Types Of Cilia Research Articles

Vertebrate primary cilia: a sensory part of centrosomal complex in tissue cells, but a "sleeping beauty" in cultured cells?

Primary cilium development along with other components of the centrosome in mammalian cells was analysed ultrastructurally and by immunofluorescent staining with anti-acetylated tubulin antibodies. We categorized two types of primary cilia, nascent cilia that are about 1microm long located inside the cytoplasm, and true primary cilia that are several microm long and protrude from the plasma membrane. The primary cilium is invariably associated with the older centriole of each diplosome, having appendages at the distal end and pericentriolar satellites with cytoplasmic microtubules emanating from them. Only one cilium per cell is formed normally through G(0), S and G(2)phases. However, in some mouse embryo fibroblasts with two mature centrioles, bicilates were seen. Primary cilia were not observed in cultured cells where the mature centriole had no satellites and appendages (Chinese hamster kidney cells, line 237, some clones of l-fibroblasts). In contrast to primary cilia, striated rootlets were found around active and non-active centrioles with the same frequency. In proliferating cultured cells, a primary cilium can be formed several hours after mitosis, in fibroblasts 2-4 h after cell division and in PK cells only during the S-phase. In interphase cells, formation of the primary cilium can be stimulated by the action of metabolic inhibitors and by reversed depolymerization of cytoplasmic microtubules with cold or colcemid treatments. In mouse renal epithelial cells in situ, the centrosome was located near the cell surface and mature centrioles in 80% of the cells had primary cilium protruding into the duct lumen. After cells were explanted and subcultured, the centrosome comes closer to the nucleus and the primary cilium was depolymerized or reduced. Later primary cilia appeared in cells that form islets on the coverslip. However, the centrosome in cultured ciliated cells was always located near the cell nucleus and primary cilium never formed a characteristic distal bulb. A sequence of the developmental stages of the primary cilium is proposed and discussed. We also conclude that functioning primary cilium does not necessarily operate in culture cells, which might explain some of the contradictory data on cell ciliation in vitro reported in the literature.

Cell Biology of Normal and Abnormal Ciliogenesis in the Ciliated Epithelium

Ciliogenesis is divided into four stages: (1) generation of centrioles, (2) migration of duplicated centrioles, (3) formation of the basal body-associated structures, and (4) elongation of cilia. The ultrastructural profile of ciliogenesis is fundamentally the same among various kinds of animal species. In acentriolar centriologenesis, centrioles are generated around deuterosomes by the use of fibrous granules. Components of the centriolar precursor structures, and genes that regulate the differentiation of ciliated cells, have been revealed. Ciliary abnormalities are classified into two categories: specific congenital defects of ciliary structure and acquired nonspecific anomalies of the ciliary apparatus. When ciliogenesis is disturbed, various nonspecific ciliary abnormalities develop in the cell. Inhibition of centriole migration results in the development of intracytoplasmic axonemes, cilia within periciliary sheaths, and intracellular ciliated vacuoles. Swollen cilia and the bulging type of compound cilia are formed during ciliary budding and elongation. Primary cilia can also develop from one of a pair of centrioles. They lack dynein arms and are immobile, but work as a mechanosensor and play a role during morphogenesis of the kidney. Abnormal function or structure of primary cilia results in the development of polycystic kidney disease. The axonemes of primary cilia or monocilia in the embryonic node cells are associated with dynein arms and move vortically. They have a role in determining the left-right (L-R) asymmetry of the fetus. This review also discusses the ciliogenesis of a primary cilium in the cell.

Immunohistochemical and ultrastructural study of chordoid glioma of the third ventricle: its tanycytic differentiation

A chordoid glioma in the third ventricle was studied immunohistochemically and ultrastructurally. In this report, special attention is paid to the histogenesis in relation to the pathological appearance and unique anatomic location of this tumor. Light microscopic and immunohistochemical findings were similar to those reported previously. Ultrastructurally, microvilli were frequently seen, but three types of abnormal cilia were rarely observed. Basement membrane around the tumor cells and microvessels was extensive. Poorly to moderately developed intermediate (adherent) junctions were frequently seen. Resemblance of these ultrastructural features of the tumor to embryonic tanycytes suggests the tanycytic differentiation of chordoid glioma. Neuroradiologically, all of the previously reported cases of chordoid gliomas seem to arise in the anterior part of the third ventricular floor. This region includes the lamina terminalis, infundibular recess and median eminence, which corresponds to a tanycyte-rich area. These findings suggest a tanycytic origin of chordoid glioma.

