Comprehensive Physiology Wiley Online Library

Cilia and Related Microtubular Arrays in the Eukaryotic Cell

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Cell Biology of Microtubules
1.1 Microtubules and the Cytoskeleton
1.2 Structure, Assembly, and Disassembly
1.3 Stability and Pattern Formation
1.4 Primary Cilia
2 Evolution of Centrioles, Cilia, and Microtubules
3 Motor Molecules of Cilia and Microtubule‐Based Arrays
3.1 Dynein‐ and Microtubule‐Based Motility
3.2 Axonemal Dynein
3.3 Cytoplasmic Dynein
3.4 Kinesin
3.5 The Kinesin Superfamily
3.6 Interactions Between Dynein and Kinesin
3.7 Other Putative Motors
4 Motile Cilia and the Mechanism of Motility
4.1 Introduction to Ciliary Structure
4.2 Experimental Analysis of Motility
4.3 Cellular Control of Ciliary Motility
Figure 1. Figure 1.

Some representative microtubule patterns in cells with (+) and (−) ends of microtubules indicated. A: Cycling, motile interphase cells. B: Mitotic cell. C: G0 cell with 1° cilium. D: G0 cell with centrioles. E: Neuron.

From Satir et al. with permission
Figure 2. Figure 2.

A: Domain organization of tubulin dimers and protofilaments. α and β subunits of heterodimers are shown adding to ends of two protofilaments. One end has cap of exposed β subunits; other, a cap of α subunits. B: Outside and inside views of microtubule protofilament. Speculative model based on x‐ray diffraction analysis. C: Model of microtubule calculated by 3D reconstruction methods. D: Summary of some structural features of tubulin. Representations of the 1° structure of α and β tubulin. N (open) and C (black) terminal domains are defined by cleavage sites at arg 339 and cys 354. Regions I‐IV are predicted to participate in nucleotide binding; regions of Tau, MAP2, and monoclonal antibody binding are indicated.

From Mandelkow and Mandelkow with permission. From Amos and Amos with permission. From Amos and Amos with permission. From Mandelkow and Mandelkow with permission
Figure 3. Figure 3.

A: Treadmilling in microtubule. Thickened region moves through microtubule toward (−) end. Bar, 10 μm. B: Dynamic instability of microtubules. At 84 s, (+) end undergoes catastrophic shortening. Bar, 2 μm C: Effect of MAPs on dynamic instability of microtubules. Changes in microtubule length with time at (+) (black symbols) and (−) (open symbols) ends of microtubule are shown. In absence of MAPs (circles) catastrophic depolymerization is seen. This is suppressed in presence of MAPs (squares).

From Hotani and Horio with permission. From Walker et al. with permission. From Hotani and Horio with permission
Figure 4. Figure 4.

A: Microtubule distribution in cultured hepatocytes. Confocal microscopic reconstruction of group of cells showing tubulin immunofluorescent pattern. Arrow marks cell where array radiating from centrioles is seen. Bar, 10 μm. B: Model of microtubule distribution in cultured hepatocyte. C: Vesicular trafficking along microtubule. Top: Kinesin‐based motility. Bottom: Cytoplasmic dynein‐based motility. The (+) and (−) ends of the microtubule are indicated. D: Model of microtubule‐based vesicular trafficking in a polarized epithelial cell with 1° cilium. Microtubule‐based motors could move vesicles in basal to apical direction or apical to basal direction along polarized array of microtubules. This would require, respectively, (−) end‐directed motor, such as cytoplasmic dynein and (+) end‐directed motor such as kinesin to interact with vesicular membranes.

From Novikoff et al. with permission. From Satir et al. with permission. From Phillips and Satir with permission
Figure 5. Figure 5.

