Fibroblast growth factor (FGF) gene expression in the developing cerebellum suggests multiple roles for FGF signaling during cerebellar morphogenesis and development

Developmental Dynamics

Volumn 238, Issue 8, 2008, Pages 2058-2072

  Yaguchi, Yuichiro ^a,b   Yu, Tian ^a   Ahmed, Mohi U ^a,c   Berry, Mary ^a   Mason, Ivor ^a   Basson, M Albert ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebellum; Development; FGF; Gene expression; Morphogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 15; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 5; FIBROBLAST GROWTH FACTOR 6; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL TYPE; CEREBELLUM; EMBRYO DEVELOPMENT; GENE EXPRESSION; MORPHOGENESIS; MOUSE; NEUROMERE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; FEMALE; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LIGANDS; MICE; MICE, TRANSGENIC; PREGNANCY; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 67650821924     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22013     Document Type: Article

References (85)

1. Altman J, Bayer SA. 1997. Development of the cerebellar system: in relation to its evolution, structure and functions. Boca Raton, FL: CRC Press.
2. Alvarez Y, Alonso MT, Vendrell V, Zelarayan LC, Chamero P, Theil T, Bosl MR, Kato S, Maconochie M, Riethmacher D, Schimmang T. 2003. Requirements for FGF3 and FGF10 during inner ear formation. Development 130:6329-6338.
3. Baertschi S, Zhuang L, Trueb B. 2007. Mice with a targeted disruption of the Fgfrl1 gene die at birth due to alterations in the diaphragm. FEBS J 274:6241-6253.
4. Basson MA, Echevarria D, Ahn CP, Sudarov A, Joyner AL, Mason IJ, Martinez S, Martin GR. 2008. Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135:889-898.
5. Blak AA, Naserke T, Weisenhorn DM, Prakash N, Partanen J, Wurst W. 2005. Expression of Fgf receptors 1, 2, and 3 in the developing mid- and hindbrain of the mouse. Dev Dyn 233:1023-1030.
6. Catela C, Bilbao-Cortes D, Slonimsky E, Kratsios P, Rosenthal N, Te Welscher P. 2009. Multiple congenital malformations of Wolf-Hirschhorn syndrome are recapitulated in Fgfrl1 null mice. Dis Model Mech 2:283-294.
7. Chellaiah A, Yuan W, Chellaiah M, Ornitz DM. 1999. Mapping ligand binding domains in chimeric fibroblast growth factor receptor molecules. Multiple regions determine ligand binding specificity. J Biol Chem 274:34785-34794.
8. Chi CL, Martinez S, Wurst W, Martin GR. 2003. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130:2633-2644.
9. deLapeyriere O, Ollendorff V, Planche J, Ott MO, Pizette S, Coulier F, Birnbaum D. 1993. Expression of the Fgf6 gene is restricted to developing skeletal muscle in the mouse embryo. Development 118:601-611.
10. Dono R, Texido G, Dussel R, Ehmke H, Zeller R. 1998. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213-4225.
11. Echevarria D, Vieira C, Gimeno L, Martinez S. 2003. Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res Brain Res Rev 43:179-191.
12. Espinosa JS, Luo L. 2008. Timing neurogenesis and differentiation: insights from quantitative clonal analyses of cerebellar granule cells. J Neurosci 28:2301-2312.
13. Fiore F, Planche J, Gibier P, Sebille A, deLapeyriere O, Birnbaum D. 1997. Apparent normal phenotype of Fgf6-/- mice. Int J Dev Biol 41:639-642.
14. Floss T, Arnold HH, Braun T. 1997. A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11:2040-2051.
15. Fogarty MP, Emmenegger BA, Grasfeder LL, Oliver TG, Wechsler-Reya RJ. 2007. Fibroblast growth factor blocks Sonic hedgehog signaling in neuronal precursors and tumor cells. Proc Natl Acad Sci U S A 104:2973-2978.
16. Gimeno L, Brulet P, Martinez S. 2003. Study of Fgf15 gene expression in developing mouse brain. Gene Expr Patterns 3:473-481.
17. Goldowitz D, Hamre K. 1998. The cells and molecules that make a cerebellum. Trends Neurosci 21:375-382.
18. Hajihosseini MK, Dickson C. 1999. A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol Cell Neurosci 14:468-485.
19. Han JK, Martin GR. 1993. Embryonic expression of Fgf-6 is restricted to the skeletal muscle lineage. Dev Biol 158:549-554.
20. Hashimoto M, Mikoshiba K. 2003. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J Neurosci 23:11342-11351.
21. Hatten ME, Heintz N. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385-408.
22. Hattori Y, Miyake A, Mikami T, Ohta M, Itoh N. 1997. Transient expression of FGF-5 mRNA in the rat cerebellar cortex during post-natal development. Brain Res Mol Brain Res 47:262-266.