Early Ontogeny of the Japanese Common Squid Todarodes pacificus (Cephalopoda, Ommastrephidae) with Special Reference to its Characteristic Morphology and Ecological Significance

Early ontogeny of the Japanese Common Squid Todarodes pacificus was described for artificially inseminated and collected specimens to present new criteria for developmental stages in relation to its ecological adaptation. For the purpose, details for formation of the following organs and tissues were observed with special attention: cilia on the integument, mouth part, shell sac and stellate ganglia, visceral mass, funnel-collar complex, statocysts, eye parts, and ventral photosensitive vesicles. At the embryonic stage (i.e., pre-hatching), various types of epidermal cilia that seem to work as the embryonic rotation were detected. At the early postembryonic stage (i.e., post-hatching), the epidermal lines were characteristically arranged at the scattered condition on arms, tentacles, head, and funnel. Novel strong muscle fibers were distinct in the base of tentacles and funnel retractor muscles at the early postembryonic stage, which is clearly related to the head withdrawal behavior of the paralarvae. The lip cilia and toothed beak developed at the early postembryonic stage, but disappeared later; these apparatus were considered to be related with a change of unique feeding mode in the paralarval life. Based on such morphological features, four distinct stages, namely, paralarval stage 1, 2, 3, and juvenile stage are proposed. The present observations are discussed in relation to survival strategy at early life of T. pacificus and they are compared with those in other cephalopods.

Ciliogenesis and ciliary abnormalities.

Cilia are motile processes extending from the basal bodies, playing important roles in the mucociliary clearance in the respiratory tract and the transport of the ovum from the ovary to the uterus in mammals. Ciliogenesis is divided into four stages: (1) duplication of centrioles; (2) migration of centrioles to the apical cell surface to become basal bodies; (3) elongation of cilia containing the axoneme; and (4) formation of accessory structures of basal bodies. The orderly course of ciliogenesis appears to be disturbed by various internal and external factors and, as a result, various unusual forms of the ciliary apparatus develop in the cell. Inhibition of basal body migration results in development of intracytoplasmic axonemes, cilia within periciliary sheaths, and intracellular ciliated cysts. Swollen cilia and the bulging type of compound cilia are formed during ciliary budding and elongation. This review also discusses the origin, composition, and function of the centriolar precursor structures.

Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice.

Cilia have been classified as sensory or motile types on the basis of functional and structural characteristics; however, factors important for regulation of assembly of different cilia types are not well understood. Hepatocyte nuclear factor-3/forkhead homologue 4 (HFH-4) is a winged helix/forkhead transcription factor expressed in ciliated cells of the respiratory tract, oviduct, and ependyma in late development through adulthood. Targeted deletion of the Hfh4 gene resulted in defective ciliogenesis in airway epithelial cells and randomized left-right asymmetry so that half the mice had situs inversus. In HFH-4-null mice, classic motile type cilia with a 9 + 2 microtubule ultrastructure were absent in epithelial cells, including those in the airways. In other organs, sensory cilia with a 9 + 0 microtubule pattern, such as those on olfactory neuroepithelial cells, were present. Ultrastructural analysis of mutant cells with absent 9 + 2 cilia demonstrated that defective ciliogenesis was due to abnormal centriole migration and/or apical membrane docking, suggesting that HFH-4 functions to direct basal body positioning or anchoring. Evaluation of wild-type embryos at gestational days 7.0 to 7.5 revealed Hfh4 expression in embryonic node cells that have monocilium, consistent with a function for this factor at the node in early determination of left- right axis. Analysis of the node of HFH-4 mutant embryos revealed that, in contrast to absent airway cilia, node cilia were present. These observations indicate that there are independent regulatory pathways for node ciliogenesis compared with 9 + 2 type ciliogenesis in airways, and support a central role for HFH-4 in ciliogenesis and left-right axis formation.

Rotation of the central pair microtubules in eukaryotic flagella.

