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Cilia – Definition, Structure, Types, Function

Cilia Definition

  • Cilia are minute, hair-like structures present on the surface of numerous cell types in living creatures. They have a diameter of 0.25 to 0.5 micrometres and a length of several micrometres.
  • The origin of the term “cilia” is the Latin word for “eyelash,” which aptly describes their appearance. Microtubules are organised in a circular arrangement around a central core to form the cilia.
  • Cilia are present in a wide range of creatures, from unicellular organisms such as paramecia and amoebas to sophisticated multicellular organisms such as humans. In the pulmonary system, where they help move mucus and other debris out of the lungs, and in the reproductive system, where they help move eggs and sperm, they play a crucial role.
  • Cilia also serve a critical function in the embryonic development of many different types of creatures, directing the migration of developing cells. In addition, they perform sensory activities, such as light detection in some creatures and chemical detection in others.
  • Cilia are an essential and highly specialised component of a variety of biological systems, playing critical roles in mobility, development, sensing, and communication.
  • Cilia are motile structures, which means they have the ability to move. They move in synchronised waves or beats that drive fluids or particles across the cell surface or in a fluid environment.
  • Proteins, enzymes, and signalling molecules comprise a complex molecular mechanism that coordinates the beating of cilia.
  • Cilia are remarkably conserved among diverse creatures, indicating that they originated early in the evolution of life on Earth.
  • Cilia are present in a variety of organs in humans, including the respiratory tract, where they help clear mucus and debris, the fallopian tubes, where they help transfer eggs towards the uterus, and the brain, where they are involved in the circulation of cerebrospinal fluid.
  • Cilial dysfunction can result in ciliopathies, a group of disorders that includes respiratory infections, infertility, hydrocephalus, and polycystic kidney disease.
  • Primary cilia are a form of non-motile, non-beating cilia that serve as sensors. Several cell types include them, including neurons and kidney cells.
  • The unique bending motion of cilia is produced by a protein called dynein, which utilises ATP energy to slide microtubules past one another and generate the characteristic bending motion of cilia.
  • Many proteins and signalling pathways regulate the length and structure of cilia with great precision.
  • Certain species, such as the unicellular algae Chlamydomonas, use their motile cilia to swim towards light sources through a process known as phototaxis.
  • In the early stages of embryonic development, cilia aid in cell movement and guide the synthesis of organs and tissues.

Characteristics of Cilium

  • Cilia are slender, hair-like protrusions from the cell surface.
  • They are composed of microtubules, which are cylindrical structures that serve as the cilia’s framework.
  • Cilia typically have a diameter of 0.25 to 0.5 micrometres and a length of several micrometres.
  • They are linked to the cell by a basal body, which resembles a centriole in structure.
  • Cilia are motile structures that move in unison to generate fluid flow or drive cells through fluid environments.
  • The movement of cilia is driven by dynein, a motor protein that utilises ATP energy to slide microtubules past one another.
  • Cilia have a wave-like action wherein the microtubules bend and straighten in a synchronised manner.
  • The plasma membrane that surrounds cilia is continuous with the cell membrane.
  • The quantity and location of cilia on a cell might vary based on the kind and function of the cell.
  • Cilia are highly specialised structures that perform crucial roles in numerous biological processes, including respiratory clearance, mucus transport, sensing, and embryonic development.

Structure of Cilium

Cilia are extracellular protrusions that are membrane-bound, microtubule-containing, and formed from centrioles. They are structurally durable, as well as flexible and dynamic, having different mechanisms that regulate their composition and functions. On the basis of the patterns of microtubules found in the axonemes of the cilia, motile cilia and nonmotile cilia can be separated. Except for the axoneme, the main basic structure of both cilia is the same.

Elements of the microtubule cytoskeleton within the cilium
Elements of the microtubule cytoskeleton within the cilium

1. Ciliary membrane

  • The ciliary membrane is the outer coating of the cilia that encompasses the interior axoneme and ciliary core.
  • The membrane is continuous with the cell membrane but is different from the cell membrane in its overall composition. The membrane is approximately 9,5 nanometers thick and contains much less proteins than the cell membrane.
  • Several of the proteins present in the membrane are special to the cilia and serve a crucial function in limiting the loss of ATP and other ions necessary at certain quantities to supply energy for the ciliary movement.
  • Especially in unicellular species, specialised receptor and channel proteins are also located in the ciliary membrane.
  • The ciliary membrane in all somatic cilia comprises an area within the membrane made of numerous strands called a cilia necklace.
  • During the passage of particles from the cytoplasm, the cilia necklace works as a selective barrier at the cilium’s entrance.

