Sonic hedgehog and Wnt: Antagonists in morphogenesis but collaborators in axon guidance

Frontiers in Cellular Neuroscience

Volumn , Issue MAY, 2013, Pages

  Avilés, Evelyn C ^a   Wilson, Nicole H ^a   Stoeckli, Esther T ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Attraction; Frizzled; Morphogen; Neural circuit; Repulsion; Ryk; Smoothened; Spinal cord

Indexed keywords

CALCIUM; CHEMOATTRACTANT; CYCLIC NUCLEOTIDE; DOUBLE STRANDED RNA; MORPHOGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; WNT PROTEIN; WNT1 PROTEIN; WNT5A PROTEIN;

BRAIN STEM; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL POPULATION; CELL SPECIFICITY; CELL STIMULATION; CHEMOATTRACTION; CHEMOREPULSION; CONCENTRATION RESPONSE; CONNECTOME; DEVELOPMENTAL STAGE; DOPAMINERGIC NERVE CELL; EMBRYO DEVELOPMENT; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MESENCEPHALON; MOLECULAR MECHANICS; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE CONDUCTANCE; NERVE FIBER; NERVE FIBER TRANSPORT; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEURITE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; REGULATORY MECHANISM; RETINA GANGLION CELL; REVIEW; SPINAL CORD; STEM CELL; WNT SIGNALING PATHWAY;

EID: 84878286656     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00086     Document Type: Review

References (92)