SUMMARY It has been 20 years since the phenomenon of centralpair rotation in eukaryotic flagella was reported(Omoto, and Kung, 1979). At that time, a model wasproposed in which the central pair functions as adistributor to regulate dynein activity among the outerdoublet microtubules. The video evidence obtainedsince then and gathered together in this essay is con-sistent with this model. Geometric arguments indicatethat there must be circumferential and longitudinalregulation of shear forces to produce effective bendingmotion of an axoneme. Central pair microtubules areideally situated to perform this regulatory function.The regulation of outer doublet sliding by the centralpair, together with the rotation of the latter, where thisoccurs, may explain the wide diversity of two- andthree-dimensional flagellar and ciliary waveforms thatis found in organisms using the same basic 9 1 2structure. ACKNOWLEDGMENTS We thank Mike McLaughlin of Material Media Services, Washing-ton State University for converting 16-mm film to video format, andDenise A. Palmen (Technical Services, Washington State University)for editing the videos, assembling the QuickTime movies, and pro-ducing the jpeg images to use as figures. The research based onvideo images shown in this essay was first published by Kamiya(1982), Omoto and Witman (1981), Gibbons

Embryogenesis, Morphology and Ultrastructure of the Pericalymma Larva of Acila castrensis (Bivalvia: Protobranchia: Nuculoida)

The pericalymma larva of the protobranch bivalve Acila castrensis is described from sections and whole mounts using light and electron microscopy. This is one of few published descriptions of a protobranch larva and the first ultrastructural study of a member of the order Nuculoida. Comparisons with other protobranch pericalymmae are made with respect to size, morphology, ciliation, development mode, and larval period. Early embryogenesis follows a typical bivalve pattern and by day 5 results in a fully formed, barrel-shaped pericalymma with prominent apical tuft. The larva is planktic and lecithotrophic. It propels itself with three transverse bands of cilia and a patch of accessory locomotory cilia. Late-stage larvae become laterally compressed as the shell develops. Metamorphosis occurs at day 8 with shedding of the larval test. The pericalymma of A. castrensis most closely resembles that of Nucula proxima and N. turgida. They share features that are possibly unique to the Nuculidae including an ovoid form, 2 ab-apical openings in the test, a post-anal structure, no statocyst, and reduced musculature. The post-anal organ of A. castrensis is a unique larval organ possessing two types of cilia and a small cavity near the tip. The organ begins to form during mid-embryogenesis and most likely serves as a sensory device in site selection or as a locomotory director, but may perform other functions. The protobranch pericalymma may represent a modification of the veliger larva form, a precursor to the veliger form, or the veliger and pericalymma may have diverged from a common ancestral developmental form. The pericalymma also shares morphological similarities with the developmental forms of aplacophorans, archaeogastropods, polyplacophorans, and scaphopods; all possess a test or velum with ciliary bands, and some possess a posterior protrusion. Further work is needed among these developmental forms to ascertain structural homologies and phylogenetic affinities. Additional key words: bivalve evolution, developmental form, larval organ, test, velum The pericalymma larva of protobranch bivalves differs from the typical veliger larvae of most marine lamellibranchs in being barrel-shaped and cloaked with an outer, cellular, locomotory test or calyrnma. The test entirely covers the developing larva, including the shell, and is cast off at metamorphosis at which time the new juvenile commences a benthic existence. The term pericalymma was originally applied to a larval form considered primitive among the annelids, molluscs, and sipunculans (Salvini-Plawen 1972, 1973, 1980). We have adopted the term in a narrower sense, as others have, to refer to the larval form of protobranch bivalves and aplacophorans (Jablonski & a Author for correspondence. E-mail: jzardus @ lynx.neu.edu Currently on leave at the National Science Foundation, Arlington, Virginia 22230, USA Lutz 1983; Gustafson & Reid 1986, 1988a, 1988b; Gustafson 1987; Gustafson & Lutz 1992; Morse & Zardus 1997). Though distinct from other bivalve developmental forms, pericalymma morphology and embryogenesis are not uniform within the subclass Protobranchia, which includes the orders Nuculoida and Solemyoida and 11 or 12 families (Allen & Hannah 1986; Maxwell 1988). The full range of form and development in this subclass remains largely unknown, as few species have been examined. Previous descriptions consist of early accounts of 3 nuculoids (Drew 1897, 1899a, 1899b, 1901) and recent ultrastructural investigations of 2 solemyoids (Gustafson & Reid 1986, 1988a, 1988b; Gustafson 1987; Gustafson & Lutz 1992). Only 3 of these studies follow development from the single-cell stage (Drew 1901; Gustafson & Reid 1986; Gustafson & Lutz 1992).

