Receptor tyrosine phosphatases regulate birth order-dependent axonal fasciculation and midline repulsion during development of the Drosophila mushroom body

Kurusu, Mitsuhiko; Zinn, Kai

doi:10.1016/j.mcn.2008.01.015

Cited by 18 publications

(29 citation statements)

References 54 publications

(63 reference statements)

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“…Earlier studies reported that Ptp10D is only expressed by neurons (Tian et al, 1991;Yang et al, 1991), but we found that newer mAbs made against native Ptp10D (Kurusu and Zinn, 2008) selectively stained the apical surfaces of all tracheal cells (Fig. 1C,D).…”

Section: Cysts Form On Unicellular and Terminal Tracheal Branches In supporting

confidence: 44%

“…Ptp10D regulates axon guidance in embryos and larvae (Sun et al, 2000;Sun et al, 2001;Kurusu and Zinn, 2008). It is selectively expressed on CNS axons and tracheal branches, and is apically localized in tracheal cells (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Ptp10D mutations alter axonal branching and fasciculation in the mushroom body (Kurusu and Zinn, 2008), and produce longterm memory deficits (Qian et al, 2007). Ptp10D works together with Ptp69D to control axon guidance across the CNS midline (Sun et al, 2000) and bifurcation of the SNa motor nerve (Sun et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

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Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling

Jeon

Zinn

2009

Development

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The formation of epithelial tubes with defined shapes and sizes is essential for organ development. We describe a unique tracheal tubulogenesis phenotype caused by loss of both Drosophila type III receptor tyrosine phosphatases (RPTPs), Ptp4E and Ptp10D. Ptp4E is the only widely expressed Drosophila RPTP, and is the last of the six fly RPTPs to be genetically characterized. We recently isolated mutations in Ptp4E, and discovered that, although Ptp4E null mutants have no detectable phenotypes, double mutants lacking both Ptp4E and Ptp10D display synthetic lethality at hatching owing to respiratory failure. In these double mutants, unicellular and terminal tracheal branches develop large bubble-like cysts that selectively incorporate apical cell surface markers. Cysts in unicellular branches are enlargements of the lumen that are sealed by adherens junctions, whereas cysts in terminal branches are cytoplasmic vacuoles. Cyst size and number are increased by tracheal expression of activated Egfr tyrosine kinase, and decreased by reducing Egfr levels. Ptp10D forms a complex with Egfr in transfected cells. Downregulation of Egfr signaling by the RPTPs is required for the construction of tubular lumens, whether extracellular or intracellular, by cells that undergo remodeling during branch morphogenesis. The Ptp4E Ptp10D phenotype represents the first evidence of an essential role for RPTPs in epithelial organ development. These findings might be relevant to organ development and disease in mammals, because PTPRJ (DEP-1), an ortholog of Ptp4E/Ptp10D, interacts with the hepatocyte growth factor receptor tyrosine kinase. PTPRJ corresponds to the murine Scc1 (suppressor of colon cancer) gene.

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Section: Cysts Form On Unicellular and Terminal Tracheal Branches In supporting

confidence: 44%

Section: Discussionmentioning

confidence: 99%

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Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling

Jeon

Zinn

2009

Development

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“…In the Ptp69D mutant embryonic nervous systems, motoneurons did not innervate their respective muscles due to guidance defects (Desai and Purdy, 2003; Desai et al, 1996; Desai et al, 1997; Song et al, 2008). In addition, a role for PTP69D in axonal branching of mushroom body neurons has been described (Kurusu and Zinn, 2008). We found that the missense mutations in the first Ig domain and the Cat1 domain of Ptp69D 10 and Ptp69D 20 mutants did not affect GF guidance, branching or targeting.…”

Section: Discussionmentioning

confidence: 99%

“…PTP69D has a role during periods of axon outgrowth (Desai and Purdy, 2003) and along with other RPTPs, such as DLAR and PTP99A, is required for proper motor axon guidance (Desai et al, 1996; Desai et al, 1997; Song et al, 2008). PTP69D is also known to play a role in axon fasciculation and branching in the mushroom bodies (Kurusu and Zinn, 2008). In the Drosophila visual system, PTP69D is required for lamina specific targeting of the photoreceptor neurons R1-R6 (Garrity et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Structure–function analyses of tyrosine phosphatase PTP69D in giant fiber synapse formation of Drosophila

Lee

Godenschwege

2015

Molecular and Cellular Neuroscience

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PTP69D is a receptor protein tyrosine phosphatase (RPTP) with two intracellular catalytic domains (Cat1 and Cat2) and has been shown to play a role in axon guidance of embryonic motoneurons as well as targeting of photoreceptor neurons in the visual system of Drosophila melanogaster. Here, we characterized the developmental role of PTP69D in the giant fiber (GF) neurons, two interneurons in the central nervous system (CNS) that control the escape response of the fly. Our studies revealed that PTP69D has a function in synaptic terminal growth in the CNS. We found that missense mutations in the first immunoglobulin (Ig) domain and in the Cat1 domain, present inPtp69D10 and Ptp69D20 mutants, respectively, did not affect axon guidance or targeting but resulted in stunted terminal growth of the GFs. Cell autonomous rescue experiments demonstrated a function for the Cat1 and the first Ig domain of PTP69D in the GFs but not in its postsynaptic target neurons. In addition, complementation studies and structure-function analyses revealed that for GF terminal growth Cat1 function of PTP69D requires the immunoglobulin and the Cat2 domains, but not the fibronectin III or the membrane proximal region domains. In contrast, the fibronectin III but not the immunoglobulin domains were previously shown to be essential for axon targeting of photoreceptor neurons. Thus, our studies uncover a novel role for PTP69D in synaptic terminal growth in the CNS that is mechanistically distinct from its function in photoreceptor targeting.

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Structure and evolution of neuronal wiring receptors and ligands

Cortés

Pak

Özkan

2022

Developmental Dynamics

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One of the fundamental properties of a neuronal circuit is the map of its connections. The cellular and developmental processes that allow for the growth of axons and dendrites, selection of synaptic targets, and formation of functional synapses use neuronal surface receptors and their interactions with other surface receptors, secreted ligands, and matrix molecules. Spatiotemporal regulation of the expression of these receptors and cues allows for specificity in the developmental pathways that wire stereotyped circuits. The families of molecules controlling axon guidance and synapse formation are generally conserved across animals, with some important exceptions, which have consequences for neuronal connectivity. Here, we summarize the distribution of such molecules across multiple taxa, with a focus on model organisms, evolutionary processes that led to the multitude of such molecules, and functional consequences for the diversification or loss of these receptors.

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Receptor tyrosine phosphatases regulate birth order-dependent axonal fasciculation and midline repulsion during development of the Drosophila mushroom body

Cited by 18 publications

References 54 publications

Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling

Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling

Structure–function analyses of tyrosine phosphatase PTP69D in giant fiber synapse formation of Drosophila

Structure and evolution of neuronal wiring receptors and ligands

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