1. Andre P, Wang Q, Wang N, Gao B, Schilit A, Halford MM, Stacker SA, Zhang X, and Yang Y. (2012). The Wnt coreceptor Ryk regulates Wnt/planar cell polarity by modulating the degradation of the core planar cell polarity component Vangl2. J Biol Chem. 287, 44518-44525.
2. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, and Tessier-Lavigne M. (2002). Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33, 233-248.
3. Barresi MJF, Hutson LD, Chien C, and Karlstrom RO. (2005). Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132, 3643-3656.
4. Birgbauer E, Cowan CA, Sretavan DW, and Henkemeyer M. (2000). Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127, 1231-1241.
5. Blaess S, Corrales JD, and Joyner AL. (2006). Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133, 1799-1809.
6. Blakely BD, Bye CR, Fernando CV, Horne MK, Macheda ML, Stacker SA, Arenas E, and Parish CL. (2011) Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS One 6, e18373.
7. Bourikas D, Pekarik V, Baeriswyl T, Grunditz A, Sadhu R, Nardó M, and Stoeckli ET. (2005). Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci 8, 297-304.
8. Boutros M, Paricio N, Strutt DI, and Mlodzik M. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118.
9. Bovolenta P and Dodd J. (1990). Guidance of commissural growth cones at the floor plate in embryonic rat spinal cord. Development 109, 435-447.
10. Charron F, Stein E, Jeong J, McMahon AP, and Tessier-Lavigne M. (2003). The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11-23.
11. Chédotal A. (2011). Further tales of the midline. Curr. Opin. Neurobiol 21, 68-75.
12. Chuang P and McMahon AP. (1999). Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397, 617-621.
13. Clark CEJ, Nourse CC, and Cooper HM. (2012). The tangled web of non-canonical Wnt signalling in neural migration. Neurosignals 20, 202-220.
14. Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, and Sretavan DW. (1997). Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19, 575-89.
15. Dessaud E, McMahon AP, and Briscoe J. (2008). Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503.
16. Domanitskaya E, Wacker A, Mauti O, Baeriswyl T, Esteve P, Bovolenta P, and Stoeckli ET. (2010). Sonic hedgehog guides post-crossing commissural axons both directly and indirectly by regulating Wnt activity. J Neurosci 30, 11167-11176.
17. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, and Edlund T. (1995). Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81, 747-756.
18. Erskine L and Herrera E. (2007). The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev Biol 308, 1-14.
19. Fabre PJ, Shimogori T, and Charron F. (2010). Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J Neurosci. 30, 266-275.
20. Fantetti KN and Fekete DM. (2012). Members of the BMP, Shh, and FGF morphogen families promote chicken statoacoustic ganglion neurite outgrowth and neuron survival in vitro. Dev Neurobiol 72, 1213-1228.
21. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, and Weinberg RA. (1997). Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804.
22. Fenstermaker AG, Prasad AA, Bechara A, Adolfs Y, Tissir F, Goffinet A, Zou Y, and Pasterkamp JR. (2010). Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J Neurosci 30, 16053-16064.
23. Gordon L, Mansh M, Kinsman H, and Morris AR. (2010). Xenopus sonic hedgehog guides retinal axons along the optic tract. Dev Dyn 239, 2921-2932.
24. Guo W, Jiang H, Gray V, Dedhar S, and Rao Y. (2007). Role of the integrin-linked kinase (ILK) in determining neuronal polarity. Dev. Biol 306, 457-468.
25. Guo D, Standley C, Bellve K, Fogarty K, and Bao Z. (2012). Protein kinase Cα and integrin -linked kinase mediate the negative axon guidance effects of Sonic hedgehog. Mol. Cell. Neurosci 50, 82-92.
26. Hammond R, Blaess S, and Abeliovich A. (2009). Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS One 4, e7007.
27. Hannigan G, Troussard AA, and Dedhar S. (2005). Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat. Rev. Cancer, 51-63.
28. Harwell CC, Parker PR, Gee SM, Okada A, McConnell SK, Kreitzer AC, and Kriegstein AR. (2012). Sonic hedgehog expression in corticofugal projection neurons directs cortical microcircuit formation. Neuron 73, 1116-26.
29. Hindges R, McLaughlin T, Genoud N, Henkemeyer M, and O'Leary DDM. (2002). EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 35, 475-487.
30. Hutchins BI, Li L, and Kalil K. (2011). Wnt/calcium signaling mediates axon growth and guidance in the developing corpus callosum. Devel Neurobio 71, 269-283.
31. Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, and Rosenthal, A. (1995). Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron 15, 35-44.
32. Ishii T, Satoh E, and Nishimura M. (2001). Integrin-linked kinase controls neurite outgrowth in N1E-115 neuroblastoma cells. J. Biol. Chem 276, 42994-43003.