Postembryonic Growth of Two Peripheral Sensory Systems in the Medicinal Leech Hirudo medicinalis.

The midbody segments of Hirudo medicinalis have two types of sensory cilia that project from the skin into the surrounding water. These are the proposed mechanosensory S cilia and the putative chemosensory G cilia. The cells bearing these cilia are clustered together into structures known as sensilla. The skin of each midbody segment is externally divided into five annuli. Fourteen large sensilla carrying S and G cilia are found on the central annulus of each segment. Small sensilla carrying only G cilia are found on all five annuli. In this paper we show a positive correlation between the size of a neural sensillum and the number of S and G cilia it contains. Any one leech contains a range of sizes of neural sensilla, but the average area increases with the weight of the leech. In contrast, the annular sensilla show only a modest increase in size with leech weight.

Generation of monoclonal antibodies detecting specific epitopes in olfactory and respiratory epithelia

Two panels of monoclonal antibodies have been generated, each panel having a distinct specificity for antigens located in the ciliary zone of either the olfactory or respiratory epithelium of rats. Tissue specificity was confirmed in enzyme-linked immunosorbent assays on membrane fractions from various tissues. During ontogeny, the expression of olfactory-specific antigens preceeds that of respiratory-specific antigens; this observation correlates with differences in the genesis of the respective cilia type and confirms that different molecular entities are recognized. A spatial segregation of immunoreactivity in the chemosensory epithelium was observed for one of the olfactory-specific monoclonal antibodies; negative zones were located in the dorsal recess of the nasal cavity and on the tips of the turbinates. Olfactory-specific antibodies reacted with distinct polypeptide bands on Western blots from olfactory ciliary preparations.

Con A Binds to the Membranellar and Somatic Cilia of Stentor and to the Developing Oral Primordium During Oral Regeneration1

ABSTRACTBinding sites for Concanavalin A have been located in the ciliate Stentor coeruleus by utilizing FITC‐Con A and fluorescence microscopy. When both nonregenerating and regenerating Stentor are fixed prior to FITC‐Con A exposure, FITC‐Con A binds intensely to the cilia of the membranellar band and to the somatic cilia that cover much of the cell surface. No binding is observed between the ciliary rows. The FITC‐Con A also binds to the developing oral primordia of regenerating cells. Binding of FITC‐Con A in the early stages of regeneration (prior to stage 4) appears to be less intense than that in the later stages. Additional FITC‐Con A binding appeared as a granular fluorescence in the area of the developing buccal cavity beginning at about stage 4 and disappearing around stages 6–7. The presence of α‐D‐methyl mannoside prevented the binding of FITC‐Con A to either regenerating or nonregenerating cells. If nonregenerating Stentor are exposed to FITC‐Con A prior to fixation, the binding pattern is entirely different with the fluorescence primarily in the form of random, granular patches spread over much of the cell but with no binding to either type of cilia. These results demonstrate that membrane glycoproteins capable of binding Con A are located primarily in the membranellar and somatic cilia and in the developing oral primordia during oral regeneration in Stentor. Concanavalin A binding to these sites may be involved in the Con A‐induced inhibition of oral regeneration observed in earlier studies.

Functional morphology of the larval tentacles of Phragmatopoma californica (Polychaeta: Sabellariidae): composite larval and adult organs of multifunctional significance

