Transport of fungal RAB11 secretory vesicles involves myosin-5, dynein/dynactin/p25, and kinesin-1 and is independent of kinesin-3

Peñalva, Miguel; Zhang, Jun; Xiang, Xin; Pantazopoulou, Areti

doi:10.1091/mbc.e16-08-0566

Cited by 58 publications

(113 citation statements)

References 86 publications

(158 reference statements)

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“…The deletion of kinA in A. nidulans or kin-1 in N. crassa impaired hyphal growth and the delivery of exoenzymes, but it did not abolish hyphal extension (33,(151)(152)(153). There is recent convincing evidence that conventional kinesin indeed transports secretion vesicles toward the hyphal tip (85,154). The deletion of other kinesins, such as UncA, kinesin-7 (KipA), or kinesin-8 (KipB), possibly involved in plus-end-directed transportation, as well as double or triple deletions thereof, did not affect hyphal extension (155).…”

Section: The Fungal Cytoskeleton the Microtubule Cytoskeletonmentioning

confidence: 99%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

273

246

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SUMMARYFilamentous fungi constitute a large group of eukaryotic microorganisms that grow by forming simple tube-like hyphae that are capable of differentiating into more-complex morphological structures and distinct cell types. Hyphae form filamentous networks by extending at their tips while branching in subapical regions. Rapid tip elongation requires massive membrane insertion and extension of the rigid chitin-containing cell wall. This process is sustained by a continuous flow of secretory vesicles that depends on the coordinated action of the microtubule and actin cytoskeletons and the corresponding motors and associated proteins. Vesicles transport cell wall-synthesizing enzymes and accumulate in a special structure, the Spitzenkörper, before traveling further and fusing with the tip membrane. The place of vesicle fusion and growth direction are enabled and defined by the position of the Spitzenkörper, the so-called cell end markers, and other proteins involved in the exocytic process. Also important for tip extension is membrane recycling by endocytosis via early endosomes, which function as multipurpose transport vehicles for mRNA, septins, ribosomes, and peroxisomes. Cell integrity, hyphal branching, and morphogenesis are all processes that are largely dependent on vesicle and cytoskeleton dynamics. When hyphae differentiate structures for asexual or sexual reproduction or to mediate interspecies interactions, the hyphal basic cellular machinery may be reprogrammed through the synthesis of new proteins and/or the modification of protein activity. Although some transcriptional networks involved in such reprogramming of hyphae are well studied in several model filamentous fungi, clear connections between these networks and known determinants of hyphal morphogenesis are yet to be established.

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Section: The Fungal Cytoskeleton the Microtubule Cytoskeletonmentioning

confidence: 99%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

273

246

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“…The identification of the Slm‐related protein AN4171 as a RabE RAB11 effector was intriguing, considering that yeast Slm1/2p localize(s) to eisosomes (Grossmann et al ., ; Olivera‐Couto et al ., ). In contrast RabE RAB11 , which regulates the biogenesis of secretory vesicles (SVs) destined to the PM, localizes to the TGN, to SVs en route to the apex and, strongly, to the apical gathering of SVs at the Spitzenkörper (SPK) (Pantazopoulou et al ., ; Pinar et al ., ; Peñalva et al ., ). This led us to use subcellular localization as the means to emphasize the predictably different physiological roles of these proteins.…”

Section: Resultsmentioning

confidence: 97%

“…B) and movies (Supporting Information Movie 1). Figure C shows that the SPK localization of BapH was rapidly (within 5 min) dispersed by latrunculin B treatment, as would be expected if BapH were a component of RabE RAB11 carriers, whose dynamic localization to the SPK is dependent on F‐actin (Pantazopoulou et al ., ; Peñalva et al ., ). Therefore, BapH is not a component of eisosomes and its localization is consistent with its being a RabE RAB11 effector.…”

Section: Resultsmentioning

confidence: 97%

“…RabE RAB11 SVs ‘released’ from the SPK by F‐actin depolymerization undergo rapid bidirectional movement on microtubules, using kinesin‐1 and dynein (Peñalva et al ., ). This movement was not affected by bapHΔ (Supporting Information Fig.…”

