Hedgehog On The Move: A Precise Spatial Control Of Hedgehog Dispersion Shapes The Gradient

Current Opinion in Genetics and Development

Volumn 23, Issue 4, 2013, Pages 363-373

  Gradilla, Ana Citlali ^a   Guerrero, Isabel ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BROTHER OF IHOG CORECEPTOR; CELL RECEPTOR; CHOLESTEROL; GLYPICAN; INSECT PROTEIN; INTERFERENCE HEDGEHOG CORECEPTOR; LIPOPHORIN; MEMBRANE PROTEIN; MORPHOGEN; OLIGOMER; PROTEASOME; PROTEIN DALLY; PROTEIN DISPATCHED; PROTEIN DLP; PROTEIN PATCHED; PROTEIN SCUBE 2; PROTEIN SHIFTED; PROTEOHEPARAN SULFATE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT INHIBITORY FACTOR 1; DROSOPHILA PROTEIN; HEDGEHOG PROTEIN, DROSOPHILA;

AMINO TERMINAL SEQUENCE; CELL CONTACT; CELL DIFFERENTIATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CYTONEME; CYTOPLASM VESICLE; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; EPITHELIUM; EXOSOME; EXTRACELLULAR MATRIX; FORELIMB; HOLOPROSENCEPHALY; HUMAN; HYDROPHOBICITY; INTERNALIZATION; MULTIVESICULAR BODY; NONHUMAN; OLIGOMERIZATION; PALMITOYLATION; PHOTORECEPTOR; PLASTICITY; POLARIZATION; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; ANIMAL; CHEMICAL PHENOMENA; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM;

ERINACEIDAE;

ANIMALS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID METABOLISM; SIGNAL TRANSDUCTION; WING;

EID: 84883451581     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2013.04.011     Document Type: Review

References (92)

