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Who drives the ciliary highway?

Malicki J - Bioarchitecture (2012)

Bottom Line: In multicellular organisms, multiple kinesins are known to drive ciliary transport, and frequently cilia of a single cell type require more than one kinesin for their formation and function.In addition to kinesin-2 family motors, which function in cilia of all species investigated so far, kinesins from other families contribute to the transport of signaling proteins in a tissue-specific manner.It is becoming increasingly obvious that functional relationships between ciliary kinesins are complex, and a good understanding of these relationships is essential to comprehend the basis of biological processes as diverse as olfaction, vision, and embryonic development.

View Article: PubMed Central - PubMed

Affiliation: MRC Centre for Developmental and Biomedical Genetics; Department of Biomedical Science; The University of Sheffield; Sheffield, UK.

ABSTRACT
Cilia are protrusions on the surface of cells. They are frequently motile and function to propel cells in an aqueous environment or to generate fluid flow. Equally important is the role of immotile cilia in detecting environmental changes or in sensing extracellular signals. The structure of cilia is supported by microtubules, and their formation requires microtubule-dependent motors, kinesins, which are thought to transport both structural and signaling ciliary proteins from the cell body into the distal portion of the ciliary shaft. In multicellular organisms, multiple kinesins are known to drive ciliary transport, and frequently cilia of a single cell type require more than one kinesin for their formation and function. In addition to kinesin-2 family motors, which function in cilia of all species investigated so far, kinesins from other families contribute to the transport of signaling proteins in a tissue-specific manner. It is becoming increasingly obvious that functional relationships between ciliary kinesins are complex, and a good understanding of these relationships is essential to comprehend the basis of biological processes as diverse as olfaction, vision, and embryonic development.

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Figure 2. A subset of cilia differentiate in kif3bjj203 mutant embryos. In (A, A’, B and B’), shown are wild-type (A and B) and mutant (A’ and B’) embryos stained with anti-acetylated tubulin antibody at 3 (B and B’) and 7 (A and A’) dpf. (A and A’) Confocal images of a macula in the zebrafish ear. Cilia (arrows) are present in both wild type and mutant. (B and B’) Confocal images of a crista of the zebrafish ear. Cilia (arrows) are absent in the mutant. (C, C’ and D’) Electron micrographs of sections through wild-type (C and D) and mutant (C’ and D’) photoreceptor cells at 3.5 (C and C’) and 5 (D and D’) dpf. Photoreceptor outer segments [OS, asterisks in (C?E)] are initially absent in the mutant. (E) A schematic drawing of the vertebrate photoreceptor cell (after Kennedy and Malicki, 2009). The outer segment membrane is in red. Microtubules that support its structure are in blue. In this work, term “cilium” is used to mean the structure that includes the connecting cilium and the outer segment. The outer segment (OS) forms in the distal part of photoreceptor cilia, which differentiates membrane folds. The connecting cilium (CC), on the other hand, is the proximal region of photoreceptor cilia, and displays characteristics of the ciliary transition zone. OLM, outer limiting membrane.
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Figure 2: Figure 2. A subset of cilia differentiate in kif3bjj203 mutant embryos. In (A, A’, B and B’), shown are wild-type (A and B) and mutant (A’ and B’) embryos stained with anti-acetylated tubulin antibody at 3 (B and B’) and 7 (A and A’) dpf. (A and A’) Confocal images of a macula in the zebrafish ear. Cilia (arrows) are present in both wild type and mutant. (B and B’) Confocal images of a crista of the zebrafish ear. Cilia (arrows) are absent in the mutant. (C, C’ and D’) Electron micrographs of sections through wild-type (C and D) and mutant (C’ and D’) photoreceptor cells at 3.5 (C and C’) and 5 (D and D’) dpf. Photoreceptor outer segments [OS, asterisks in (C?E)] are initially absent in the mutant. (E) A schematic drawing of the vertebrate photoreceptor cell (after Kennedy and Malicki, 2009). The outer segment membrane is in red. Microtubules that support its structure are in blue. In this work, term “cilium” is used to mean the structure that includes the connecting cilium and the outer segment. The outer segment (OS) forms in the distal part of photoreceptor cilia, which differentiates membrane folds. The connecting cilium (CC), on the other hand, is the proximal region of photoreceptor cilia, and displays characteristics of the ciliary transition zone. OLM, outer limiting membrane.

