A novel role of the hedgehog pathway in lens regeneration

Developmental Biology

Volumn 267, Issue 2, 2004, Pages 450-461

  Tsonis, Panagiotis A ^a   Vergara, M Natalia ^b   Spence, Jason R ^b   Madhavan, Mayur ^b   Kramer, Elizabeth L ^b   Call, Mindy K ^a   Santiago, William G ^a   Vallance, Jefferson E ^c   Robbins, David J ^c   Del Rio Tsonis, Katia ^b  

^a UNIVERSITY OF DAYTON   (United States)

^b MIAMI UNIVERSITY   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

HIP; Ihh; KAAD; Lens; ptc 1; ptc 2; Regeneration; Shh; Transdifferentiation

Indexed keywords

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

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EYE DEVELOPMENT; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LENS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGENERATION; SIGNAL TRANSDUCTION;

ERINACEIDAE; SALAMANDRIDAE;

EID: 12144288186     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.12.005     Document Type: Article

References (63)

1. 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. 14(3):1996;353-356.
2. Brockes J.P., Kumar A. Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat. Rev., Mol. Cell Biol. 3(8):2002;566-574.
3. Carpenter D., Stone D.M., Brush J., Ryan A., Armanini M., Frantz G., Rosenthal A., de Sauvage F.J. Characterization of two patched receptors for the vertebrate hedgehog protein family. Proc. Natl. Acad. Sci. U. S. A. 95(23):1998;13630-13634.
4. Chen J.K., Taipale J., Cooper M.K., Beachy P.A. Inhibition of hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16(21):2002;2743-2748.
5. 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. 383(6599):1996;407-413.
6. Chuang P.T., McMahon A.P. Vertebrate hedgehog signaling modulated by induction of a hedgehog-binding protein. Nature. 397(6720):1999;617-621.
7. Cooper M.K., Porter J.A., Young K.E., Beachy P.A. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science. 280(5369):1998;1603-1607.
8. Del Rio-Tsonis K., Tsonis P.A. Eye regeneration at the molecular age. Dev. Dyn. 226(2):2003;211-224.
9. Del Rio-Tsonis K., Tomarev S.I., Tsonis P.A. Regulation of Prox 1 during lens regeneration. Invest. Ophthalmol. Vis. Sci. 40(9):1999;2039-2045.
10. Drossopoulou G., Lewis K.E., Sanz-Ezquerro J.J., Nikbakht N., McMahon A.P., Hofmann C., Tickle C. A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signaling and Bmp signaling. Development. 127(7):2000;1337-1348.
11. Eguchi G. Transdifferentiation as the basis of eye lens regeneration. Ferreti P., Géraudie J. Cellular and Molecular Basis of Regeneration. From Invertebrates to Humans. 1998;207-228 Wiley, Chichester.
12. Eguchi G., Shingai R. Cellular analysis on localization of lens forming potency in the newt iris epithelium. Dev. Growth Differ. 13:1971;337-349.
13. Ekker S.C., Ungar A.R., Greenstein P., von Kessler D.P., Porter J.A., Moon R.T., Beachy P.A. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr. Biol. 5(8):1995;944-955.
14. Endo T., Yokoyama H., Tamura K., Ide H. Shh expression in developing and regenerating limb buds of Xenopus laevis. Dev. Dyn. 209(2):1997;227-232.
15. Ericson J., Morton S., Kawakami A., Roelink H., Jessell T.M. Two critical periods of sonic hedgehog signaling required for the specification of motor neuron identity. Cell. 87(4):1996;661-673.
16. Ferguson C., Alpern E., Miclau T., Helms J.A. Does adult fracture repair recapitulate embryonic skeletal formation? Mech. Dev. 87(1-2):1999;57-66.
17. Gritli-Linde A., Lewis P., McMahon A.P., Linde A. The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev. Biol. 236(2):2001;364-386.
18. Huh S., Hatini V., Marcus R.C., Li S.C., Lai E. Dorsal-ventral patterning defects in the eye of BF-1-deficient mice associated with a restricted loss of shh expression. Dev. Biol. 211(1):1999;53-63.