2. Ciliary matrix

  • The space generated by a watery matrix within the ciliary membrane called the ciliary matrix. The matrix is composed of embedded microtubules that create the cilium’s axoneme.

3. Axoneme

  • The microtubular structure known as an axoneme is the most significant feature of cilia.
  • Axoneme forms an axial structure within cilia that is responsible for ciliary movement.
  • The axoneme of cilia has a diameter between 0.2 and 10 µm and a length between a few microns and 1 millimetre.
  • The axoneme of motile cilia is made of a 9+2 arrangement of microtubules. The microtubules are composed of nine doublets encircling a pair of singlet microtubules in the centre.
  • In the ciliary tip, microtubules are polymerized from -tubulin heterodimers with a fast polymerizing end.
  • In addition, the axoneme possesses outer and inner dynein arms, radial spikes, and central-pair projections. Hundreds of proteins are connected to these structures and are responsible for the assembly and function of the cilia.

Cilia formation mechanism/ Ciliogenesis

Stage 1: Centriole Duplication and Axoneme Nucleation

  • The process of ciliogenesis begins after the cell division cycle, where the centrioles duplicate, and one pair migrates to the apical surface of the cell.
  • These centrioles serve as basal bodies for the formation of cilia. The basal bodies undergo axoneme nucleation, where the microtubules, which form the core of the cilium, start to grow from the centrioles. The axoneme nucleation is a highly regulated process and involves several proteins, including SAS-6, PLK4, CEP152, and CPAP.

Stage 2: Formation of Distal and Subdistal Appendages

  • After the basal bodies undergo axoneme nucleation, they start to acquire various distal and subdistal appendages.
  • The distal appendages are critical for the docking of ciliary vesicles, which help in the extension of the ciliary membrane. The subdistal appendages play a role in anchoring the basal bodies to the cell membrane.

Stage 3: Ciliary Membrane Extension and Fusion

  • The distal appendages interact with the post-Golgi vesicles, which help in the flattening of the ciliary membrane and its fusion with the cell membrane. The positioning and orientation of the cilia depend on the original positioning of the basal bodies and centrioles.

Stage 4: Formation of the Axoneme

  • The final step of ciliogenesis is the formation of the axoneme, which is composed of microtubules arranged in a specific pattern. The process of axoneme formation involves various molecular motors, such as kinesin and dynein, which transport the tubulin protein subunits to the growing end of the microtubules.
  • The assembly of tubulin subunits occurs through two routes: intracellular and extracellular. In the intracellular route, tubulin subunits are assembled at the distal growing end of the microtubules, while in the extracellular route, the basal body is present at the apical membrane, and protein accumulation follows.

Stage 5: Stabilization of Cilia

  • The stability of cilia is crucial for their proper function. The stability of the cilium is maintained by post-translational modifications of the tubulin protein subunits, such as acetylation and detyrosination. These modifications prevent the degradation of the microtubules and help in maintaining their stability and motility.

Regulation of Ciliogenesis

  • The process of ciliogenesis is carefully regulated by various mechanisms. Mutations in genes encoding the proteins involved in ciliogenesis can lead to several diseases known as ciliopathies.
  • These diseases are characterized by defects in cilia structure and function and can affect various organs and tissues, including the kidney, brain, and eyes.
  • Several signaling pathways, including Wnt, Hedgehog, and Notch, play a crucial role in regulating ciliogenesis.

Types of cilia

There are numerous varieties of cilia present in a variety of creatures, each with its own form and function. Among the most prevalent forms of cilia are:

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1. Motile Cilia

These are the most well-known type of cilia, and they are responsible for movement. They can be found in various organisms, including humans, and are found in tissues like the respiratory tract and fallopian tubes. Motile cilia move in a coordinated, wave-like motion to move substances along surfaces.

