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Function‐Structure Correlations in Cilia from Mammalian Respiratory Tract

Peter Satir, Ellen Roter Dirksen

10.1002/cphy.cp030115

Source: Supplement 10: Handbook of Physiology, The Respiratory System, Circulation and Nonrespiratory Functions

Originally published: 1985

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Distribution and General Organization of Cilia
2 Ciliogenesis
3 Axoneme
4 Ciliary Membrane
4.1 Ciliary Crown
4.2 Freeze‐Fracture Studies and Membrane Organization
4.3 Ciliary Necklace
5 Sliding‐Microtubule Mechanism
5.1 Geometry of Sliding
5.2 Direct Examination of Sliding
5.3 Structure and Function of the Dynein Arm
5.4 Human Dynein
6 Control of Sliding
6.1 Mutant Studies
6.2 Sliding and Switching Mechanisms
6.3 Calcium Ions and Ciliary Arrest
6.4 Membrane Control of Calcium Ion Concentration
6.5 Calmodulin
7 Ciliary Beat
8 Mucociliary Transport
8.1 Periciliary Fluid
8.2 Mucous Layer
9 Function of Metachronism
10 Factors Influencing Mucociliary Clearance
10.1 Effects of Sympathomimetic and Parasympathomimetic Drugs
10.2 Effect of Local Anesthetics
10.3 Relationship of Drug Effects to Axonemal Controls
11 Ciliary Dysfunction in Humans
11.1 Genetic and Structural Implications
12 Summary
Figure 1. Figure 1.

Mucus‐transport velocities (left) and ciliary beat frequencies (right) at different levels of mammalian respiratory tract.

From Sanderson and Sleigh 56
Figure 2. Figure 2.

Scanning electron micrograph of newborn hamster trachea showing distribution of cilia on the epithelium, × 1,900.
Figure 3. Figure 3.

Transmission electron micrograph of rabbit trachea. Interspersed between densely packed cilia are many thin microvilli (m). Basal feet (arrowhead) on cilia point to the left and indicate effective stroke direction. Majority of cilia lie in a gentle curve representing a position near beginning of the recovery stroke, × 16,000.
Figure 4. Figure 4.

A: axoneme as viewed from base to tip. B: isolated axoneme prepared by removing ciliary membrane and staining with tannic acid to demonstrate the number of protofilaments in microtubules and other details of axonemal organization, × 300,000.

A from Satir 86
Figure 5. Figure 5.

A: rabbit tracheal cilia that show the ciliary crown (arrowhead) at their tips. Typical trilaminar unit membrane encloses each cilium. × 93,000. B: rabbit tracheal cilia in cross‐section, demonstrating a few reduced tips with 9 single microtubules (arrowheads). × 81,000.
Figure 6. Figure 6.

Freeze‐fracture image of rat tracheal cilia. At the base of each cilium there is a ciliary necklace. Six necklace strands are labeled (arrowheads) on the protoplasmic fracture face (P). × 80,000. [From Gilula and Satir 31.]
Figure 7. Figure 7.

Transmission electron micrographs of negatively stained preparations of ciliary doublet microtubules, showing sliding after addition of ATP. A: low magnification of a Tetrahymena preparation including regions of overlap of individual doublets (arrows) in a telescoping axoneme. × 9,500. B: Tetrahymena cilia doublets at a higher magnification to demonstrate direction of sliding and doublets numbered N, N + 1, N + 2. The A subfibers of each doublet are marked by the spoke group repeat, × 50,000. C: rabbit tracheal ciliary doublets with overlap as in B. × 26,000.

Micrographs A and B courtesy of W. Sale
Figure 8. Figure 8.

Mechanochemical cycle of dynein arm. Two successive binding sites on subfiber B of doublet N + 1 are indicated. A: 21‐nm‐long arm is bound to distal site in the absence of ATP (rigor). B: addition of ATP causes release and maximal shortening of arm to open an ∼10‐nm interdoublet gap. Release is independent of hydrolysis of ATP. C: arm reextends. In its fully extended position, arm is ∼26‐nm long and tilts basally at an ∼40° angle. D: arm reattaches to subfiber B at the more proximal site. Reextension and reattachment require hydrolysis of ATP, but point at which product release occurs is speculative. E: arm returns to the rigor equilibrium position by relative sliding of doublets N and N + 1 by 16 nm.

From Satir et al. 66
Figure 9. Figure 9.

