Essential role for ligand-dependent feedback antagonism of vertebrate hedgehog signaling by PTCH1, PTCH2 AND HHIP1 during neural patterning

Development (Cambridge)

Volumn 140, Issue 16, 2013, Pages 3423-3434

  Holtz, Alexander M ^a,b   Peterson, Kevin A ^c,i   Nishi, Yuichi ^c,i   Morin, Steves ^d   Song, Jane Y ^a   Charron, Frédéric ^d,e,f   Mcmahon, Andrew P ^c,g,h,i   Allen, Benjamin L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Harvard University   (United States)

^d CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f MCGILL UNIVERSITY   (Canada)

^g HARVARD STEM CELL INSTITUTE   (United States)

^h HARVARD UNIVERSITY   (United States)

ⁱ UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Hedgehog; Negative feedback; Neural tube

Indexed keywords

HEDGEHOG INTERACTING PROTEIN 1; PROTEIN PATCHED 1; PROTEIN PATCHED 2; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; MOUSE; NEGATIVE FEEDBACK; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VERTEBRATE;

HEDGEHOG; NEGATIVE FEEDBACK; NEURAL TUBE;

3T3 CELLS; ANIMALS; BODY PATTERNING; CARRIER PROTEINS; CHICK EMBRYO; EMBRYO, MAMMALIAN; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIGANDS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL TUBE; PROTEIN BINDING; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84880934981     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.095083     Document Type: Article

References (60)