  • Motile cilia or moving cilia are cilia whose primary function is to facilitate the movement of animals or substances along a passage.
  • Typically, these are located on the specialised epithelial lining of the airways, paranasal sinuses, oviduct, and ventricular system of the brain.
  • Many motile cilia exist and move in a coordinated manner, exhibiting pendulous, unciform, infundibuliform, or undulating motion.
  • Only motile cilia are present in ciliates that employ them for movement or to transport fluids over their surface.
  • Motile cilia consist of a 9+2 structure with nine microtubule doublets on the periphery and two singlet microtubules in the centre.
  • A complete A tubule with 13 protofilaments and an incomplete B tubule with 10 protofilaments make up the doublet microtubules.
  • Connecting the doublets are nexin bridges, which are responsible for the bending movements of the cilia. Using radial spikes, the doublets are connected to the centre apparatus or two singlets.
  • The appropriate levels of periciliary fluid around motor cilia are responsible for regulating their movement. This cilia’s ciliary membrane consists of sodium channels that function as sensors for determining the fluid level surrounding the cilia.

2. Primary Cilia

These are immotile, and are present on almost all cell types in the human body. They act as sensory organelles, and play a crucial role in cellular signaling and communication. They are shorter than motile cilia and have a single microtubule arrangement.

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  • Primary cilia are solitary, nonmotile cilia found on the apical surface of polarised and differentiated cells in the majority of mammalian cells.
  • Primary cilia are specialised cellular organelles, similar to mitochondria, the endoplasmic reticulum, and the Golgi apparatus.
  • In the presence of a 9+0 microtubule arrangement in the axoneme, primary cilia are distinguished from other forms of cilia.
  • They lack the centre singlet of microtubules that is responsible for cilia motion. The cilia are attached to the cell via a basal body that is nucleated by the centriole.
  • Zimmerman discovered primary cilia in 1898, but Sergei Sorokin gave them their name in 1968.
  • There are a variety of hypotheses on the function and structure of primary cilia.
  • The primary cilia are vestigial organelles inherited from an ancestor with motile cilia, according to the first hypothesis. The second clause adds that these are crucial for cell cycle regulation. According to the third idea, they are sensory organelles.
  • Primary cilia are present in various mammalian cells, including stem cells, epithelial, endothelial, connective tissue, and muscle cells.
  • Cilia not involved in locomotion are frequently involved in sensory functions. These cilia function as antennae that receive environmental cues and turn them into signalling cascades.
  • These cascades originate in the ciliary compartment and are then transmitted to the cell body. Included in the process are several receptors, channels, and signalling proteins, which are located on the ciliary membrane.
  • Diverse and distinct signalling pathways are utilised by primary cilia in various cell types.
  • Disorders known as ciliopathies may develop from abnormal primary cilia structure and function. The clinical symptoms of these illnesses range from Bardet-Biedl syndrome to oral-facial-digital syndrome.
 Primary cilia structure.
Primary cilia structure.

3. Nodal Cilia

These are found in the embryonic node of vertebrate embryos and play a critical role in establishing the left-right axis of the developing embryo. They rotate in a clockwise motion, generating a flow of extracellular fluid that results in asymmetric gene expression.

  • Nodal cilia are motile cilia with a 9+0 arrangement of microtubules in the axoneme that are exclusive to the early stages of embryo development.
  • Nodal cilia are structurally similar to primary cilia, except that they contain the dynein arms required for movement and spinning.
  • These cilia can move in a clockwise orientation, causing extraembryonic fluid to pass across the nodal surface.
  • These cilia are found in the cells of the embryo’s node or embryonic organiser during the gastrula stage.
  • Nodal cilia are essential for determining left-right orientation and facilitating the passage of liquid matrix around the embryo.
  • These cilia are frequently surrounded by primary cilia that play a role in the embryo’s reception of sensory stimuli.

4. Sensory Cilia

These are similar to primary cilia, but are specialized for sensory functions. They are found in specialized tissues like the retina and inner ear, where they play a crucial role in vision and hearing.

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  • Sensory cilia are hair-like protrusions that extend from the surface of cells in diverse organs, including the retina and inner ear.
  • They are specialised for sensory functions and are essential for processes such as vision, hearing, and olfaction.
  • Sensory cilia are located in sensory neurons, the specialised cells responsible for transferring sensory information from the body to the brain.
  • Similar to primary cilia, sensory cilia consist of a core of microtubules surrounded by a plasma membrane.
  • A central pair is surrounded by nine pairs of microtubules, forming a 9+0 arrangement.
  • The outer membrane of sensory cilia comprises a variety of ion channels and receptors involved in the detection of diverse stimuli.
  • The opening of ion channels and the production of electrical impulses are caused by the bending of sensory cilia in response to stimuli such as sound waves or light.
  • Length and form of sensory cilia can vary based on their location and function. The cilia of the inner ear, for instance, are longer and more flexible than those of the retina.
  • Destruction to or failure of sensory cilia can result in a variety of sensory problems, including deafness and impaired vision.
  • In order to create new medicines and treatments, scientists are doing continuing research on sensory cilia to better comprehend their structure, function, and role in disease.

