Akt1 interacts with epidermal growth factor receptors and hedgehog signaling to increase stem/transit amplifying cells in the embryonic mouse cortex

Developmental Neurobiology

Volumn 71, Issue 9, 2011, Pages 759-771

  Sinor Anderson, Amy ^a   Lillien, Laura ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Thermo Fisher Scientific   (United States)

Author keywords

Akt1; Cerebral cortex; EGF receptor; Hedgehog; Stem cell

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN; PROTEIN AKT1; PROTEIN PRECURSOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SURVIVAL; WILD TYPE;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; ENZYME INDUCTION; HEDGEHOG PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL STEM CELLS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 79961193877     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20878     Document Type: Article

References (67)

1. Alvarez-Buylla A, Lim DA. 2004. For the long run: Maintaining germinal niches in the adult brain. Neuron 41: 683-686.
2. Assimacopoulos S, Grove EA, Ragsdale CW. 2003. Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci 23: 6399-6403.
3. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140.
4. Brazil DP, Hemmings BA. 2001. Ten years of protein kinase B signalling: A hard Akt to follow. Trends Biochem Sci 26: 657-664.
5. Brewster R, Mullor JL, Ruiz i Altaba A. 2000. Gli2 functions in FGF signaling during antero-posterior patterning. Development 127: 4395-4405.
6. 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.
7. Caric D, Raphael H, Viti J, Feathers A, Wancio D, Lillien L. 2001. EGFRs mediate chemotactic migration in the developing telencephalon. Development 128: 4203-4216.
8. Chan JA, Balasubramanian S, Witt RM, Nazemi KJ, Choi Y, Pazyra-Murphy MF, Walsh CO, et al. 2009. Proteoglycan interactions with Sonic Hedgehog specify mitogenic responses. Nat Neurosci 12: 409-417.
9. Ciccolini F, Svendsen CN. 1998. Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: Identification of neural precursors responding to both EGF and FGF-2. J Neurosci 18: 7869-7880.
10. Danesin C, Agius E, Escalas N, Ai X, Emerson C, Cochard P, Soula C. 2006. Ventral neural progenitors switch toward an oligodendroglial fate in response to increased Sonic hedgehog (Shh) activity: involvement of Sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J Neurosci 26: 5037-5048.
11. Dihlmann S, Kloor M, Fallsehr C, von Knebel Doeberitz M. 2005. Regulation of AKT1 expression by beta-catenin/Tcf/Lef signaling in colorectal cancer cells. Carcinogenesis 26: 1503-1512.
12. Doetsch F. 2003. A niche for adult neural stem cells. Curr Opin Genet Dev 13: 543-550.
13. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. 2002. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36: 1021-1034.
14. Eagleson KL, Ferri RT, Levitt P. 1996. Complementary distribution of collagen type IV and the epidermal growth factor receptor in the rat embryonic telencephalon. Cereb Cortex 6: 540-549.
15. Eswarakumar VP, Lax I, Schlessinger J. 2005. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149.
16. Franke TF, Kaplan DR, Cantley LC. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88: 435-437.
17. Freeman M, Gurdon JB. 2002. Regulatory principles of developmental signaling. Annu Rev Cell Dev Biol 18: 515-539.
18. Gabay L, Lowell S, Rubin LL, Anderson DJ. 2003. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40: 485-499.
19. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. 2002. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22: 6309-6314.
20. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-7265.
21. Groszer M, Erickson R, Scripture-Adams DD, Dougherty JD, Le Belle J, Zack JA, Geschwind DH, et al. 2006. PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc Natl Acad Sci USA 103: 111-116.
22. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, et al. 2001. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294: 2186-2189.
23. Hahn H, Wojnowski L, Specht K, Kappler R, Calzada-Wack J, Potter D, Zimmer A, et al. 2000. Patched target Igf2 is indispensable for the formation of medulloblastoma and rhabdomyosarcoma. J Biol Chem 275: 28341-28344.
24. Hu Q, Zhang L, Wen J, Wang S, Li M, Feng R, Yang X, Li L. 2010. The EGF receptor-sox2-EGF receptor feedback loop positively regulates the self-renewal of neural precursor cells. Stem Cells 28: 279-286.
25. Huang X, Liu J, Ketova T, Fleming JT, Grover VK, Cooper MK, Litingtung Y, et al. 2010. Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc Natl Acad Sci USA 107: 8422-8427.
26. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev 15: 3059-3087.
27. Johansson PA, Cappello S, Götz M. 2010. Stem cells niches during development-lessons from the cerebral cortex. Curr Opin Neurobiol 20: 400-407.
28. Kanda S, Mochizuki Y, Suematsu T, Miyata Y, Nomata K, Kanetake H. 2003. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J Biol Chem 278: 8244-8249.
29. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S, Blaas L, Schmid C, et al. 2006. Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol Cell Biol 26: 6283-6298.
