Bone morphogenic protein signaling is a major determinant of dentate development

Journal of Neuroscience

Volumn 33, Issue 16, 2013, Pages 6766-6775

  Choe, Youngshik ^a   Kozlova, Anastasiia ^c   Graf, Daniel ^c   Pleasure, Samuel J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN; KI 67 ANTIGEN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR FOXC1;

ACETYLATION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPORATION; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL NICHE;

ACTIVIN RECEPTORS, TYPE I; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BONE MORPHOGENETIC PROTEINS; BROMODEOXYURIDINE; DENTATE GYRUS; ELECTROPORATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; ESTROGEN ANTAGONISTS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HOMEODOMAIN PROTEINS; KI-67 ANTIGEN; LUMINESCENT PROTEINS; LYMPHOID ENHANCER-BINDING FACTOR 1; MALE; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NEURAL CREST; NEUROGENESIS; ONCOGENE PROTEINS; PREGNANCY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; ROSA; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TAMOXIFEN; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84876269766     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0128-13.2013     Document Type: Article

References (50)

1. Ahn S, Joyner AL (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118:505-516.
2. Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437:894-897.
3. Altman J, Bayer SA (1990a) Mosaic organization of the hippocampal neu-roepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325-342.
4. Altman J, Bayer SA (1990b) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381.
5. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ (2002) The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249-4260.
6. Bardeesy N, Cheng KH, Berger JH, Chu GC, Pahler J, Olson P, Hezel AF, Horner J, Lauwers GY, Hanahan D, DePinho RA (2006) Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev 20:3130-3146.
7. Bonaguidi MA, Peng CY, McGuire T, Falciglia G, Gobeske KT, Czeisler C, Kessler JA (2008) Noggin expands neural stem cells in the adult hippocampus. J Neurosci 28:9194-9204.
8. Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T (2006) Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 169:154-164.
9. Caronia G, Wilcoxon J, Feldman P, Grove EA (2010) Bone morphogenetic protein signaling in the developing telencephalon controls formation of the hippocampal dentate gyrus and modifies fear-related behavior. J Neu-rosci 30:6291-6301.
10. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369.
11. Choe Y, Pleasure SJ (2012) Wnt signaling regulates intermediate precursor production in the postnatal dentate gyrus by regulating Cxcr4 expression. Dev Neurosci 34:502-514.
12. Choe Y, Siegenthaler JA, Pleasure SJ (2012) A cascade of morphogenic signaling initiated by the meanings controls corpus callosum formation. Neuron 73:698-712.
13. Chytil A, Magnuson MA, Wright CV, Moses HL (2002) Conditional inactivation of the TGF-beta type II receptor using Cre:Lox. Genesis 32:73-75.
14. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, Mummery C, Sommer L, Götz M (2008) Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28:434-446.
15. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8:1323-1326.
16. Derynck R, Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425:577-584.
17. Favaro R, Valotta M, Ferri AL, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V, Nicolis SK (2009) Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci 12:1248-1256.
18. Filali M, Cheng N, Abbott D, Leontiev V, Engelhardt JF (2002) Wnt-3A/ beta-catenin signaling induces transcription from the LEF-1 promoter. J Biol Chem 277:33398-33410.
19. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH (2006) Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 124:161-173.
20. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) asregulators of dorsal forebrain development. Development 124: 2203-2212.
21. Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R (2000) Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 127:469-482.
22. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125: 2315-2325.
23. Guo W, Zhang L, Christopher DM, Teng ZQ, Fausett SR, Liu C, George OL, Klingensmith J, Jin P, Zhao X (2011) RNA-binding protein FXR2 regulates adult hippocampal neurogenesis by reducing Noggin expression. Neuron 70:924-938.
