Ptch1-mediated dosage-dependent action of Shh signaling regulates neural progenitor development at late gestational stages

Developmental Biology

Volumn 349, Issue 2, 2011, Pages 147-159

  Shikata, Yayoi ^a   Okada, Toshiaki ^a   Hashimoto, Mitsuhiro ^a   Ellis, Tammy ^b   Matsumaru, Daisuke ^c   Shiroishi, Toshihiko ^d   Ogawa, Masaharu ^a   Wainwright, Brandon ^b   Motoyama, Jun ^a,e  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c KUMAMOTO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e DOSHISHA UNIVERSITY   (Japan)

Author keywords

Differentiation; Neural progenitor cell; Neurogenesis; Proliferation; Sonic hedgehog

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE DOSAGE; GESTATION PERIOD; MOUSE; MOUSE EMBRYO; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PTCH1 GENE; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; TELENCEPHALON; UPREGULATION;

ERINACEIDAE; MUS;

EID: 78650844253     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.10.014     Document Type: Article

References (65)

1. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
2. Ahn S., Joyner A.L. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005, 437:894-897.
3. Aoto K., Shikata Y., Higashiyama D., Shiota K., Motoyama J. Fetal ethanol exposure activates protein kinase A and impairs Shh expression in prechordal mesendoderm cells in the pathogenesis of holoprosencephaly. Birth Defects Res. Clin. Mol. Teratol. 2008, 82:224-231.
4. Aoto K., Shikata Y., Imai H., Matsumaru D., Tokunaga T., Shioda S., Yamada G., Motoyama J. Mouse Shh is required for prechordal plate maintenance during brain and craniofacial morphogenesis. Dev. Biol. 2009, 327:106-120.
5. Asada H., Kawamura Y., Maruyama K., Kume H., Ding R.G., Kanbara N., Kuzume H., Sanbo M., Yagi T., Obata K. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl Acad. Sci. USA 1997, 94:6496-6499.
6. Belloni E., Muenke M., Roessler E., Traverso G., Siegel-Bartelt J., Frumkin A., Mitchell H.F., Donis-Keller H., Helms C., Hing A.V., Heng H.H., Koop B., Martindale D., Rommens J.M., Tsui L.C., Scherer S.W. Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat. Genet. 1996, 14:353-356.
7. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 1996, 383:407-413.
8. Chiasson B.J., Tropepe V., Morshead C.M., van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J. Neurosci. 1999, 19:4462-4471.
9. Cohen M.M., Shiota K. Teratogenesis of holoprosencephaly. Am. J. Med. Genet. 2002, 109:1-15.
10. Dahmane N., Sanchez P., Gitton Y., Palma V., Sun T., Beyna M., Weiner H., Ruiz i Altaba A. The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 2001, 128:5201-5212.
11. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C.C. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 1998, 125:2533-2543.
12. Echelard Y., Epstein D.J., St-Jacques B., Shen L., Mohler J., McMahon J.A., McMahon A.P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993, 75:1417-1430.
13. Ellis T., Smyth I., Riley E., Graham S., Elliot K., Narang M., Kay G.F., Wicking C., Wainwright B. Patched 1 conditional null allele in mice. Genesis 2003, 36:158-161.
14. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 1996, 10:301-312.
15. Goodrich L.V., Milenković L., Higgins K.M., Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997, 277:1109-1113.
16. Grindley J.C., Davidson D.R., Hill R.E. The role of Pax-6 in eye and nasal development. Development 1995, 121:1433-1442.
17. Gulacsi A., Lillien L. Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro. J. Neurosci. 2003, 23:9862-9872.
18. Haraguchi R., Motoyama J., Sasaki H., Satoh Y., Miyagawa S., Nakagata N., Moon A., Yamada G. Molecular analysis of coordinated bladder and urogenital organ formation by Hedgehog signaling. Development 2007, 134:525-533.
19. Hashimoto M., Mikoshiba K. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J. Neurosci. 2003, 23:11342-11351.
20. Hashimoto M., Mikoshiba K. Neuronal birthdate-specific gene transfer with adenoviral vectors. J. Neurosci. 2004, 24:286-296.
21. Hirabayashi Y., Itoh Y., Tabata H., Nakajima K., Akiyama T., Masuyama N., Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004, 131:2791-2801.
22. Ishii Y., Nakamura S., Osumi N. Demarcation of early mammalian cortical development by differential expression of fringe genes. Brain Res. Dev. Brain Res. 2000, 119:307-320.
23. Kohtz J.D., Baker D.P., Corte G., Fishell G. Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic Hedgehog. Development 1998, 125:5079-5089.
24. Kohtz J.D., Lee H.Y., Gaiano N., Segal J., Ng E., Larson T., Baker D.P., Garber E.A., Williams K.P., Fishell G. N-terminal fatty-acylation of sonic hedgehog enhances the induction of rodent ventral forebrain neurons. Development 2001, 128:2351-2363.
25. Komada M., Saitsu H., Kinboshi M., Miura T., Shiota K., Ishibashi M. Hedgehog signaling is involved in development of the neocortex. Development 2008, 135:2717-2727.
26. Li M., Indra A.K., Warot X., Brocard J., Messaddeq N., Kato S., Metzger D., Chambon P. Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature 2000, 407:633-636.
27. Machold R., Hayashi S., Rutlin M., Muzumdar M.D., Nery S., Corbin J.G., Gritli-Linde A., Dellovade T., Porter J.A., Rubin L.L., Dudek H., McMahon A.P., Fishell G. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 2003, 39:937-950.
