Characterization of neuroprogenitor cells expressing the PDGF β-receptor within the subventricular zone of postnatal mice

Molecular and Cellular Neuroscience

Volumn 37, Issue 3, 2008, Pages 507-518

  Ishii, Yoko ^a,b   Matsumoto, Yoshiki ^a   Watanabe, Rie ^a   Elmi, Muna ^a   Fujimori, Toshihiko ^c   Nissen, Johan ^d   Cao, Yihai ^d   Nabeshima, Yo Ichi ^c   Sasahara, Masakiyo ^b   Funa, Keiko ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF TOYAMA   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

FGF; Neural stem cells; Neurosphere; PDGF receptor

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CRE RECOMBINASE; DOUBLECORTIN; IMATINIB; KI 67 ANTIGEN; NESTIN; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD VESSEL; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE ACTIVITY; GENE DELETION; IMMUNOFLUORESCENCE TEST; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEURAL STEM CELL; NEUROBLAST; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SUBVENTRICULAR ZONE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; ENZYME INHIBITORS; GENE EXPRESSION; INTERMEDIATE FILAMENT PROTEINS; KI-67 ANTIGEN; LATERAL VENTRICLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; PIPERAZINES; PYRIMIDINES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; STEM CELLS; TRANSFECTION;

MUS;

EID: 39649111521     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.11.006     Document Type: Article

References (48)