5. Photoreceptor Cilia

These are found in the outer segment of rod and cone cells in the retina, and are responsible for the detection of light. They are also involved in the processing of visual information.

Each type of cilia has a unique structure and function, and plays an essential role in the overall health and development of organisms.

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  • Photoreceptor cilia are specialised sensory cilia in the retina of the eye that are essential for vision.
  • They are located in the outer segments of photoreceptor cells, which are specialised cells that sense light and send visual information to the brain.
  • The outer segment of a photoreceptor cell consists of stacked discs holding the light-sensitive pigments rhodopsin or photopsin.
  • From the base of the outer segment, photoreceptor cilia deliver newly synthesised photopigments to the disc membranes.
  • Similar to primary cilia, photoreceptor cilia consist of a core of microtubules surrounded by a plasma membrane.
  • Microtubules in cilia function as tracks for motor proteins that transport photopigments and other proteins to and from the outer segment.
  • In reaction to light, the ciliary membrane contains a variety of ion channels and receptors that generate electrical impulses.
  • The length of photoreceptor cilia is tightly regulated, and shorter cilia correspond to faster visual reaction times.
  • Mutations in genes involved in ciliary transport can result in photoreceptor malfunction and a variety of retinal diseases, including retinitis pigmentosa and Leber congenital amaurosis.
  • Scientists are conducting continuing research on photoreceptor cilia to better understand their structure, function, and role in disease in order to create new therapies and treatments for retinal ailments.

Functions of cilia

  • Movement: Mobility is one of the most recognisable functions of cilia. Cilia are responsible for the coordinated movement of cells or particles. The cilia lining the respiratory tract, for instance, move in a wave-like pattern to assist in clearing mucus and debris from the airways.
  • Sensory perception: Some types of cilia, such as the sensory cilia in the inner ear, play an essential part in sensory perception. They assist in detecting environmental changes, such as sound waves, and send this data to the brain.
  • Cell signaling: Cilia participate in multiple signalling pathways that regulate cellular processes such as cell division, differentiation, and migration.
  • Development: Cilia play a significant function in embryonic development by contributing to the establishment of the left-right axis and other positional information.
  • Fluid flow: Cilia in the brain and other organs generate a directed flow to regulate the movement of cerebrospinal fluid, bile, and other fluids.
  • Reproduction: Flagella on sperm cells are specialised cilia that drive sperm towards the egg for fertilisation.
  • Nutrition: Some single-celled creatures, such as paramecia, utilise cilia to generate a current that assists in transporting food particles to their oral cavity.
  • Protection: Cilia in the eyes create a coating of tears that prevents foreign particles from penetrating the cornea.
  • Maintenance of tissue architecture: Cilia assist in maintaining the structure and form of specific tissues, such as the renal tubules in the kidneys.
  • Disease: Dysfunction or abnormalities in cilia can result in a variety of diseases and syndromes known together as ciliopathies. Among these are respiratory infections, hearing loss, kidney problems, and a variety of genetic abnormalities.