Top, series of profiles of rabbit tracheal cilia traced from high‐speed cinematographic film (250 frames/s) shows the change in shape of each cilium at intervals of 4 ms during recovery and effective strokes of the beat cycle. Middle, angular position (in degrees) of cilium at different stages of effective stroke. These profiles are a composite of several beat cycles of different cilia because it was not possible to trace successive stages of movement of a single cilium through an entire beat. Bottom, profiles of recovery stroke taken from scanning electron micrographs.

From Sanderson and Sleigh 55
Figure 10. Figure 10.

Demonstration of relationship between propulsive cilia and overlying mucus during the 2 phases of the beat cycle. A, B: scanning electron micrographs of 2 consecutive sections (1 μm thick). Overlying mucus is preserved as a thin continuous sheet. Cilia are seen in profile in various beat positions underneath sheet. C: diagrammatic reconstruction of the relationship. Recovery strokes of cilia occur within the periciliary layer, whereas the effective stroke penetrates, lifts, and propels the mucus.

From Sanderson and Sleigh 56
Figure 11. Figure 11.

Scanning electron micrograph of rabbit trachea showing details of the mucous blanket over the ciliated epithelium. Mucus (M) is situated at tips of the cilia. × 13,500.

From Sturgess 70
Figure 12. Figure 12.

Scanning electron micrographs of rabbit tracheal ciliated epithelia showing different areas of activity. A, B: numerous independent patches of activity that are restricted to areas at the crest of irregular surface undulations. A: × 600. B: × 1,200. C, D: higher magnification of individual areas of activity show resting cilia lying in position reached at end of previous effective stroke. In each patch of beating cilia various stages of the beat cycle surround a central hollow. Cilia at lower and left edges of formation are performing a recovery stroke (R) when viewed from above. Metachronal wave (m) that results moves toward the bottom left of the micrographs. Curved effective stroke (E) moves across the hollow from left to right. C: × 3,000. D: × 4,800. E: large areas of activity are seen in this figure, × 3,900.

From Sanderson and Sleigh 55
Figure 13. Figure 13.

Clearance pattern of a subject with con‐genitally nonfunctioning cilia. Retention of inhaled test particles remains unchanged until subject coughs (A), which helps eliminate some particles. When subject lies down on his side and presses his hands against the other side of his thorax and coughs voluntarily (B), particle clearance increases.

Adapted from Camner et al. 12
Figure 14. Figure 14.

A: normal human cilium from a patient with chronic bronchitis, × 122,000. B: human cilium from a patient whose cilia lack dynein arms, × 122,000. C: human cilium with radial spokes missing; central pair of single microtubules is eccentric and one of the outer doublets is displaced toward axoneme center. × 122,000. D: cross‐section of a human cilium, transposition mutant. In the region of transposition, one of the outer doublets moves to the center. Central pair of microtubules is missing, × 130,000.

Courtesy of J. Sturgess


Figure 1.

Mucus‐transport velocities (left) and ciliary beat frequencies (right) at different levels of mammalian respiratory tract.

From Sanderson and Sleigh 56


Figure 2.

Scanning electron micrograph of newborn hamster trachea showing distribution of cilia on the epithelium, × 1,900.



Figure 3.

Transmission electron micrograph of rabbit trachea. Interspersed between densely packed cilia are many thin microvilli (m). Basal feet (arrowhead) on cilia point to the left and indicate effective stroke direction. Majority of cilia lie in a gentle curve representing a position near beginning of the recovery stroke, × 16,000.



Figure 4.

A: axoneme as viewed from base to tip. B: isolated axoneme prepared by removing ciliary membrane and staining with tannic acid to demonstrate the number of protofilaments in microtubules and other details of axonemal organization, × 300,000.

A from Satir 86


Figure 5.

A: rabbit tracheal cilia that show the ciliary crown (arrowhead) at their tips. Typical trilaminar unit membrane encloses each cilium. × 93,000. B: rabbit tracheal cilia in cross‐section, demonstrating a few reduced tips with 9 single microtubules (arrowheads). × 81,000.



Figure 6.

Freeze‐fracture image of rat tracheal cilia. At the base of each cilium there is a ciliary necklace. Six necklace strands are labeled (arrowheads) on the protoplasmic fracture face (P). × 80,000. [From Gilula and Satir 31.]



Figure 7.

