Adenomatous polyposis coli regulates oligodendroglial development

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 3113-3130

  Lang, Jordan ^a   Maeda, Yoshiko ^a   Bannerman, Peter ^a   Xu, Jie ^a   Horiuchi, Makoto ^a   Pleasure, David ^a   Guo, Fuzheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CTNNB1 GENE; DEMYELINATION; GENE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MOUSE; MYELINATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REMYELINIZATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; ANTIBODIES; BETA CATENIN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; ESTROGEN ANTAGONISTS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MICROSCOPY, CONFOCAL; MYELIN-ASSOCIATED GLYCOPROTEIN; NERVE REGENERATION; OLIGODENDROGLIA; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; STEM CELLS; TAMOXIFEN;

EID: 84873651744     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3467-12.2013     Document Type: Article

References (62)

1. Aoki K, Taketo MM (2007) Adenomatous polyposis coli (APC): a multifunctional tumor suppressor gene. J Cell Sci 120:3327-3335. CrossRef Medline
2. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7:812-821. CrossRef Medline
3. Barres BA, Raff MC (1999) Axonal control of oligodendrocyte development. J Cell Biol 147:1123-1128. CrossRef Medline
4. Bauer NG, Richter-Landsberg C, Ffrench-Constant C (2009) Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 57: 1691-1705. CrossRef Medline
5. Bhat RV, Baraban JM, Johnson RC, Eipper BA, Mains RE (1994) High levels of expression of the tumor suppressor gene APC during development of the rat central nervous system. J Neurosci 14:3059-3071. Medline
6. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17:169-174. CrossRef Medline
7. Bloom K (2004) Microtubule composition: cryptography of dynamic polymers. Proc Natl Acad Sci U S A 101:6839-6840. CrossRef edline
8. Brakeman JS, Gu SH, Wang XB, Dolin G, Baraban JM (1999) Neuronal localization of the adenomatous polyposis coli tumor suppressor protein. Neuroscience 91:661-672. CrossRef Medline
9. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R (2001) Inactivation of the beta β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253-1264. Medline
10. Chen Y, Tian X, Kim WY, Snider WD (2011) Adenomatous polyposis coli regulates axon arborization and cytoskeleton organization via its N-terminus. PLoS One 6:e24335. CrossRef Medline
11. Chew LJ, Shen W, Ming X, Senatorov VV Jr, Chen HL, Cheng Y, Hong E, Knoblach S, Gallo V (2011) SRY-box containing gene 17 regulates the Wnt/ β-catenin signaling pathway in oligodendrocyte progenitor cells. J Neurosci 31:13921-13935. CrossRef Medline
12. Chung AY, Kim S, Kim H, Bae YK, Park HC (2011) Microarray screening for genes involved in oligodendrocyte differentiation in the zebrafish CNS. Exp Neurobiol 20:85-91. CrossRef Medline
13. Cobas M, Wilson A, Ernst B, Mancini SJ, MacDonald HR, Kemler R, Radtke F (2004) Beta β-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 199:221-229. CrossRef Medline
14. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A (2005) Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol 170:895-901. CrossRef Medline
15. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23:1571-1585. CrossRef Medline
16. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, Bruce CC, Otero JJ, Huang EJ, Nusse R, Franklin RJ, Rowitch DH (2011) Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 14:1009-1016. CrossRef Medline
17. Feigenson K, Reid M, See J, Crenshaw EB 3rd, Grinspan JB (2009) Wnt signaling is sufficient to perturb oligodendrocyte maturation. Mol Cell Neurosci 42:255-265. CrossRef Medline
18. Gounari F, Aifantis I, Khazaie K, Hoeflinger S, Harada N, Taketo MM, von Boehmer H (2001) Somatic activation of beta β-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat Immunol 2:863-869. CrossRef Medline