Section: Resultsmentioning

confidence: 97%

“…Recruitment of this regulatory GTPase to TGN membranes is promoted by the oligomeric guanine nucleotide exchange factor (GEF) complex TRAPPII (Pinar et al ., ). Once RabE RAB11 levels reach a certain threshold on TGN cisternae these compartments, or domains thereof, acquire SV identity and subsequently engage molecular motors to be transported to the apex (Pantazopoulou et al ., ; Peñalva et al ., ), where SVs accumulate in a structure denoted Spitzenkörper (SPK), awaiting fusion with the plasma membrane. TGN cisternae also deliver clathrin‐coated carriers to the endosomal system (Schultzhaus et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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Aspergillus nidulans BapH is a RAB11 effector that connects membranes in the Spitzenkörper with basal autophagy

Pinar

Peñalva

2017

Molecular Microbiology

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Using affinity chromatography we identified the Aspergillus nidulans F-BAR-and-PH domain-containing protein BapH as a RabE effector. BapH localizes to the Spitzenkörper (SPK) in an F-actin- and Sec7-dependent manner, becoming cytosolic after inactivation of Trs120 in TRAPPII, the oligomeric GEF for RabE . Therefore, RabE contributes to the recruitment of BapH to secretory vesicles in vivo. BapH has a close homologue, SlmA, which is related to yeast Slm1p/Slm2p, localizes to eisosomes and does not bind RabE . bapHΔ, slmAΔ and double bapHΔ slmAΔ mutations do not affect growth, although slmAΔ results in myriocin hypersensitivity. Both the PH and the F-BAR domain in BapH are necessary to recruit the protein to membranes, whereas its C-terminal moiety negatively regulates localization to the SPK. Strong overexpression of full-length BapH or of BapH lacking the C-terminal moiety impairs growth. The tandemly duplicated PH domain is recruited to the plasma membrane in a manner dependent on critical Lys residues in its 'noncanonical' lipid binding pocket, suggesting that it binds to biological membranes containing PtdIns(4,5)P . Ablation of BapH, or deletion of the PH or BAR domains critical for the SPK localization increases autophagy under nitrogen-replete conditions. Therefore, BapH localizing to SPK vesicles influences basal levels of autophagy.

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Kymolyzer, a Semi‐Autonomous Kymography Tool to Analyze Intracellular Motility

et al. 2020

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The movement of intracellular cargo, such as transcripts, proteins, and organelles, is fundamental to cellular function. Neurons, due to their long axons and dendrites, are particularly dependent on proper intracellular trafficking and vulnerable to defects in the movement of intracellular cargo that are noted in neurodegenerative and neurodevelopmental disorders. Accurate quantification of intracellular transport is therefore needed for studying the mechanisms of cargo trafficking, the influence of mutations, and the effects of potentially therapeutic pharmaceuticals. In this article, we introduce an algorithm called “Kymolyzer.” The algorithm can quantify intracellular trafficking along a defined path, such as that formed by the aligned microtubules of axons and dendrites. Kymolyzer works as a semi‐autonomous kymography software application. It constructs and analyzes kymographs to measure the movement and distribution of fluorescently tagged objects along a user‐defined path. The algorithm can be used under a wide variety of experimental conditions and can extract a diverse array of motility parameters describing intracellular movement, including time spent in motion, percentage of objects in motion, percentage of objects that are stationary, and velocities of motile objects. This article serves as a user manual describing the design of Kymolyzer, providing a stepwise protocol for its use and illustrating its functions with common examples. © 2020 Wiley Periodicals LLC Basic Protocol: Kymolyzer, a semi‐autonomous kymography tool to analyze intracellular motility

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Transport of fungal RAB11 secretory vesicles involves myosin-5, dynein/dynactin/p25, and kinesin-1 and is independent of kinesin-3

Abstract: In Aspergillus nidulans, the distribution of exocytic carriers involves interplay between kinesin-1, myosin-5, and dynein. Engagement of the dynein complex to these carriers requires dynactin p25, but, unlike that of early endosomes, it does not require the Hook complex.

Cited by 58 publications

References 86 publications

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Aspergillus nidulans BapH is a RAB11 effector that connects membranes in the Spitzenkörper with basal autophagy

Kymolyzer, a Semi‐Autonomous Kymography Tool to Analyze Intracellular Motility

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