Sonic hedgehog (Shh)/Gli modulates the spatial organization of neuroepithelial cell proliferation in the developing chick optic tectum

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Rapacioli, Melina ^a   Botelho, Joao ^b   Cerda, Gustavo ^b   Duarte, Santiago ^c   Elliot, Matías ^b   Palma, Verónica ^b   Flores, Vladimir ^a,c  

^a FAVALORO UNIVERSITY   (Argentina)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

In ovo cyclopamine treatment; Neuroepithelial cell proliferation; Non linear signal analyses; Optic tectum; Purmorphamine; Shh Gli pathway

Indexed keywords

ALKALOID DERIVATIVE; BINDING PROTEIN; CYCLOPAMINE; GLI PROTEIN; GLIA PROTEIN; PURMORPHAMINE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL EXPANSION; CELL PROLIFERATION; CELL VACUOLE; CHICK; CONTROLLED STUDY; DORSAL ROOT; ELECTROPORATION; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MORPHOGENESIS; NEUROEPITHELIUM; NEUROMODULATION; NONHUMAN; NONLINEAR REGRESSION ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPATIAL DISCRIMINATION; SUPERIOR COLLICULUS;

ANIMALS; CELL PROLIFERATION; CHICK EMBRYO; ELECTROPORATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MORPHOLINES; NEUROEPITHELIAL CELLS; NEUROGENESIS; ONCOGENE PROTEINS; PURINES; SIGNAL TRANSDUCTION; SUPERIOR COLLICULI; TERATOGENS; TRANS-ACTIVATORS; VERATRUM ALKALOIDS;

EID: 84866775922     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-117     Document Type: Article

References (42)

