BMP Signaling in astrocytes downregulates EGFR to modulate survival and maturation

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Scholze, Anja R ^a   Foo, Lynette C ^b   Mulinyawe, Sara ^a   Barres, Ben A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 5; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN S100B; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SOMATOMEDIN B; WNT7A PROTEIN; EGFR PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; IMMUNOBLOTTING; IMMUNOREACTIVITY; IN VITRO STUDY; NONHUMAN; OLIGODENDROGLIA; PROSPECTIVE STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PURIFICATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; ASTROCYTES; BONE MORPHOGENETIC PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; PHOSPHORYLATION; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84908147797     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110668     Document Type: Article

References (57)

1. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26: 523-530. doi:10.1016/j.tins.2003.08.008.
2. Zhang Y, Barres BA (2010) Astrocyte heterogeneity: An underappreciated topic in neurobiology. Curr Opin Neurobiol 20: 588-594. doi:10.1016/j.conb.2010.06.005.
3. Skoff RP, Knapp PE (1991) Division of astroblasts and oligodendroblasts in postnatal rodent brain: evidence for separate astrocyte and oligodendrocyte lineages. Glia 4: 165-174. doi:10.1002/glia.440040208.
4. Levison SW, Goldman JE (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10: 201-212. doi:10.1016/0896-6273(93)90311-E.
5. Ge W-P, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484: 376-380. doi:10.1038/nature10959.
6. Freeman MR (2010) Specification and morphogenesis of astrocytes. Science 330: 774-778. doi:10.1126/science.1190928.
7. Sloan SA, Barres BA (2014) Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr Opin Neurobiol 27: 75-81. doi:10.1016/j.conb.2014.03.005.
8. Krueger BK, Burne JF, Raff MC (1995) Evidence for large-scale astrocyte death in the developing cerebellum. J Neurosci 15: 3366-3374.
9. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, et al. (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70: 31-46.
10. Foo LC, Allen NJ, Bushong E a, Ventura PB, Chung W-S, et al. (2011) Development of a method for the purification and culture of rodent astrocytes. Neuron 71: 799-811. doi:10.1016/j.neuron.2011.07.022.
11. Bandeira F, Lent R, Herculano-Houzel S (2009) Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci U S A 106: 14108-14113. doi:10.1073/pnas.0804650106.
12. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264-278. doi:10.1523/JNEUROSCI.4178-07.2008.
13. Daneman R, Zhou L, Agalliu D, Cahoy JD, Kaushal A, et al. (2010) The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells. PLoS One 5: e13741. doi:10.1371/journal.pone.0013741.
14. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, et al. (2014) An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex. J Neurosci 34: 11929-11947. doi:10.1523/JNEUROSCI.1860-14.2014.
15. Laestander C, Engström W (2014) Role of fibroblast growth factors in elicitation of cell responses. Cell Prolif 47: 3-11. doi:10.1111/cpr.12084.
16. Mueller TD, Nickel J (2012) Promiscuity and specificity in BMP receptor activation. FEBS Lett 586: 1846-1859. doi:10.1016/j.febslet.2012.02.043.
17. See J, Mamontov P, Ahn K, Wine-Lee L, Crenshaw EB, et al. (2007) BMP signaling mutant mice exhibit glial cell maturation defects. Mol Cell Neurosci 35: 171-182. doi:10.1016/j.mcn.2007.02.012.
18. D'Alessandro JS, Wang EA (1994) Bone morphogenetic proteins inhibit proliferation, induce reversible differentiation and prevent cell death in astrocyte lineage cells. Growth Factors 11: 45-52.
19. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, et al. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17: 595-606.
20. Kohyama J, Sanosaka T, Tokunaga A, Takatsuka E, Tsujimura K, et al. (2010) BMP-induced REST regulates the establishment and maintenance of astrocytic identity. J Cell Biol 189: 159-170. doi:10.1083/jcb.200908048.
21. Marshall CAG, Suzuki SO, Goldman JE (2003) Gliogenic and neurogenic progenitors of the subventricular zone: who are they, where did they come from, and where are they going? Glia 43: 52-61. doi:10.1002/glia.10213.
22. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
23. Walz W, Lang MK (1998) Immunocytochemical evidence for a distinct GFAP-negative subpopulation of astrocytes in the adult rat hippocampus. Neurosci Lett 257: 127-130.
24. Sofroniew M V, Vinters H V (2010) Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35. doi:10.1007/s00401-009-0619-8.
25. D'Alessandro JS, Yetz-Aldape J, Wang EA (1994) Bone morphogenetic proteins induce differentiation in astrocyte lineage cells. Growth Factors 11: 53-69. doi:10.3109/08977199409015051.
26. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, et al. (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132: 5503-5514. doi:10.1242/dev.02166.