Larvae of the sabellariid polychaete Phragmatopoma californica (Fewkes), which were collected in San Diego, California and were competent to metamorphose after 18 to 30 d of development were observed in vivo by videoequipped light microscopy, and the fine structure of the larval tentacles was examined by transmission and scanning electron microscopy. Each tentacle has tufts of at least two types of immotile cilia arranged in dorsolateral and ventrolateral rows, and a ventral groove covered by two types of motile cilia that beat independently of each other. The epidermis is regionalized into glandular, sensory, locomotory, and support cell types and contains four longitudinal bundles of basiepithelial nerve fibers. A layer of connective tissue separates the epidermis and the nerve tracts from obliquely striated muscles that occur within the peritoneum that lines the central coelomic cavities. The peritoneum forms an intact coelomic epithelium that overlies and interdigitates with the muscle cells, with no intervening basal lamina. The muscle cells are considered to be intraperitoneal because they are located above the basal lamina and they lack intercellular junctions with the peritoneal cells. Specialized peritoneal cells form a striated myoepithelial blood vessel that partitions the coelom into medial and lateral cavities. No neuromuscular junctions were found, but both muscular and ciliary movement seem to be under neuronal control. The basiepithelial nerve terminals appear to synapse into the connective tissue layer toward the intraperitoneal muscle. Several similarities in tissue organization are noted between the larval tentacles of P. californica and the tube feet of echinoderms. Observations on the ontogeny, morphology, and behavior of the tentacles suggest that they are multifunctional organs involved in feeding, construction of the juvenile sand tube, locomotion, attachment, and sensory perception during larval and adult lives.

Abnormal cilia in the small airways of mice induced by bleomycin

The frequency and types of abnormal cilia in the small airways before and after parenteral administration of bleomycin were examined by transmission electron microscopy. Bleomycin was injected subcutaneously at a dose of 40 mg/kg twice weekly for 6 weeks. Bronchioles less than 0.1 mm in diameter from animals sacrificed 1 day after a single dose, 1 day after three doses, 3 days after 8 doses, and 13 days after 12 doses were selected for evaluation. Although ciliated cells proper did not show pronounced alterations, abnormal cilia such as swollen cilia, compound cilia, and cilia with abnormal axonemes frequently occurred. Repeated injections did not necessarily induce much more abnormal cilia than one dose. The results suggested that ciliated cells remain undamaged and that normal cilia can be restored. The specific type of abnormal cilia induced by bleomycin was not identified.

Cilia in the fetal and neonatal canine retina

Cilia in the canine retina were examined at 40, 46 and 50 days of gestation and at birth by scanning electron microscopy, transmission electron microscopy, and by the freeze-fracture technique. Cilia were similar in all age groups examined. Scanning electron micrographs showed them to be smooth-surfaced conical to tubular extensions arising from putative photoreceptor inner segments. Cilia when frecze-fractured contained variable numbers ot circumferential rows of 10 nm P-face particles: these constitute the ciliary necklace. Transmission electron micrographs showed the ciliary membrane to contain electron-dense beads which corresponded to the ciliary necklace seen in freeze-fracture replicas. The ciliary necklace identified in the developing canine retina was similar to those found in other types of motile and sensory cilia.

Changes in morphology and physiology of olfactory receptor cilia during development

Ciliated olfactory receptor neurons in vertebrates turn over throughout life. We show that these neurons bear different types of cilia at different developmental stages; cilia on newly differentiating cells are short and motile; cilia on mature cells are longer and immotile; Mg 2+ and adenosine 5′-triphosphate are requisite for ciliary motion; stimulation with odorants can induce synchronous motion and that this process is mediated by Ca 2+. We propose that receptor neurons have two distinguishable developmental states. In the first, before the growing axon establishes synaptic connection to the brain, the cells bear motile cilia and are generally irritable. In the second, the cilia are long and immotile and the cells can distinguish between odorants.

Fine structure of the 'wulst' region of the domestic fowl in organotypic cultures.

Parts of the ‘Wulst’ region of the chick embryo brain were maintained for 39 days in vitro. Processes of adjacent glial cell form zonulae occludentes and desmosomal junctions in the uppermost stratum of the cultures. Subjacent to this layer, in the neuropil, axodendritic synapses are abundant. 10–20 μm below the surface the perikarya of glial cells and neurons are found. The latter form small clusters, plasma membranes of contiguous cells being directly apposed to each other. Axosomatic synapses terminate on the perikarya. Occasionally one terminal synapses on two nerve cells simultaneously. Two types of cilia arise from basal bodies in the cytoplasm of nerve cells. Type I is a slender protrusion of about 0.5 μm in diameter, extending into the neuropil. On transverse sections it displays a 9 + 0 pattern of organization of paired micro tubules proximally, and an 8 + 1 configuration more distally. The length of the cilium is approximately 7 μm. Type II cilia also originate in the neuronal cytoplasm. The structure of the proximal portion is identical with that of type I cilia. Toward the tip, however, the type II cilium is characterized by a bulbous enlargement which is filled with loosely folded membranes. The fine structural details of this cilium correlate closely to the outer segments of retinal photoreceptor cells during differentiation. The possible role of a light receptor in the ‘Wulst’ region of birds, controlling biological rhythms, is discussed.