1. Beachy P.A., Karhadkar S.S., Berman D.M. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004, 432:324-331.
2. Nieuwenhuis E., Hui C.C. Hedgehog signaling and congenital malformations. Clin Genet 2005, 67:193-208.
3. Porter J.A., Young K.E., Beachy P.A. Cholesterol modification of hedgehog signaling proteins in animal development. Science 1996, 274:255-259.
4. Lee J.J., Ekker S.C., von Kessler D.P., Porter J.A., Sun B.I., Beachy P.A. Autoproteolysis in hedgehog protein biogenesis. Science 1994, 266:1528-1537.
5. Lee J.D., Treisman J.E. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr Biol 2001, 11:1147-1152.
6. Pepinsky R.B., Zeng C., Wen D., Rayhorn P., Baker D.P., Williams K.P., Bixler S.A., Ambrose C.M., Garber E.A., Miatkowski K., et al. Identification of a palmitic acid-modified form of human Sonic hedgehog. J Biol Chem 1998, 273:14037-14045.
7. Micchelli C.A., The I., Selva E., Mogila V., Perrimon N. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 2002, 129:843-851.
8. Amanai K., Jiang J. Distinct roles of Central missing and Dispatched in sending the Hedgehog signal. Development 2001, 128:5119-5127.
9. Willert K., Brown J.D., Danenberg E., Duncan A.W., Weissman I.L., Reya T., Yates J.R., Nusse R. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003, 423:448-452.
10. Chamoun Z., Mann R.K., Nellen D., von Kessler D.P., Bellotto M., Beachy P.A., Basler K. Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 2001, 293:2080-2084.
11. Steinhauer J., Treisman J.E. Lipid-modified morphogens: functions of fats. Curr Opin Genet Dev 2009, 19:308-314.
12. Guerrero I., Chiang C. A conserved mechanism of Hedgehog gradient formation by lipid modifications. Trends Cell Biol 2007, 17:1-5.
13. Chen M.H., Li Y.J., Kawakami T., Xu S.M., Chuang P.T. Palmitoylation is required for the production of a soluble multimeric Hedgehog protein complex and long-range signaling in vertebrates. Genes Dev 2004, 18:641-659.
14. Roessler E., El-Jaick K.B., Dubourg C., Velez J.I., Solomon B.D., Pineda-Alvarez D.E., Lacbawan F., Zhou N., Ouspenskaia M., Paulussen A., et al. The mutational spectrum of holoprosencephaly-associated changes within the SHH gene in humans predicts loss-of-function through either key structural alterations of the ligand or its altered synthesis. Hum Mutat 2009, 30:E921-E935.
15. Chen X., Tukachinsky H., Huang C.H., Jao C., Chu Y.R., Tang H.Y., Mueller B., Schulman S., Rapoport T.A., Salic A. Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. J Cell Biol 2011, 192:825-838.
16. Tokhunts R., Singh S., Chu T., D'Angelo G., Baubet V., Goetz J.A., Huang Z., Yuan Z., Ascano M., Zavros Y., et al. The full-length unprocessed hedgehog protein is an active signaling molecule. J Biol Chem 2010, 285:2562-2568.
17. Palm W., Swierczynska M.M., Kumari V., Ehrhart-Bornstein M., Bornstein S.R., Eaton S. Secretion and signaling activities of lipoprotein-associated hedgehog and non-sterol-modified hedgehog in flies and mammals. PLoS Biol 2013, 11:e1001505.
18. Callejo A., Torroja C., Quijada L., Guerrero I. Hedgehog lipid modifications are required for Hedgehog stabilization in the extracellular matrix. Development 2006, 133:471-483.
19. Gallet A., Ruel L., Staccini-Lavenant L., Therond P.P. Cholesterol modification is necessary for controlled planar long-range activity of Hedgehog in Drosophila epithelia. Development 2006, 133:407-418.
20. Peters C., Wolf A., Wagner M., Kuhlmann J., Waldmann H. The cholesterol membrane anchor of the Hedgehog protein confers stable membrane association to lipid-modified proteins. Proc Natl Acad Sci U S A 2004, 101:8531-8536.
21. 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 2001, 105:599-612.
22. Li Y., Zhang H., Litingtung Y., Chiang C. Cholesterol modification restricts the spread of Shh gradient in the limb bud. Proc Natl Acad Sci U S A 2006, 103:6548-6553.
23. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 1998, 394:85-88.
24. Bornemann D.J., Duncan J.E., Staatz W., Selleck S., Warrior R. Abrogation of heparan sulfate synthesis in Drosophila disrupts the Wingless, Hedgehog and Decapentaplegic signaling pathways. Development 2004, 131:1927-1938.