33. Jin Z, Zhang J, Klar A, Chédotal A, Rao Y, Cepko CL, and Bao, Z. (2003) Irx4-mediated regulation of Slit1 expression contributes to the definition of early axonal paths inside the retina. Development 130, 1037-1048.
34. Keeble TR, Halford MM, Seaman C, Kee N, Macheda M, Anderson RB, Stacker, SA, and Cooper HM. (2006). The Wnt receptor Ryk is required for Wnt5a-mediated axon guidance on the contralateral side of the corpus callosum. J Neurosci 26, 5840-5848.
35. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, and Tessier-Lavigne M. (1996). Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
36. Kent CB, Shimada T, Ferraro GB, Ritter B, Yam PT, McPherson PS, Charron F, Kennedy TE, and Fournier AE. (2010). 14-3-3 proteins regulate protein kinase a activity to modulate growth cone turning responses. J Neurosci 30, 14059-14067.
37. Kohn AD and Moon RT. (2005). Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38, 439-446.
38. Kolpak A, Zhang J, and Bao Z. (2005). Sonic hedgehog has a dual effect on the growth of retinal ganglion axons depending on its concentration. J. Neurosci 25, 3432-3441.
39. Kolpak AL, Jiang J, Guo D, Standley C, Bellve K, Fogarty K, and Bao Z. (2009). Negative guidance factor-induced macropinocytosis in the growth cone plays a critical role in repulsive axon turning. J Neurosci 29, 10488-10498.
40. Lee CS, Buttitta LA, May NR, Kispert A, and Fan CM. (2000). SHH-N upregulates Sfrp2 to mediate its competitive interaction with WNT1 and WNT4 in the somitic mesoderm. Development 127, 109-118.
41. Li L, Hutchins BI, and Kalil K. (2009). Wnt5a induces simultaneous cortical axon outgrowth and repulsive axon guidance through distinct signaling mechanisms. J Neurosci 29, 5873-5883.
42. Lin L, Rao Y, and Isacson O. (2005). Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci 28, 547-555.
43. Liu Y, Shi J, Lu C, Wang Z, Lyuksyutova AI, Song X, Song, X, and Zou Y. (2005). Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat. Neurosci 8, 1151-1159.
44. Liu G, Beggs H, Jurgensen C, Park HT, Tang H, Gorski J, Jones KR, Reichardt LF, Wu J, and Rao Y. (2007). Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat Neurosci 7, 1222-1232.
45. Lyuksyutova AI, Lu C, Milanesio N, King LA, Guo N, Wang Y, Nathans J, Tessier-Lavigne M, and Zou Y. (2003). Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988.
46. Macdonald BT, Semenov MV, and He X. (2007). SnapShot: Wnt/beta-catenin signaling. Cell 131, 1204.
47. Macheda ML, Sun WW, Kugathasan K, Hogan BM, Bower NI, Halford MM, Zhang YF, Jacques BE, Lieschke GJ, Dabdoub A, and Stacker SA. (2012). The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. J Biol Chem 287, 29312-29323.
48. Maro GS, Klassen MP, and Shen K. (2009). A beta-catenin-dependent Wnt pathway mediates anteroposterior axon guidance in C. elegans motor neurons. PLoS One 4: e4690.
49. Nusse R. (2012). Wnt signaling. Cold Spring Harb Perspect Biol 4, a011163.
50. Okada A, Charron F, Morin S, Shin DS, Wong K, Fabre PJ, Tessier-Lavigne M, and McConnell, SK. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
51. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, and Wechsler-Reya RJ. (2003). Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc. Natl. Acad. Sci. U.S.A 100, 7331-7336.
52. Pan C, Howell JE, Clark SG, Hilliard M, Cordes S, Bargmann CI, and Garriga G. (2006). Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell 10, 367-377.
53. Parra LM and Zou Y. (2010). Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat Neurosci 13, 29-35.
54. Persson M, Stamataki D, te Welscher P, Andersson E, Böse J, Rüther U, Ericson J, and Briscoe J. (2002). Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev 16, 2865-2878.
55. Petros TJ, Rebsam A, and Mason CA. (2008). Retinal axon growth at the optic chiasm: to cross or not to cross. Annu. Rev. Neurosci. 31, 295-315.
56. Riobo NA, Haines GM, and Emerson CP. (2006). Protein kinase C-delta and mitogen-activated protein/extracellular signal-regulated kinase-1 control GLI activation in hedgehog signaling. Cancer Res 66, 839-845.
57. Robles E, Woo S, and Gomez TM. (2005). Src-dependent tyrosine phosphorylation at the tips of growth cone filopodia promotes extension. J Neurosci 25, 7669-7681.
58. Ruiz de Almodovar C, Fabre PJ, Knevels E, Coulon C, Segura I, Haddick PC, Aerts L, Delattin N, Strasser G, Oh WJ, Lange C, Vinckier S, Haigh J, Fouquet C, Gu C, Alitalo K, Castellani V, Tessier-Lavigne M, Chedotal A, Charron F, and Carmeliet P. (2011). VEGF mediates commissural axon chemoattraction through its receptor Flk1. Neuron 70, 966-78.
59. Salinas PC and Zou Y. (2008). Wnt signaling in neural circuit assembly. Annu. Rev. Neurosci 31, 339-358.
60. Salinas PC. (2012). Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb Perspect Biol 4, a008003.
61. Sanchez-Camacho C and Bovolenta P. (2008). Autonomous and non-autonomous Shh signaling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 135, 3531-3541.
