FKBP8 is a negative regulator of mouse sonic hedgehog signaling in neural tissues

Development

Volumn 131, Issue 9, 2004, Pages 2149-2159

  Bulgakov, Oleg V ^a   Eggenschwiler, Jonathan T ^b,c   Hong, Dong Hyun ^a   Anderson, Kathryn V ^b   Li, Tiansen ^a  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

FKBP38; FKBP8; Mouse; Neural tube patterning; Signaling; Sonic hedgehog

Indexed keywords

FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 8; MEMBRANE PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FATE; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; GENE DISRUPTION; GENE EXPRESSION; GENE TARGETING; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE DEFECT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; EMBRYO; EYE; GENE TARGETING; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; PHENOTYPE; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS; TRANS-ACTIVATORS;

ANIMALIA; ERINACEIDAE; MAMMALIA;

EID: 2542555722     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01122     Document Type: Article

References (69)

1. Alvarez Martinez, C. E., Binato, R., Gonzalez, S., Pereira, M., Robert, B. and Abdelhay, E. (2002). Characterization of a Smad motif similar to Drosophila mad in the mouse Msx 1 promoter. Biochem. Biophys. Res. Commun. 291, 655-662.
2. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and de Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
3. Briscoe, J. and Ericson, J. (2001). Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49.
4. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T. M., Rubenstein, J. L. and Ericson, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627.
5. Cameron, A. M., Steiner, J. P., Roskams, A. J., Ali, S. M., Ronnett, G. V. and Snyder, S. H. (1995). Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83, 463-472.
6. Chen, Y. and Struhl, G. (1996). Dual roles for patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
7. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
8. Chuang, P. T. and McMahon, A. P. (1999). Vertebrate Hedgehog signalling modulated by induction of a Hedgehog- binding protein. Nature 397, 617-621.
9. Clipstone, N. A. and Crabtree, G. R. (1992). Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357, 695-697.
10. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
11. Eggenschwiler, J. T. and Anderson, K. V. (2000). Dorsal and lateral fates in the mouse neural tube require the cell-autonomous activity of the open brain gene. Dev. Biol. 227, 648-660.
12. Eggenschwiler, J. T., Espinoza, E. and Anderson, K. V. (2001). Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412, 194-198.
13. Ekker, S. C., Ungar, A. R., Greenstein, P., von Kessler, D. P., Porter, J. A., Moon, R. T. and Beachy, P. A. (1995). Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr. Biol. 5, 944-955.
14. Ericson, J., Briscoe, J., Rashbass, P., van Heyningen, V. and Jessell, T. M. (1997). Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 62, 451-466.
15. Furuta, Y., Piston, D. W. and Hogan, B. L. (1997). Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203-2212.
16. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
17. Gunther, T., Struwe, M., Aguzzi, A. and Schughart, K. (1994). Open brain, a new mouse mutant with severe neural tube defects, shows altered gene expression patterns in the developing spinal cord. Development 120, 3119-3130.
18. Hemenway, C. S. and Heitman, J. (1999). Calcineurin. Structure, function, and inhibition. Cell Biochem. Biophys. 30, 115-151.
19. Hill, R. E., Favor, J., Hogan, B. L., Ton, C. C., Saunders, G. F., Hanson, I. M., Prosser, J., Jordan, T., Hastie, N. D. and van Heyningen, V. (1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522-525.
20. Hong, D. H., Yue, G., Adamian, M. and Li, T. (2001). Retinitis pigmentosa GTPase regulator (RPGR)-interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J. Biol. Chem. 276, 12091-12099.
21. Huang, Y., Roelink, H. and McKnight, G. S. (2002). Protein kinase A deficiency causes axially localized neural tube defects in mice. J. Biol. Chem. 277, 19889-19896.
22. Huangfu, D., Liu, A., Rakeman, A. S., Murcia, N. S., Niswander, L. and Anderson, K. V. (2003). Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426, 83-87.
23. Hui, Y. N., Wu, Y. Q., Xiao, Q. S., Kirchhof, B. and Heimann, K. (1993). Repair of outer blood-retinal barrier after severe ocular blunt trauma in rabbits. Graefes Arch. Clin. Exp. Ophthalmol. 231, 365-369.
24. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
25. Ishibashi, M. and McMahon, A. P. (2002). A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development 129, 4807-4819.
26. Izraeli, S., Lowe, L. A., Bertness, V. L., Campaner, S., Hahn, H., Kirsch, I. R. and Kuehn, M. R. (2001). Genetic evidence that Sil is required for the Sonic Hedgehog response pathway. Genesis 31, 72-77.
27. Jayaraman, T., Brillantes, A. M., Timerman, A. P., Fleischer, S., Erdjument-Bromage, H., Tempst, P. and Marks, A. R. (1992). FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol. Chem. 267, 9474-9477.
28. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
29. Kernan, M., Cowan, D. and Zuker, C. (1994). Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12, 1195-1206.
30. Lee, K. J., Mendelsohn, M. and Jessell, T. M. (1998). Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev. 12, 3394-3407.
31. Lee, C. S., Buttitta, L. and Fan, C. M. (2001). Evidence that the WNT-inducible growth arrest-specific gene 1 encodes an antagonist of sonic hedgehog signaling in the somite. Proc. Natl. Acad. Sci. USA 98, 11347-11352.
32. Liem, K. F., Jr, Tremml, G., Roelink, H. and Jessell, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979.