19. Gounari F, Chang R, Cowan J, Guo Z, Dose M, Gounaris E, Khazaie K (2005) Loss of adenomatous polyposis coli gene function disrupts thymic development. Nat Immunol 6:800-809. CrossRef Medline
20. Guo F, Ma J, McCauley E, Bannerman P, Pleasure D (2009) Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J Neurosci 29:7256-7270. CrossRef Medline
21. Guo F, Maeda Y, Ma J, Xu J, Horiuchi M, Miers L, Vaccarino F, Pleasure D (2010) Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J Neurosci 30:12036-12049. CrossRef Medline
22. Guo F, Maeda Y, Ma J, Delgado M, Sohn J, Miers L, Ko EM, Bannerman P, Xu J, Wang Y, Zhou C, Takebayashi H, Pleasure D (2011) Macroglial plasticity and the origins of reactive astroglia in experimental autoimmune encephalomyelitis. J Neurosci 31:11914-11928. CrossRef Medline
23. Guo F, Maeda Y, Ko EM, Delgado M, Horiuchi M, Soulika A, Miers L, Burns T, Itoh T, Shen H, Lee E, Sohn J, Pleasure D (2012) Disruption of NMDA receptors in oligodendroglial lineage cells does not alter their susceptibility to experimental autoimmune encephalomyelitis or their normal development. J Neurosci 32:639-645. CrossRef Medline
24. Horiuchi M, Lindsten T, Pleasure D, Itoh T (2010) Differing in vitro survival dependency of mouse and rat NG2 oligodendroglial progenitor cells. J Neurosci Res 88:957-970. Medline
25. Huang da W, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1-13. CrossRef Medline
26. Huang da W, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. CrossRef Medline
27. Huang da W, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA (2009c) Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics Chapter 13:Unit 13.11. CrossRef Medline
28. Imura T, Wang X, Noda T, Sofroniew MV, Fushiki S (2010) Adenomatous polyposis coli is essential for both neuronal differentiation and maintenance of adult neural stem cells in subventricular zone and hippocampus. Stem Cells 28:2053-2064. CrossRef Medline
29. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, Grinspan JB, Pleasure D (2002) AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 81:390-402. CrossRef Medline
30. Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, Haraguchi K, Akiyama T (2002) Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 4:323-327. CrossRef Medline
31. Kipp M, Clarner T, Dang J, Copray S, Beyer C (2009) The cuprizone animal model: new insights into an old story. Acta Neuropathol 118:723-736. CrossRef Medline
32. Kuraguchi M, Wang XP, Bronson RT, Rothenberg R, Ohene-Baah NY, Lund JJ, Kucherlapati M, Maas RL, Kucherlapati R (2006) Adenomatous polyposis coli (APC) is required for normal development of skin and thymus. PLoS Genet 2:e146. CrossRef Medline
33. Langseth AJ, Munji RN, Choe Y, Huynh T, Pozniak CD, Pleasure SJ (2010) Wnts influence the timing and efficiency of oligodendrocyte precursor cell generation in the telencephalon. J Neurosci 30:13367-13372. CrossRef Medline
34. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366-374. CrossRef Medline
35. Li A, Xing Y, Chan B, Heisterkamp N, Groffen J, Borok Z, Minoo P, Li C (2010) Cell type-specific expression of adenomatous polyposis coli in lung development, injury, and repair. Dev Dyn 239:2288-2297. CrossRef Medline
36. Lunn KF, Baas PW, Duncan ID (1997) Microtubule organization and stability in the oligodendrocyte. J Neurosci 17:4921-4932. Medline
37. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S (2003) Mapping Wnt/beta β-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100:3299-3304. CrossRef Medline
38. Mason JL, Toews A, Hostettler JD, Morell P, Suzuki K, Goldman JE, Matsushima GK (2004) Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 164: 1673-1682. CrossRef Medline
39. Mili S, Moissoglu K, Macara IG (2008) Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453:115-119. CrossRef Medline