Ciliogenesis

  • Ciliation is referred to as ciliogenesis. Ciliogenesis is linked to cell division and takes place during the G1/G0 phase of the cell cycle. Reabsorption or disassembly of the cilium begins following re-entry into the cell cycle.
  • At the initial stage of ciliogenesis, the centrosome migrates to the cell surface, where the mother centriole forms a basal body and nucleates the ciliary axoneme during the G1/G0 phase of the cell cycle.
  • This initial phase is controlled by distal appendage proteins, including centrosomal protein 164. Once the cilium is mature, nuclear distribution gene E homolog 1 (Nde1) controls the elongation of the cilium during the second step.
  • Cilia resorption is the third step, followed by axonemal shortening during cell cycle reentry. The Aurora A-HDAC6, Nek2-Kif24, and Plk1-Kif2A pathways regulate this third process. In the fourth step, the basal body is detached from the cilia, releasing the centrioles that serve as microtubule organising centres or spindle poles for mitosis.
  • Coordination of the assembly and disassembly equilibrium, the IFT system, and membrane trafficking influence the production of immobile cilia. The ciliary membrane has a microtubule bundle when the axoneme nucleates from the basal body.
  • Some signalling molecules and ion channels are enclosed therein. Because cilia lack the machinery required to generate ciliary proteins, proteins made by the cell’s Golgi apparatus must be delivered through a ciliary ‘gate’ and transition zone near the base of the cilium. T
  • he transition zone, identified by the change from triplet to doublet microtubules, is positioned at the distal end of the basal body. In unicellular organisms, basal body docking with the plasma membrane can be permanent, whereas in metazoans, it can be temporary.
  • Within the transition zone, transition fibres, which are found in unicellular organisms, or distal and subdistal appendages, which are present in mammals, are connected to microtubules. Transition fibres serve as protein intraflagellar transfer (IFT) docking sites.
  • IFT delivers cargo in both directions throughout the length of cilia and is mediated by kinesin-2 (anterograde) and cytoplasmic dynein-2 (retrograde) motors linked to multisubunit protein complexes referred to as IFT particles. In the majority of organisms, Y-linkers present at the distal end of the transition zone and secure the doublet microtubules to the ciliary membrane.

What is Multicilia?

  • MCCs are present in a wide array of various tissue types in vertebrates. In mammals, ependymal MCCs line the airway epithelium and brain ventricles. Multicilia are generated by specialised cells for specialised purposes.
  • MCCs are often characterised by the presence of more than two cilia on their surface, however this is not extensively described or understood. MCCs have recently been found in unicellular eukaryotes and protists, as well as in numerous metazoans and even in some plant sperm.
  • MCCs result in the development of motile axonemes, with the exception of olfactory cilia in mammals. Even though they have a 9 + 2 configuration, these olfactory MCCs lack dynein arms and are therefore termed immobile.
  • This indicates that MCCs are a solution to the demand for local fluid flow, presumably due to their hydrodynamic coupling capability.
  • Multicilia perform their activities through beating, and the fundamental machinery and structure of cilia beating appear to be highly conserved among eukaryotes, as well as between single motile cilia and multicilia.
  • Some factors, such as beat frequency, are controlled by cells and vary between cell types. However, only motile cilia and sperm flagella contain the dynein machinery required to drive axonemal beating during ATP hydrolysis.
  • Two phases comprise the ciliary beat cycle: the effective stroke and the recovery stroke. The effective stroke is the initial bending from the upright position, whereas the recovery stroke is the return to the upright position.
  • Controlling ciliary motion are outer and inner axonemal dynein arms that slide adjacent doublets relative to one another. Protein bridges between doublets and the basal anchoring of the axoneme facilitate the sliding. Therefore, cilia bend.
  • When cilia are structured in such a way that each cilium in a two-dimensional array beats at the same frequency but with a phase shift, the phenomenon of metachrony occurs. As a result, a wave of ciliary movement propagates across the array, propelling fluids in a current.
  • Even if each cilium in an array begins in synchrony, hydrodynamic forces between each cilium will push them back towards metachrony, probably because in a metachronal array, the amount of effort each cilium must perform is lowered and more fluid is moved. Thus, it is believed that multiciliation is an evolutionarily more efficient approach to generate fluid flow.

Examples of Cilia

1. Cilia in Paramecium

  • Cilia are one of the most significant cell organelles in Paramecium because they are involved in the organism’s water-based motility and food absorption into the cytosome.
  • The majority of cilia are involved in motility and are present throughout the organism’s body. In the gullet, caudal cilia are typically longer and immobile.
  • In addition, cilia participate in the initial step of the mating reaction in Paramecium, which is conjugation.
  • The cilia sweep prey creatures and water into the mouth groove, which also assists in feeding.
  • Similar to other eukaryotes, the cilia of Paramecium have a basal body, an axoneme, and a ciliary membrane.