19. Imokawa Y., Yoshizato K. Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. Proc. Natl. Acad. Sci. U. S. A. 94(17):1997;9159-9164.
20. Incardona J.P., Gaffield W., Kapur R.P., Roelink H. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development. 125(18):1998;3553-3562.
21. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15(23):2001;3059-3087.
22. Ito H., Akiyama H., Shigeno C., Iyama K., Matsuoka H., Nakamura T. Hedgehog signaling molecules in bone marrow cells at the initial stage of fracture repair. Biochem. Biophys. Res. Commun. 262(2):1999;443-451.
23. Khan P.A., Tsilfidis C., Liversage R.A. Hox C6 expression during development and regeneration of forelimbs in larval Notophthalmus viridescens. Dev. Genes Evol. 209(6):1999;323-329.
24. Kondoh H., Uchikawa M., Yoda H., Takeda H., Furutani-Seiki M., Karlstrom R.O. Zebrafish mutations in Gli-mediated hedgehog signaling lead to lens transdifferentiation from the adenohypophysis anlage. Mech. Dev. 96(2):2000;165-174.
25. Laforest L., Brown C.W., Poleo G., Geraudie J., Tada M., Ekker M., Akimenko M.A. Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development. 125(21):1998;4175- 4184.
26. Lai K., Kaspar B.K., Gage F.H., Schaffer D.V. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6(1):2003;21-27.
27. Levine E.M., Roelink H., Turner J., Reh T.A. Sonic hedgehog promotes rod photoreceptor differentiation in mammalian retinal cells in vitro. J. Neurosci. 17(16):1997;6277-6288.
28. Lewis P.M., Dunn M.P., McMahon J.A., Logan M., Martin J.F., St-Jacques B., McMahon A.P. Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell. 105(5):2001;599-612.
29. Macdonald R., Barth K.A., Xu Q., Holder N., Mikkola I., Wilson S.W. Midline signaling is required for Pax gene regulation and patterning of the eyes. Development. 121(10):1995;3267-3278.
30. Marigo V., Davey R.A., Zuo Y., Cunningham J.M., Tabin C.J. Biochemical evidence that patched is the hedgehog receptor. Nature. 384(6605):1996;176-179.
31. Murakami S., Noda M. Expression of Indian hedgehog during fracture healing in adult rat femora. Calcif. Tissue Int. 66(4):2000;272-276.
32. Neumann C.J., Nuesslein-Volhard C. Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science. 289(5487):2000;2137-2139.
33. Panman L., Zeller R. Patterning the limb before and after SHH signaling. J. Anat. 202(1):2003;3-12.
34. Perron M., Boy S., Amato M.A., Viczian A., Koebernick K., Pieler T., Harris W.A. A novel function for hedgehog signaling in retinal pigment epithelium differentiation. Development. 130(8):2003;1565-1577.
35. Quint E., Smith A., Avaron F., Laforest L., Miles J., Gaffield W., Akimenko M.A. Bone patterning is altered in the regenerating zebrafish caudal fin after ectopic expression of sonic hedgehog and bmp2b or exposure to cyclopamine. Proc. Natl. Acad. Sci. U. S. A. 99(13):2002;8713-8718.
36. Reyer R.W. The amphibian eye: development and regeneration. Crescitelli F. Handbook of Sensory Physiology. The visual system in vertebrates. vol. II/5:1977;309-390 Springer-Verlag, Berlin.
37. Riddle R.D., Johnson R.L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75(7):1993;1401-1416.
38. 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. 14(3):1996;357-360.
39. 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. 19(20):1999;8954-8965.
40. Roy S., Gardiner D.M. Cyclopamine induces digit loss in regenerating axolotl limbs. J. Exp. Zool. 293(2):2002;186-190.
41. Roy S., Gardiner D.M., Bryant S.V. Vaccinia as a tool for functional analysis in regenerating limbs: ectopic expression of Shh. Dev. Biol. 218(2):2000;199-205.
42. Sasagawa S., Takabatake T., Takabatake Y., Muramatsu T., Takeshima K. Axes establishment during eye morphogenesis in Xenopus by coordinate and antagonistic actions of BMP4, Shh, and RA. Genesis. 33(2):2002;86-96.
