DOI: 10.1242/dev.124.10.1941. Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in <i>Drosophila</i>

Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila

10.1242/dev.124.10.1941

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The neural receptor tyrosine phosphatases DPTP69D, DPTP99A and DLAR are involved in motor axon guidance in the Drosophila embryo. Here we analyze the requirements for these three phosphatases in growth cone guidance decisions along the ISN and SNb motor pathways. Any one of the three suffices for the progression of ISN pioneer growth cones beyond their first intermediate target in the dorsal muscle field. DLAR or DPTP69D can facilitate outgrowth beyond a second intermediate target, and DLAR is uniquely required for formation of a normal terminal arbor. A different pattern of partial redundancy among the three phosphatases is observed for the SNb pathway. Any one of the three suffices to allow SNb axons to leave the common ISN pathway at the exit junction. When DLAR is not expressed, however, SNb axons sometimes bypass their ventrolateral muscle targets after leaving the common pathway, instead growing out as a separate bundle adjacent to the ISN. This abnormal guidance decision can be completely suppressed by also removing DPTP99A, suggesting that DLAR turns off or counteracts a DPTP99A signal that favors the bypass axon trajectory. Our results show that the relationships among the tyrosine phosphatases are complex and dependent on cellular context. At growth cone choice points along one nerve, two phosphatases cooperate, while along another nerve these same phosphatases can act in opposition to one another.

Bibliography

Desai, C. J., Krueger, N. X., Saito, H., & Zinn, K. (1997). Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila. Development, 124(10), 1941â1952.

Authors 4

Chand J. Desai (first)
Neil X. Krueger (additional)
Haruo Saito (additional)
Kai Zinn (additional)

References 27 Referenced 125

{'key': '2025021403034398000_DEVELOP_124_10_1941C1', 'first-page': '1013', 'volume-title': 'The development of Drosophila melanogaster', 'author': 'Bate', 'year': '1993'} / The development of Drosophila melanogaster by Bate (1993)
10.1242/dev.113.1.79 / Development / Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila by Bate (1991)
10.1083/jcb.127.3.825 / J. Cell Biol / NCAM-dependent neurite outgrowth is inhibited in neurons from fyn-minus mice by Beggs (1994)
10.1016/0959-4388(94)90030-2 / Curr. Opin. Neurobiol / Cytoskeletal events in growth cone steering by Bentley (1994)
10.1038/382555a0 / Nature / Structural basis for inhibition of receptor protein-tyrosine phosphatase-α by dimerization by Bilwes (1996)
10.1038/376171a0 / Nature / Control of neuronal pathway selection by a Drosophila receptor protein tyrosine kinase family member by Callahan (1995)
10.1016/0092-8674(95)90363-1 / Cell / GTPase cascades choreographing cellular behavior: movement, morphogenesis, and more by Chant (1995)
10.1016/S0896-6273(00)80131-2 / Neuron / PY in the fly: receptor-like tyrosine phosphatases in axonal pathfinding by Chien (1996)
10.1073/pnas.93.11.5466 / Proc. Natl. Acad. Sci. USA / The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains by Debant (1996)
10.1016/S0092-8674(00)81035-1 / Cell / Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo by Desai (1996)
10.1016/0092-8674(93)90141-C / Cell / Ligand-mediated negative regulation of a chimeric transmembrane receptor tyrosine phosphatase by Desai (1993)
10.1016/0896-6273(95)90284-8 / Neuron / Localized collapsing cues can steer growth cones without inducing their full collapse by Fan (1995)
10.1016/S0960-9822(95)00272-7 / Curr. Biol / The ins and outs of receptor tyrosine phosphatases by Fashena (1995)
10.1146/annurev.ne.19.030196.002013 / Annu. Rev. Neurosci / Mechanisms and molecules that control growth cone guidance by Goodman (1996)
10.1007/BF00241271 / Roux’s Arch. Dev. Biol / Targeted mutagenesis and genetic analysis of a Drosophila receptor-linked protein tyrosine phosphatase gene by Hamilton (1995)
10.1016/0896-6273(95)90000-4 / Neuron / From tags to RAGS: chemoaffinity finally has receptors and ligands by Harris (1995)
10.1016/S0092-8674(00)80075-6 / Cell / Nuk controls pathfinding of commissural axons in the mammalian central nervous system by Henkemeyer (1996)
10.1016/0896-6273(94)90339-5 / Neuron / Impaired neurite outgrowth of src-minus cerebellar nuerons on the cell-adhesion molecule L1 by Ignelzi (1994)
10.1146/annurev.ne.19.030196.002553 / Ann. Rev. Neur / The Drosophila neuromuscular junction – a model system for studying synaptic development and function by Keshishian (1996)
10.1016/S0092-8674(00)81036-3 / Cell / The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila by Krueger (1996)
10.1016/0896-6273(94)90022-1 / Neuron / Ectopic and increased expression of fasiclin II alters motoneuron growth cone guidance by Lin (1994)
10.1002/j.1460-2075.1996.tb00992.x / EMBO J / Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation by Orioli (1996)
10.1002/j.1460-2075.1995.tb07282.x / EMBO J / The LAR transmembrane protein-tyrosine phosphatase and a coiled-coil LAR-interacting protein colocalize at focal adhesions by Serrapages (1995)
10.1002/neu.480220309 / J. Neurobiol / Location and connectivity of abdominal motoneurons in the embryo and larvae of Drosophila melanogaster by Sink (1991)
10.1242/dev.121.6.1833 / Development / Axonal localisation of the CAM-like tyrosine phosphatase CRYPα: a signaling molecule of embryonic growth cones by Stoker (1995)
10.1016/0092-8674(91)90063-5 / Cell / Three receptor-linked protein-tyrosine phosphatases are selectively expressed on central nervous system axons in the Drosophila embryo by Tian (1991)
10.1016/0092-8674(93)90643-5 / Cell / Genes that control neuromuscular specificity in Drosophila by Van Vactor (1993)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 3:01 p.m.)
Deposited	6 months, 2 weeks ago (Feb. 13, 2025, 10:04 p.m.)
Indexed	1 month, 3 weeks ago (July 2, 2025, 3:11 p.m.)
Issued	28 years, 3 months ago (May 15, 1997)
Published	28 years, 3 months ago (May 15, 1997)
Published Online	28 years, 3 months ago (May 15, 1997)
Published Print	28 years, 3 months ago (May 15, 1997)

Funders 0

None

BibTeX

@article{Desai_1997, title={Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.10.1941}, DOI={10.1242/dev.124.10.1941}, number={10}, journal={Development}, publisher={The Company of Biologists}, author={Desai, Chand J. and Krueger, Neil X. and Saito, Haruo and Zinn, Kai}, year={1997}, month=may, pages={1941–1952} }

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