25. Takei Y., Ozawa Y., Sato M., Watanabe A., Tabata T Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 2004, 131:73-82.
26. The I., Bellaiche Y., Perrimon N. Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol Cell 1999, 4:633-639.
27. Gallet A., Rodriguez R., Ruel L., Therond P.P. Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetric cellular response to hedgehog. Dev Cell 2003, 4:191-204.
28. Burke R., Nellen D., Bellotto M., Hafen E., Senti K.A., Dickson B.J., Basler K. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 1999, 99:803-815.
29. Ma Y., Erkner A., Gong R., Yao S., Taipale J., Basler K., Beachy P.A. Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 2002, 111:63-75.
30. Callejo A., Bilioni A., Mollica E., Gorfinkiel N., Andres G., Ibanez C., Torroja C., Doglio L., Sierra J., Guerrero I. Dispatched mediates Hedgehog basolateral release to form the long-range morphogenetic gradient in the Drosophila wing disk epithelium. Proc Natl Acad Sci U S A 2011, 108:12591-12598.
31. Ohlig S., Farshi P., Pickhinke U., Van Den Boom J., Hoing S., Jakuschev S., Hoffmann D., Dreier R., Scholer H.R., Dierker T., et al. Sonic hedgehog shedding results in functional activation of the solubilized protein. Dev Cell 2011, 20:764-774.
32. Taylor F.R., Wen D., Garber E.A., Carmillo A.N., Baker D.P., Arduini R.M., Williams K.P., Weinreb P.H., Rayhorn P., Hronowski X., et al. Enhanced potency of human Sonic hedgehog by hydrophobic modification. Biochemistry 2001, 40:4359-4371.
33. Lee J.D., Kraus P., Gaiano N., Nery S., Kohtz J., Fishell G., Loomis C.A., Treisman J.E. An acylatable residue of Hedgehog is differentially required in Drosophila and mouse limb development. Dev Biol 2001, 233:122-136.
34. Bilioni A., Sanchez-Hernandez D., Callejo A., Gradilla A.C., Ibanez C., Mollica E., Carmen Rodriguez-Navas M., Simon E., Guerrero I. Balancing hedgehog, a retention and release equilibrium given by Dally, Ihog, Boi and shifted/dWif. Dev Biol 2013, 376:198-212.
35. Ayers K.L., Gallet A., Staccini-Lavenant L., Therond P.P. The long-range activity of Hedgehog is regulated in the apical extracellular space by the glypican Dally and the hydrolase Notum. Dev Cell 2010, 18:605-620.
36. Ayers K.L., Mteirek R., Cervantes A., Lavenant-Staccini L., Therond P.P., Gallet A. Dally and Notum regulate the switch between low and high level Hedgehog pathway signalling. Development 2012, 139:3168-3179.
37. Torroja C., Gorfinkiel N., Guerrero I. Patched controls the Hedgehog gradient by endocytosis in a dynamin-dependent manner, but this internalization does not play a major role in signal transduction. Development 2004, 131:2395-2408.
38. Liegeois S., Benedetto A., Garnier J.M., Schwab Y., Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol 2006, 173:949-961.
39. Huang Z., Kunes S. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 1996, 86:411-422.
40. Chu T., Chiu M., Zhang E., Kunes S. A C-terminal motif targets Hedgehog to axons, coordinating assembly of the Drosophila eye and brain. Dev Cell 2006, 10:635-646.
41. Song Y., Chung S., Kunes S. Combgap relays wingless signal reception to the determination of cortical cell fate in the Drosophila visual system. Mol Cell 2000, 6:1143-1154.
42. Tian H., Jeong J., Harfe B.D., Tabin C.J., McMahon A.P. Mouse Disp1 is required in sonic hedgehog-expressing cells for paracrine activity of the cholesterol-modified ligand. Development 2005, 132:133-142.
43. Etheridge L.A., Crawford T.Q., Zhang S., Roelink H. Evidence for a role of vertebrate Disp1 in long-range Shh signaling. Development 2010, 137:133-140.
44. Tukachinsky H., Kuzmickas R.P., Jao C.Y., Liu J., Salic A. Dispatched and scube mediate the efficient secretion of the cholesterol-modified hedgehog ligand. Cell Rep 2012, 2:308-320.
45. Takeo S., Akiyama T., Firkus C., Aigaki T., Nakato H. Expression of a secreted form of Dally, a Drosophila glypican, induces overgrowth phenotype by affecting action range of Hedgehog. Dev Biol 2005, 284:204-218.
46. Lum L., Yao S., Mozer B., Rovescalli A., Von Kessler D., Nirenberg M., Beachy P.A. Identification of Hedgehog pathway components by RNAi in Drosophila cultured cells. Science 2003, 299:2039-2045.
47. Desbordes S.C., Sanson B. The glypican Dally-like is required for Hedgehog signalling in the embryonic epidermis of Drosophila. Development 2003, 130:6245-6255.