27. Gao W-L, Tian F, Zhang S-Q, Zhang H, Yin Z-S (2014) Epidermal growth factor increases the expression of Nestin in rat reactive astrocytes through the Ras-Raf-ERK pathway. Neurosci Lett 562: 54-59. doi:10.1016/j.neu-let.2014.01.018.
28. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, et al. (2006) Role of Sox2 in the development of the mouse neocortex. Dev Biol 295: 52-66. doi:10.1016/j.ydbio.2006.03.007.
29. Komitova M, Eriksson PS (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369: 24-27. doi:10.1016/j.neulet.2004.07.035.
30. Martynoga B, Mateo JL, Zhou B, Andersen J, Achimastou A, et al. (2013) Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 27: 1769-1786. doi:10.1101/gad.216804.113.
31. Sun Y, Hu J, Zhou L, Pollard SM, Smith A (2011) Interplay between FGF2 and BMP controls the self-renewal, dormancy and differentiation of rat neural stem cells. J Cell Sci 124: 1867-1877. doi:10.1242/jcs.085506.
32. Sibilia M, Steinbach JP, Stingl L, Aguzzi A, Wagner EF (1998) A strain-independent postnatal neurodegeneration in mice lacking the EGF receptor. EMBO J 17: 719-731. doi:10.1093/emboj/17.3.719.
33. Kornblum HI, Hussain R, Wiesen J, Miettinen P, Zurcher SD, et al. (1998) Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res 53: 697-717.
34. Viti J, Feathers A, Phillips J, Lillien L (2003) Epidermal growth factor receptors control competence to interpret leukemia inhibitory factor as an astrocyte inducer in developing cortex. J Neurosci 23: 3385-3393.
35. Olayioye MA, Neve RM, Lane HA, Hynes NE (2000) The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J 19: 3159-3167. doi:10.1093/emboj/19.13.3159.
36. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, et al. (2008) Application of a Translational Profiling Approach for the Comparative Analysis of CNS Cell Types. Cell 135: 749-762. doi:10.1016/j.cell.2008.10.029.
37. Mabie PC, Mehler MF, Kessler JA (1999) Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19: 7077-7088.
38. Gomes WA, Mehler MF, Kessler JA (2003) Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255: 164-177.
39. Shimizu T, Kayamori T, Murayama C, Miyamoto A (2012) Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptosis via different pathways: BMP-4 via PI3K/PDK-1/Akt and BMP-7 via PI3K/PDK-1/PKC. Biochem Biophys Res Commun 417: 869-873. doi:10.1016/j.bbrc.2011.12.064.
40. Liu Z, Shen J, Pu K, Katus HA, Plöger F, et al. (2009) GDF5 and BMP2 inhibit apoptosis via activation of BMPR2 and subsequent stabilization of XIAP. Biochim Biophys Acta 1793: 1819-1827. doi:10.1016/j.bbamcr.2009.09.012.
41. Derynck R, Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584. doi:10.1038/nature02006.
42. Greenblatt MB, Shim J-H, Glimcher LH (2010) TAK1 mediates BMP signaling in cartilage. Ann N Y Acad Sci 1192: 385-390. doi:10.1111/j.1749-6632.2009.05222.x.
43. Lee-Hoeflich ST, Causing CG, Podkowa M, Zhao X, Wrana JL, et al. (2004) Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J 23: 4792-4801. doi:10.1038/sj.emboj.7600418.
44. Hegarty S V, O'Keeffe GW, Sullivan AM (2013) BMP-Smad 1/5/8 signalling in the development of the nervous system. Prog Neurobiol 109: 28-41. doi:10.1016/j.pneurobio.2013.07.002.
45. Haas RJ, Werner J, Fliedner TM (1970) Cytokinetics of neonatal brain cell development in rats as studied by the "complete 3H-thymidine labelling" method. J Anat 107: 421-437.
46. Sofroniew M V (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647. doi:10.1016/j.tins.2009.08.002.
47. Oberheim NA, Goldman SA, Nedergaard M (2012) Heterogeneity of astrocytic form and function. Methods Mol Biol 814: 23-45. doi:10.1007/978-1-61779-452-0-3.
48. Chaboub LS (2012) Developmental Origins of Astrocyte Heterogeneity: The Final Frontier of CNS: 379-388. doi:10.1159/000343723.
49. Wang K, Walz W (2003) Unusual topographical pattern of proximal astrogliosis around a cortical devascularizing lesion. J Neurosci Res 73: 497-506. doi:10.1002/jnr.10683.
50. Burrows RC, Wancio D, Levitt P, Lillien L (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19: 251-267.
51. Lillien L, Raphael H (2000) BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 127: 4993-5005.
52. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, et al. (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32: 6391-6410. doi:10.1523/JNEUROSCI.6221-11.2012.
53. Fuller ML, DeChant AK, Rothstein B, Caprariello A, Wang R, et al. (2007) Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions. Ann Neurol 62: 288-300. doi:10.1002/ana.21179.
54. Sahni V, Mukhopadhyay A, Tysseling V, Hebert A, Birch D, et al. (2010) BMPR1a and BMPR1b signaling exert opposing effects on gliosis after spinal cord injury. J Neurosci 30: 1839-1855. doi:10.1523/JNEUROSCI.4459-09.2010.
55. Huang PH, Xu AM, White FM (2009) Oncogenic EGFR signaling networks in glioma. Sci Signal 2: re6. doi:10.1126/scisignal.287re6.
56. Kalman B, Szep E, Garzuly F, Post DE (2013) Epidermal growth factor receptor as a therapeutic target in glioblastoma. Neuromolecular Med 15: 420-434. doi:10.1007/s12017-013-8229-y.
57. Piccirillo SGM, Reynolds BA, Zanetti N, Lamorte G, Binda E, et al. (2006) Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765. doi:10.1038/nature05349.