24. Hayashi H, Kume T (2008) Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem Biophys Res Commun 367:584-589.
25. Hébert JM, Mishina Y, McConnell SK (2002) BMP signaling is required locallytopattern the dorsal telencephalic midline. Neuron 35:1029-1041.
26. Hodge RD, Kowalczyk TD, Wolf SA, Encinas JM, Rippey C, Enikolopov G, Kempermann G, Hevner RF (2008) Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J Neurosci 28:3707-3717.
27. Hovanes K, Li TW, Munguia JE, Truong T, Milovanovic T, Lawrence Marsh J, Holcombe RF, Waterman ML (2001) Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28:53-57.
28. Kaartinen V, Nagy A (2001) Removal of the floxed neo gene from a conditional knockout allele by the adenoviral Cre recombinase in vivo. Genesis 31:126-129.
29. Karalay O, Doberauer K, Vadodaria KC, Knobloch M, Berti L, Miquelajau-regui A, Schwark M, Jagasia R, Taketo MM, Tarabykin V, Lie DC, Jess-berger S (2011) Prospero-related homeobox 1 gene (Prox1) is regulated by canonical Wnt signaling and has a stage-specific role in adult hip-pocampal neurogenesis. Proc Natl Acad Sci USA 108:5807-5812.
30. Kratochwil K, Dull M, Farinas I, Galceran J, Grosschedl R (1996) Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev 10:1382-1394.
31. Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457-467.
32. Li G, Pleasure SJ (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27:93-99.
33. Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136:327-335.
34. Lie DC, Colamarino SA, Song HJ, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.
35. Mabie PC, Mehler MF, Kessler JA (1999) Multiple roles of bone morphoge-netic protein signaling in the regulation of cortical cell number and phe-notype. J Neurosci 19:7077-7088.
36. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39:937-950.
37. Machon O, Backman M, Machonova O, Kozmik Z, Vacik T, Andersen L, Krauss S (2007) Adynamic gradient ofWnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 311:223-237.
38. Macías-Silva M, Hoodless PA, Tang SJ, Buchwald M, Wrana JL (1998) Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem 273:25628-25636.
39. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Sub-ramanian L, Shetty AS, Martynoga B, Paul J, Mai MV, Li Y, Flanagan LA, Tole S, Monuki ES (2008) Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 319:304-309.
40. Mira H, Andreu Z, Suh H, Lie DC, Jessberger S, Consiglio A, San Emeterio J, Hortigüela R, Marqués-Torrejón MA, Nakashima K, Colak D, Götz M, Fariñas I, Gage FH (2010) Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7:78-89.
41. Monuki ES, Porter FD, Walsh CA (2001) Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32:591- 604.
42. Munji RN, Choe Y, Li G, Siegenthaler JA, Pleasure SJ (2011) Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J Neurosci 31:1676-1687.
43. Segklia A, Seuntjens E, Elkouris M, Tsalavos S, Stappers E, Mitsiadis TA, Huylebroeck D, Remboutsika E, Graf D (2012) Bmp7 regulates the survival, proliferation, and neurogenic properties of neural progenitor cells during corticogenesis in the mouse. PLoS One 7:e34088.
44. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, Napoli JL, Peterson AS, Pleasure SJ (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597-609.
45. Visser JA, Olaso R, Verhoef-Post M, Kramer P, Themmen AP, Ingraham HA (2001) The serine/threonine transmembrane receptor ALK2 mediates Mullerian inhibiting substance signaling. Mol Endocrinol 15:936-945.
46. Wrana JL, Attisano L, Cárcamo J, Zentella A, Doody J, Laiho M, Wang XF, Massagué J (1992) TGF beta signals through a heteromeric protein ki-nase receptor complex. Cell 71:1003-1014.
47. Zarbalis K, Siegenthaler JA, Choe Y, May SR, Peterson AS, Pleasure SJ (2007) Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 104:14002-14007.
48. Zhou CJ, Zhao C, Pleasure SJ (2004) Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci 24:121-126.
49. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A (2001) HGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31:85-94.
50. Zouvelou V, Passa O, Segklia K, Tsalavos S, Valenzuela DM, Economides AN, Graf D (2009) Generation and functional characterization of mice with a conditional BMP7 allele. Int J Dev Biol 53:597-603.