Home :: Chapter 7 :: Web Topic 7.1

Web Topic 7.1
Cilia and Sensory Receptors

Introduction

Cilia and flagella are widely used by eukaryotic organisms for locomotion, stimulus reception, or both. Although separate names were originally assigned to these organelles depending upon their size and the number per cell, the internal structure and functions of cilia and flagella have turned out to be identical. We shall thus refer to all such organelles as cilia. One of the most intriguing questions is why cilia have been recruited so often as sensory receptors. Below, we provide a general review of how ciliary structure appears to be correlated with function, and outline some possible reasons for their use as receptor devices.

Cell skeletons and cilia

Animal cells require an internal scaffolding or cytoskeleton to hold their shape. A mesh of actin protein filaments usually underlies most cell membranes. This cell surface support is complemented by a network of intermediately sized proteins that maintains the three-dimensional structure of the cell’s cytoplasm. Finally, the centrosome of the cell, consisting of two perpendicularly oriented centrioles, produces a third meshwork of microtubules throughout the cell that is used for additional support and as “rails” for the transport of internal cell components. The centrosome network also mediates the partitioning of cellular components during cell division. These microtubules are largely composed of tubulin proteins. Each centriole is a barrel-shaped organelle whose walls consist of parallel microtubules arrayed into nine clusters with three tubules per cluster.

Animal sensory cells respond to stimuli by varying the permeability of specific ion channels in their membranes. This changes the ionic composition inside the cell’s cytoplasm, produces a change in electrical fields across the cell membrane, or both. Either effect is maximized when the area of the responding cell membrane is large relative to the volume of cytoplasm that it encloses. There are several ways sensory cells can achieve this high surface area/volume ratio. One is to elaborate the membrane surface exposed to stimuli into a large number of small fingers called microvilli. The membrane surrounding each microvillus is continuous with the overall cell membrane, and actin filaments that extend from the mesh under the cell membrane into the cytoplasm of the microvilli provide the necessary support (Cooper and Hausman 2007). An alternative is to place one or more cilia on the exposed cell surface. Like microvilli, the membranes enclosing each cilium are continuous with the adjacent cell membrane. The cytoplasm inside the cilium is usually somewhat isolated from that in the rest of the cell by a terminal plate at its base (Singla and Reiter 2006). Cilia differ from microvilli in that they are typically larger in both diameter and length, and their support is provided by parallel microtubules generated by adjacent centrioles. Whereas the centrioles consist of nine triplets of parallel microtubules, the cilia attached to them usually have nine or more pairs of microtubules forming an internal cylinder of support. The ensemble of parallel pairs of tubules in a cilium is called its axoneme.

Structural types of cilia

Cilia can usually be assigned to one of two classes depending upon their axoneme structure:

Ciliary function

As noted earlier, cilia can have either or both of two functions: (a) propelling the organism and/or the adjacent medium relative to each other by beating rhythmically, and (b) acting as sensory receptors. It was originally believed that 9+2 cilia were always motile and locomotory organelles, whereas 9+0 cilia were always immotile and sensory in function (Satir 1977). Subsequent studies have shown that a variety of combinations of structure and function exist in nature (Ibañez-Tallon et al. 2003). We give examples below of some of these combinations:

Cilia as preadaptations for sensory receptors

Several factors, either singly or in concert, appear to have pre-adapted cilia as sensory receptors:

Ciliary versus non-ciliary receptor systems

Given the abundant reasons why cilia might be recruited into sensory organs, why are they not the only such source? The fact is that they are not. While all vertebrates so far examined have primary cilium sensitivity to hedgehog proteins, this is not the only way that cells can respond to hedgehog proteins, and the latter are not the only way that cell differentiation during development is regulated (Goetz and Anderson 2010; Vincensini et al. 2011). Drosophila development proceeds with a type of hedgehog proteins, but cilia do not play an important role in signaling. We noted above that photoreceptors exist in both ciliary and rhabdomeric configurations, and that each has its own set of photoreceptor (opsin) proteins and associated genes (Arendt 2001; Arendt and Wittbrodt 2001; Arendt et al. 2004; Fernald 2006). We noted in Chapter 6 that chemoreceptive organs may have receptor cells that are ciliary (olfaction), microvillar (taste), or both (vomeronasal organs). And as discussed in Chapter 7, mechanoreceptors can rely on either of two widely distributed but distinct stimulation mechanisms, each having its own depolarizing ion (calcium or sodium), ion channel proteins (TRP or degenerin/ENaC), and associated genes. For each modality, the two alternative mechanisms seem to be equally ancient in the animal lineage. Why should most sensory modalities have evolved two alternative ways of doing the same thing? While there may be differences in sensitivities of the two alternatives in any given modality, the same receptor cells never seem to employ both mechanisms: if the dual alternatives are present in the same organism, they are invariably assigned to different kinds of cells in different parts of the body. There is clearly more to the story of when and why cilia are recruited as sensory receptors that remains to be discovered.

References cited

Arendt, D. 2001. Evolution of eyes and photoreceptor cell types. International Journal of Developmental Biology 47: 563–571.

Arendt, D., K. Tessmar-Raible, H. Snyman, A. W. Dorresteijn, and J. Wittbrodt. 2004. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306: 869–871.

Arendt, D. and J. Wittbrodt. 2001. Reconstructing the eyes of Urbilateria. Philosophical Transactions of the Royal Society of London, B-Biological Sciences 356: 1545–1563.

