Summary
Long ciliary rootlets are a characteristic feature of the dendritic inner segments of the sensory cells in insect sensilla. These rootlets are composed of highly ordered filaments and are regularly cross-striated. Collagenase digestion and immunohistochemistry reveal that the rootlets are probably not composed of collagen fibers. However, double-labeling experiments with phalloidin and anti-α-actinins show that antibodies to α-actinin react with the ciliary rootlets of the sensilla, but do not stain the scolopale, which is composed of actin filaments as visualized by phalloidin. Antibodies to centrin, a contractile protein isolated from flagellar rootlets of green algae, also stain the ciliary rootlets. Within the ciliary rootlets of insect sensilla, α-actinin may be associated with filaments other than actin filaments. The immunohistochemical localization of a centrin-like protein suggests that contractions probably occur within the rootlets. The centrin-like protein may play a role during the mechanical transduction or adaptation of the sensilla.
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References
Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1983) The molecular biology of the cell. Garland, New York, London, pp 697–701
Ashhurst DE (1968) The connective tissue of insects. Annu Rev Entomol 13:45–74
Ashhurst DE, Bailey AJ (1980) Locust collagen: morphological and biochemical characterization. Eur J Biochem 103:75–83
Bloom JW, Zacharuk RY, Holodniuk AE (1981) Ultrastructure of a terminal chordotonal sensillum in larval antennae of the yellow mealworm, Tenebrio molitor L. Can J Zool 59:515–524
Carlson SD, Chi C (1979) The functional morphology of the insect photoreceptor. Annu Rev Entomol 24:379–416
Chapman JA, Tzaphlidou M, Meek KM, Kadler KE (1990) The collagen fibril — a model system for studying the staining and fixation of a protein. Electron Microsc Rev 3:143–182
Drenckhahn D, Franz H (1986) Identification of actin, alpha-actinin, and vinculin-containing plaques at the lateral membrane of epithelial cells. J Cell Biol 102:1843–1852
Faulstich H, Zobeley S, Rinnerthaler G, Small JV (1988) Fluorescent phallotoxins as probes for filamentous actin. J Muscle Res Cell Motil 9:370–383
Fawcett D (1961) Cilia and flagella. In: Brachet J, Mirsky AE (eds) The cell. Biochemistry, physiology, morphology, 2nd edn. Academic Press, New York, pp 217–298
French AS (1988) Tansduction mechanisms of mechanosensilla. Annu Rev Entomol 33:39–58
Füller H, Ernst A (1973) Die Ultrastruktur der femoralen Chordotonalorgane von Carausius morosus. Br Zool Jb Anat Bd 91:574–601
Gaffal KP, Bassemir U (1974) Vergleichende Untersuchungen modifizierter Cilienstrukturen in den Dendriten mechano-und chemosensitiver Rezeptorzellen der Baumwollwanze Dysdercus und der Libelle Agrion. Protoplasma 82:177–202
Geiger B, Dutton AH, Tokuyasu KT, Singer SJ (1981) Immunoelectron microscope studies of membrane-microfilament interactions: distribution of alpha-actinin, topomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J Cell Biol 91:614–628
Gray EG (1960) The fine structure of insect ear. Philos Trans R Soc Lond [Biol] 243:190–209
Harrison F (1989) Primary cilia associated with striated rootlets in granulated and folliculo-stellate cells of the avian adenohypophysis. Anat Embryol 180:543–547
Höhfeld I, Otten J, Melkonian M (1988) Contractile eukaryotic flagella: centrin is involved. Protoplasma 147:16–24
Howse PE (1968) The fine structure and functional organisation of chordotonal organs. Symp Zool Soc (Lond) 23:16–198
Koutoulis A, McFadden GI, Wetherbee R (1988) Spine-scale reorientation in Apedinella radians (Pedinellales, Chrysophyceae): the microarchitecture and immunocytochemistry of the associated cytoskeleton. Protoplasma 147:25–41
Larson DE, Dingle AD (1981) Isolation, ultrastructure, and protein composition of the flagellar rootlet of Naegleria gruberi. J Cell Biol 89:424–432
Martindale VE, Salisbury JL (1990) Phosphorylation of algal centrin is rapidly responsive to changes in the external milieu. J Cell Science 96:396–402
Maruyama K (1986) Connectin, an elastic filamentous protein from striated muscle. Int Rev Cytol 104:81–114
McIver SB (1985) Mechanoreception. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 6. Nervous system: sensory. Pergamon, Oxford, pp 71–132
Melkonian M, Schulze D, McFadden GI, Robenek H (1988) A polyclonal antibody (anticentrin) distinguishes between two types of fibrous flagellar roots in green algae. Protoplasma 144:56–61
Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus Degeer (Saltatoria, Gryllidae). Z Morphol Tiere 77:285–315
Michel K (1975) Das Tympanalorgan von Cicada orni L. (Cicadina, Homoptera). Zoomorphologie 82:79–103
Moor H (1987) Theory and practice of high-pressure freezing. In: Steinbrecht RA, Zierhold K (eds) Cryotechniques in biological electron microscopy. Springer, Berlin Heidelberg New York, pp 175–191
Moran DT, Rawley JC (1975) The fine structure of the cockroach subgenual organ. Tissue Cell 7:91–106
Moran DT, Rawley JC, Varel FG (1975) Ultrastructure of the grasshopper proximal femural chordotonal organ. Cell Tissue Res 161:445–457