Top: Demonstration of microtubule sliding in beating sea urchin sperm axoneme. Gold beads placed on different doublets of axoneme move apart as sliding proceeds. Bottom: Diagram of in vitro translocation system at high magnification. Individual three‐headed dynein molecules are placed on substratum. Microtubules are introduced. Dynein binds to microtubules, translocating them across field when ATP is added. Inset: Two structural forms of dynein.

From Brokaw with permission. Courtesy K. Barkalow and T. Hamasaki
Figure 6. Figure 6.

Molecular motors. Left: Rotary shadowed images of (a) ciliary dynein, (b) cytoplasmic dynein, (c) myosin II, and (d) kinesin.

Courtesy of John Heuser, Washington University. Bar, 40 nm. Right: Diagrams. From Vale with permission. Adapted from Vale
Figure 7. Figure 7.

A: a: Alignment of putative nucleotide‐binding sites in dynein β heavy chain. Residues identical in two or more sites appear in boxes. b: Alignment of probable hydrolytic ATP‐binding sites of dynein β chain (GKT2) with other motors and E. coli Clp protease A subunit. Residues identical to dynein GKT2 sequence appear in boxes. B: Map of principal tryptic and proteolytic cleavage sites on dynein β chain. Numbers above middle line give masses of tryptic peptides (M X10−3) for comparison to numbers in parentheses calculated from derived sequence. N‐termini of the 110k, 215k, 130k, and 124k tryptic peptides are indicated as T4, T1, T2, and T3, respectively. V1 and V2 vanadate‐sensitive photocleavage sites are indicated. Thick regions of map indicate peptides that are stable to trypsin at 37°C. 6S region may represent tail, 12S region the globular domain of heavy chain.

From Gibbons et al. with permission. From Gibbons et al. with permission
Figure 8. Figure 8.

Above: Cross sections of an intact cilium (left) and axoneme after detergent treatment (right). Bar = 0.1 μm. Below: Three‐dimensional computer model of ciliary axoneme at resolution approaching 4 nm, based on electron micrographs of ciliary axoneme.

From Satir with permission. See Sugrue et al. for details. With permission
Figure 9. Figure 9.

Sliding of axonemal microtubules captured in negative stain electron microscopy; active arms on subfiber A of doublet N push doublet N+1 in a tipward (+) direction, while doublet N moves relatively baseward. Bar, 0.1 μm.

Satir with permission
Figure 10. Figure 10.

Axonemal splitting in “hands down” vs. “hands up” axonemes supports “switch point hypothesis” of dynein arm activity. Above: Predictions of arm activity in axonemes arrested by ions shown. Shaded areas and black arms indicate predicted active arms. Below: Split axonemes Left: “hands down.” Right: “hands up.” The central pair splits with active half axoneme. Bar = 0.1 μm.

From Satir with permission
Figure 11. Figure 11.

Top: Cross and longitudinal sections of mussel gill filaments with active (left panels) and arrested (middle, right panels) lateral cilia (arrows). Repeating pattern shows metachronal waves of beating cilia captured by fixation. Arrested cilia are in either “hands down” (middle panels) or “hands up” (right panels) configuration, corrresponding to end of effective and recovery strokes, respectively. Bar, 10 μm. Bottom: Rat sperm flagellar axonemes reactivated in low ATP concentrations (0.3 mM) under conditions where only half beats are present (a) in EGTA with no added Ca2+ or (b) with Ca2+, balancing chelator concentration. Bends form in one direction only. At higher ATP concentrations, full beating resumes.

From Satir and Matsuoka with permission. From Lindemann and Goltz with permission
Figure 12. Figure 12.

Computer‐generated bending patterns reconstructed for wild type (wt) and mutant Chlamydomonas. Each pattern shows images of 0.125 cycle intervals with cell body fixed in position. Above: Mutants missing outer dynein arms compared to wt in form and beat frequency. Below: Mutants missing inner dynein arms. Sample size indicated.

From Brokaw and Kamiya with permission
Figure 13. Figure 13.

