Dendrite Reshaping of Adult Drosophila Sensory Neurons Requires Matrix Metalloproteinase-Mediated Modification of the Basement Membranes

Yasunaga, Kei-ichiro; Kanamori, Takashi; Morikawa, Rei; Suzuki, Emiko; Emoto, Kazuo

doi:10.1016/j.devcel.2010.02.010

Cited by 61 publications

(80 citation statements)

References 55 publications

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“…Additionally, Schwann cells activate MMP expression following nerve injury, and MMPs have been implicated in Schwann cell myelination (Ferguson and Muir, 2000;La Fleur et al, 1996;Lehmann et al, 2009;Mantuano et al, 2008). Intriguingly, MMP2 was recently shown to have a role in degrading the basement membrane to allow dendrite remodeling in Drosophila sensory neurons (Yasunaga et al, 2010). Future experiments will determine whether MMPs or other enzymes are involved in basement membrane remodeling.…”

Section: Research Articlementioning

confidence: 99%

Schwann cells reposition a peripheral nerve to isolate it from postembryonic remodeling of its targets

2010

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SUMMARYAlthough much is known about the initial construction of the peripheral nervous system (PNS), less well understood are the processes that maintain the position and connections of nerves during postembryonic growth. Here, we show that the posterior lateral line nerve in zebrafish initially grows in the epidermis and then rapidly transitions across the epidermal basement membrane into the subepidermal space. Our experiments indicate that Schwann cells, which myelinate axons in the PNS, are required to reposition the nerve. In mutants lacking Schwann cells, the nerve is mislocalized and the axons remain in the epidermis. Transplanting wild-type Schwann cells into these mutants rescues the position of the nerve. Analysis of chimeric embryos suggests that the process of nerve relocalization involves two discrete steps -the degradation and recreation of the epidermal basement membrane. Although the outgrowth of axons is normal in mutants lacking Schwann cells, the nerve becomes severely disorganized at later stages. In wild-type embryos, exclusion of the nerve from the epidermis isolates axons from migration of their targets (sensory neuromasts) within the epidermis. Without Schwann cells, axons remain within the epidermis and are dragged along with the migrating neuromasts. Our analysis of the posterior lateral line system defines a new process in which Schwann cells relocate a nerve beneath the epidermal basement membrane to insulate axons from the postembryonic remodeling of their targets.

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Section: Research Articlementioning

confidence: 99%

Schwann cells reposition a peripheral nerve to isolate it from postembryonic remodeling of its targets

2010

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“…During pupariation, the dendrites of class IV neurons are pruned completely while the cell body and axons remain in place (Williams and Truman, 2005a). At the end of the pupal stage, dendrites regrow into the adult body wall (Shimono et al, 2009;Yasunaga et al, 2010). These cells are thus a useful model for studying large-scale developmental dendrite pruning.…”

Section: Introductionmentioning

confidence: 99%

The microtubule-severing protein fidgetin acts after dendrite injury to promote their degeneration

Tao

Feng

Rolls

2016

Journal of Cell Science

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After being severed from the cell body, axons initiate an active degeneration program known as Wallerian degeneration. Although dendrites also seem to have an active injury-induced degeneration program, no endogenous regulators of this process are known. Because microtubule disassembly has been proposed to play a role in both pruning and injury-induced degeneration, we used a Drosophila model to identify microtubule regulators involved in dendrite degeneration. We found that, when levels of fidgetin were reduced using mutant or RNA interference (RNAi) strategies, dendrite degeneration was delayed, but axon degeneration and dendrite pruning proceeded with normal timing. We explored two possible ways in which fidgetin could promote dendrite degeneration: (1) by acting constitutively to moderate microtubule stability in dendrites, or (2) by acting specifically after injury to disassemble microtubules. When comparing microtubule dynamics and stability in uninjured neurons with and without fidgetin, we could not find evidence that fidgetin regulated microtubule stability constitutively. However, we identified a fidgetin-dependent increase in microtubule dynamics in severed dendrites. We conclude that fidgetin acts after injury to promote disassembly of microtubules in dendrites severed from the cell body.

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“…ECM modification plays important roles in regulating dendrite structural plasticity in several contexts (Mataga et al, 2002;Oray et al, 2004;Yasunaga et al, 2010), thus we reasoned that ban-regulated changes in epithelium-ECM attachment might alter substrate permissivity for dendrite growth and hence C4da dendrite plasticity. To test this possibility, we ablated second instar Cd4a neurons and monitored dendrite invasion of the unoccupied territory by spared Fig.…”

Section: Epithelium-ecm Interactions Influence Dendrite Growth and Plmentioning

confidence: 99%

The microRNA bantam regulates a developmental transition in epithelial cells that restricts sensory dendrite growth

et al. 2014

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As animals grow, many early born structures grow by cell expansion rather than cell addition; thus growth of distinct structures must be coordinated to maintain proportionality. This phenomenon is particularly widespread in the nervous system, with dendrite arbors of many neurons expanding in concert with their substrate to sustain connectivity and maintain receptive field coverage as animals grow. After rapidly growing to establish body wall coverage, dendrites of Drosophila class IV dendrite arborization (C4da) neurons grow synchronously with their substrate, the body wall epithelium, providing a system to study how proportionality is maintained during animal growth. Here, we show that the microRNA bantam (ban) ensures coordinated growth of C4da dendrites and the epithelium through regulation of epithelial endoreplication, a modified cell cycle that entails genome amplification without cell division. In Drosophila larvae, epithelial endoreplication leads to progressive changes in dendrite-extracellular matrix (ECM) and dendrite-epithelium contacts, coupling dendrite/substrate expansion and restricting dendrite growth beyond established boundaries. Moreover, changes in epithelial expression of cell adhesion molecules, including the beta-integrin myospheroid (mys), accompany this developmental transition. Finally, endoreplication and the accompanying changes in epithelial mys expression are required to constrain late-stage dendrite growth and structural plasticity. Hence, modulating epithelium-ECM attachment probably influences substrate permissivity for dendrite growth and contributes to the dendrite-substrate coupling that ensures proportional expansion of the two cell types.

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Dendrite Reshaping of Adult Drosophila Sensory Neurons Requires Matrix Metalloproteinase-Mediated Modification of the Basement Membranes

Cited by 61 publications

References 55 publications

Schwann cells reposition a peripheral nerve to isolate it from postembryonic remodeling of its targets

Schwann cells reposition a peripheral nerve to isolate it from postembryonic remodeling of its targets

The microtubule-severing protein fidgetin acts after dendrite injury to promote their degeneration

The microRNA bantam regulates a developmental transition in epithelial cells that restricts sensory dendrite growth

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