28. Makino S., Masuya H., Ishijima J., Yada Y., Shiroishi T. A spontaneous mouse mutation, mesenchymal dysplasia (mes), is caused by a deletion of the most C-terminal cytoplasmic domain of patched (ptc). Dev. Biol. 2001, 239:95-106.
29. Marti E., Bumcrot D.A., Takada R., McMahon A.P. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 1995, 375:322-325.
30. Marti E., Takada R., Bumcrot D.A., Sasaki H., McMahon A.P. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 1995, 121:2537-2547.
31. Milenkovic L., Goodrich L.V., Higgins K.M., Scott M.P. Mouse patched1 controls body size determination and limb patterning. Development 1999, 126:4431-4440.
32. Motoyama J., Milenkovic L., Iwama M., Shikata Y., Scott M.P., Hui C.C. Differential requirement for Gli2 and Gli3 in ventral neural cell fate specification. Dev. Biol. 2003, 259:150-161.
33. Nieuwenhuis E., Barnfield P.C., Makino S., Hui C.C. Epidermal hyperplasia and expansion of the interfollicular stem cell compartment in mutant mice with a C-terminal truncation of Patched1. Dev. Biol. 2007, 308:547-560.
34. Niwa H., Yamamura K., Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991, 108:193-199.
35. Oh S., Huang X., Liu J., Litingtung Y., Chiang C. Shh and Gli3 activities are required for timely generation of motor neuron progenitors. Dev. Biol. 2009, 331:261-269.
36. Ohsawa R., Ohtsuka T., Kageyama R. Mash1 and Math3 are required for development of branchiomotor neurons and maintenance of neural progenitors. J. Neurosci. 2005, 25:5857-5865.
37. Palma V., Ruiz i Altaba A. Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 2004, 131:337-345.
38. Porteus M.H., Bulfone A., Ciaranello R.D., Rubenstein J.L. Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 1991, 7:221-229.
39. Quinn J.C., Molinek M., Mason J.O., Price D.J. Gli3 is required autonomously for dorsal telencephalic cells to adopt appropriate fates during embryonic forebrain development. Dev. Biol. 2009, 327:204-215.
40. Rallu M., Machold R., Gaiano N., Corbin J.G., McMahon A.P., Fishell G. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 2002, 129:4963-4974.
41. Rash B.G., Grove E.A. Patterning the dorsal telencephalon: a role for sonic hedgehog?. J. Neurosci. 2007, 27:11595-11603.
42. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 1996, 175:1-13.
43. Roelink H., Porter J.A., Chiang C., Tanabe Y., Chang D.T., Beachy P.A., Jessell T.M. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 1995, 81:445-455.
44. Roessler E., Belloni E., Gaudenz K., Jay P., Berta P., Scherer S.W., Tsui L.C., Muenke M. Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat. Genet. 1996, 14:357-360.
45. Rowitch D.H., S-Jacques B., Lee S.M., Flax J.D., Snyder E.Y., McMahon A.P. Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 1999, 19:8954-8965.
46. Sasai Y., Kageyama R., Tagawa Y., Shigemoto R., Nakanishi S. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 1992, 6:2620-2634.
47. Sasaki H., Hui C., Nakafuku M., Kondoh H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 1997, 124:1313-1322.
48. Sessa A., Mao C.A., Hadjantonakis A.K., Klein W.H., Broccoli V. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 2008, 60:56-69.
49. Shimamura K., Hartigan D.J., Martinez S., Puelles L., Rubenstein J.L. Longitudinal organization of the anterior neural plate and neural tube. Development 1995, 121:3923-3933.
50. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
51. St-Jacques B., Dassule H.R., Karavanova I., Botchkarev V.A., Li J., Danielian P.S., McMahon J.A., Lewis P.M., Paus R., McMahon A.P. Sonic hedgehog signaling is essential for hair development. Curr. Biol. 1998, 8:1058-1068.
52. Sulik K.K., Johnston M.C., Webb M.A. Fetal alcohol syndrome: embryogenesis in a mouse model. Science 1981, 214:936-938.
53. Sweet H.O., Bronson R.T., Donahue L.R., Davisson M.T. Mesenchymal dysplasia: a recessive mutation on chromosome 13 of the mouse. J. Hered. 1996, 87:87-95.
54. Tabata H., Nakajima K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 2001, 103:865-872.
55. Theil T., Alvarez-Bolado G., Walter A., Ruther U. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development 1999, 126:3561-3571.
56. Thibert C., Teillet M.A., Lapointe F., Mazelin L., Le Douarin N.M., Mehlen P. Inhibition of neuroepithelial patched-induced apoptosis by sonic hedgehog. Science 2003, 301:843-846.
57. Ulloa F., Itasaki N., Briscoe J. Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signaling. Curr. Biol. 2007, 17:545-550.
58. Vescovi A.L., Snyder E.Y. Establishment and properties of neural stem cell clones: plasticity in vitro and in vivo. Brain Pathol. 1999, 9:569-598.
59. Viti J., Gulacsi A., Lillien L. Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J. Neurosci. 2003, 23:5919-5927.
60. Webster A.J. Environmental stress and the physiology, performance and health of ruminants. J. Anim. Sci. 1983, 57:1584-1593.
61. Wechsler-Reya R.J., Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999, 22:103-114.
62. Woodhead G.J., Mutch C.A., Olson E.C., Chenn A. Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J. Neurosci. 2006, 26:12620-12630.
63. Xu Q., Wonders C.P., Anderson S.A. Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 2005, 132:4987-4998.
64. Yu W., Wang Y., McDonnell K., Stephen D., Bai C.B. Patterning of ventral telencephalon requires positive function of Gli transcription factors. Dev. Biol. 2009, 334:264-275.
65. Zhou C.J., Borello U., Rubenstein J.L., Pleasure S.J. Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience 2006, 142:1119-1131.