40. Moser AR, Mattes EM, Dove WF, Lindstrom MJ, Haag JD, Gould MN (1993) ApcMin, a mutation in the murine Apc gene, predisposes to mammary carcinomas and focal alveolar hyperplasias. Proc Natl Acad Sci USA 90:8977-8981. CrossRefMedline
41. Näthke I (2006) Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat Rev Cancer 6:967-974. CrossRef Medline
42. Prlic M, Bevan MJ (2011) Cutting edge: beta β-catenin is dispensable for T cell effector differentiation, memory formation, and recall responses. J Immunol 187:1542-1546. CrossRef Medline
43. Qian Z, Chen L, Fernald AA, Williams BO, Le Beau MM (2008) A critical role for Apc in hematopoietic stem and progenitor cell survival. J Exp Med 205:2163-2175. CrossRef Medline
44. Rajasekharan S, Baker KA, Horn KE, Jarjour AA, Antel JP, Kennedy TE (2009) Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA. Development 136:415-426. CrossRef Medline
45. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392-1401. CrossRef Medline
46. Sasaki T, Irie-Sasaki J, Horie Y, Bachmaier K, Fata JE, Li M, Suzuki A, Bouchard D, Ho A, Redston M, Gallinger S, Khokha R, Mak TW, Hawkins PT, Stephens L, Scherer SW, Tsao M, Penninger JM (2000) Colorectal carcinomas in mice lacking the catalytic subunit of PI(3)Kgamma. Nature 406:897-902. CrossRef Medline
47. Saxton WM, Stemple DL, Leslie RJ, Salmon ED, Zavortink M, McIntosh JR (1984) Tubulin dynamics in cultured mammalian cells. J Cell Biol 99: 2175-2186. CrossRef Medline
48. Schulze E, Kirschner M (1987) Dynamic and stable populations of microtubules in cells. J Cell Biol 104:277-288. CrossRef Medline
49. Shintani T, Ihara M, Tani S, Sakuraba J, Sakuta H, Noda M (2009) APC2 plays an essential role in axonal projections through the regulation of microtubule stability. J Neurosci 29:11628-11640. CrossRef Medline
50. Soulika AM, Lee E, McCauley E, Miers L, Bannerman P, Pleasure D (2009) Initiation and progression of axonopathy in experimental autoimmune encephalomyelitis. J Neurosci 29:14965-14979. CrossRef Medline
51. Stacey DW (2003) Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Curr Opin Cell Biol 15:158-163. CrossRef Medline
52. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16:165-170. CrossRef Medline
53. Takebayashi H, Nabeshima Y, Yoshida S, Chisaka O, Ikenaka K, Nabeshima Y (2002) The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol 12:1157-1163. CrossRef Medline
54. Traka M, Wollmann RL, Cerda SR, Dugas J, Barres BA, Popko B (2008) Nur7 is a nonsense mutation in the mouse aspartoacylase gene that causes spongy degeneration of the CNS. J Neurosci 28:11537-11549. CrossRef Medline
55. Wang X, Imura T, Sofroniew MV, Fushiki S (2011) Loss of adenomatous polyposis coli in Bergmann glia disrupts their unique architecture and leads to cell nonautonomous neurodegeneration of cerebellar Purkinje neurons. Glia 59:857-868. CrossRef Medline
56. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6:820-830. CrossRef Medline
57. Wickline ED, Awuah PK, Behari J, Ross M, Stolz DB, Monga SP (2011) Hepatocyte gamma β-catenin compensates for conditionally deleted beta β-catenin at adherens junctions. J Hepatol 55:1256-1262. CrossRef Medline
58. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta β-catenin-TCF interaction. Nat Neurosci 12:829-838. CrossRef Medline
59. Yokota Y, Kim WY, Chen Y, Wang X, Stanco A, Komuro Y, Snider W, Anton ES (2009) The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 61:42-56. CrossRef Medline
60. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912. CrossRef Medline
61. Zhou J, Qu J, Yi XP, Graber K, Huber L, Wang X, Gerdes AM, Li F (2007) Upregulation of gamma β-catenin compensates for the loss of beta β-catenin in adult cardiomyocytes. Am J Physiol Heart Circ Physiol 292:H270-H276. Medline
62. Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligoden-drocytes and gray matter astrocytes. Development 135:145-157. Medline