33. Liem, K. F., Jr, Jessell, T. M. and Briscoe, J. (2000). Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127, 4855-4866.
34. Litingtung, Y. and Chiang, C. (2000). Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3, 979-985.
35. Macdonald, R., Barth, K. A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S. W. (1995). Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267-3278.
36. Marigo, V., Davey, R. A., Zuo, Y., Cunningham, J. M. and Tabin, C. J. (1996). Biochemical evidence that patched is the Hedgehog receptor. Nature 384, 176-179.
37. Marti, E. and Bovolenta, P. (2002). Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci. 25, 89-96.
38. Matise, M. P., Epstein, D. J., Park, H. L., Platt, K. A. and Joyner, A. L. (1998). Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770.
39. McCarthy, R. A., Barth, J. L., Chintalapudi, M. R., Knaak, C. and Argraves, W. S. (2002). Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277, 25660-25667.
40. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
41. Methot, N. and Basler, K. (2001). An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development 128, 733-742.
42. Milenkovic, L., Goodrich, L. V., Higgins, K. M. and Scott, M. P. (1999). Mouse patched1 controls body size determination and limb patterning. Development 126, 4431-4440.
43. Motoyama, J., Milenkovic, L., Iwama, M., Shikata, Y., Scott, M. P. and Hui, C. C. (2003). Differential requirement for Gli2 and Gli3 in ventral neural cell fate specification. Dev. Biol. 259, 150-161.
44. Muroyama, Y., Fujihara, M., Ikeya, M., Kondoh, H. and Takada, S. (2002). Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16, 548-553.
45. Nybakken, K. and Perrimon, N. (2002). Hedgehog signal transduction: recent findings. Curr. Opin. Genet. Dev. 12, 503-511.
46. Ohlmeyer, J. T. and Kalderon, D. (1998). Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396, 749-753.
47. Pathi, S., Pagan-Westphal, S., Baker, D. P., Garber, E. A., Rayhorn, P., Bumcrot, D., Tabin, C. J., Blake Pepinsky, R. and Williams, K. P. (2001). Comparative biological responses to human Sonic, Indian, and Desert hedgehog. Mech. Dev. 106, 107-117.
48. Pedersen, K. M., Finsen, B., Celis, J. E. and Jensen, N. A. (1999). muFKBP38: a novel murine immunophilin homolog differentially expressed in Schwannoma cells and central nervous system neurons in vivo. Electrophoresis 20, 249-255.
49. Perron, M., Boy, S., Amato, M. A., Viczian, A., Koebernick, K., Pieler, T. and Harris, W. A. (2003). A novel function for Hedgehog signalling in retinal pigment epithelium differentiation. Development 130, 1565-1577.
50. Persson, M., Stamataki, D., te Welscher, P., Andersson, E., Bose, J., Ruther, U., Ericson, J. and Briscoe, J. (2002). Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16, 2865-2878.
51. Pierani, A., Brenner-Morton, S., Chiang, C. and Jessell, T. M. (1999). A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915.
52. Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M. and Jessell, T. M. (2001). Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29, 367-384.
53. Price, M. A. and Kalderon, D. (1999). Proteolysis of cubitus interruptus in Drosophila requires phosphorylation by protein kinase A. Development 126, 4331-4339.
54. Ray, K., Perez, S. E., Yang, Z., Xu, J., Ritchings, B. W., Steller, H. and Goldstein, L. S. (1999). Kinesin-II is required for axonal transport of choline acetyltransferase in Drosophila. J. Cell Biol. 147, 507-518.
55. Robbins, D. J., Nybakken, K. E., Kobayashi, R., Sisson, J. C., Bishop, J. M. and Therond, P. P. (1997). Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90, 225-234.
56. Roelink, H., Porter, J. A., Chiang, C., Tanabe, Y., Chang, D. T., Beachy, P. A. and Jessell, T. M. (1995). Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81, 445-455.
57. Sasaki, H. and Hogan, B. L. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
58. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). 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 124, 1313-1322.
59. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
60. Shirane, M. and Nakayama, K. I. (2003). Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis. Nat. Cell Biol. 5, 28-37.
61. Shoji, H., Ito, T., Wakamatsu, Y., Hayasaka, N., Ohsaki, K., Oyanagi, M., Kominami, R., Kondoh, H. and Takahashi, N. (1996). Regionalized expression of the Dbx family homeobox genes in the embryonic CNS of the mouse. Mech. Dev. 56, 25-39.
62. Snyder, S. H., Lai, M. M. and Burnett, P. E. (1998). Immunophilins in the nervous system. Neuron 21, 283-294.
63. te Welscher, P., Zuniga, A., Kuijper, S., Drenth, T., Goedemans, H. J., Meijlink, F. and Zeller, R. (2002). Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298, 827-830.
64. Therond, P. P., Limbourg Bouchon, B., Gallet, A., Dussilol, F., Pietri, T., van den Heuvel, M. and Tricoire, H. (1999). Differential requirements of the fused kinase for hedgehog signalling in the Drosophila embryo. Development 126, 4039-4051.
65. Walther, C. and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
66. Wang, B., Fallon, J. F. and Beachy, P. A. (2000). Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100, 423-434.
67. Wijgerde, M., McMahon, J. A., Rule, M. and McMahon, A. P. (2002). A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 16, 2849-2864.
68. Young, J. C., Barral, J. M. and Ulrich Hartl, F. (2003). More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28, 541-547.
69. Zhang, X. M., Ramalho-Santos, M. and McMahon, A. P, (2001). Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R asymmetry by the mouse node. Cell 105, 781-792.