PDGFRα-Positive B Cells Are Neural Stem Cells in the Adult SVZ that Form Glioma-like Growths in Response to Increased PDGF Signaling

Neuron

Volumn 51, Issue 2, 2006, Pages 187-199

  Jackson, Erica L ^a   Garcia Verdugo, Jose Manuel ^c   Gil Perotin, Sara ^c   Roy, Monica ^a   Quinones Hinojosa, Alfredo ^a   VandenBerg, Scott ^b   Alvarez Buylla, Arturo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

DEVBIO; MOLNEURO; STEMCELL

Indexed keywords

PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR;

ADULT; AGED; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL GROWTH; CELL PROLIFERATION; GLIOMA; HUMAN; HUMAN CELL; HYPERPLASIA; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ADOLESCENT; AGED, 80 AND OVER; ANIMALS; CELL PROLIFERATION; GLIOMA; HUMANS; LATERAL VENTRICLES; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEURONS; PLATELET-DERIVED GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 33745880884     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.06.012     Document Type: Article

References (70)

1. Andrae J., Hansson I., Afink G.B., and Nister M. Platelet-derived growth factor receptor-alpha in ventricular zone cells and in developing neurons. Mol. Cell. Neurosci. 17 (2001) 1001-1013
2. Barres B.A., Hart I.K., Coles H.S.R., Burne J.F., Voyvodic J.T., Richardson W.D., and Raff M.C. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70 (1992) 31-46
3. Bickenbach J.R. Identification and behavior of label-retaining cells in oral mucosa and skin. J. Dent. Res. 60 (1981) 1611-1620
4. Bonfanti L., and Theodosis D.T. Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62 (1994) 291-305
5. Buick R.N., Minden M.D., and McCulloch E.A. Self-renewal in culture of proliferative blast progenitor cells in acute myeloblastic leukemia. Blood 54 (1979) 95-104
6. Calver A.R., Hall A.C., Yu W.-P., Walsh F.S., Heath J.K., Betsholtz C., and Richardson W.D. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20 (1998) 869-882
7. Chatterjee G., Rosner A., Han Y., Zelazny E.T., Li B., Cardiff R.D., and Perkins A.S. Acceleration of mouse mammary tumor virus-induced murine mammary tumorigenesis by a p53 172H transgene: influence of FVB background on tumor latency and identification of novel sites of proviral insertion. Am. J. Pathol. 161 (2002) 2241-2253
8. Chojnacki A., and Weiss S. Isolation of a novel platelet-derived growth factor-responsive precursor from the embryonic ventral forebrain. J. Neurosci. 24 (2004) 10888-10899
9. Dai C., Celestino J.C., Okada Y., Louis D.N., Fuller G.N., and Holland E.C. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 15 (2001) 1913-1925
10. Di Pasquale G., Davidson B.L., Stein C.S., Martins I., Scudiero D., Monks A., and Chiorini J.A. Identification of PDGFR as a receptor for AAV-5 transduction. Nat. Med. 9 (2003) 1306-1312
11. Doetsch F., Caille I., Lim D.A., García-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 (1999) 1-20
12. Doetsch F., Garcia-Verdugo J.M., and Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96 (1999) 11619-11624
13. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., and Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36 (2002) 1021-1034
14. Ellison J.A., and De Vellis J. Platelet-derived growth factor receptor is expressed by cells in the early oligodendrocyte lineage. J. Neurosci. Res. 37 (1994) 116-128
15. Erlandsson A., Enarsson M., and Forsberg-Nilsson K. Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J. Neurosci. 21 (2001) 3483-3491
16. Ffrench-Constant C., Miller R.H., Kruse J., Schachner M., and Raff M.C. Molecular specialization of astrocyte processes at nodes of ranvier in rat optic nerve. J. Cell Biol. 102 (1986) 844-852
17. Fruttiger M., Karlsson L., Hall A.C., Abramsson A., Calver A.R., Bostrom H., Willetts K., Bertold C.H., Heath J.K., Betsholtz C., and Richardson W.D. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126 (1999) 457-467
18. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64 (2004) 7011-7021
19. Garcia A.D., Doan N.B., Imura T., Bush T.G., and Sofroniew M.V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7 (2004) 1233-1241
20. Globus J.H., and Kuhlenbeck H. The Subependymal cell plate (matrix) and its relationship to brain tumors of the ependymal type. J. Neuropathol. Exp. Neurol. 3 (1944) 1-35
