Abstract
Cilia are ancient organelles used by unicellular and multicellular organisms not only for motility but also to receive and respond to multiple environmental cues, including light, odorants, morphogens, growth factors, and contact with cilia of other cells. Much is known about the cellular mechanisms that deliver membrane proteins to cilia during ciliogenesis. Execution of a ciliary signaling pathway, however, can critically depend on rapid alterations in the receptor composition of the cilium itself, and our understanding of the mechanisms that underlie these rapid, regulated alterations remains limited [1–6]. In the bi-ciliated, unicellular alga Chlamydomonas reinhardtii, interactions between cilia of mating type plus and mating type minus gametes mediated by adhesion receptors SAG1 and SAD1 activate a ciliary signaling pathway [7]. In response, a large, inactive pool of SAG1 on the plasma membrane of plus gametes rapidly becomes enriched in the peri-ciliary membrane and enters the cilia to become active and maintain and enhance ciliary adhesion and signaling [8–14]. Ciliary entry per se of SAG1 is independent of anterograde intraflagellar transport (IFT) [13], but the rapid apical enrichment requires cytoplasmic microtubules and the retrograde IFT motor, dynein 1b [14]. Whether the receptors move laterally within the plasma membrane or transit internally during redistribution is unknown. Here, in coupled immunolocalization/biochemical studies on SAG1, we show that, within minutes after gamete activation is initiated, cell-surface SAG1 is internalized, associates with an apico-basally polarized array of cytoplasmic microtubules, and returns to the cell surface at a peri-ciliary staging area for entry into cilia.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 2942-2947.e2 |
| Journal | Current Biology |
| Volume | 29 |
| Issue number | 17 |
| DOIs | |
| State | Published - Sep 9 2019 |
| Externally published | Yes |
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Keywords
- Chlamydomonas
- cilia
- ciliary entry
- ciliary signaling
- cytoplasmic microtubules
- membrane protein polarization
- membrane protein trafficking
- peri-ciliary membrane
- protein internalization
- protein redistribution
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Agricultural and Biological Sciences(all)
Cite this
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.
In: Current Biology, Vol. 29, No. 17, 09.09.2019, p. 2942-2947.e2.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Transient Internalization and Microtubule-Dependent Trafficking of a Ciliary Signaling Receptor from the Plasma Membrane to the Cilium
AU - Ranjan, Peeyush
AU - Awasthi, Mayanka
AU - Snell, William J.
PY - 2019/9/9
Y1 - 2019/9/9
N2 - Cilia are ancient organelles used by unicellular and multicellular organisms not only for motility but also to receive and respond to multiple environmental cues, including light, odorants, morphogens, growth factors, and contact with cilia of other cells. Much is known about the cellular mechanisms that deliver membrane proteins to cilia during ciliogenesis. Execution of a ciliary signaling pathway, however, can critically depend on rapid alterations in the receptor composition of the cilium itself, and our understanding of the mechanisms that underlie these rapid, regulated alterations remains limited [1–6]. In the bi-ciliated, unicellular alga Chlamydomonas reinhardtii, interactions between cilia of mating type plus and mating type minus gametes mediated by adhesion receptors SAG1 and SAD1 activate a ciliary signaling pathway [7]. In response, a large, inactive pool of SAG1 on the plasma membrane of plus gametes rapidly becomes enriched in the peri-ciliary membrane and enters the cilia to become active and maintain and enhance ciliary adhesion and signaling [8–14]. Ciliary entry per se of SAG1 is independent of anterograde intraflagellar transport (IFT) [13], but the rapid apical enrichment requires cytoplasmic microtubules and the retrograde IFT motor, dynein 1b [14]. Whether the receptors move laterally within the plasma membrane or transit internally during redistribution is unknown. Here, in coupled immunolocalization/biochemical studies on SAG1, we show that, within minutes after gamete activation is initiated, cell-surface SAG1 is internalized, associates with an apico-basally polarized array of cytoplasmic microtubules, and returns to the cell surface at a peri-ciliary staging area for entry into cilia.
AB - Cilia are ancient organelles used by unicellular and multicellular organisms not only for motility but also to receive and respond to multiple environmental cues, including light, odorants, morphogens, growth factors, and contact with cilia of other cells. Much is known about the cellular mechanisms that deliver membrane proteins to cilia during ciliogenesis. Execution of a ciliary signaling pathway, however, can critically depend on rapid alterations in the receptor composition of the cilium itself, and our understanding of the mechanisms that underlie these rapid, regulated alterations remains limited [1–6]. In the bi-ciliated, unicellular alga Chlamydomonas reinhardtii, interactions between cilia of mating type plus and mating type minus gametes mediated by adhesion receptors SAG1 and SAD1 activate a ciliary signaling pathway [7]. In response, a large, inactive pool of SAG1 on the plasma membrane of plus gametes rapidly becomes enriched in the peri-ciliary membrane and enters the cilia to become active and maintain and enhance ciliary adhesion and signaling [8–14]. Ciliary entry per se of SAG1 is independent of anterograde intraflagellar transport (IFT) [13], but the rapid apical enrichment requires cytoplasmic microtubules and the retrograde IFT motor, dynein 1b [14]. Whether the receptors move laterally within the plasma membrane or transit internally during redistribution is unknown. Here, in coupled immunolocalization/biochemical studies on SAG1, we show that, within minutes after gamete activation is initiated, cell-surface SAG1 is internalized, associates with an apico-basally polarized array of cytoplasmic microtubules, and returns to the cell surface at a peri-ciliary staging area for entry into cilia.
KW - Chlamydomonas
KW - cilia
KW - ciliary entry
KW - ciliary signaling
KW - cytoplasmic microtubules
KW - membrane protein polarization
KW - membrane protein trafficking
KW - peri-ciliary membrane
KW - protein internalization
KW - protein redistribution
UR - http://www.scopus.com/inward/record.url?scp=85071684326&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85071684326&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2019.07.022
DO - 10.1016/j.cub.2019.07.022
M3 - Article
C2 - 31422889
AN - SCOPUS:85071684326
VL - 29
SP - 2942-2947.e2
JO - Current Biology
JF - Current Biology
SN - 0960-9822
IS - 17
ER -