Evidence for role of flagella as sensory transducers in mating of Chlamydomonas reinhardi

Solter, Kenneth M.; Gibor, Aharon

doi:10.1038/265444a0

Cited by 64 publications

(28 citation statements)

References 10 publications

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“…CALK, kinesins and signal transduction To our knowledge, the work reported here is the first evidence for a role of kinesin II in protein translocation induced during sensory transduction (Solter and Gibor, 1977) in cilia or flagella. Chemosensation in C. elegans has been shown to require a functional IFT system (Cole et al, 1998;Haycraft et al, 2001;Qin et al, 2001;Signor et al, 1999a;Signor et al, 1999b), but the requirement is indirect: the C. elegans IFT mutants fail to undergo sensory transduction because of their inability to assemble structurally intact cilia, not because of the failure of their assembled cilia to function (Collet et al, 1998;Haycraft et al, 2001;Perkins et al, 1986).…”

Section: Discussionmentioning

confidence: 97%

Kinesin II and regulated intraflagellar transport ofChlamydomonasaurora protein kinase

Pan

Snell

2003

Journal of Cell Science

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The assembly and functioning of cilia and flagella depend on a complex system of traffic between the organelles and the cell body. Two types of transport into these organelles have been identified. The best characterized is constitutive: in a process termed intraflagellar transport (IFT), flagellar structural components are continuously carried into cilia and flagella on transport complexes termed IFT particles via the microtubule motor protein kinesin II. Previous studies have shown that the flagella of the unicellular green alga Chlamydomonas exhibit a second type of protein import that is regulated. During fertilization, the Chlamydomonas aurora protein kinase CALK undergoes regulated translocation from the cell body into the flagella. The motor that powers this second, regulated type of movement is unknown. Here, we have examined the cellular properties of the CALK in Chlamydomonas and used a kinesin II mutant to test the idea that the motor protein is essential for regulated translocation of proteins into flagella. We found that the CALK that is transported into flagella of wild-type gametes becomes part of a membrane-associated complex, that kinesin II is essential for the normal localization of this Chlamydomonasaurora protein kinase in unactivated gametes and that the cAMP-induced translocation of the protein kinase into flagella is disrupted in the fla10 mutants. Our results indicate that, in addition to its role in the constitutive transport of IFT particles and their cargo, kinesin II is essential for regulated translocation of proteins into flagella.

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Section: Discussionmentioning

confidence: 97%

Kinesin II and regulated intraflagellar transport ofChlamydomonasaurora protein kinase

Pan

Snell

2003

Journal of Cell Science

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“…CALK and Gamete Activation during Fertilization-It is likely that the function of CALK in flagella is more related to the sensory and signaling properties of Chlamydomonas flagella than to their motile functions (65,66). For example, it could be one of the protein kinase activities implicated in known steps in gamete activation and fertilization.…”

Section: Discussionmentioning

confidence: 99%

Regulated Targeting of a Protein Kinase into an Intact Flagellum

Pan

Snell

2000

Journal of Biological Chemistry

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In the green alga Chlamydomonas reinhardtii flagellar adhesion between gametes of opposite mating types leads to rapid cellular changes, events collectively termed gamete activation, that prepare the gametes for cell-cell fusion. As is true for gametes of most organisms, the cellular and molecular mechanisms that underlie gamete activation are poorly understood. Here we report on the regulated movement of a newly identified protein kinase, Chlamydomonas aurora/Ipl1p-like protein kinase (CALK), from the cell body to the flagella during gamete activation. CALK encodes a protein of 769 amino acids and is the newest member of the aurora/ Ipl1p protein kinase family. Immunoblotting with an anti-CALK antibody showed that CALK was present as a 78/80-kDa doublet in vegetative cells and unactivated gametes of both mating types and was localized primarily in cell bodies. In cells undergoing fertilization, the 78-kDa CALK was rapidly targeted to the flagella, and within 5 min after mixing gametes of opposite mating types, the level of CALK in the flagella began to approach levels normally found in the cell body. Protein synthesis was not required for targeting, indicating that the translocated CALK and the cellular molecules required for its movement are present in unactivated gametes. CALK was also translocated to the flagella during flagellar adhesion of nonfusing mutant gametes, demonstrating that cell fusion was not required for movement. Finally, the requirement for flagellar adhesion could be bypassed; incubation of cells of a single mating type in dibutyryl cAMP led to CALK translocation to flagella in gametes but not vegetative cells. These experiments document a new event in gamete activation in Chlamydomonas and reveal the existence of a mechanism for regulated translocation of molecules into an intact flagellum.Cell-cell interactions leading to fusion between gametes of opposite sexes during fertilization are complex processes that involve dramatic changes in each of the interacting gametes. In most multicellular organisms, interactions between adhesion molecules/receptors on the sperm plasma membrane and ligands on the egg surface activate poorly understood signaling pathways that bring about transformation of the sperm into a fusion competent, activated gamete (1). For example, the sperm surface is remodeled as a consequence of the acrosome reaction, an event that accompanies gamete activation, and previously existing adhesion molecules are mobilized to new sites on the sperm (2-4). The molecular mechanisms that underlie and regulate signal transduction and movement of molecules between different gamete compartments during gamete activation largely are unknown (2).As in multicellular organisms, gamete activation and fertilization in the unicellular green alga Chlamydomonas (5) depend on adhesion-induced signaling pathways and intercompartmental communication. At the completion of gametogenesis, during which asexually growing mtϩ and mtϪ vegetative cells differentiate into sexually competent cells, the resultin...

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“…In Caenorhabditis elegans, cilia are present in 60 out of the 302 neurons, in which they function as sensory organelles (Bargmann and Horvitz, 1991;Dwyer et al, 1998). In Chlamydomonas, flagella transduce signals during gamete adhesion in mating (Solter and Gibor, 1977;Pan and Snell, 2002). Furthermore, in the mouse, the polaris protein is required for formation both of 9+0 cilia such as node monocilia (Murcia et al, 2000) and of 9+2 cilia such as those in brain ependymal cells.…”

Section: Role Of Inv In Lr Determinationmentioning

confidence: 99%

The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia

et al. 2003

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Inv (Inv∆C) including the ankyrin repeats also localized to the node cilia and rescued the left-right defects of Inv/Inv mutants. Although no obvious abnormalities were detected in the node monocilia of Inv/Inv embryos, the laterality defects of such embryos were corrected by an artificial leftward flow of fluid in the node, suggesting that nodal flow is impaired by the Inv mutation. These results suggest that the Inv protein contributes to left-right determination as a component of monocilia in the node and is essential for the generation of normal nodal flow.Movie available online

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Evidence for role of flagella as sensory transducers in mating of Chlamydomonas reinhardi

Cited by 64 publications

References 10 publications

Kinesin II and regulated intraflagellar transport ofChlamydomonasaurora protein kinase

Kinesin II and regulated intraflagellar transport ofChlamydomonasaurora protein kinase

Regulated Targeting of a Protein Kinase into an Intact Flagellum

The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia

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