The centriole, a central enigma of cell biology

The Centriole: A Central Enigma of Cell Biology. By D. N. Wheatley. Amsterdam: Elsevier Biomedical Press (distributed in New York by Elsevier Science Publishing Company). (1982). 232 pp. $88.50. doo-die-bug, n: any unscientific device with which it is claimed that minerals may be located (Webster’s New Collegiate Dictionary, 2d ed., 1960). During the last quarter of the nineteenth century, Van Beneden, Boveri and others described “a body of extreme minuteness” they named the centriole, with a surrounding granular centrosome. Their remarkable observations- some accurate, others not-led them to view the centriole as an autonomous organelle that divides in anticipation of division, serves as the “dynamic centre of the cell” and “exerts an extraor- dinary influence on the cytoplasmic network during cell-division” (E. B. Wilson, The Cell in Development and Inheritance, 1896, MacMillan; reprinted in 1966 by Johnson Reprint Corporation, New York). By 1883, Van Beneden conceived of cell polarity as being de- fined by a line drawn through the center of the nucleus and the centriole. As the century was about to turn, Henneguy and Lenhossek observed that centrioles could form the basal bodies of flagella and cilia, and the interconvertibility of centrioles and basal bodies became a part of our understanding of centrioles. Light microscopists’ studies of centriole behavior con- tinued, as a tiny part of the biological literature, until World War II; one of my favorites is Huettner’s classic study of the continuity of centrioles in Drosophila (Z. Zellforsch. 79, 119-l 34, 1933). Beginning in the 1950s the electron microscope revealed the beauty of centrioles and basal bodies: nine blades, each formed of a triplet microtubule, equally spaced around the perimeter of a circle, mak- ing a short cylindrical structure about 0.2 pm in di- ameter- almost too minute to see in the light micro- scope. Elegant structural studies followed, including that by Anderson (J. Cell Biol. 54, 246-265, 1972). The centriolar pinwheel was found in representatives of all major groups of eucaryotes, supporting the conclusions that the first eucatyote had this ninefold symmetric structure and that it had been conserved throughout 3 billion years of subsequent evolution. Only a few variations have been found, including nine- singlet centrioles in the nematode Ascaris (Goldstein, J. Morphol. 154, 317-337, 1977) which was one of the major organisms studied by Van Beneden and Boveri, and centrioles of two insects that contain 12 and 14 triplets (Baccetti et al. J. Cell Sci. 73, 321- 335, 1973). The “replication” of centrioles was con- firmed, but because a “daughter” centriole forms perpendicular to the axis of its “parent,” replication through one pinwheel serving as template for another did not seem plausible. Some fantastic forms of rep- lication were described, especially in cells that were producing quantities of basal bodies for multiple cilia (for example, Steinman, Am. J. Anat. 722, 19-55, 1968). Biologists began to seek DNA in centrioles. DNA was not found, but evidence that centrioles may contain RNA has accumulated (for example, Dip- pell, J. Cell Biol. 69, 622-637, 1976). Overwhelming evidence has accumulated that the centriolar pinwheel can form in the absence of “parent” pinwheels, even in cells that lack centrioles. In the amebo-flagellate Naegleria, for example, the amebae migrate and di- vide with a celerity that puts vertebrate cells to shame, but without pinwheels; whereas during differentiation to flagellates, the cells form classical nine-triplet basal bodies. A direct role of centriolar pinwheels in kary- okinesis has become suspect (Berns et al., Science 273, 505-513, 1981) yet when the organelles persist through mitosis, they pass through an orderly dance in relation to cell division. All eucaryotic cells that form cilia or flagella appear to build this structure from a specific end of the pinwheel, perhaps using the triplet microtubules as seeds for the assembly of the outer- doublet microtubules of the motile appendage (typical 9 + 2 formula) or, usually, the nonmotile appendage (9 + 0)-the latter, often found on vertebrate cells, misnamed a primary cilium. In at least one case, after a 9 + 2 flagellum is assembled, the basal body dis- integrates but the flagellum remains and functions. So while the pinwheel may be needed for flagellar assembly, it may be dispensable for function (Fawcett, Dev. Biol. 44, 394-436, 1975). Centrioles and cen- trosomes act as microtubule-organizing centers in two distinct ways, which are not mutually exclusive. In the basal body mode, the outer-doublet microtubules of cilia and flagella form a direct continuity with the pinwheel microtubules; whereas in assemblages the aster type, microtubules form with centriole as the focal point, but usually terminate in the pericen- triolar matrix. Recently, a first success has been achieved in the characterization of centriolar proteins (Anderson and Floyd, Biochemistry 7 9, 5625-5631, 1980). The centriole has been proposed to be a rotary engine- a proposal for which no evidence has been forthcoming, although it appears that the central-pair microtubules of flagella do rotate within the outer doublets (Omoto and Kung, J. Cell Biol. 87, 33-46, 1980). It has been reported that centrioles contain silicon. Bornens (Biol. Cell. 35, 1 15-l 32, 1979) has presented an imaginative view of centrioles as “gyroscopic oscillators. ” Albrecht-Buehler, whose work has indicated that centrioles and primary cilia are oriented with respect to the orientation of migrat-