Adenomatous polyposis coli is essential for both neuronal differentiation and maintenance of adult neural stem cells in subventricular zone and hippocampus

Stem Cells

Volumn 28, Issue 11, 2010, Pages 2053-2064

  Imura, Tetsuya ^a   Wang, Xiaohong ^a   Noda, Tetsuo ^b   Sofroniew, Michael V ^c   Fushiki, Shinji ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b CANCER INSTITUTE   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Catenin; Glial fibrillary acid protein; Neural stem cells; Neurogenesis; Wnt

Indexed keywords

ADENOMATOUS POLYP COLI; BETA CATENIN; GLIAL FIBRILLARY ACIDIC PROTEIN; TRANSCRIPTION FACTOR MASH1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLFACTORY BULB; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUBVENTRICULAR ZONE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CELL DIFFERENTIATION; CEREBRAL VENTRICLES; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL STEM CELLS; NEURONS; POLYMERASE CHAIN REACTION;

MUS;

EID: 78649844418     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.524     Document Type: Article

References (57)

1. Vescovi AL, Galli R, and Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006;6:425-436.
2. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008;132:645-660.
3. Parent JM. Adult neurogenesis in the intact and epileptic dentate gyrus. Prog Brain Res 2007;163:529-540.
4. Kalani MY, Cheshier SH, Cord BJ et al. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci USA 2008;105:16970-16975.
5. Lie DC, Colamarino SA, Song HJ et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005;437:1370-1375.
6. Wexler EM, Paucer A, Kornblum HI et al. Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells 2009;27:1130-1141.
7. Michaelidis TM, Lie DC. Wnt signaling and neural stem cells: Caught in the Wnt web. Cell Tissue Res 2008;331:193-210.
8. Kinzler KW, Nilbert MC, Su LK et al. Identification of FAP locus genes from chromosome 5q21. Science 1991;253:661-665.
9. Nishisho I, Nakamura Y, Miyoshi Y et al. Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 1991;253:665-669. (Pubitemid 21917200)
10. Aoki K, Taketo MM. Adenomatous polyposis coli (APC): A multifunctional tumor suppressor gene. J Cell Sci 2007;120:3327-3335.
11. Nathke IS. The adenomatous polyposis coli protein: The Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 2004;20:337-366.
12. Rossi A, Caracciolo V, Russo G et al. Medulloblastoma: From molecular pathology to therapy. Clin Cancer Res 2008;14:971-976.
13. Sutter R, Shakhova O, Bhagat H et al. Cerebellar stem cells act as medulloblastoma-initiating cells in a mouse model and a neural stem cell signature characterizes a subset of human medulloblastomas. Oncogene 2010;29:1845-1856.
14. Bhat RV, Baraban JM, Johnson RC et al. High levels of expression of the tumor suppressor gene APC during development of the rat central nervous system. J Neurosci 1994;14:3059-3071.
15. Brakeman JS, Gu SH, Wang XB et al. Neuronal localization of the Adenomatous polyposis coli tumor suppressor protein. Neuroscience 1999;91:661-672.
16. Etienne-Manneville S, Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 2003;421:753-756.
17. Temburni MK, Rosenberg MM, Pathak N et al. Neuronal nicotinic synapse assembly requires the adenomatous polyposis coli tumor suppressor protein. J Neurosci 2004;24:6776-6784.
18. Zhou FQ, Zhou J, Dedhar S et al. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 2004;42:897-912.
19. Oshima M, Oshima H, Kitagawa K et al. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc Natl Acad Sci USA 1995;92:4482-4486.
20. Shibata H, Toyama K, Shioya H et al. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 1997;278:120-123.
21. Ivaniutsin U, Chen Y, Mason JO et al. Adenomatous polyposis coli is required for early events in the normal growth and differentiation of the developing cerebral cortex. Neural Develop 2009;4:3.
22. Yokota Y, Kim WY, Chen Y et al. The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 2009;61:42-56.
23. Colnot S, Decaens T, Niwa-Kawakita M et al. Liver-targeted disruption of Apc in mice activates beta-catenin signaling and leads to hepatocellular carcinomas. Proc Natl Acad Sci USA 2004;101:17216-17221.
24. Martinez G, Wijesinghe M, Turner K et al. Conditional mutations of beta-catenin and APC reveal roles for canonical Wnt signaling in lens differentiation. Invest Ophthalmol Vis Sci 2009;50:4794-4806.