1. Betsholtz C. Role of platelet-derived growth factors in mouse development. Int. J. Dev. Biol. 39 (1995) 817-825
2. Cao R., Brakenhielm E., Pawliuk R., Wariaro D., Post M.J., Wahlberg E., Leboulch P., and Cao Y. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat. Med. 9 (2003) 604-613
3. 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
4. Doetsch F., Garcia-Verdugo J.M., and Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17 (1997) 5046-5061
5. 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
6. Dore-Duffy P., Katychev A., Wang X., and Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J. Cereb. Blood Flow Metab. 26 (2006) 613-624
7. Eriksson A., Siegbahn A., Westermark B., Heldin C.H., and Claesson-Welsh L. PDGF alpha- and beta-receptors activate unique and common signal transduction pathways. EMBO J. 11 (1992) 543-550
8. 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
9. Erlandsson A., Brannvall K., Gustafsdottir S., Westermark B., and Forsberg-Nilsson K. Autocrine/paracrine platelet-derived growth factor regulates proliferation of neural progenitor cells. Cancer Res. 66 (2006) 8042-8048
10. Eves E.M., Xiong W., Bellacosa A., Kennedy S.G., Tsichlis P.N., Rosner M.R., and Hay N. Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell. Biol. 18 (1998) 2143-2152
11. Felling R.J., and Levison S.W. Enhanced neurogenesis following stroke. J. Neurosci. Res. 73 (2003) 277-283
12. Fomchenko E.I., and Holland E.C. Platelet-derived growth factor-mediated gliomagenesis and brain tumor recruitment. Neurosurg. Clin. N. Am. 18 (2007) 39-58 (viii)
13. Forsberg-Nilsson K., Behar T.N., Afrakhte M., Barker J.L., and McKay R.D. Platelet-derived growth factor induces chemotaxis of neuroepithelial stem cells. J. Neurosci. Res. 53 (1998) 521-530
14. Funa K., Yamada N., Brodin G., Pietz K., Ahgren A., Wictorin K., Lindvall O., and Odin P. Enhanced synthesis of platelet-derived growth factor following injury induced by 6-hydroxydopamine in rat brain. Neuroscience 74 (1996) 825-833
15. Gao Z., Sasaoka T., Fujimori T., Oya T., Ishii Y., Sabit H., Kawaguchi M., Kurotaki Y., Naito M., Wada T., Ishizawa S., Kobayashi M., Nabeshima Y., and Sasahara M. Deletion of the PDGFR-beta gene affects key fibroblast functions important for wound healing. J. Biol. Chem. 280 (2005) 9375-9389
16. Goold R.G., and Gordon-Weeks P.R. Glycogen synthase kinase 3beta and the regulation of axon growth. Biochem. Soc. Trans. 32 (2004) 809-811
17. Hamada T., Ui-Tei K., Imaki J., Takahashi F., Onodera H., Mishima T., and Miyata Y. The expression of SCDGF/PDGF-C/fallotein and SCDGF-B/PDGF-D in the rat central nervous system. Mech. Dev. 112 (2002) 161-164
18. Hellstrom M., Kalen M., Lindahl P., Abramsson A., and Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development (Cambridge, England) 126 (1999) 3047-3055
19. Hermanson M., Olsson T., Westermark B., and Funa K. PDGF and its receptors following facial nerve axotomy in rats: expression in neurons and surrounding glia. Exp. Brain Res. 102 (1995) 415-422
20. Hermanson M., Funa K., Koopmann J., Maintz D., Waha A., Westermark B., Heldin C.H., Wiestler O.D., Louis D.N., von Deimling A., and Nister M. Association of loss of heterozygosity on chromosome 17p with high platelet-derived growth factor alpha receptor expression in human malignant gliomas. Cancer Res. 56 (1996) 164-171
21. Ishii Y., Oya T., Zheng L., Gao Z., Kawaguchi M., Sabit H., Matsushima T., Tokunaga A., Ishizawa S., Hori E., Nabeshima Y., Sasaoka T., Fujimori T., Mori H., and Sasahara M. Mouse brains deficient in neuronal PDGF receptor-beta develop normally but are vulnerable to injury. J. Neurochem. 98 (2006) 588-600
22. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., and Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51 (2006) 187-199
23. Kaneko M., Yang W., Matsumoto Y., Watt F., and Funa K. Activity of a novel PDGF beta-receptor enhancer during the cell cycle and upon differentiation of neuroblastoma. Exp. Cell Res. 312 (2006) 2028-2039
24. Kano M.R., Morishita Y., Iwata C., Iwasaka S., Watabe T., Ouchi Y., Miyazono K., and Miyazawa K. VEGF-A and FGF-2 synergistically promote neoangiogenesis through enhancement of endogenous PDGF-B-PDGFRbeta signaling. J. Cell Sci. 118 (2005) 3759-3768
25. Koyama N., Hart C.E., and Clowes A.W. Different functions of the platelet-derived growth factor-alpha and -beta receptors for the migration and proliferation of cultured baboon smooth muscle cells. Circ. Res. 75 (1994) 682-691
26. Laurent M., Martinerie C., Thibout H., Hoffman M.P., Verrecchia F., Le Bouc Y., Mauviel A., and Kleinman H.K. NOVH increases MMP3 expression and cell migration in glioblastoma cells via a PDGFR-alpha-dependent mechanism. FASEB J. 17 (2003) 1919-1921
27. Lobsiger C.S., Schweitzer B., Taylor V., and Suter U. Platelet-derived growth factor-BB supports the survival of cultured rat Schwann cell precursors in synergy with neurotrophin-3. Glia 30 (2000) 290-300
28. Lois C., and Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 2074-2077
29. Lokker N.A., Sullivan C.M., Hollenbach S.J., Israel M.A., and Giese N.A. Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res. 62 (2002) 3729-3735
30. Ma D., Nutt C.L., Shanehsaz P., Peng X., Louis D.N., and Kaetzel D.M. Autocrine platelet-derived growth factor-dependent gene expression in glioblastoma cells is mediated largely by activation of the transcription factor sterol regulatory element binding protein and is associated with altered genotype and patient survival in human brain tumors. Cancer Res. 65 (2005) 5523-5534
31. Magnusson P.U., Looman C., Ahgren A., Wu Y., Claesson-Welsh L., and Heuchel R.L. Platelet-derived growth factor receptor-beta constitutive activity promotes angiogenesis in vivo and in vitro. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 2142-2149
32. Manuelidis L. Genomic stability and instability in different neuroepithelial tumors. A role for chromosome structure?. J. Neuro-Oncol. 18 (1994) 225-239
33. 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. U. S. A. 101 (2004) 17528-17532
34. Ming G., Lohof A.M., and Zheng J.Q. Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic Xenopus spinal neurons. J. Neurosci. 17 (1997) 7860-7871
35. Mokry J., Cizkova D., Filip S., Ehrmann J., Osterreicher J., Kolar Z., and English D. Nestin expression by newly formed human blood vessels. Stem Cells Dev. 13 (2004) 658-664
36. Nissen L.J., Cao R., Hedlund E.M., Wang Z., Zhao X., Wetterskog D., Funa K., Brakenhielm E., and Cao Y. Angiogenic factors FGF2 and PDGF-BB synergistically promote murine tumor neovascularization and metastasis. J. Clin. Invest. 117 (2007) 2766-2777
37. Noble M., Wolswijk G., and Wren D. The complex relationship between cell division and the control of differentiation in oligodendrocyte-type-2 astrocyte progenitor cells isolated from perinatal and adult rat optic nerves. Prog. Growth Factor Res. 1 (1989) 179-194
38. Otaegi G., Yusta-Boyo M.J., Vergano-Vera E., Mendez-Gomez H.R., Carrera A.C., Abad J.L., Gonzalez M., de la Rosa E.J., Vicario-Abejon C., and de Pablo F. Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. J. Cell Sci. 119 (2006) 2739-2748
39. Owen R., and Gordon-Weeks P.R. Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol. Cell. Neurosci. 23 (2003) 626-637
40. Park K.I., Hack M.A., Ourednik J., Yandava B., Flax J.D., Stieg P.E., Gullans S., Jensen F.E., Sidman R.L., Ourednik V., and Snyder E.Y. Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp. Neurol. 199 (2006) 156-178
41. Richards G.R., Smith A.J., Cuddon P., Ma Q.P., Leveridge M., Kerby J., Roderick H.L., Bootman M.D., and Simpson P.B. The JAK3 inhibitor WHI-P154 prevents PDGF-evoked process outgrowth in human neural precursor cells. J. Neurochem. 97 (2006) 201-210
42. Ronnstrand L., and Heldin C.H. Mechanisms of platelet-derived growth factor-induced chemotaxis. Int. J. Cancer 91 (2001) 757-762
43. Sjoborg M., Pietz K., Ahgren A., Yamada N., Lindvall O., Funa K., and Odin P. Expression of platelet-derived growth factor after intrastriatal ibotenic acid injury. Exp. Brain Res. 119 (1998) 245-250
44. Snyder E.Y., and Macklis J.D. Multipotent neural progenitor or stem-like cells may be uniquely suited for therapy for some neurodegenerative conditions. Clin. Neurosci. 3 (1995) 310-316
45. Soriano P. The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124 (1997) 2691-2700
46. Suslov O.N., Kukekov V.G., Ignatova T.N., and Steindler D.A. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 14506-14511
47. Sun P., Watanabe H., Takano K., Yokoyama T., Fujisawa J., and Endo T. Sustained activation of M-Ras induced by nerve growth factor is essential for neuronal differentiation of PC12 cells. Genes Cells 11 (2006) 1097-1113
48. Sun Y., Goderie S.K., and Temple S. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45 (2005) 873-886