1. Allen, B. L., Song, J. Y., Izzi, L., Althaus, I. W., Kang, J.-S., Charron, F., Krauss, R. S. and McMahon, A. P. (2011). Overlapping roles and collective requirement for the coreceptors GAS1, CDO, and BOC in SHH pathway function. Dev. Cell 20, 775-787.
2. Bae, G.-U., Domené, S., Roessler, E., Schachter, K., Kang, J.-S., Muenke, M. and Krauss, R. S. (2011). Mutations in CDON, encoding a hedgehog receptor, result in holoprosencephaly and defective interactions with other hedgehog receptors. Am. J. Hum. Genet. 89, 231-240.
3. Balaskas, N., Ribeiro, A., Panovska, J., Dessaud, E., Sasai, N., Page, K. M., Briscoe, J. and Ribes, V. (2012). Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 148, 273-284
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. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445.
6. Briscoe, J., Chen, Y., Jessell, T. M. and Struhl, G. (2001). A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 7, 1279-1291.
7. Capurro, M. I., Xu, P., Shi, W., Li, F., Jia, A. and Filmus, J. (2008). Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev. Cell 14, 700-711.
8. Carpenter, D., Stone, D. M., Brush, J., Ryan, A., Armanini, M., Frantz, G., Rosenthal, A. and de Sauvage, F. J. (1998). Characterization of two patched receptors for the vertebrate hedgehog protein family. Proc. Natl. Acad. Sci. USA 95, 13630-13634.
9. Chen, Y. and Struhl, G. (1996). Dual roles for patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
10. Chen, C. H., von Kessler, D. P., Park, W., Wang, B., Ma, Y. and Beachy, P. A. (1999). Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell 98, 305-316
11. Christ, A., Christa, A., Kur, E., Lioubinski, O., Bachmann, S., Willnow, T. E. and Hammes, A. (2012). LRP2 is an auxiliary SHH receptor required to condition the forebrain ventral midline for inductive signals. Dev. Cell 22, 268-278.
12. Chuang, P. T. and McMahon, A. P. (1999). Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397, 617-621
13. Chuang, P. T., Kawcak, T. and McMahon, A. P. (2003). Feedback control of mammalian Hedgehog signaling by the Hedgehog-binding protein, Hip1, modulates Fgf signaling during branching morphogenesis of the lung. Genes Dev. 17, 342-347.
14. Cooper, A. F., Yu, K. P., Brueckner, M., Brailey, L. L., Johnson, L., McGrath, J. M. and Bale, A. E. (2005). Cardiac and CNS defects in a mouse with targeted disruption of suppressor of fused. Development 132, 4407-4417
15. Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y. R. and Reiter, J. F. (2005). Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018-1021.
16. Dessaud, E., Yang, L. L., Hill, K., Cox, B., Ulloa, F., Ribeiro, A., Mynett, A., Novitch, B. G. and Briscoe, J. (2007). Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450, 717-720.
17. Dessaud, E., McMahon, A. P. and Briscoe, J. (2008). Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503.
18. Diez del Corral, R., Olivera-Martinez, I., Goriely, A., Gale, E., Maden, M. and Storey, K. (2003). Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40, 65-79.
19. Dudley, A. T. and Robertson, E. J. (1997). Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 208, 349-362.
20. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
21. Fan, Z., Li, J., Du, J., Zhang, H., Shen, Y., Wang, C.-Y. and Wang, S. (2008). A missense mutation in PTCH2 underlies dominantly inherited NBCCS in a Chinese family. J. Med. Genet. 45, 303-308.
22. Fan, Z., Du, J., Liu, H., Zhang, H., Dlugosz, A. A., Wang, C.-Y., Fan, M., Shen, Y. and Wang, S. (2009). A susceptibility locus on 1p32-1p34 for congenital macrostomia in a Chinese family and identification of a novel PTCH2 mutation. Am. J. Med. Genet. A. 149A, 521-524.
23. Freeman, M. (2000). Feedback control of intercellular signalling in development. Nature 408, 313-319.
24. Goodrich, L. V., Johnson, R. L., Milenkovic, L., McMahon, J. A. and Scott, M. P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 10, 301-312.
25. Goodrich, L. V., Milenković, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
26. Hooper, J. E. and Scott, M. P. (1989). The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751-765.
27. 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.
28. Hui, C. C. and Joyner, A. L. (1993). A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3, 241-246.
29. Ingham, P. W., Nystedt, S., Nakano, Y., Brown, W., Stark, D., van den Heuvel, M. and Taylor, A. M. (2000). Patched represses the Hedgehog signaling pathway by promoting modification of the Smoothened protein. Curr. Biol. 10, 1315-1318.
30. Izzi, L., Lévesque, M., Morin, S., Laniel, D., Wilkes, B. C., Mille, F., Krauss, R. S., McMahon, A. P., Allen, B. L. and Charron, F. (2011). Boc and Gas1 each form distinct Shh receptor complexes with Ptch1 and are required for Shh-mediated cell proliferation. Dev. Cell 20, 788-801.