21. + oligodendrocyte pre-progenitor cells. J. Neurosci. Res. 41 (1995) 540-551
22. Guha A., Dashner K., Black P.M., Wagner J.A., and Stiles C.D. Expression of PDGF and PDGF receptors in human astrocytoma operation specimens supports the existence of an autocrine loop. Int. J. Cancer 60 (1995) 168-173
23. Hack M.A., Saghatelyan A., de Chevigny A., Pfeifer A., Ashery-Padan R., Lledo P.M., and Gotz M. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8 (2005) 865-872
24. Hall A., Giese N.A., and Richardson W.D. Spinal cord oligodendrocytes develop from ventrally derived progenitor cells that express PDGF alpha-receptors. Development 122 (1996) 4085-4094
25. Hart I.K., Richardson W.D., Bolsover S.R., and Raff M.C. PDGF and intracellular signaling in the timing of oligodendrocyte differentiation. J. Cell Biol. 109 (1989) 3411-3417
26. He W., Ingraham C., Rising L., Goderie S., and Temple S. Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J. Neurosci. 21 (2001) 8854-8862
27. Hemmati H.D., Nakano I., Lazareff J.A., Masterman-Smith M., Geschwind D.H., Bronner-Fraser M., and Kornblum H.I. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. USA 100 (2003) 15178-15183
28. Holland E.C., and Varmus H.E. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc. Natl. Acad. Sci. USA 95 (1998) 1218-1223
29. Holland E.C., Hively W.P., DePinho R., and Varmus H.E. Constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 12 (1998) 3675-3685
30. Ignatova T.N., Kukekov V.G., Laywell E.D., Suslov O.N., Vrionis F.D., and Steindler D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39 (2002) 193-206
31. Johe K.K., Hazel T.G., Muller T., Dugich-Djordjevic M.M., and McKay R.D.G. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10 (1996) 3129-3140
32. Klinghoffer R.A., Hamilton T.G., Hoch R., and Soriano P. An allelic series at the PDGFαR locus indicates unequal contributions of distinct signaling pathways during development. Dev. Cell 2 (2002) 103-113
33. Kondo T., and Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289 (2000) 1754-1757
34. Lachapelle F., Avellana-Adalid V., Nait-Oumesmar B., and Baron-Van Evercooren A. Fibroblast growth factor-2 (FGF-2) and platelet-derived growth factor AB (PDGF AB) promote adult SVZ-derived oligodendrogenesis in vivo. Mol. Cell. Neurosci. 20 (2002) 390-403
35. Lendahl U., Zimmerman L.B., and McKay R.D.G. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
36. Ligon K.L., Alberta J.A., Kho A.T., Weiss J., Kwaan M.R., Nutt C.L., Louis D.N., Stiles C.D., and Rowitch D.H. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J. Neuropathol. Exp. Neurol. 63 (2004) 499-509
37. Lim D.A., and Alvarez-Buylla A. Glial Characteristics of Adult Subventricular Zone Stem Cells. In: Rao M.S. (Ed). Stem Cells in CNS Development (2001), Humana Press, Towton, NJ 71-92
38. Lois C., and Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 264 (1994) 1145-1148
39. Lotery A.J., Yang G.S., Mullins R.F., Russell S.R., Schmidt M., Stone E.M., Lindbloom J.D., Chiorini J.A., Kotin R.M., and Davidson B.L. Adeno-associated virus type 5: transduction efficiency and cell-type specificity in the primate retina. Hum. Gene Ther. 14 (2003) 1663-1671
40. Lu Q.R., Park J.K., Noll E., Chan J.A., Alberta J., Yuk D., Alzamora M.G., Louis D.N., Stiles C.D., Rowitch D.H., and Black P.M. Oligodendrocyte lineage genes (OLIG) as molecular markers for human glial brain tumors. Proc. Natl. Acad. Sci. USA 98 (2001) 10851-10856
41. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., and Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109 (2002) 75-86
42. Luskin M.B., and Boone M.S. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses 19 (1994) 695-714
43. Marshall C.A., Novitch B.G., and Goldman J.E. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neurosci. 25 (2005) 7289-7298
44. McCarthy G.F., and Leblond C.P. Radioautographic evidence for slow astrocyte turnover and modest oligodendrocyte production in the corpus callosum of adult mice infused with 3H-thymidine. J. Comp. Neurol. 271 (1988) 589-603
45. Menn B., Garcia-Verdugo J.M., Yaschine C., Gonzalez-Perez D., Rowitch D., and Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. (2006) in press