62. Schmitt AM, Shi J, Wolf AM, Lu C, King LA, and Zou Y. (2006). Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 439, 31-37.
63. Semenov MV, Habas R, Macdonald BT, and He X. (2007). SnapShot: Noncanonical Wnt Signaling Pathways. Cell 131, 1378.
64. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, and Tessier-Lavigne M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
65. Shafer B, Onishi K, Lo C, Colakoglu G, and Zou Y. (2011). Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Dev Cell 20, 177-191.
66. Sieber B, Kuzmin A, Canals JM, Danielsson A, Paratcha G, Arenas E, Alberch J, Ogren SO, and Ibáñez CF. (2004). Disruption of EphA/ephrin-a signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine. Mol. Cell. Neurosci 26, 418-428.
67. Simons M and Mlodzik M. (2008). Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42, 517-540.
68. Song HJ, Ming GL, and Poo MM. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279.
69. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, and Poo MM. (1998). Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518.
70. Song L, Liu Y, Yu Y, Duan X, Qi S, and Liu Y. (2012). Shh signaling guides spatial pathfinding of raphespinal tract axons by multidirectional repulsion. Cell Res 22, 697-716.
71. Stacher Hörndli C and Chien C. (2012). Sonic hedgehog is indirectly required for intraretinal axon pathfinding by regulating chemokine expression in the optic stalk. Development 139, 2604-2613.
72. Steinberg SF. (2008). Structural basis of protein kinase C isoform function. Physiol. Rev 88, 1341-1378.
73. Stein E and Tessier-Lavigne M. (2001). Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291, 1928-38.
74. Suter DM and Forscher P. (2001). Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J. Cell Biol 155, 427-438.
75. Terman JR and Kolodkin AL. (2004). Nervy links protein kinase a to plexin-mediated semaphorin repulsion. Science 303, 1204-1207.
76. Torban E, Wang H, Patenaude A, Riccomagno M, Daniels E, Epstein D, and Gros P. (2007). Tissue, cellular and sub-cellular localization of the Vangl2 protein during embryonic development: effect of the Lp mutation. Gene Expr Patterns 7, 346-354.
77. Traiffort E, Moya KL, Faure H, Hässig R, and Ruat M. (2001). High expression and anterograde axonal transport of aminoterminal sonic hedgehog in the adult hamster brain. Eur. J. Neurosci 14, 839-850.
78. Trousse F, Martí E, Gruss P, Torres M, and Bovolenta P. (2001). Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. Development 128, 3927-3936.
79. Ulloa F and Martí E. (2010). Wnt won the war: antagonistic role of Wnt over Shh controls dorsoventral patterning of the vertebrate neural tube. Dev. Dyn 239, 69-76.
80. van Amerongen R, Mikels A, and Nusse R. (2008). Alternative Wnt signaling is initiated by distinct receptors. Sci Signal 1, re 9.
81. van Amerongen R and Nusse R. (2009). Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214.
82. Wang Y and Nathans J. (2007). Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134, 647-658.
83. Wilson NH and Stoeckli ET. (2012). Sonic hedgehog regulates Wnt activity during neural circuit formation. Vitam Horm 88,173-209.
84. Wolf AM, Lyuksyutova AI, Fenstermaker AG, Shafer B, Lo CG, and Zou Y. (2008). Phosphatidylinositol-3-kinase-atypical protein kinase C signaling is required for Wnt attraction and anterior-posterior axon guidance. J. Neurosci 28, 3456-3467.
85. Yamauchi K, Mizushima S, Tamada A, Yamamoto N, Takashima S, and Murakami F. (2009). FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F. J Neurosci 29, 4044-4055.
86. Yam PT, Langlois SD, Morin S, and Charron F. (2009). Sonic hedgehog guides axons through a noncanonical, Src-family-kinase-dependent signaling pathway. Neuron 62, 349-362.
87. Yam PT, Kent CB, Morin S, Farmer WT, Alchini R, Lepelletier L, Colman DR, Tessier-Lavigne M, Fournier AE, and Charron F. (2012). 14-3-3 proteins regulate a cell-intrinsic switch from sonic hedgehog-mediated commissural axon attraction to repulsion after midline crossing. Neuron 76, 735-749.
88. Yoon BC, Zivraj KH, and Holt CE. (2009). Local translation and mRNA trafficking in axon pathfinding. Results Probl Cell Differ 48, 269-288.
89. Yoshikawa S, McKinnon RD, Kokel M, and Thomas JB. (2003). Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 422, 583-8.
90. Yu M, Gipp J, Yoon JW, Iannaccone P, Walterhouse D, and Bushman W. (2008). Sonic hedgehogresponsive genes in the fetal prostate. J Biol Chem. 284, 5620-5629.
91. Zisman S, Marom K, Avraham O, Rinsky-Halivni L, Gai U, Kligun G, Tzarfaty-Majar V, Suzuki T, and Klar A. (2007). Proteolysis and membrane capture of F-spondin generates combinatorial guidance cues from a single molecule. J. Cell Biol 178, 1237-1249.
92. Zou Y, Stoeckli E, Chen H, and Tessier-Lavigne M. (2000). Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375.