Blumer, M. 1994. The ultrastructure of the eyes of the veliger larvae of Aporrhais sp and Bittium reticulatum (Mollusca, Caenogastropoda). Zoomorphology 114: 149–159.

Brusca, R. C. and G. J. Brusca. 2003. Invertebrates, 2nd Edition. Sunderland, MA: Sinauer Associates.

Christensen, S. T., L. B. Pedersen, L. Schneider, and P. Satir. 2007. Sensory cilia and integration of signal transduction in human health and disease. Traffic 8: 97–109.

Cooper, G. M. and R. E. Hausman. 2007. The Cell: A Molecular Approach, 4th Edition. Sunderland, MA: Sinauer Associates.

Eakin, R. M. 1979. Evolutionary significance of photoreceptors-retrospect. American Zoologist 19: 647–653.

Eakin, R. M. 1982. Morphology of invertebrate photoreceptors. Methods in Enzymology 81: 17–25.

Fernald, R. D. 2006. Casting a genetic light on the evolution of eyes. Science 313: 1914–1918.

Goetz, S. C. and K. V. Anderson. 2010. The primary cilium: a signalling centre during vertebrate development. Nature Reviews Genetics 11: 331–344.

Göpfert, M. C. and D. Robert. 2003. Motion generation by Drosophila mechanosensory neurons. Proceedings of the National Academy of Sciences of the United States of America 100: 5514–5519.

Govorunova, E. G., K. H. Jung, and O. A. Sineshchekov. 2004. Rhodopsin-mediated photomotility in Chlamydomonas and related algae. Biofizika 49: 278–293.

Grünert, U. and B. W. Ache. 1988. Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell and Tissue Research 251: 95–103.

Hegemann, P. 1997. Vision in microalgae. Planta 203: 265–274.

Ibañez-Tallon, I., N. Heintz, and H. Omran. 2003. To beat or not to beat: roles of cilia in development and disease. Human Molecular Genetics 12: R27–R35.

Inglis, P. N., K. A. Boroevich, and M. R. Leroux. 2006. Piecing together a ciliome. Trends in Genetics 22: 491–500.

Karp, G. 2007. Cell and Molecular Biology: Concepts and Experiments, 5th Edition. Hoboken, NJ: John Wiley.

Keil, T. A. 1997. Functional morphology of insect mechanoreceptors. Microscopy Research and Technique 39: 506–531.

Lidow, M. S. and B. P. M. Menco. 1984. Observations on axonemes and membranes of olfactory and respiratory cilia in frogs and rats using tannic acid-supplemented fixation and photographic rotation. Journal of Ultrastructure Research 86: 18–30.

Louvi, A. and E. A. Grove. 2011. Cilia in the CNS: the quiet organelle claims center stage. Neuron 69: 1046–1060.

Machemer, H., R. Braucker, S. Machemer-Rohnisch, U. Nagel, D. C. Neugebauer, and M. Weskamp. 1998. The linking of extrinsic stimuli to behaviour: roles of cilia in ciliates. European Journal of Protistology 34: 254–261.

Popper, A. N. and R. R. Fay. 1999. The auditory periphery in fishes. In Comparative Hearing: Fish and Amphibians (Fay, R. R. and A. N. Popper, eds.), pp. 43–100. New York: Springer-Verlag.

Porter, M. E. and W. S. Sale. 2000. The 9+2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. Journal of Cell Biology 151: F37–F42.

Praetorius, H. A. and K. R. Spring. 2005. A physiological view of the primary cilium. Annual Review of Physiology 67: 515–529.

Quarmby, L. M. and D. K. Parker. 2005. Cilia and the cell cycle? Journal of Cell Biology 169: 707–710.

Rosenbaum, J. L. and G. B. Witman. 2002. Intraflagellar transport. Nature Reviews Molecular Cell Biology 3: 813–825.

Satir, P. 1977. Microvilli and cilia: surface specializations of mammalian cells. In Mammalian Cell Membranes. 2. The Diversity of Membranes (Jamieson, G. A. and D. M. Robinson, eds.), pp. 323–353. Boston, MA: Butterworths.

Scholey, J. M. 2003. Intraflagellar transport. Annual Review of Cell and Developmental Biology 19: 423–443.

Singla, V. and J. F. Reiter. 2006. The primary cilium as the cell’s antenna: Signaling at a sensory organelle. Science 313: 629–633.

Teeter, J. H., R. B. Szamier, and M. V. L. Bennett. 1980. Ampullary electroreceptors in the sturgeon Scaphirhynchus platorynchus (Rafinesque). Journal of Comparative Physiology 138: 213–223.

Vincensini, L., T. Blisnick, and P. Bastin. 2011. 1001 model organisms to study cilia and flagella. Biology of the Cell 103: 109–130.

Whitfield, J. F. 2004. The neuronal primary cilium—an extrasynaptic signaling device. Cellular Signaling 16: 763–767.

Yack, J. E. 2004. The structure and function of auditory chordotonal organs in insects. Microscopy Research and Technique 63: 315–337.

Yamada, E. 1982. Morphology of vertebrate photoreceptors. Methods in Enzymology 81: 3–17.

Zakon, H. H. 1986. The electroreceptive periphery. In Electroreception (Bullock, T. H. and W. Heiligenberg, eds.), pp. 103–156. New York: John Wiley and Sons.

Go