25. Garcia AD, Doan NB, Imura T et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004;7:1233-1241.
26. Kawamoto S, Niwa H, Tashiro F et al. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett 2000;470:263-268.
27. Imura T, Kornblum HI, Sofroniew MV. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 2003;23:2824-2832.
28. Imura T, Nakano I, Kornblum HI et al. Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: Differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 2006;53:277-293.
29. Petreanu L, Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: Role of olfaction. J Neurosci 2002;22:6106-6113.
30. Vandesompele J, De Preter K, Pattyn F et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3:34.1-34.11.
31. Coulson DT, Brockbank S, Quinn JG et al. Identification of valid reference genes for the normalization of RT qPCR gene expression data in human brain tissue. BMC Mol Biol 2008;9:46.
32. Laywell ED, Rakic P, Kukekov VG et al. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 2000;97:13883-13888.
33. Seri B, Garcia-Verdugo JM, McEwen BS et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001;21:7153-7160.
34. Doetsch F, Caille I, Lim DA et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716.
35. Herrmann JE, Imura T, Song B et al. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 2008;28:7231-7243.
36. Zhuo L, Theis M, Alvarez-Maya I et al. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 2001;31:85-94.
37. Bhat RV, Axt KJ, Fosnaugh JS et al. Expression of the APC tumor suppressor protein in oligodendroglia. Glia 1996;17:169-174.
38. Bush TG, Savidge TC, Freeman TC et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998;93:189-201.
39. Hatfield JS, Skoff RP, Maisel H et al. Glial fibrillary acidic protein is localized in the lens epithelium. J Cell Biol 1984;98:1895-1898.
40. Boyer S, Maunoury R, Gomes D et al. Expression of glial fibrillary acidic protein and vimentin in mouse lens epithelial cells during development in vivo and during proliferation and differentiation in vitro: Comparison with the developmental appearance of GFAP in the mouse central nervous system. J Neurosci Res 1990;27:55-64.
41. Imayoshi I, Sakamoto M, Ohtsuka T et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008;11:1153-1161.
42. Alvarez-Buylla A, Garcia-Verdugo J M, Neurogenesis in adult subventricular zone. J Neurosci 2002;22:629-634.
43. Bull ND, Bartlett PF. The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 2005;25:10815-10821.
44. Chojnacki AK, Mak GK, Weiss S. Identity crisis for adult periventricular neural stem cells: Subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci 2009;10:153-163.
45. Leroy K, Duyckaerts C, Bovekamp L et al. Increase of adenomatous polyposis coli immunoreactivity is a marker of reactive astrocytes in Alzheimer's disease and in other pathological conditions. Acta Neuropathol 2001;102:1-10.
46. Menn B, Garcia-Verdugo JM, Yaschine C et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006;26:7907-7918.
47. Parras CM, Galli R, Britz O et al. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 2004;23:4495-4505.
48. Woodhead GJ, Mutch CA, Olson EC et al. Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci 2006;26:12620-12630.
49. Adachi K, Mirzadeh Z, Sakaguchi M et al. Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 2007;25:2827-2836.
50. Israsena N, Hu M, Fu W et al. The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev Biol 2004;268:220-231. (Pubitemid 38367863)
51. Qu Q, Sun G, Li W et al. Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat Cell Biol 2010;12:31-40; sup pp 1-9.
52. Chenn A, Walsh CA. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 2002;297:365-369.
53. Zechner D, Fujita Y, Hulsken J et al. Beta-catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 2003;258:406-418.
54. Fodde R, Kuipers J, Rosenberg C et al. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 2001;3:433-438.
55. Kaplan KB, Burds AA, Swedlow JR et al. A role for the adenomatous polyposis coli protein in chromosome segregation. Nat Cell Biol 2001;3:429-432.
56. Gounari F, Chang R, Cowan J et al. Loss of adenomatous polyposis coli gene function disrupts thymic development. Nat Immunol 2005;6:800-809.
57. Qian Z, Chen L, Fernald AA et al. A critical role for Apc in hematopoietic stem and progenitor cell survival. J Exp Med 2008;205:2163-2175.