2. Cilia in ciliated epithelium

  • Many areas of the human body have epithelial cells with cilia, resulting in ciliated epithelium.
  • This form of epithelium is typically found in locations with frequent and intimate interaction with the external environment.
  • The respiratory tract’s ciliated epithelium is responsible for expelling dust particles, mucus, trapped dust, and bacteria from the body.
  • In the retina and kidney, ciliated epithelium functions as sensory tissues involved in sensory reception.
  • The cilia in the oviduct transport the ovum from the ovaries to the fallopian tubes, where it is fertilised.

FAQ

What are cilia?

Cilia are tiny hair-like structures that extend from the surface of cells in the body. They are involved in various functions, such as moving fluids, sensing the environment, and aiding in reproduction.

What is the structure of cilia?

Cilia consist of a core of microtubules surrounded by a plasma membrane. They are anchored to the cell body by a basal body and have a characteristic 9+2 arrangement of microtubules.

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What is the function of cilia in the respiratory system?

Cilia in the respiratory system help move mucus and debris out of the lungs and airways. This helps to protect the lungs from infection and other respiratory problems.

What is the function of cilia in the reproductive system?

Cilia in the female reproductive system help move the egg through the fallopian tube and towards the uterus. In the male reproductive system, cilia in the epididymis aid in the movement of sperm.

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What is the function of cilia in the digestive system?

Cilia in the digestive system help move food and waste materials through the digestive tract. This aids in digestion and helps to prevent blockages in the intestines.

What is primary ciliary dyskinesia (PCD)?

PCD is a genetic disorder that affects the structure and function of cilia. It can cause respiratory problems, fertility issues, and other health problems.

Can cilia regenerate?

Yes, cilia can regenerate after damage or injury. This process is important for maintaining normal ciliary function.

Can cilia be affected by environmental factors?

Yes, environmental factors such as pollution, smoke, and toxins can damage cilia and impair their function.

How are cilia studied in research?

Cilia can be studied using a variety of techniques, such as microscopy, genetic analysis, and ciliary beat frequency measurements.

What is the role of cilia in cancer?

Cilia have been implicated in various types of cancer, including lung, breast, and ovarian cancer. Some research suggests that cilia may play a role in regulating cell proliferation and differentiation.

References

  • Verma, P. S., & Agrawal, V. K. (2006). Cell Biology, Genetics, Molecular Biology, Evolution & Ecology. First Edition. S .Chand and company Ltd.
  • Satir P, Pedersen LB, Christensen ST. The primary cilium at a glance. J Cell Sci. 2010 Feb 15;123(Pt 4):499-503. doi: 10.1242/jcs.050377. PMID: 20144997; PMCID: PMC2818190.
  • Watanabe, T. (1990). The Role of Ciliary Surfaces in Mating in Paramecium . In: Bloodgood, R.A. (eds) Ciliary and Flagellar Membranes. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0515-6_6
  • Hoyer-Fender, S. (2013). Primary and Motile Cilia: Their Ultrastructure and Ciliogenesis. In: Tucker, K., Caspary, T. (eds) Cilia and Nervous System Development and Function. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5808-7_1
  • Higgins, M., Obaidi, I., & McMorrow, T. (2019). Primary cilia and their role in cancer (Review). Oncology Letters. doi:10.3892/ol.2019.9942
  • Mirvis, M., Stearns, T., & James Nelson, W. (2018). Cilium structure, assembly, and disassembly regulated by the cytoskeleton. Biochemical Journal, 475(14), 2329–2353. doi:10.1042/bcj20170453
  • Ishikawa T. Axoneme Structure from Motile Cilia. Cold Spring Harb Perspect Biol. 2017 Jan 3;9(1):a028076. doi: 10.1101/cshperspect.a028076. PMID: 27601632; PMCID: PMC5204319.
  • Mizuno, Naoko & Taschner, Michael & Engel, Benjamin & Lorentzen, Esben. (2012). Structural Studies of Ciliary Components. Journal of molecular biology. 422. 163-80. 10.1016/j.jmb.2012.05.040.
  • Satir P, Christensen ST. Overview of structure and function of mammalian cilia. Annu Rev Physiol. 2007;69:377-400. doi: 10.1146/annurev.physiol.69.040705.141236. PMID: 17009929.
  • https://citations.springernature.com/item?doi=10.1007/978-1-4613-0515-6_6
  • https://www.jomfp.in/article.asp?issn=0973-029X;year=2017;volume=21;issue=1;spage=8;epage=10;aulast=Venkatesh
  • https://encyclopedia.pub/entry/history/show/62288
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