1. Marti E, Takada R, Bumcrot DA, Sasaki H, McMahon AP. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 1995, 121(8):2537-2547.
2. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001, 15(23):3059-3087. 10.1101/gad.938601, 11731473.
3. Lai K, Kaspar BK, Gage FH, Schaffer DV. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 2003, 6(1):21-27. 10.1038/nn983, 12469128.
4. 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(24):5201-5212.
5. Ruiz i Altaba A, Palma V, Dahmane N. Hedgehog-Gli signalling and the growth of the brain. Nat Rev Neurosci 2002, 3(1):24-33. 10.1038/nrn704, 11823802.
6. Ruiz i Altaba A, Nguyen V, Palma V. The emergent design of the neural tube: prepattern, SHH morphogen and GLI code. Curr Opin Genet Dev 2003, 13(5):513-521. 10.1016/j.gde.2003.08.005, 14550418.
7. Bayly RD, Ngo M, Aglyamova GV, Agarwala S. Regulation of ventral midbrain patterning by Hedgehog signaling. Development 2007, 134(11):2115-2124. 10.1242/dev.02850, 17507412.
8. Agarwala S, Sanders TA, Ragsdale CW. Sonic hedgehog control of size and shape in midbrain pattern formation. Science 2001, 291(5511):2147-2150. 10.1126/science.1058624, 11251119.
9. Li N, Hornbruch A, Klafke R, Katzenberger B, Wizenmann A. Specification of dorsoventral polarity in the embryonic chick mesencephalon and its presumptive role in midbrain morphogenesis. Dev Dyn 2005, 233(3):907-920. 10.1002/dvdy.20434, 15906380.
10. Rapacioli M, Duarte S, Rodriguez Celin A, Fiore L, Teruel L, Scicolone G, Sanchez V, Flores V. Optic tectum morphogenesis: a step-by-step model based on the temporal-spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization. Dev Dyn 2012, 241(6):1043-1061. 10.1002/dvdy.23785, 22473829.
11. Rapacioli M, Rodriguez Celin A, Duarte S, Ortalli AL, Di Napoli J, Teruel L, Sanchez V, Scicolone G, Flores V. The chick optic tectum developmental stages. A dynamic table based on temporal- and spatial-dependent histogenetic changes: a structural, morphometric and immunocytochemical analysis. J Morphol 2011, 272(6):675-697. 10.1002/jmor.10943, 21484853.
12. Scherz PJ, McGlinn E, Nissim S, Tabin CJ. Extended exposure to Sonic hedgehog is required for patterning the posterior digits of the vertebrate limb. Dev Biol 2007, 308(2):343-354. 10.1016/j.ydbio.2007.05.030, 2100419, 17610861.
13. Cowan WM, Martin AH, Wenger E. Mitotic patterns in the optic tectum of the chick during normal development and after early removal of the optic vesicle. J Exp Zool 1968, 169(1):71-92. 10.1002/jez.1401690110, 5696645.
14. LaVail JH, Cowan WM. The development of the chick optic tectum. II. Autoradiographic studies. Brain Res 1971, 28(3):421-441. 10.1016/0006-8993(71)90054-0, 5111721.
15. LaVail JH, Cowan WM. The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res 1971, 28(3):391-419. 10.1016/0006-8993(71)90053-9, 5111720.
16. Wilson DB. Distribution of thymidine-H3 in the overgrown brain of the chick embryo. J Comp Neurol 1971, 141(1):37-51. 10.1002/cne.901410104, 5538889.
17. Goldberger AL, West BJ. Fractals in physiology and medicine. Yale J Biol Med 1987, 60(5):421-435. 2590346, 3424875.
18. Abry MFP. Wavelets in Medicine and Biology; Point processes, long-range dependence and wavelets 1996, CRC Press, Boca Raton.
19. Eke A, Herman P, Kocsis L, Kozak LR. Fractal characterization of complexity in temporal physiological signals. Physiol Meas 2002, 23(1):R1-R38. 10.1088/0967-3334/23/1/201, 11876246.
20. Jovani R, Tella JL. Fractal bird nest distribution produces scale-free colony sizes. Proc Biol Sci 2007, 274(1624):2465-2469. 10.1098/rspb.2007.0527, 2274970, 17666378.
21. Camazine SDJ-L, Franks NR, Sneyd J, Theraulaz G, Bonabeau E. Self-organization in biological systems 2001, Princeton University Press, Princeton.
22. Watanabe Y, Nakamura H. Control of chick tectum territory along dorsoventral axis by Sonic hedgehog. Development 2000, 127(5):1131-1140.
23. Litingtung Y, Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat Neurosci 2000, 3(10):979-985. 10.1038/79916, 11017169.
24. Ishibashi M, McMahon AP. A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development 2002, 129(20):4807-4819.
25. Britto J, Tannahill D, Keynes R. A critical role for sonic hedgehog signaling in the early expansion of the developing brain. Nat Neurosci 2002, 5(2):103-110. 10.1038/nn797, 11788837.
26. Balaskas N, Ribeiro A, Panovska J, Dessaud E, Sasai N, Page KM, Briscoe J, Ribes V. Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 2012, 148(1-2):273-284. 3267043, 22265416.
27. Komada M, Saitsu H, Kinboshi M, Miura T, Shiota K, Ishibashi M. Hedgehog signaling is involved in development of the neocortex. Development 2008, 135(16):2717-2727. 10.1242/dev.015891, 18614579.
28. 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(2):337-345.
29. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005, 132(2):335-344. 10.1242/dev.01567, 1431583, 15604099.
30. Wijgerde M, McMahon JA, Rule M, McMahon AP. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev 2002, 16(22):2849-2864. 10.1101/gad.1025702, 187482, 12435628.
31. Roessler E, Belloni E, Gaudenz K, Vargas F, Scherer SW, Tsui LC, Muenke M. Mutations in the C-terminal domain of Sonic Hedgehog cause holoprosencephaly. Hum Mol Genet 1997, 6(11):1847-1853. 10.1093/hmg/6.11.1847, 9302262.
32. Dahmane N, Ruiz i Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 1999, 126(14):3089-3100.
33. Wallace VA. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 1999, 9(8):445-448. 10.1016/S0960-9822(99)80195-X, 10226030.
34. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999, 22(1):103-114. 10.1016/S0896-6273(00)80682-0, 10027293.
35. Stecca B, Ruiz i Altaba A. Brain as a paradigm of organ growth: Hedgehog-Gli signaling in neural stem cells and brain tumors. J Neurobiol 2005, 64(4):476-490. 10.1002/neu.20160, 16041742.
36. Aglyamova GV, Agarwala S. Gene expression analysis of the hedgehog signaling cascade in the chick midbrain and spinal cord. Dev Dyn 2007, 236(5):1363-1373. 10.1002/dvdy.21146, 17436280.
37. Feijoo CG, Onate MG, Milla LA, Palma VA. Sonic hedgehog (Shh)-Gli signaling controls neural progenitor cell division in the developing tectum in zebrafish. Eur J Neurosci 2011, 33(4):589-598. 10.1111/j.1460-9568.2010.07560.x, 21219478.
38. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 1992, 195(4):231-272. 10.1002/aja.1001950404, 1304821.
39. Stamataki D, Ulloa F, Tsoni SV, Mynett A, Briscoe J. A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev 2005, 19(5):626-641. 10.1101/gad.325905, 551582, 15741323.
40. Scicolone G, Pereyra-Alfonso S, Brusco A, Pecci Saavedra J, Flores V. Development of the laminated pattern of the chick tectum opticum. Int J Dev Neurosci 1995, 13(8):845-858. 10.1016/0736-5748(95)00069-0, 8770658.
41. Wilson DB. Chronological changes in the cell cycle of chick neuroepithelial cells. J Embryol Exp Morphol 1973, 29(3):745-751.
42. Coggeshall RE, Lekan HA. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 1996, 364(1):6-15. 10.1002/(SICI)1096-9861(19960101)364:1<6::AID-CNE2>3.0.CO;2-9, 8789272.