48. Han C., Belenkaya T.Y., Khodoun M., Tauchi M., Lin X., Lin X. Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development 2004, 131:1563-1575.
49. Williams E.H., Pappano W.N., Saunders A.M., Kim M.S., Leahy D.J., Beachy P.A. Dally-like core protein and its mammalian homologues mediate stimulatory and inhibitory effects on Hedgehog signal response. Proc Natl Acad Sci U S A 2010, 107:5869-5874.
50. Gallet A., Staccini-Lavenant L., Therond P.P. Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis. Dev Cell 2008, 14:712-725.
51. Zheng X., Mann R.K., Sever N., Beachy P.A. Genetic and biochemical definition of the Hedgehog receptor. Genes Dev 2010, 24:57-71.
52. Camp D., Currie K., Labbe A., van Meyel D.J., Charron F. Ihog and Boi are essential for Hedgehog signaling in Drosophila. Neural Dev 2010, 5:28.
53. Yan D., Wu Y., Yang Y., Belenkaya T.Y., Tang X., Lin X. The cell-surface proteins Dally-like and Ihog differentially regulate Hedgehog signaling strength and range during development. Development 2010, 137:2033-2044.
54. Gao L., Wu L., Hou X., Zhang Q., Zhang F., Ye X., Yang Y., Lin X. Drosophila miR-932 modulates hedgehog signaling by targeting its co-receptor Brother of ihog. Dev Biol 2013, 377:166-176.
55. Yao S., Lum L., Beachy P. The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell 2006, 125:343-357.
56. Hartman T.R., Zinshteyn D., Schofield H.K., Nicolas E., Okada A., O'Reilly A.M. Drosophila Boi limits Hedgehog levels to suppress follicle stem cell proliferation. J Cell Biol 2010, 191:943-952.
57. Wojcinski A., Nakato H., Soula C., Glise B. DSulfatase-1 fine-tunes Hedgehog patterning activity through a novel regulatory feedback loop. Dev Biol 2011, 358:168-180.
58. Sanchez-Hernandez D., Sierra J., Ortigao-Farias J.R., Guerrero I. The WIF domain of the human and Drosophila Wif-1 secreted factors confers specificity for Wnt or Hedgehog. Development 2012, 139:3849-3858.
59. Glise B., Miller C.A., Crozatier M., Halbisen M.A., Wise S., Olson D.J., Vincent A., Blair S.S. Shifted, the Drosophila ortholog of Wnt inhibitory factor-1, controls the distribution and movement of Hedgehog. Dev Cell 2005, 8:255-266.
60. Gorfinkiel N., Sierra J., Callejo A., Ibanez C., Guerrero I. The Drosophila ortholog of the human Wnt inhibitor factor Shifted controls the diffusion of lipid-modified Hedgehog. Dev Cell 2005, 8:241-253.
61. Avanesov A., Blair S.S. The Drosophila WIF1 homolog Shifted maintains glypican-independent Hedgehog signaling and interacts with the Hedgehog co-receptors Ihog and Boi. Development 2013, 140:107-116.
62. Avanesov A., Honeyager S.M., Malicki J., Blair S.S. The role of glypicans in Wnt inhibitory factor-1 activity and the structural basis of Wif1's effects on Wnt and Hedgehog signaling. PLoS Genet 2012, 8:e1002503.
63. Woods I.G., Talbot W.S. The you gene encodes an EGF-CUB protein essential for Hedgehog signaling in zebrafish. PLoS Biol 2005, 3:e66.
64. Kawakami A., Nojima Y., Toyoda A., Takahoko M., Satoh M., Tanaka H., Wada H., Masai I., Terasaki H., Sakaki Y., et al. The zebrafish-secreted matrix protein you/scube2 is implicated in long-range regulation of hedgehog signaling. Curr Biol 2005, 15:480-488.
65. Hollway G.E., Maule J., Gautier P., Evans T.M., Keenan D.G., Lohs C., Fischer D., Wicking C., Currie P.D. Scube2 mediates Hedgehog signalling in the zebrafish embryo. Dev Biol 2006, 294:104-118.
66. Creanga A., Glenn T.D., Mann R.K., Saunders A.M., Talbot W.S., Beachy P.A. Scube/You activity mediates release of dually lipid-modified Hedgehog signal in soluble form. Genes Dev 2012, 26:1312-1325.
67. Tsai M.T., Cheng C.J., Lin Y.C., Chen C.C., Wu A.R., Wu M.T., Hsu C.C., Yang R.B. Isolation and characterization of a secreted, cell-surface glycoprotein SCUBE2 from humans. Biochem J 2009, 422:119-128.
68. Zeng X., Goetz J.A., Suber L.M., Scott W.J., Schreiner C.M., Robbins D.J. A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 2001, 411:716-720.
69. Chen Z., Heine T., Jiao H., Hirsch A., Thiel W., Schleyer P. Theoretical studies on the smallest fullerene: from monomer to oligomers and solid States. Chemistry 2004, 10:963-970.