30. Kessaris N, Jamen F, Rubin LL, Richardson WD. 2004. Cooperation between sonic hedgehog and fibroblast growth factor/MAPK signalling pathways in neocortical precursors. Development 131: 1289-1298.
31. Komada M, Saitsu H, Kinboshi M, Miura T, Shiota K, Ishibashi M. 2008. Hedgehog signaling is involved in development of the neocortex. Development 135: 2717-2727.
32. Kornblum HI, Hussain RJ, Bronstein JM, Gall CM, Lee DC, Seroogy KB. 1997. Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain. J Comp Neurol 380: 243-261.
33. Lillien L, Gulacsi A. 2006. Environmental signals elicit multiple responses in dorsal telencephalic progenitors by threshold-dependent mechanisms. Cereb Cortex. Suppl 1: i74-i81.
34. Lillien L, Raphael H. 2000. BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 127: 4993-5005.
35. Long F, Zhang XM, Karp S, Yang Y, McMahon AP. 2001. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128: 5099-5108.
36. Mairet-Coello G, Tury A, DiCicco-Bloom E. 2009. Insulin-like growth factor-1 promotes G(1)/S cell cycle progression through bidirectional regulation of cyclins and cyclin-dependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. J Neurosci 29: 775-788.
37. Meng F, D'Mello SR. 2003. NF-kappaB stimulates Akt phosphorylation and gene expression by distinct signaling mechanisms. Biochim Biophys Acta 1630: 35-40.
38. Miller FD, Gauthier-Fisher A. 2009. Home at last: Neural stem cell niches defined. Cell Stem Cell 4: 507-510.
39. Morrison SJ, Spradling AC. 2008. Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life. Cell 132: 598-611.
40. Okano J, Gaslightwala I, Birnbaum MJ, Rustgi AK, Nakagawa H. 2000. Akt/protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J Biol Chem 275: 30934-30942.
41. Palma V, Ruiz i Altaba A. 2004. Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131: 337-345.
42. Pastrana E, Cheng LC, Doetsch F. 2009. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA 106: 6387-6392.
43. Peltier J, O'Neill A, Schaffer DV. 2007. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol 67: 1348-1361.
44. Qian X, Davis AA, Goderie SK, Temple S. 1997. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18: 81-93.
45. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
46. Reynolds BA, Tetzlaff W, Weiss S. 1992. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12: 4565-4574.
47. Riobó NA, Lu K, Ai X, Haines GM, Emerson CPJr. 2006a. Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc Natl Acad Sci USA 103: 4505-4510.
48. Riobo NA, Lu K, Emerson CPJr. 2006b. Hedgehog signal transduction: Signal integration and cross talk in development and cancer. Cell Cycle 15: 1612-1615.
49. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM. 1995. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81: 445-455.
50. Ruiz i Altaba A, Nguyên V, Palma V. 2003. The emergent design of the neural tube: Prepattern. SHH morphogen and GLI code. Curr Opin Genet Dev 13: 513-521.
51. Sinor AD, Lillien L. 2004. Akt-1 expression level regulates CNS precursors. J Neurosci 24: 8531-8541.
52. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, et al. 1998. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95: 29-39.
53. Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V, Beermann F, et al. 2007. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci USA 104: 5895-5900.
54. Sun Y, Goderie SK, Temple S. 2005. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45: 873-886.
55. Takanaga H, Tsuchida-Straeten N, Nishide K, Watanabe A, Aburatani H, Kondo T. 2009. Gli2 is a novel regulator of sox2 expression in telencephalic neuroepithelial cells. Stem Cells 27: 165-174.
56. Temple S. 2001. The development of neural stem cells. Nature 414: 112-117.
57. Theiler K. 1972. The House Mouse. New York: Springer-Verlag.
58. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, et al. 1995. Targeted disruption of mouse EGF receptor: Effect of genetic background on mutant phenotype. Science 269: 230- 234.
59. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D. 1999. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208: 166-188.
60. Vanhaesebroeck B, Alessi DR. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 346: 561-576.
61. Viti J, Gulacsi A, Lillien L. 2003. Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J Neurosci 23: 5919-5927.
62. Watt FM, Hogan BL. 2000. Out of Eden: Stem cells and their niches. Science 287: 1427-1430.
63. Xie J, Aszterbaum M, Zhang X, Bonifas JM, Zachary C, Epstein E, McCormick F. 2001. A role of PDGFRalpha in basal cell carcinoma proliferation. Proc Natl Acad Sci USA 98: 9255-9259.
64. Xu Q, Guo L, Moore H, Waclaw RR, Campbell K, Anderson SA. 2010. Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 65: 328-340.
65. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, Ahn CP, Marshall D, et al. 2008. A paracrine requirement for hedgehog signalling in cancer. Nature 455: 406-410.
66. Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, Pisarek AJ, Stocker AM, et al. 2010. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev Cell 18: 472-479.
67. Zhang XM, Ramalho-Santos M, McMahon AP. 2001. Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R asymmetry by the mouse node. Cell 105: 781-792.