Moran DT, Varela FJ, Rawley JC (1977) Evidence for active role of cilia in sensory transduction. Proc Natl Acad Sci USA 74:793–797
Moulins M (1976) Ultrastructure of chordotonal organs. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 387–426
Müller M, Moor H (1984) Cryofixation of thick specimens by high pressure freezing. In: Revel J-P, Barnard T, Haggis GH (eds) Science of biological specimen preparation. SEM. AMF O'Hare, Chicago, pp 131–138
Nave R, Weber K (1990) A myofibrillar protein of insect muscle related to vertebrate titin connects Z band and A band: purification and molecular characterization of invertebrate mini-titin. J Cell Sci 95:535–544
Nave R, Fürst DO, Weber K (1990) Interaction of alpha-actinin and nebulin in vitro-support for the existence of a 4th filament system in skeletal muscle. FEBS Lett 269:163–166
Pitelka DR (1974) Basal bodies and root structures. In: Sleigh MA (ed) Cilia and flagella. Academic Press, London New York, pp 437–469
Pollard TD, Cooper JA (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55:987–1035
Prockop DJ, Kivirikko KJ, Tuderman L, Guzman NA (1979a) The biosynthesis of collagen and its disorders. N Engl J Med 301:13–23
Prockop DJ, Kivirikko KJ, Tuderman L, Guzman NA (1979b) The biosynthesis of collagen and its disorders (second of two parts). N Engl J Med 301:77–85
Salisbury JL (1983) Contractile flagellar roots: the role of calcium. J Submicrosc Cytol 15:105–110
Salisbury JL, Floyd GL (1978) Calcium-induced contraction of the rhizoplast of a quadriflagellate green algae. Science 202:975–976
Salisbury JL, Baron A, Surek B, Melkonian M (1984) Striated flagellar roots: isolation and characterization of a calcium-modulated contractile organelle. J Cell Biol 99:962–970
Salisbury JL, Sanders MA, Harpst L (1987) Flagellar root contraction and nuclear movement during flagellar regeneration in chlamydomonas reinhardthii. J Cell Biol 105:1799–1805
Sandoz D, Chailley B, Boisvieux-Ulrich E, Lemullois M, Laine M-C, Bautista-Harris G (1988) Organisation and functions of cytoskeleton in metazoan ciliated cells. Biol Cell 63:183–193
Schmidt K (1969) Der Feinbau der stiftführenden Sinnesorgane im Pedicellus der Florfliege Chrysopa Leach (Chrysopidae, Planipennia). Z Zellforsch 99:357–388
Schmidt K (1970) Vergleichende morphologische Untersuchungen über den Feinbau der Ciliarstrukturen in den Scolopidien des Johnstonschen Organs holometaboler Insekten. Verh Dtsch Zool Ges 64:88–92
Schmidt K (1974) Die Mechanorezeptoren im Pedicellus der Eintagsfliege (Insecta, Ephemeroptera). Z Morphol Tiere 78:193–220
Schmidt M (1989) The hair-peg organs of the shore crab, Carcinus maenas (Crustacea, Decapoda): ultrastructure and functional properties of sensilla sensitive to the changes in seawater concentration. Cell Tissue Res 257:609–621
Schmidt M (1990) Ultrastructure of a possible new type of crustacean cuticular strain receptor in Carcinus meanus (Crustacea, Decapoda). J Morphol 204:335–344
Schmidt M, Gnatzy W (1984) Are the funnel-canal organs the ‘campaniform sensilla’ of the shore crab, Carcinus maenas (Decapoda, Crustacea)? II. Ultrastructure. Cell Tissue Res 237:81–93
Sleigh M (1979) Contractility of roots of flagella and cilia. Nature 277:263–264
Spira AW, Milman GE (1979) The structure and distribution of the cross-striated fibril and associated membranes in guinea pig photoreceptores. Am J Anat 155:319–338
Stephens RE (1975) The basal apparatus. J Cell Biol 64:408–420
Studer D, Michel M, Müller M (1989) High pressure freezing comes of age. In: Albrecht R, Ornberg R (eds) The science of specimen preparation. SEM. AMF O'Hare, Chicago, pp 253–269
Toh Y (1981) Fine structure of sense organs on the antennal pedicel and scape of the mate cockroach, Periplaneta americana. J Ultrastruct Res 77:119–132
Toh Y, Yokohari F (1985) Structure of the antennal chordotonal sensilla of the American cockroach. J Ultrastruc Res 90:124–132
Trelstad RL (1982) Multistep assemply of type I collagen fibrils. Cell 26:197–198
Wang K, Wright J (1988) Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line. J Cell Biol 107:2199–2212
Witman GB (1990) Introduction to cilia and flagella. In: Bloodgood RA (ed) Ciliary and flagellar membranes. Plenum, New York, pp 1–30
Wolfrum U (1990) Actin filaments: the main components of the scolopale in insect sensilla. Cell Tissue Res 261:85–96
Wolfrum U (1991a) Distribution of F-actin in the compound eye of Challiphora erythrocephala (Diptera, Insecta). Cell Tissue Res 263:399–403
Wolfrum U (1991 b) Tropomyosin is co-localized with the actin filaments of the scolopale in insect sensilla. Cell Tissue Res 265:11–17
Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76:4498–4502
Yajima T (1986) Acid phosphatase activity and intercellular collagen degradation by fibroblasts in vitro. Cell Tissue Res 245:253–260
Young D (1970) The structure and function of a connective chordotonal organ in the cockroach leg. Philos Trans R Soc Lond [Biol] 256:401–426
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Wolfrum, U. Centrin- and α-actinin-like immunoreactivity in the ciliary rootlets of insect sensilla. Cell Tissue Res 266, 231–238 (1991). https://doi.org/10.1007/BF00318178
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DOI: https://doi.org/10.1007/BF00318178