70. Goetz J.A., Singh S., Suber L.M., Kull F.J., Robbins D.J. A highly conserved amino-terminal region of sonic hedgehog is required for the formation of its freely diffusible multimeric form. J Biol Chem 2006, 281:4087-4093.
71. Dierker T., Dreier R., Migone M., Hamer S., Grobe K. Heparan sulfate and transglutaminase activity are required for the formation of covalently cross-linked hedgehog oligomers. J Biol Chem 2009, 284:32562-32571.
72. Feng J., White B., Tyurina O.V., Guner B., Larson T., Lee H.Y., Karlstrom R.O., Kohtz J.D. Synergistic and antagonistic roles of the Sonic hedgehog N- and C-terminal lipids. Development 2004, 131:4357-4370.
73. Katanaev V.L., Solis G.P., Hausmann G., Buestorf S., Katanayeva N., Schrock Y., Stuermer C.A., Basler K. Reggie-1/flotillin-2 promotes secretion of the long-range signalling forms of Wingless and Hedgehog in Drosophila. EMBO J 2008, 27:509-521.
74. Greco V., Hannus M., Eaton S. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 2001, 106:633-645.
75. Tanaka Y., Okada Y., Hirokawa N. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 2005, 435:172-177.
76. Panakova D., Sprong H., Marois E., Thiele C., Eaton S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 2005, 435:58-65.
77. Beckett K., Monier S., Palmer L., Alexandre C., Green H., Bonneil E., Raposo G., Thibault P., Borgne R.L., Vincent J.P. Drosophila S2 cells secrete wingless on exosome-like vesicles but the wingless gradient forms independently of exosomes. Traffic 2012, 14:82-96.
78. Koles K., Nunnari J., Korkut C., Barria R., Brewer C., Li Y., Leszyk J., Zhang B., Budnik V. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 2012, 287:16820-16834.
79. Kutty R.K., Kutty G., Kambadur R., Duncan T., Koonin E.V., Rodriguez I.R., Odenwald W.F., Wiggert B. Molecular characterization and developmental expression of a retinoid- and fatty acid-binding glycoprotein from Drosophila. A putative lipophorin. J Biol Chem 1996, 271:20641-20649.
80. Sundermeyer K., Hendricks J.K., Prasad S.V., Wells M.A. The precursor protein of the structural apolipoproteins of lipophorin: cDNA and deduced amino acid sequence. Insect Biochem Mol Biol 1996, 26:735-738.
81. Eugster C., Panakova D., Mahmoud A., Eaton S. Lipoprotein-heparan sulfate interactions in the Hh pathway. Dev Cell 2007, 13:57-71.
82. Callejo A., Culi J., Guerrero I. Patched, the receptor of Hedgehog, is a lipoprotein receptor. Proc Natl Acad Sci U S A 2008, 105:912-917.
83. Khaliullina H., Panakova D., Eugster C., Riedel F., Carvalho M., Eaton S. Patched regulates Smoothened trafficking using lipoprotein-derived lipids. Development 2009, 136:4111-4121.
84. Queiroz K.C., Tio R.A., Zeebregts C.J., Bijlsma M.F., Zijlstra F., Badlou B., de Vries M., Ferreira C.V., Spek C.A., Peppelenbosch M.P., et al. Human plasma very low density lipoprotein carries Indian hedgehog. J Proteome Res 2010, 9:6052-6059.
85. Brankatschk M., Eaton S. Lipoprotein particles cross the blood-brain barrier in Drosophila. J Neurosci 2010, 30:10441-10447.
86. Ramirez-Weber F.A., Kornberg T.B. Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 1999, 97:599-607.
87. Hsiung F., Ramirez-Weber F.A., Iwaki D.D., Kornberg T.B. Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature 2005, 437:560-563.
88. Roy S., Hsiung F., Kornberg T.B. Specificity of Drosophila cytonemes for distinct signaling pathways. Science 2011, 332:354-358. Cytonemes express different morphogen receptors suggesting cytoneme-mediated transport might be a general mechanism of direct transfer of morphogens between non-adjacent cells with a specific cytoneme for each morphogen.
89. Rojas-Rios P., Guerrero I., Gonzalez-Reyes A. Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila. PLoS Biol 2012, 10:e1001298.
90. Deshpande G., Swanhart L., Chiang P., Schedl P. Hedgehog signaling in germ cell migration. Cell 2001, 106:759-769.
91. Deshpande G., Schedl P. HMGCoA reductase potentiates hedgehog signaling in Drosophila melanogaster. Dev Cell 2005, 9:629-638.
92. Deshpande G., Godishala A., Schedl P. Ggamma1, a downstream target for the hmgcr-isoprenoid biosynthetic pathway, is required for releasing the Hedgehog ligand and directing germ cell migration. PLoS Genet 2009, 5:e1000333.