Spastin, atlastin, and ER relocalization are involved in axon but not dendrite regeneration

Rao, Kavitha S.; Stone, Michelle C.; Weiner, Alexis T.; Gheres, Kyle W.; Zhou, Chaoming; Deitcher, David L.; Levitan, Edwin S.; Rolls, Melissa M.

doi:10.1091/mbc.e16-05-0287

Cited by 62 publications

(72 citation statements)

References 65 publications

(106 reference statements)

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“…The morphological and molecular changes that occur following dendritic severing remain mostly unexplored (Standler and Bernstein 1982; Oren-Suissa and Podbilewicz 2010; Oren-Suissa et al 2010; Stone et al 2010, 2014; Nawabi et al 2012; Song et al 2012; Rao et al 2016; Tao et al 2016). To study the process of regeneration of the PVD dendrites following injury, we performed dendrotomy of arborized neurites using a femtosecond laser (Yanik et al 2004; Bourgeois and Ben-Yakar 2007; Wu et al 2007; Ghosh-Roy and Chisholm 2010).…”

Section: Resultsmentioning

confidence: 99%

Extrinsic Repair of Injured Dendrites as a Paradigm for Regeneration by Fusion inCaenorhabditis elegans

Oren‐Suissa

Gattegno

Kravtsov³

et al. 2017

Genetics

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Section: Resultsmentioning

confidence: 99%

Extrinsic Repair of Injured Dendrites as a Paradigm for Regeneration by Fusion inCaenorhabditis elegans

Oren‐Suissa

Gattegno

Kravtsov³

et al. 2017

Genetics

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“…Similarly, axonal regenerative ability declines drastically as nematodes advance through development and age (Byrne et al, 2014;Zou et al, 2013). Our knowledge is still poor regarding the regenerative capacity of the dendrite, and how aging affects this process of neuronal repair (Bekkers and Hausser, 2007;Nawabi et al, 2012;Rao et al, 2016). To study dendritic regeneration, we severed the primary dendrites of a PVD neuron in aging adults.…”

Section: Age-dependent Dendrite Remodeling Can Be Modulated By Eff-1mentioning

confidence: 99%

AFF-1 fusogen can rejuvenate the regenerative potential of adult dendritic trees via self-fusion

2017

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The aging brain undergoes structural changes that affect brain homeostasis, neuronal function and consequently cognition. The complex architecture of dendritic arbors poses a challenge to understanding age-dependent morphological alterations, behavioral plasticity and remodeling following brain injury. Here, we use the PVD polymodal neurons of C. elegans as a model to study how aging affects neuronal plasticity. Using confocal live imaging of C. elegans PVD neurons, we demonstrate age-related progressive morphological alterations of intricate dendritic arbors. We show that mutations in daf-2, which encodes an insulin-like growth factor receptor ortholog, fail to inhibit the progressive morphological aging of dendrites and do not prevent the minor decline in response to harsh touch during aging. We uncovered that PVD aging is characterized by a major decline in the regenerative potential of dendrites following experimental laser dendrotomy. Furthermore, the remodeling of transected dendritic trees by AFF-1-mediated self-fusion can be restored in old animals by daf-2 mutations, and can be differentially re-established by ectopic expression of the fusion protein AFF-1. Thus, ectopic expression of the fusogen AFF-1 in the PVD and mutations in daf-2 differentially rejuvenate some aspects of dendritic regeneration following injury.

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“…Like other DRPs (Ferguson and De Camilli, 2012), ATLs have a unique sub-cellular localization and function. ATLs are resident to the tubular ER, where they catalyze membrane fusion to maintain ER morphology; proper control of this process is essential for axonal development, integrity, and signaling (Hu et al, 2009; Muriel et al, 2009; Orso et al, 2009; Rao et al, 2016; Renvoisé and Blackstone, 2010; Rismanchi et al, 2008; Yan et al, 2015; Li et al, 2017). Whereas hATL1 and hATL2 appear to be distributed throughout the tubular ER, hATL3 has a tendency to form puncta at tubule three-way junctions (Wang et al, 2016; Yan et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Timing and Reset Mechanism of GTP Hydrolysis-Driven Conformational Changes of Atlastin

et al. 2017

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Summary The endoplasmic reticulum (ER) forms a branched, dynamic membrane tubule network that is vital for cellular function. Branching arises from membrane fusion facilitated by the GTPase atlastin (ATL). Many metazoan genomes encode for three ATL isoforms that appear to fulfill partially redundant function despite differences in their intrinsic GTPase activity and localization within the ER; however, the underlying mechanistic differences between the isoforms are poorly understood. Here, we identify discrete temporal steps in the catalytic cycle for the two most dissimilar isoforms, ATL1 and ATL3, revealing an overall conserved progression of molecular events from nucleotide binding and hydrolysis, to ATL dimerization and phosphate release. A crystal structure of ATL3 suggests a mechanism for the displacement of the catalytic Mg2+ ion following GTP hydrolysis. Together, the data extend the mechanistic framework for how GTP hydrolysis drives conformational changes in ATL and how the cycle is reset for subsequent rounds of catalysis.

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Spastin, atlastin, and ER relocalization are involved in axon but not dendrite regeneration

Abstract: A Drosophila model system is used to show that the hereditary spastic paraplegia proteins spastin and atlastin help axons but not dendrites regenerate. The endoplasmic reticulum concentrates at tips of regenerating axons but not dendrites, and this depends on spastin and atlastin.

Cited by 62 publications

References 65 publications

Extrinsic Repair of Injured Dendrites as a Paradigm for Regeneration by Fusion inCaenorhabditis elegans

Extrinsic Repair of Injured Dendrites as a Paradigm for Regeneration by Fusion inCaenorhabditis elegans

AFF-1 fusogen can rejuvenate the regenerative potential of adult dendritic trees via self-fusion

Timing and Reset Mechanism of GTP Hydrolysis-Driven Conformational Changes of Atlastin

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