31. Jeong, J. and McMahon, A. P. (2005). Growth and pattern of the mammalian neural tube are governed by partially overlapping feedback activities of the hedgehog antagonists patched 1 and Hhip1. Development 132, 143-154
32. Kawamura, S., Hervold, K., Ramirez-Weber, F.-A. and Kornberg, T. B. (2008). Two patched protein subtypes and a conserved domain of group I proteins that regulates turnover. J. Biol. Chem. 283, 30964-30969.
33. Kutejova, E., Briscoe, J. and Kicheva, A. (2009). Temporal dynamics of patterning by morphogen gradients. Curr. Opin. Genet. Dev. 19, 315-322.
34. Lee, Y., Miller, H. L., Russell, H. R., Boyd, K., Curran, T. and McKinnon, P. J. (2006). Patched2 modulates tumorigenesis in patched1 heterozygous mice. Cancer Res. 66, 6964-6971.
35. Li, F., Shi, W., Capurro, M. and Filmus, J. (2011). Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J. Cell Biol. 192, 691-704.
36. McMahon, A. P., Ingham, P. W. and Tabin, C. J. (2003). Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53, 1-114
37. 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.
38. Motoyama, J., Heng, H., Crackower, M. A., Takabatake, T., Takeshima, K., Tsui, L. C. and Hui, C. (1998a). Overlapping and non-overlapping Ptch2 expression with Shh during mouse embryogenesis. Mech. Dev. 78, 81-84
39. Motoyama, J., Takabatake, T., Takeshima, K. and Hui, C.-C. (1998b). Ptch2, a second mouse Patched gene is co-expressed with Sonic hedgehog. Nat. Genet. 18, 104-106.
40. Nakano, Y., Guerrero, I., Hidalgo, A., Taylor, A., Whittle, J. R. and Ingham, P. W. (1989). A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508-513
41. Nieuwenhuis, E., Motoyama, J., Barnfield, P. C., Yoshikawa, Y., Zhang, X., Mo, R., Crackower, M. A. and Hui, C.-C. (2006). Mice with a targeted mutation of patched2 are viable but develop alopecia and epidermal hyperplasia. Mol. Cell. Biol. 26, 6609-6622.
42. Novitch, B. G., Wichterle, H., Jessell, T. M. and Sockanathan, S. (2003). A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40, 81-95
43. Nybakken, K., Vokes, S. A., Lin, T.-Y., McMahon, A. P. and Perrimon, N. (2005). A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nat. Genet. 37, 1323-1332.
44. Okada, A., Charron, F., Morin, S., Shin, D. S., Wong, K., Fabre, P. J., Tessier-Lavigne, M. and McConnell, S. K. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
45. Parr, B. A., Shea, M. J., Vassileva, G. and McMahon, A. P. (1993). Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247-261.
46. Perrimon, N. and McMahon, A. P. (1999). Negative feedback mechanisms and their roles during pattern formation. Cell 97, 13-16.
47. Peterson, K. A., Nishi, Y., Ma, W., Vedenko, A., Shokri, L., Zhang, X., McFarlane, M., Baizabal, J.-M., Junker, J. P., van Oudenaarden, A. et al. (2012). Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning. Genes Dev. 26, 2802-2816.
48. Rahnama, F., Toftgård, R. and Zaphiropoulos, P. G. (2004). Distinct roles of PTCH2 splice variants in Hedgehog signalling. Biochem. J. 378, 325-334.
49. Ribes, V., Balaskas, N., Sasai, N., Cruz, C., Dessaud, E., Cayuso, J., Tozer, S., Yang, L. L., Novitch, B., Martí, E. et al. (2010). Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev. 24, 1186-1200.
50. 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.
51. Rohatgi, R., Milenkovic, L. and Scott, M. P. (2007). Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372-376.
52. Sockanathan, S., Perlmann, T. and Jessell, T. M. (2003). Retinoid receptor signaling in postmitotic motor neurons regulates rostrocaudal positional identity and axonal projection pattern. Neuron 40, 97-111.
53. Taipale, J., Cooper, M. K., Maiti, T. and Beachy, P. A. (2002). Patched acts catalytically to suppress the activity of Smoothened. Nature 418, 892-896
54. Tseng, T. T., Gratwick, K. S., Kollman, J., Park, D., Nies, D. H., Goffeau, A. and Saier, M. H., Jr (1999). The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1, 107-125.
55. Ulloa, F. and Briscoe, J. (2007). Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6, 2640-2649.
56. Vokes, S. A., Ji, H., McCuine, S., Tenzen, T., Giles, S., Zhong, S., Longabaugh, W. J. R., Davidson, E. H., Wong, W. H. and McMahon, A. P. (2007). Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134, 1977-1989.
57. Vokes, S. A., Ji, H., Wong, W. H. and McMahon, A. P. (2008). A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 22, 2651-2663
58. Wilkinson, D. G. (1992). In Situ Hybridization: A Practical Approach. Oxford, New York: IRL Press at Oxford University Press.
59. Xie, J., Murone, M., Luoh, S. M., Ryan, A., Gu, Q., Zhang, C., Bonifas, J. M., Lam, C. W., Hynes, M., Goddard, A. et al. (1998). Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391, 90-92
60. Xiong, F., Tentner, A. R., Huang, P., Gelas, A., Mosaliganti, K. R., Souhait, L., Rannou, N., Swinburne, I. A., Obholzer, N. D., Cowgill, P. D. et al. (2013). Specified neural progenitors sort to form sharp domains after noisy Shh signaling. Cell 153, 550-561.