547(19961115)46:4<456::AID-JNR7>3.0.CO;2-F CAS PubMed Web of Science® Google Scholar
- Hart IK, Richardson WD, Heldin C-H, Westermark B, Raff MC (1989): PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O2-A) lineage. Development 105: 595–603.
- Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin CH, Westermark, Nister M (1992): Platelet-derived growth factor and its receptors in human glioma tissue: Expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52: 3213–3219.
- Levine JM, Stincone F, Lee Y-S (1993): Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7: 307–321.
- Logan A (1990): The role of fibroblast growth factors in the central nervous system. TEM Jan/Feb: 149–154.
- Ludwin SK (1997): The pathobiology of the oligodendrocyte. J Neuropath Exp Neurol 56: 111–124.
- McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA (1990): FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5: 603–614.
- Mocchetti I, Rabin SJ, Colangelo AM, Whittemore SR, Wrathall JR (1996): Increased basic fibroblast growth factor expression following contusive spinal cord injury. Exp Neurol 141: 154–164.
-
Nishiyama A,
Lin X-H,
Giese N,
Heldin C-H,
Stallcup WB
(1996):
Co-localization of NG2 proteoglycan and PDGF a-receptor on O2A progenitor cells in the developing rat brain.
J Neurosci Res
43:
299–314.
10.1002/(SICI)1097-4547(19960201)43:3<299::AID-JNR5>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
-
Nishiyama A,
Yu M,
Drazba JA,
Tuohy VK
(1997):
Normal and reactive NG2+ glial cells are distinct from resting and activated microglia.
J Neurosci Res
48:
299–312.
10.1002/(SICI)1097-4547(19970515)48:4<299::AID-JNR2>3.0.CO;2-6 CAS PubMed Web of Science® Google Scholar
-
Oh LYS,
Yong VW
(1996):
Astrocytes promote process outgrowth by adult human oligodendrocytes in vitro through interaction between bFGF and astrocyte extracellular matrix.
Glia
17:
237–253.
10.1002/(SICI)1098-1136(199607)17:3<237::AID-GLIA6>3.0.CO;2-Y CAS PubMed Web of Science® Google Scholar
- Ohno M, Komiyama A, Martin PM, Suzuki K (1993): Proliferation of microglia/macrophages in the demyelinating CNS and PNS of twitcher mouse. Brain Res 602: 268–274.
- Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho E-S (1993): Multiple sclerosis: Remyelination of nascent lesions. Ann Neurol 33: 137–151.
- Pringle N, Mudhar HS, Collarini EJ, Richardson WD (1992): PDGF receptors in the rat CNS: During late neurogenesis, PDGF alpha receptor appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115: 535–551.
- Raible DW, McMorris FA (1989): Cyclic AMP regulates the rate of differentiation of oligodendrocyte without changing the lineage commitment of their progenitors. Dev Biol 133: 437–446.
- Raine CS (1990): Demyelinating diseases. In RL Davis, DM Robertson (eds): “ Textbook of Neuropathology.” Baltimore, MD: Williams and Wilkins, pp. 535–620.
- Raine CS, Wu E (1993): Multiple sclerosis: Remyelination in acute lesions. J Neuropath Exp Neurol 52: 199–204.
- Reiser G, Kunzelmann U, Steinhilber G, Binmoller F-J (1994): Generation of a monoclonal antibody against the myelin protein CNP (2′,3′-cyclic nucleotide 3′-phosphodiesterase) suitable for biochemical and for immunohistochemical investigations of CNP. Neurochem Res 19: 1479–1485.
-
Reynolds R,
Hardy R
(1997):
Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo.
J Neurosci Res
47:
455–470.
10.1002/(SICI)1097-4547(19970301)47:5<455::AID-JNR1>3.0.CO;2-G CAS PubMed Web of Science® Google Scholar
- Venkateswaran S, Blanckaert V, Schelling M (1992): Production of anti-fibroblast growth factor receptor monoclonal antibodies by in vitro immunization. Hybridoma 11: 729–739.
- Vick RS, DeVries GH (1992): Mitotic potential of adult rat oligodendrocytes in culture. J Neurosci Res 33: 68–74.
- Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D (1996): Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 19: 387–393.
- Wolswijk G, Noble M (1995): In vitro studies of the development, maintenance and regeneration of the oligodendrocyte-type-2 astrocyte (O-2A) lineage in the adult central nervous system. In H Kettenmann, BR Ransom (eds): “ Neuroglia.” New York: Oxford University Press, pp. 149–161.
- Wood PM, Bunge RP (1991): The origin of remyelinating cells in the adult central nervous system: the role of the mature oligodendrocyte. Glia 4: 225–232.
- Wood PM, Mora J (1993): Source of remyelinating oligodendrocytes. Adv Neurol 59: 113–123.
- Yazaki N, Hosoi Y, Kawabata K, Miyake A, Minami M, Satoh M, Ohta M, Kawasaki T, Itoh N (1994): Differential expression patterns of mRNAs for members of the fibroblast growth factor receptor family, FGFR-1-FGFR-4, in rat brain. J Neurosci Res 37: 445–452.
- Yeh H-J, Ruit KG, Wang Y-X, Parks WC, Snider WD, Deuel TF (1991): PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell 64: 209–216.