Velocity profiles of microtubule translocation over Paramecium 22S dynein comparing controls (open bars), dynein pretreated with cAMP to phosphorylate p29 (black bars), and dynein pretreated with cAMP and Ca2+ (hatched bars).

From Hamasaki et al. with permission
Figure 14. Figure 14.

Transduction cascade by which cAMP activates 22S outer arm dynein to increase microtubule sliding velocity, beat frequency, and speed of ciliate swimming.

Adapted from Satir et al. with permission


Figure 1.

Some representative microtubule patterns in cells with (+) and (−) ends of microtubules indicated. A: Cycling, motile interphase cells. B: Mitotic cell. C: G0 cell with 1° cilium. D: G0 cell with centrioles. E: Neuron.

From Satir et al. with permission


Figure 2.

A: Domain organization of tubulin dimers and protofilaments. α and β subunits of heterodimers are shown adding to ends of two protofilaments. One end has cap of exposed β subunits; other, a cap of α subunits. B: Outside and inside views of microtubule protofilament. Speculative model based on x‐ray diffraction analysis. C: Model of microtubule calculated by 3D reconstruction methods. D: Summary of some structural features of tubulin. Representations of the 1° structure of α and β tubulin. N (open) and C (black) terminal domains are defined by cleavage sites at arg 339 and cys 354. Regions I‐IV are predicted to participate in nucleotide binding; regions of Tau, MAP2, and monoclonal antibody binding are indicated.

From Mandelkow and Mandelkow with permission. From Amos and Amos with permission. From Amos and Amos with permission. From Mandelkow and Mandelkow with permission


Figure 3.

A: Treadmilling in microtubule. Thickened region moves through microtubule toward (−) end. Bar, 10 μm. B: Dynamic instability of microtubules. At 84 s, (+) end undergoes catastrophic shortening. Bar, 2 μm C: Effect of MAPs on dynamic instability of microtubules. Changes in microtubule length with time at (+) (black symbols) and (−) (open symbols) ends of microtubule are shown. In absence of MAPs (circles) catastrophic depolymerization is seen. This is suppressed in presence of MAPs (squares).

From Hotani and Horio with permission. From Walker et al. with permission. From Hotani and Horio with permission


Figure 4.

A: Microtubule distribution in cultured hepatocytes. Confocal microscopic reconstruction of group of cells showing tubulin immunofluorescent pattern. Arrow marks cell where array radiating from centrioles is seen. Bar, 10 μm. B: Model of microtubule distribution in cultured hepatocyte. C: Vesicular trafficking along microtubule. Top: Kinesin‐based motility. Bottom: Cytoplasmic dynein‐based motility. The (+) and (−) ends of the microtubule are indicated. D: Model of microtubule‐based vesicular trafficking in a polarized epithelial cell with 1° cilium. Microtubule‐based motors could move vesicles in basal to apical direction or apical to basal direction along polarized array of microtubules. This would require, respectively, (−) end‐directed motor, such as cytoplasmic dynein and (+) end‐directed motor such as kinesin to interact with vesicular membranes.

From Novikoff et al. with permission. From Satir et al. with permission. From Phillips and Satir with permission


Figure 5.

Top: Demonstration of microtubule sliding in beating sea urchin sperm axoneme. Gold beads placed on different doublets of axoneme move apart as sliding proceeds. Bottom: Diagram of in vitro translocation system at high magnification. Individual three‐headed dynein molecules are placed on substratum. Microtubules are introduced. Dynein binds to microtubules, translocating them across field when ATP is added. Inset: Two structural forms of dynein.

From Brokaw with permission. Courtesy K. Barkalow and T. Hamasaki


Figure 6.

Molecular motors. Left: Rotary shadowed images of (a) ciliary dynein, (b) cytoplasmic dynein, (c) myosin II, and (d) kinesin.

Courtesy of John Heuser, Washington University. Bar, 40 nm. Right: Diagrams. From Vale with permission. Adapted from Vale


Figure 7.