46. Merkle F.T., Tramontin A.D., Garcia-Verdugo J.M., and Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. USA 101 (2004) 17528-17532
47. Morris R.J., and Potten C.S. Slowly cycling (label-retaining) epidermal cells behave like clonogenic stem cells in vitro. Cell Prolif. 27 (1994) 279-289
48. Morshead C.M., Garcia A.D., Sofroniew M.V., and van Der Kooy D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur. J. Neurosci. 18 (2003) 76-84
49. Nait-Oumesmar B., Decker L., Lachapelle F., Avellana-Adalid V., Bachelin C., and Van Evercooren A.B. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11 (1999) 4357-4366
50. Novak A., Guo C., Yang W., Nagy A., and Lobe C.G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28 (2000) 147-155
51. Parras C.M., Galli R., Britz O., Soares S., Galichet C., Battiste J., Johnson J.E., Nakafuku M., Vescovi A., and Guillemot F. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23 (2004) 4495-4505
52. Quinones-Hinojosa A., Sanai N., Soriano-Navarro M., Gonzalez-Perez O., Mirzadeh Z., Gil-Perotin S., Romero-Rodriguez R., Berger M.S., Garcia-Verdugo J.M., and Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 494 (2006) 415-434
53. Raff M.C., Miller R.H., and Noble M. A glial progenitor that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303 (1983) 390-396
54. Recht L., Jang T., Savarese T., and Litofsky N.S. Neural stem cells and neuro-oncology: quo vadis?. J. Cell. Biochem. 88 (2003) 11-19
55. Redwine J.M., Blinder K.L., and Armstrong R.C. In situ expression of fibroblast growth factor receptors by oligodendrocyte progenitors and oligodendrocytes in adult mouse central nervous system. J. Neurosci. Res. 50 (1997) 229-237
56. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia Verdugo J., et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004) 740-744
57. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., and Dirks P.B. Identification of human brain tumour initiating cells. Nature 432 (2004) 396-401
58. Smits A., Kato M., Westermark B., Nistér M., Heldin C.-H., and Funa K. Neurotrophic activity of platelet-derived growth factor (PDGF): Rat neuronal cells possess functional PDGF β-type receptors and respond to PDGF. Proc. Natl. Acad. Sci. USA 88 (1991) 8159-8163
59. Sonoda Y., Ozawa T., Hirose Y., Aldape K.D., McMahon M., Berger M.S., and Pieper R.O. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res. 61 (2001) 4956-4960
60. Takebayashi H., Nabeshima Y., Yoshida S., Chisaka O., and Ikenaka K. The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr. Biol. 12 (2002) 1157-1163
61. Tohyama T., Lee V.M.-Y., Rorke L.B., Marvin M., McKay R.D.G., and Trojanowski J.Q. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest. 66 (1992) 303-313
62. Tuveson D.A., Shaw A.T., Willis N.A., Silver D.P., Jackson E.L., Chang S., Mercer K.L., Grochow R., Hock H., Crowley D., et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5 (2004) 375-387
63. Uhrbom L., Hesselager G., Nister M., and Westermark B. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res. 58 (1998) 5275-5279
64. Varela M., Ranuncolo S.M., Morand A., Lastiri J., De Kier Joffe E.B., Puricelli L.I., and Pallotta M.G. EGF-R and PDGF-R, but not bcl-2, overexpression predict overall survival in patients with low-grade astrocytomas. J. Surg. Oncol. 86 (2004) 34-40
65. Wang J., Jani-Sait S.N., Escalon E.A., Carroll A.J., de Jong P.J., Kirsch I.R., and Aplan P.D. The t(14;21)(q11.2;q22) chromosomal translocation associated with T-cell acute lymphoblastic leukemia activates the BHLHB1 gene. Proc. Natl. Acad. Sci. USA 97 (2000) 3497-3502
66. Williams B.P., Park J.K., Alberta J.A., Muhlebach S.G., Hwang G.Y., Roberts T.M., and Stiles C.D. A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18 (1997) 553-562
67. Wolswijk G., and Noble M. Identification of an adult-specific glial progenitor cell. Development 105 (1989) 387-400
68. Woodruff R.H., Fruttiger M., Richardson W.D., and Franklin R.J. Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol. Cell. Neurosci. 25 (2004) 252-262
69. Zhou Q., and Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109 (2002) 61-73
70. Zhu Y., Guignard F., Zhao D., Liu L., Burns D.K., Mason R.P., Messing A., and Parada L.F. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8 (2005) 119-130