Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex
Morphogens function in concentration-dependent manners to instruct cell fate during tissue patterning. The cytoneme morphogen transport model posits that specialized filopodia extend between morphogen-sending and responding cells to ensure that appropriate signaling thresholds are achieved. How morp...
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doaj-15e46dd83f6a494e84eb22d438ef83652021-05-05T22:46:31ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.61432Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complexEric T Hall0https://orcid.org/0000-0001-9656-1942Miriam E Dillard1Daniel P Stewart2Yan Zhang3Ben Wagner4Rachel M Levine5Shondra M Pruett-Miller6https://orcid.org/0000-0002-3793-585XApril Sykes7Jamshid Temirov8Richard E Cheney9Motomi Mori10Camenzind G Robinson11https://orcid.org/0000-0002-7277-692XStacey K Ogden12https://orcid.org/0000-0001-8991-3065Department of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesCell and Tissue Imaging Center, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United States; Center for Advanced Genome Engineering, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United States; Center for Advanced Genome Engineering, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Biostatistics, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell Biology and Physiology, University of North Carolina School of Medicine, Chapel Hill, United StatesDepartment of Biostatistics, St. Jude Children’s Research Hospital, Memphis, United StatesCell and Tissue Imaging Center, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, United StatesMorphogens function in concentration-dependent manners to instruct cell fate during tissue patterning. The cytoneme morphogen transport model posits that specialized filopodia extend between morphogen-sending and responding cells to ensure that appropriate signaling thresholds are achieved. How morphogens are transported along and deployed from cytonemes, how quickly a cytoneme-delivered, receptor-dependent signal is initiated, and whether these processes are conserved across phyla are not known. Herein, we reveal that the actin motor Myosin 10 promotes vesicular transport of Sonic Hedgehog (SHH) morphogen in mouse cell cytonemes, and that SHH morphogen gradient organization is altered in neural tubes of Myo10-/- mice. We demonstrate that cytoneme-mediated deposition of SHH onto receiving cells induces a rapid, receptor-dependent signal response that occurs within seconds of ligand delivery. This activity is dependent upon a novel Dispatched (DISP)-BOC/CDON co-receptor complex that functions in ligand-producing cells to promote cytoneme occurrence and facilitate ligand delivery for signal activation.https://elifesciences.org/articles/61432Cytonemesignal transductionmorphogensonic hedgehogcell biologymyosin |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Eric T Hall Miriam E Dillard Daniel P Stewart Yan Zhang Ben Wagner Rachel M Levine Shondra M Pruett-Miller April Sykes Jamshid Temirov Richard E Cheney Motomi Mori Camenzind G Robinson Stacey K Ogden |
spellingShingle |
Eric T Hall Miriam E Dillard Daniel P Stewart Yan Zhang Ben Wagner Rachel M Levine Shondra M Pruett-Miller April Sykes Jamshid Temirov Richard E Cheney Motomi Mori Camenzind G Robinson Stacey K Ogden Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex eLife Cytoneme signal transduction morphogen sonic hedgehog cell biology myosin |
author_facet |
Eric T Hall Miriam E Dillard Daniel P Stewart Yan Zhang Ben Wagner Rachel M Levine Shondra M Pruett-Miller April Sykes Jamshid Temirov Richard E Cheney Motomi Mori Camenzind G Robinson Stacey K Ogden |
author_sort |
Eric T Hall |
title |
Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex |
title_short |
Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex |
title_full |
Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex |
title_fullStr |
Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex |
title_full_unstemmed |
Cytoneme delivery of Sonic Hedgehog from ligand-producing cells requires Myosin 10 and a Dispatched-BOC/CDON co-receptor complex |
title_sort |
cytoneme delivery of sonic hedgehog from ligand-producing cells requires myosin 10 and a dispatched-boc/cdon co-receptor complex |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2021-02-01 |
description |
Morphogens function in concentration-dependent manners to instruct cell fate during tissue patterning. The cytoneme morphogen transport model posits that specialized filopodia extend between morphogen-sending and responding cells to ensure that appropriate signaling thresholds are achieved. How morphogens are transported along and deployed from cytonemes, how quickly a cytoneme-delivered, receptor-dependent signal is initiated, and whether these processes are conserved across phyla are not known. Herein, we reveal that the actin motor Myosin 10 promotes vesicular transport of Sonic Hedgehog (SHH) morphogen in mouse cell cytonemes, and that SHH morphogen gradient organization is altered in neural tubes of Myo10-/- mice. We demonstrate that cytoneme-mediated deposition of SHH onto receiving cells induces a rapid, receptor-dependent signal response that occurs within seconds of ligand delivery. This activity is dependent upon a novel Dispatched (DISP)-BOC/CDON co-receptor complex that functions in ligand-producing cells to promote cytoneme occurrence and facilitate ligand delivery for signal activation. |
topic |
Cytoneme signal transduction morphogen sonic hedgehog cell biology myosin |
url |
https://elifesciences.org/articles/61432 |
work_keys_str_mv |
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