43. Sawada K., Agata K., Yoshiki A., Eguchi G. A set of anti-crystallin monoclonal ant ibodies for detecting lens specificities: beta-crystallin as a specific marker for detecting lentoidogenesis in cultures of chicken lens epithelial cells. Jpn. J. Ophthalmol. 37:1993;355-368.
44. Schauerte H.E., van Eeden F.J., Fricke C., Odenthal J., Strahle U., Haffter P. Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development. 125(15):1998;2983-2993.
45. Stark D.R., Gates P.B., Brockes J.P., Ferretti P. Hedgehog family member is expressed throughout regenerating and developing limbs. Dev. Dyn. 212(3):1998;352-363.
46. Stenkamp D.L., Frey R.A., Prabhudesai S.N., Raymond P.A. Function for hedgehog genes in zebrafish retinal development. Dev. Biol. 220(2):2000;238-252.
47. Stone D.M., Hynes M., Armanini M., Swanson T.A., Gu Q., Johnson R.L., Scott M.P., Pennica D., Goddard A., Phillips H., Noll M., Hooper J.E., de Sauvage F., Rosenthal A. The tumor-suppressor gene patched encodes a candidate receptor for sonic hedgehog. Nature. 384(6605):1996;129-134.
48. Taipale J., Chen J.K., Cooper M.K., Wang B., Mann R.K., Milenkovic L., Scott M.P., Beachy P.A. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature. 406(6799):2000;1005-1009.
49. Takabatake T., Ogawa M., Takahashi T.C., Mizuno M., Okamoto M., Takeshima K. Hedgehog and patched gene expression in adult ocular tissues. FEBS Lett. 410(2-3):1997;485-489.
50. Torok M.A., Gardiner D.M., Izpisua-Belmonte J.C., Bryant S.V. Sonic hedgehog (shh) expression in developing and regenerating axolotl limbs. J. Exp. Zool. 284(2):1999;197-206.
51. Tsonis P.A. Regeneration in vertebrates. Dev. Biol. 221:2000;273-284.
52. Tsonis P.A. Regenerative biology. The emerging field of tissue repair and restoration. Differentiation. 70(8):2002;397-409.
53. Tsonis P.A., Jang W., Del Rio-Tsonis K., Eguchi G. A human pigment epithelium cell line as a model for lens transdifferentiation. Int. J. Dev. Biol. 45(5-6):2001;753-758.
54. Vortkamp A., Pathi S., Peretti G.M., Caruso E.M., Zaleske D.J., Tabin C.J. Recapitulation of signals regulating embryonic bone formation during postnatal growth and in fracture repair. Mech. Dev. 71(1-2):1998;65-76.
55. Wallace V.A., Raff M.C. A role for sonic hedgehog in axon-to-astrocyte signaling in the rodent optic nerve. Development. 126(13):1999;2901-2909.
56. Wang Y.P., Dakubo G., Howley P., Campsall K.D., Mazarolle C.J., Shiga S.A., Lewis P.M., McMahon A.P., Wallace V.A. Development of normal retinal organization depends on Sonic hedgehog signaling from ganglion cells. Nat. Neurosci. 5(9):2002;831-832.
57. Wetmore C. Sonic hedgehog in normal and neoplastic proliferation: insight gained from human tumors and animal models. Curr. Opin. Genet Dev. 13(1):2003;34-42.
58. Wijgerde M., McMahon J.A., Rule M., McMahon A.P. A direct requirement for hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 16(22):2002;2849-2864.
59. Yang Y., Drossopoulou G., Chuang P.T., Duprez D., Marti E., Bumcrot D., Vargesson N., Clarke J., Niswander L., McMahon A., Tickle C. Relationship between dose, distance and time in sonic hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development. 124(21):1997;4393-4404.
60. Yu J., Carroll T.J., McMahon A.P. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development. 129(22):2002;5301-5312.
61. Zeng X., Goetz J.A., Suber L.M., Scott W.J. Jr., Schreiner C.M., Robbins D.J. A freely diffusible form of Sonic hedgehog mediates long-range signaling. Nature. 411(6838):2001;716-720.
62. Zhang X.M., Yang X.J. Temporal and spatial effects of sonic hedgehog signaling in chick eye morphogenesis. Dev. Biol. 233:2001;271-290.
63. Zhang X.M., Yang X.J. Regulation of retinal ganglion cell production by Sonic hedgehog. Development. 128(6):2001;943-957.