Transmission electron micrographs of negatively stained preparations of ciliary doublet microtubules, showing sliding after addition of ATP. A: low magnification of a Tetrahymena preparation including regions of overlap of individual doublets (arrows) in a telescoping axoneme. × 9,500. B: Tetrahymena cilia doublets at a higher magnification to demonstrate direction of sliding and doublets numbered N, N + 1, N + 2. The A subfibers of each doublet are marked by the spoke group repeat, × 50,000. C: rabbit tracheal ciliary doublets with overlap as in B. × 26,000.

Micrographs A and B courtesy of W. Sale


Figure 8.

Mechanochemical cycle of dynein arm. Two successive binding sites on subfiber B of doublet N + 1 are indicated. A: 21‐nm‐long arm is bound to distal site in the absence of ATP (rigor). B: addition of ATP causes release and maximal shortening of arm to open an ∼10‐nm interdoublet gap. Release is independent of hydrolysis of ATP. C: arm reextends. In its fully extended position, arm is ∼26‐nm long and tilts basally at an ∼40° angle. D: arm reattaches to subfiber B at the more proximal site. Reextension and reattachment require hydrolysis of ATP, but point at which product release occurs is speculative. E: arm returns to the rigor equilibrium position by relative sliding of doublets N and N + 1 by 16 nm.

From Satir et al. 66


Figure 9.

Top, series of profiles of rabbit tracheal cilia traced from high‐speed cinematographic film (250 frames/s) shows the change in shape of each cilium at intervals of 4 ms during recovery and effective strokes of the beat cycle. Middle, angular position (in degrees) of cilium at different stages of effective stroke. These profiles are a composite of several beat cycles of different cilia because it was not possible to trace successive stages of movement of a single cilium through an entire beat. Bottom, profiles of recovery stroke taken from scanning electron micrographs.

From Sanderson and Sleigh 55


Figure 10.

Demonstration of relationship between propulsive cilia and overlying mucus during the 2 phases of the beat cycle. A, B: scanning electron micrographs of 2 consecutive sections (1 μm thick). Overlying mucus is preserved as a thin continuous sheet. Cilia are seen in profile in various beat positions underneath sheet. C: diagrammatic reconstruction of the relationship. Recovery strokes of cilia occur within the periciliary layer, whereas the effective stroke penetrates, lifts, and propels the mucus.

From Sanderson and Sleigh 56


Figure 11.

Scanning electron micrograph of rabbit trachea showing details of the mucous blanket over the ciliated epithelium. Mucus (M) is situated at tips of the cilia. × 13,500.

From Sturgess 70


Figure 12.

Scanning electron micrographs of rabbit tracheal ciliated epithelia showing different areas of activity. A, B: numerous independent patches of activity that are restricted to areas at the crest of irregular surface undulations. A: × 600. B: × 1,200. C, D: higher magnification of individual areas of activity show resting cilia lying in position reached at end of previous effective stroke. In each patch of beating cilia various stages of the beat cycle surround a central hollow. Cilia at lower and left edges of formation are performing a recovery stroke (R) when viewed from above. Metachronal wave (m) that results moves toward the bottom left of the micrographs. Curved effective stroke (E) moves across the hollow from left to right. C: × 3,000. D: × 4,800. E: large areas of activity are seen in this figure, × 3,900.

From Sanderson and Sleigh 55


Figure 13.

Clearance pattern of a subject with con‐genitally nonfunctioning cilia. Retention of inhaled test particles remains unchanged until subject coughs (A), which helps eliminate some particles. When subject lies down on his side and presses his hands against the other side of his thorax and coughs voluntarily (B), particle clearance increases.

Adapted from Camner et al. 12


Figure 14.

A: normal human cilium from a patient with chronic bronchitis, × 122,000. B: human cilium from a patient whose cilia lack dynein arms, × 122,000. C: human cilium with radial spokes missing; central pair of single microtubules is eccentric and one of the outer doublets is displaced toward axoneme center. × 122,000. D: cross‐section of a human cilium, transposition mutant. In the region of transposition, one of the outer doublets moves to the center. Central pair of microtubules is missing, × 130,000.

Courtesy of J. Sturgess
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Article Title: Function‐Structure Correlations in Cilia from Mammalian Respiratory Tract
 

How to Cite

Peter Satir, Ellen Roter Dirksen. Function‐Structure Correlations in Cilia from Mammalian Respiratory Tract. Compr Physiol 2011, Supplement 10: Handbook of Physiology, The Respiratory System, Circulation and Nonrespiratory Functions: 473-494. First published in print 1985. doi: 10.1002/cphy.cp030115