A: a: Alignment of putative nucleotide‐binding sites in dynein β heavy chain. Residues identical in two or more sites appear in boxes. b: Alignment of probable hydrolytic ATP‐binding sites of dynein β chain (GKT2) with other motors and E. coli Clp protease A subunit. Residues identical to dynein GKT2 sequence appear in boxes. B: Map of principal tryptic and proteolytic cleavage sites on dynein β chain. Numbers above middle line give masses of tryptic peptides (M X10−3) for comparison to numbers in parentheses calculated from derived sequence. N‐termini of the 110k, 215k, 130k, and 124k tryptic peptides are indicated as T4, T1, T2, and T3, respectively. V1 and V2 vanadate‐sensitive photocleavage sites are indicated. Thick regions of map indicate peptides that are stable to trypsin at 37°C. 6S region may represent tail, 12S region the globular domain of heavy chain.

From Gibbons et al. with permission. From Gibbons et al. with permission


Figure 8.

Above: Cross sections of an intact cilium (left) and axoneme after detergent treatment (right). Bar = 0.1 μm. Below: Three‐dimensional computer model of ciliary axoneme at resolution approaching 4 nm, based on electron micrographs of ciliary axoneme.

From Satir with permission. See Sugrue et al. for details. With permission


Figure 9.

Sliding of axonemal microtubules captured in negative stain electron microscopy; active arms on subfiber A of doublet N push doublet N+1 in a tipward (+) direction, while doublet N moves relatively baseward. Bar, 0.1 μm.

Satir with permission


Figure 10.

Axonemal splitting in “hands down” vs. “hands up” axonemes supports “switch point hypothesis” of dynein arm activity. Above: Predictions of arm activity in axonemes arrested by ions shown. Shaded areas and black arms indicate predicted active arms. Below: Split axonemes Left: “hands down.” Right: “hands up.” The central pair splits with active half axoneme. Bar = 0.1 μm.

From Satir with permission


Figure 11.

Top: Cross and longitudinal sections of mussel gill filaments with active (left panels) and arrested (middle, right panels) lateral cilia (arrows). Repeating pattern shows metachronal waves of beating cilia captured by fixation. Arrested cilia are in either “hands down” (middle panels) or “hands up” (right panels) configuration, corrresponding to end of effective and recovery strokes, respectively. Bar, 10 μm. Bottom: Rat sperm flagellar axonemes reactivated in low ATP concentrations (0.3 mM) under conditions where only half beats are present (a) in EGTA with no added Ca2+ or (b) with Ca2+, balancing chelator concentration. Bends form in one direction only. At higher ATP concentrations, full beating resumes.

From Satir and Matsuoka with permission. From Lindemann and Goltz with permission


Figure 12.

Computer‐generated bending patterns reconstructed for wild type (wt) and mutant Chlamydomonas. Each pattern shows images of 0.125 cycle intervals with cell body fixed in position. Above: Mutants missing outer dynein arms compared to wt in form and beat frequency. Below: Mutants missing inner dynein arms. Sample size indicated.

From Brokaw and Kamiya with permission


Figure 13.

Velocity profiles of microtubule translocation over Paramecium 22S dynein comparing controls (open bars), dynein pretreated with cAMP to phosphorylate p29 (black bars), and dynein pretreated with cAMP and Ca2+ (hatched bars).

From Hamasaki et al. with permission


Figure 14.

Transduction cascade by which cAMP activates 22S outer arm dynein to increase microtubule sliding velocity, beat frequency, and speed of ciliate swimming.

Adapted from Satir et al. with permission
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Peter Satir. Cilia and Related Microtubular Arrays in the Eukaryotic Cell. Compr Physiol 2011, Supplement 31: Handbook of Physiology, Cell Physiology: 787-817. First published in print 1997. doi: 10.1002/cphy.cp140120