23. Hawkes R, Eisenman LM. 1997. Stripes and zones: the origins of regionalization of the adult cerebellum. Perspect Dev Neurobiol 5:95-105.
24. Hawkes R, Gravel C. 1991. The modular cerebellum. Prog Neurobiol 36:309-327.
25. Hebert JM, Rosenquist T, Gotz J, Martin GR. 1994. FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 78:1017-1025.
26. Herrup K, Kuemerle B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61-90.
27. Hoshikawa M, Ohbayashi N, Yonamine A, Konishi M, Ozaki K, Fukui S, Itoh N. 1998. Structure and expression of a novel fibroblast growth factor, FGF-17, preferentially expressed in the embryonic brain. Biochem Biophys Res Commun 244:187-191.
28. Ilagan R, Abu-Issa R, Brown D, Yang YP, Jiao K, Schwartz RJ, Klingensmith J, Meyers EN. 2006. Fgf8 is required for anterior heart field development. Development 133:2435-2445.
29. Inouye M, Oda SI. 1980. Strain-specific variations in the folial pattern of the mouse cerebellum. J Comp Neurol 190:357-362.
30. Irving C, Mason I. 2000. Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 127:177-186.
31. Itoh N, Ornitz DM. 2004. Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563-569.
32. Itoh N, Ornitz DM. 2008. Functional evolutionary history of the mouse Fgf gene family. Dev Dyn 237:18-27.
33. Johnson DE, Williams LT. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60:1-41.
34. Klein OD, Lyons DB, Balooch G, Marshall GW, Basson MA, Peterka M, Boran T, Peterkova R, Martin GR. 2008. An FGF signaling loop sustains the generation of differentiated progeny from stem cells in mouse incisors. Development 135:377-385.
35. Komuro H, Yacubova E. 2003. Recent advances in cerebellar granule cell migration. Cell Mol Life Sci 60:1084-1098.
36. Larouche M, Hawkes R. 2006. From clusters to stripes: the developmental origins of adult cerebellar compartmentation. Cerebellum 5:77-88.
37. Lin Y, Chen L, Lin C, Luo Y, Tsai RY, Wang F. 2009. Neuron-derived FGF9 is essential for scaffold formation of Bergmann radial fibers and migration of granule neurons in the cerebellum. Dev Biol 329:44-54.
38. Liu A, Li JY, Bromleigh C, Lao Z, Niswander LA, Joyner AL. 2003. FGF17b and FGF18 have different midbrain regulatory properties from FGF8b or activated FGF receptors. Development 130:6175-6185.
39. Lordkipanidze T, Dunaevsky A. 2005. Purkinje cell dendrites grow in alignment with Bergmann glia. Glia 51:229-234.
40. Machold R, Fishell G. 2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24.
41. Mahmood R, Bresnick J, Hornbruch A, Mahony C, Morton N, Colquhoun K, Martin P, Lumsden A, Dickson C, Mason I. 1995. A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr Biol 5:797-806.
42. Manni E, Petrosini L. 2004. A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 5:241-249.
43. Martinez S, Crossley PH, Cobos I, Rubenstein JL, Martin GR. 1999. FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 126:1189-1200.
44. Marzban H, Hawkes R. 2007. Fibroblast growth factor promotes the development of deep cerebellar nuclear neurons in dissociated mouse cerebellar cultures. Brain Res 1141:25-36.
45. Mason I. 2007. Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci 8:583-596.
46. Matsuda S, Ii Y, Desaki J, Yoshimura H, Okumura N, Sakanaka M. 1994. Development of Purkinje cell bodies and processes with basic fibroblast growth factor-like immunoreactivity in the rat cerebellum. Neuroscience 59:651-662.
47. McAndrew PE, Frostholm A, Evans JE, Zdilar D, Goldowitz D, Chiu IM, Burghes AH, Rotter A. 1998. Novel receptor protein tyrosine phosphatase (RPTPrho) and acidic fibroblast growth factor (FGF-1) transcripts delineate a rostrocaudal boundary in the granule cell layer of the murine cerebellar cortex. J Comp Neurol 391:444-455.
48. Meyers EN, Lewandoski M, Martin GR. 1998. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18:136-141.
49. Miale IL, Sidman RL. 1961. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4:277-296.
50. Miyake A, Minami M, Satoh M, Ohta M, Itoh N. 1995. Transient expression of FGF receptor-4 mRNA in the rat cerebellum during postnatal development. Brain Res Mol Brain Res 31:95-100.
51. Morales D, Hatten ME. 2006. Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J Neurosci 26:12226-12236.
52. Nakamura S, Todo T, Motoi Y, Haga S, Aizawa T, Ueki A, Ikeda K. 1999. Glial expression of fibroblast growth factor-9 in rat central nervous system. Glia 28:53-65.
53. Nakamura H, Watanabe Y. 2005. Isthmus organizer and regionalization of the mesencephalon and metencephalon. Int J Dev Biol 49:231-235.
