Transient Internalization and Microtubule-Dependent Trafficking of a Ciliary Signaling Receptor from the Plasma Membrane to the Cilium

Ranjan, Peeyush; Awasthi, Mayanka; Snell, William J.

doi:10.1016/j.cub.2019.07.022

Cited by 22 publications

(18 citation statements)

References 52 publications

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“…1a, upper panel) 33 using the adhesion receptors SAG1 on plus cilia and SAD1 on minus cilia. Ciliary adhesion activates a signaling pathway that brings about cellular modifications (gamete activation) that prepare the gametes for fusion 34,35 . A latent, cell wall-associated metalloprotease is converted to an active form that degrades and releases the cell wall, and the gametes generate apically-localized tubular membrane protrusions-the activated mating structures-between their two cilia.…”

Section: Resultsmentioning

confidence: 99%

Species-specific gamete recognition initiates fusion-driving trimer formation by conserved fusogen HAP2

et al. 2021

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Recognition and fusion between gametes during fertilization is an ancient process. Protein HAP2, recognized as the primordial eukaryotic gamete fusogen, is a structural homolog of viral class II fusion proteins. The mechanisms that regulate HAP2 function, and whether virus-fusion-like conformational changes are involved, however, have not been investigated. We report here that fusion between plus and minus gametes of the green alga Chlamydomonas indeed requires an obligate conformational rearrangement of HAP2 on minus gametes from a labile, prefusion form into the stable homotrimers observed in structural studies. Activation of HAP2 to undergo its fusogenic conformational change occurs only upon species-specific adhesion between the two gamete membranes. Following a molecular mechanism akin to fusion of enveloped viruses, the membrane insertion capacity of the fusion loop is required to couple formation of trimers to gamete fusion. Thus, species-specific membrane attachment is the gateway to fusion-driving HAP2 rearrangement into stable trimers.

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Section: Resultsmentioning

confidence: 99%

Species-specific gamete recognition initiates fusion-driving trimer formation by conserved fusogen HAP2

et al. 2021

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“…Mining the genome database of the organisms from diverse taxa and strata has revealed the presence of MTRs from archaea to algae inhabiting in diverse habitats from freshwater to terrestrial environments. The phototactic green alga C. reinhardtii has been extensively studied for learning various aspects of cell biology from photobehavioural responses (especially ChR-mediated) to photosynthesis, cilia biology, intraflagellar transport to vesicle, and membrane-bound trafficking and dynamics [25,26]. The early modular rhodopsins were identified in this green alga and since then very few have been reported in other organisms.…”

Section: Microbial Rhodopsins With Modular Domain Organizationmentioning

confidence: 99%

“…In C. reinhardtii, cAMP induces rapid mobilization of membrane adhesion receptor protein from cell membrane to ciliary membrane in gametes [26] which leads to the adhesion and fusion of gametes to form zygote and hence promotes the sexual life cycle of C. reinhardtii [40]. In the phototaxis mutant strain of C. reinhardtii, cyclase level biases the photobehavioural response and carotenoid biosynthesis [41].…”

Section: Cyclase Domain a Canonical Secondary Messenger Of Modular Sementioning

confidence: 99%

Novel Modular Rhodopsins from Green Algae Hold Great Potential for Cellular Optogenetic Modulation across the Biological Model Systems

Awasthi

Sushmita

Kaushik

et al. 2020

Preprint

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Light-gated ion channel and ion pump rhodopsins are widely used as optogenetic tools and these can control the electrically excitable cells as: (1) they are a single-component system i.e., their sensor and effector functions are encoded by the 7-transmembrane domains and (2) they show fast kinetics with small dark-thermal recovery time. In cellular signaling, a signal receptor, modulator and effector components are involved for attaining synchronous multicomponent regulation. Optical modulation of this network requires either receptor to effector encoded in a single ORF or direct modulation of the effector domain through bypassing all upstream players. Recently discovered modular rhodopsins like rhodopsin guanine cyclase (RhoGC) and rhodopsin phosphodiesterase (RhoPDE) paves the way to establish proof of concept. Light sensor coupled modular system could be expressed in a precise cell type and which holds great potential in the advancement of optogenetics 2.0. It would enable manipulating entire relevant cell signaling system. Here, we had identified 50 novels modular rhodopsins with variant rhodopsins domain and its diverse cognate signaling cascades encoded in a single ORF, which are associated with specialized functions in the cells. These novel modular algal rhodopsins have been characterized functionality based on their sequence and structural homology with previously characterized rhodopsins. Presented novel modular rhodopsins with various effector domains hold potential to expand optogenetics tool kit to regulate various cellular signaling pathways across the diverse biological model systems.

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“…During this flirtation with multicellularity by a unicellular organism, the signaling pathway activated by SAG1-SAD1 interactions exhibits many of the hallmarks of pathways activated by receptor-ligand interactions in animal cells, including changes in the phosphorylation states of proteins and changes in protein location [23][24][25][26]29,30 .…”

Section: Introductionmentioning

confidence: 99%

“…The primary cellular responses to the ciliary adhesion-triggered increase in cellular cAMP occur in the cell body within ~2 minutes after gametes are mixed together. The gametes release their cell walls 38 , mobilize pools of SAG1 and SAD1 from the plasma ` membrane onto the ciliary membrane in a positive feedback mechanism that sustains and enhances adhesion, 30,34,[39][40][41] and erect fusogenic membrane protuberances -mating structures 42 --as the gametes prepare for fusion to form a quadri-ciliated zygote (Fig. 1a).…”

Section: Introductionmentioning

confidence: 99%

A cytoplasmic protein kinase in Chlamydomonas couples engagement of ciliary receptors to rapid cellular responses

Awasthi

Ranjan

Kelterborn

et al. 2021

Preprint

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The principal function of the primary cilium is to convert cues from the extracellular milieu into changes in cyclic nucleotide concentration and cytoplasmic responses, but fundamental questions remain about the mechanisms of transmission of cilium-to-cytoplasm signals. During fertilization in Chlamydomonas reinhardtii, ciliary adhesion between plus and minus gametes triggers an immediate ~10-fold increase in cellular cAMP and activation for cell fusion. Here, we identify Gamete-Specific Protein Kinase (GSPK) as an essential link between cilary receptor engagement and gamete activation. The ciiary adhesion-induced increase in cAMP and cell fusion are severely impaired in gspk mutants but fusion is rescued by a cell-permeable form of cAMP, indicating that GSPK functions upstream of the cAMP increase. GSPK is cytoplasmic, and, remarkably, the entire cellular complement is phosphorylated in less than 60 seconds after ciliary contact. Thus, a cytoplasmic protein kinase rapidly converts a ciliary membrane cue into a global cellular response.

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Transient Internalization and Microtubule-Dependent Trafficking of a Ciliary Signaling Receptor from the Plasma Membrane to the Cilium

Cited by 22 publications

References 52 publications

Species-specific gamete recognition initiates fusion-driving trimer formation by conserved fusogen HAP2

Species-specific gamete recognition initiates fusion-driving trimer formation by conserved fusogen HAP2

Novel Modular Rhodopsins from Green Algae Hold Great Potential for Cellular Optogenetic Modulation across the Biological Model Systems

A cytoplasmic protein kinase in Chlamydomonas couples engagement of ciliary receptors to rapid cellular responses

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