Mentions: The zebrafish is the most recent model used to study the genetics of vertebrate ciliary kinesins.37,38 The analysis of kinesin-2 family genes in this organism has recently revealed that, surprisingly, cilia of several tissues persist in kif3b mutants. These include the cilia of two sensory cell types, auditory hair cells and cone photoreceptors, as well as some cilia in the spinal canal (ref. 37, and unpublished results). (In the context of the photoreceptor cell, I will use the term “cilium” as meaning the connecting cilium and the outer segment, Figure 2E). At least two aspects of mutant phenotypes in these cell types deserve additional commentary. First, although all wild-type auditory hair cells grossly display the same morphological features, such as the presence of the apical kinocilium and an array of stereocilia, it is only the hair cells of auditory cristae that retain cilia in kif3b mutants (Fig. 2B and B’). In the neighboring maculae, cilia of mutant hair cells are not maintained (Fig. 2A and A’). The second intriguing observation is that cilia of kif3b mutant cone photoreceptors differentiate after a delay (Fig. 2C, C’, D and D’). This has not been observed in mouse conditional mutants,39 perhaps due to a late onset of Cre expression, which may preclude the analysis of kif3a function at the earliest stages of photoreceptor differentiation. A delay of cilia formation in mutant zebrafish suggests the existence of a redundant transport mechanism that is initially absent and becomes active only at a later stage of cell differentiation. The evidence for the presence of such a mechanism is outlined below.


Who drives the ciliary highway?

Malicki J - Bioarchitecture (2012)