The Basal Apparatus of Bovine Retinal Rods

Several types of mammalian sensory receptor cells possess modified cilia which may play a primary role in stimulus detection. Axonemes and basal apparatus from other types of cilia and flagella have been isolated, characterized and compared in detail. In this communication we report results of what may be the first attempt to isolate and characterize such structures from a sensory cilium, the bovine retinal rod outer segment.Bovine eyes were obtained from a nearby abattoir, the retinas were removed and swirled vigorously in a cold solution of 50% sucrose, 5 mM Tris, 2 mM MgCl2, pH 7.5, to detach outer segments. The suspension was then filtered through cheesecloth and the filtrate was centrifuged at 20,000 rpm for 1 hr. Rod outer segments were collected from the solution surface, diluted, layered onto a continuous sucrose gradient (25-38% sucrose in Tris MgCl2 buffer) and centrifuged for 3-12 hrs. at 10,000 rpm.

The histology and fine structure of the olfactory organ of the squid Lolliguncula brevis blainville

The olfactory organ of the squid has a thick, pseudostratified epithelium containing five morphological types of ciliated receptors. In the simplest receptors the cilia originate separately in the distal pole of the cell. All other receptors have some type of cilia filled cavity, varying from a simple pocket of cilia at the surface to a completely closed vesicle filled with cilia in cells deep in the epithelium. The receptors are compared to cells in the rhinophore of Nautilus and the olfactory organs of coleoid cephalopods. Possible functions of the olfactory organ, based on its morphology, are discussed.

Ciliary membrane differentiations in Tetrahymena pyriformis. Tetrahymena has four types of cilia.

We have examined thin sections and replicas of freeze-fractured cilia of Tetrahymena pyriformis. The ciliary necklace located at the base of all freeze-fractured oral and somatic cilia has been studied in thin sections. Since electron-dense linkers have been found to connect both microtubule doublets and triplets to the ciliary membrane at the level of the necklace, the linkers and the associated necklace seem to be related to the transition region between the doublets and triplets of a cilium. Plaque structures, consisting of small rectangular patches of particles located distal to the ciliary necklace, are found in strain GL, but are absent in other strains examined in this study. In freeze-cleaved material, additional structural differentiations are observed in the distal region of the ciliary membranes of somatic and oral cilia. Somatic cilia contain many randomly distributed particles within their membrane. Oral cilia can be divided into three categories on the basis of the morphology of their freeze-fractured membranes: (a) undifferentiated cilia with very few randomly distributed particles: (b) cilia with particles arranged in parallel longitudinal rows spaced at intervals of 810-1080 A that are located on one side of the cilium; and (c) cilia with patches of particles arranged in short rows oriented obliquely to the main axis of the cilium. The latter particles, found on one side of the cilium, seem to serve as attachment sites for bristles 375-750 A long and 100 A wide which extend into the surrounding medium. The particles with bristles are located at the tips of cilia in the outermost membranelle and may be used to detect food particles and/or to modify currents in the oral region so that food particles are propelled more efficiently into the buccal cavity. Examination of thin-sectioned material indicates that the particles in oral cilia which form the longitudinal rows could be linked to microtubule doublets. Linkage between microtubule doublets and adjacent membrane areas on one side of the cilium could modify the form of ciliary beat by restricting the sliding of the microtubules. It is suggested that membrane-microtubule interactions may form the basis for the various forms of ciliary beat observed in different organisms.

The Contractile Mechanism in Cilia

A detailed analysis is made of the motion and the forces in the cilium of Sabellaria over the complete cycle. The results indicate that the stiffness of the cilium is directly related to the moments produced by the internal contractile elements. A sliding filament model is developed to generate the complete cycle of motion. The activation of the force-producing elements, the peripheral fibers, occurs over their entire length at once during the effective stroke. In the recovery stroke the sliding of peripheral fibers relative to each other produces activation. The peripheral fibers contribute to the stiffness of the cilium in the sliding filament model only when they are not free to slide because of cross-linkage. The model describes successfully the motion of a variety of types of cilia.