54. O'Hagan RC, Hassell JA. 1998. The PEA3 Ets transcription factor is a downstream target of the HER2/Neu receptor tyrosine kinase. Oncogene 16:301-310.
55. Oberdick J, Baader SL, Schilling K. 1998. From zebra stripes to postal zones: deciphering patterns of gene expression in the cerebellum. Trends Neurosci 21:383-390.
56. Ohbayashi N, Shibayama M, Kurotaki Y, Imanishi M, Fujimori T, Itoh N, Takada S. 2002. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev 16:870-879.
57. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. 1998. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci U S A 95:5672-5677.
58. Ozawa K, Uruno T, Miyakawa K, Seo M, Imamura T. 1996. Expression of the fibroblast growth factor family and their receptor family genes during mouse brain development. Brain Res Mol Brain Res 41:279-288.
59. Partanen J. 2007. FGF signalling pathways in development of the midbrain and anterior hindbrain. J Neurochem 101:1185-1193.
60. Pringle NP, Yu WP, Howell M, Colvin JS, Ornitz DM, Richardson WD. 2003. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130:93-102.
61. Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M. 1998. Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125:2381-2395.
62. Roehl H, Nusslein-Volhard C. 2001. Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr Biol 11:503-507.
63. Saarimaki-Vire J, Peltopuro P, Lahti L, Naserke T, Blak AA, Vogt Weisenhorn DM, Yu K, Ornitz DM, Wurst W, Partanen J. 2007. Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J Neurosci 27:8581-8592.
64. Schnurch H, Risau W. 1991. Differentiating and mature neurons express the acidic fibroblast growth factor gene during chick neural development. Development 111:1143-1154.
65. Shamim H, Mahmood R, Logan C, Doherty P, Lumsden A, Mason I. 1999. Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 126:945-959.
66. Sillitoe RV, Joyner AL. 2007. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23:549-577.
67. Sillitoe RV, Gopal N, Joyner AL. 2008. Embryonic origins of ZebrinII parasagittal stripes and establishment of topographic Purkinje cell projections. Neuroscience [Epub ahead of print].
68. Sleeman M, Fraser J, McDonald M, Yuan S, White D, Grandison P, Kumble K, Watson JD, Murison JG. 2001. Identification of a new fibroblast growth factor receptor, FGFR5. Gene 271:171-182.
69. Sotelo C. 2004. Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295-339.
70. Sudarov A, Joyner AL. 2007. Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev 2:26.
71. Trokovic R, Trokovic N, Hernesniemi S, Pirvola U, Vogt Weisenhorn DM, Rossant J, McMahon AP, Wurst W, Partanen J. 2003. FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J 22:1811-1823.
72. Trokovic R, Jukkola T, Saarimaki J, Peltopuro P, Naserke T, Weisenhorn DM, Trokovic N, Wurst W, Partanen J. 2005. Fgfr1-dependent boundary cells between developing mid- and hindbrain. Dev Biol 278:428-439.
73. Trueb B, Taeschler S. 2006. Expression of FGFRL1, a novel fibroblast growth factor receptor, during embryonic development. Int J Mol Med 17:617-620.
74. Umemori H, Linhoff MW, Ornitz DM, Sanes JR. 2004. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257-270.
75. Wang VY, Zoghbi HY. 2001. Genetic regulation of cerebellar development. Nat Rev Neurosci 2:484-491.
76. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22:103-114.
77. Weinstein M, Xu X, Ohyama K, Deng CX. 1998. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125:3615-3623.
78. Wilcox BJ, Unnerstall JR. 1991. Expression of acidic fibroblast growth factor mRNA in the developing and adult rat brain. Neuron 6:397-409.
79. Wilkinson DG, Bhatt S, McMahon AP. 1989. Expression pattern of the FGF-related proto-oncogene int-2 suggests multiple roles in fetal development. Development 105:131-136.
80. Wingate RJ. 2001. The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11:82-88.
81. Xu J, Liu Z, Ornitz DM. 2000. Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127:1833-1843.
82. Yeh BK, Igarashi M, Eliseenkova AV, Plotnikov AN, Sher I, Ron D, Aaronson SA, Mohammadi M. 2003. Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc Natl Acad Sci U S A 100:2266-2271.
83. Yuasa S. 1996. Bergmann glial development in the mouse cerebellum as revealed by tenascin expression. Anat Embryol (Berl) 194:223-234.
84. Zervas M, Blaess S, Joyner AL. 2005. Classical embryological studies and modern genetic analysis of midbrain and cerebellum development. Curr Top Dev Biol 69:101-138.
85. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694-15700.