Figure 2. A subset of cilia differentiate in kif3bjj203 mutant embryos. In (A, A’, B and B’), shown are wild-type (A and B) and mutant (A’ and B’) embryos stained with anti-acetylated tubulin antibody at 3 (B and B’) and 7 (A and A’) dpf. (A and A’) Confocal images of a macula in the zebrafish ear. Cilia (arrows) are present in both wild type and mutant. (B and B’) Confocal images of a crista of the zebrafish ear. Cilia (arrows) are absent in the mutant. (C, C’ and D’) Electron micrographs of sections through wild-type (C and D) and mutant (C’ and D’) photoreceptor cells at 3.5 (C and C’) and 5 (D and D’) dpf. Photoreceptor outer segments [OS, asterisks in (C?E)] are initially absent in the mutant. (E) A schematic drawing of the vertebrate photoreceptor cell (after Kennedy and Malicki, 2009). The outer segment membrane is in red. Microtubules that support its structure are in blue. In this work, term “cilium” is used to mean the structure that includes the connecting cilium and the outer segment. The outer segment (OS) forms in the distal part of photoreceptor cilia, which differentiates membrane folds. The connecting cilium (CC), on the other hand, is the proximal region of photoreceptor cilia, and displays characteristics of the ciliary transition zone. OLM, outer limiting membrane.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: Figure 2. A subset of cilia differentiate in kif3bjj203 mutant embryos. In (A, A’, B and B’), shown are wild-type (A and B) and mutant (A’ and B’) embryos stained with anti-acetylated tubulin antibody at 3 (B and B’) and 7 (A and A’) dpf. (A and A’) Confocal images of a macula in the zebrafish ear. Cilia (arrows) are present in both wild type and mutant. (B and B’) Confocal images of a crista of the zebrafish ear. Cilia (arrows) are absent in the mutant. (C, C’ and D’) Electron micrographs of sections through wild-type (C and D) and mutant (C’ and D’) photoreceptor cells at 3.5 (C and C’) and 5 (D and D’) dpf. Photoreceptor outer segments [OS, asterisks in (C?E)] are initially absent in the mutant. (E) A schematic drawing of the vertebrate photoreceptor cell (after Kennedy and Malicki, 2009). The outer segment membrane is in red. Microtubules that support its structure are in blue. In this work, term “cilium” is used to mean the structure that includes the connecting cilium and the outer segment. The outer segment (OS) forms in the distal part of photoreceptor cilia, which differentiates membrane folds. The connecting cilium (CC), on the other hand, is the proximal region of photoreceptor cilia, and displays characteristics of the ciliary transition zone. OLM, outer limiting membrane.
Mentions: The zebrafish is the most recent model used to study the genetics of vertebrate ciliary kinesins.37,38 The analysis of kinesin-2 family genes in this organism has recently revealed that, surprisingly, cilia of several tissues persist in kif3b mutants. These include the cilia of two sensory cell types, auditory hair cells and cone photoreceptors, as well as some cilia in the spinal canal (ref. 37, and unpublished results). (In the context of the photoreceptor cell, I will use the term “cilium” as meaning the connecting cilium and the outer segment, Figure 2E). At least two aspects of mutant phenotypes in these cell types deserve additional commentary. First, although all wild-type auditory hair cells grossly display the same morphological features, such as the presence of the apical kinocilium and an array of stereocilia, it is only the hair cells of auditory cristae that retain cilia in kif3b mutants (Fig. 2B and B’). In the neighboring maculae, cilia of mutant hair cells are not maintained (Fig. 2A and A’). The second intriguing observation is that cilia of kif3b mutant cone photoreceptors differentiate after a delay (Fig. 2C, C’, D and D’). This has not been observed in mouse conditional mutants,39 perhaps due to a late onset of Cre expression, which may preclude the analysis of kif3a function at the earliest stages of photoreceptor differentiation. A delay of cilia formation in mutant zebrafish suggests the existence of a redundant transport mechanism that is initially absent and becomes active only at a later stage of cell differentiation. The evidence for the presence of such a mechanism is outlined below.

Bottom Line: In multicellular organisms, multiple kinesins are known to drive ciliary transport, and frequently cilia of a single cell type require more than one kinesin for their formation and function.In addition to kinesin-2 family motors, which function in cilia of all species investigated so far, kinesins from other families contribute to the transport of signaling proteins in a tissue-specific manner.It is becoming increasingly obvious that functional relationships between ciliary kinesins are complex, and a good understanding of these relationships is essential to comprehend the basis of biological processes as diverse as olfaction, vision, and embryonic development.

View Article: PubMed Central - PubMed

Affiliation: MRC Centre for Developmental and Biomedical Genetics; Department of Biomedical Science; The University of Sheffield; Sheffield, UK.

ABSTRACT
Cilia are protrusions on the surface of cells. They are frequently motile and function to propel cells in an aqueous environment or to generate fluid flow. Equally important is the role of immotile cilia in detecting environmental changes or in sensing extracellular signals. The structure of cilia is supported by microtubules, and their formation requires microtubule-dependent motors, kinesins, which are thought to transport both structural and signaling ciliary proteins from the cell body into the distal portion of the ciliary shaft. In multicellular organisms, multiple kinesins are known to drive ciliary transport, and frequently cilia of a single cell type require more than one kinesin for their formation and function. In addition to kinesin-2 family motors, which function in cilia of all species investigated so far, kinesins from other families contribute to the transport of signaling proteins in a tissue-specific manner. It is becoming increasingly obvious that functional relationships between ciliary kinesins are complex, and a good understanding of these relationships is essential to comprehend the basis of biological processes as diverse as olfaction, vision, and embryonic development.

Show MeSH
Related in: MedlinePlus