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Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from POSTGRAD MED. J. (1966), 42, 403 CILIA OF A DISTINCTIVE STRUCTURE (g + o) IN ENDOCRINE AND OTHER TISSUES

A. R. CURRIE, BSC., F.R.C.P. (Edin. and Glas.), F.C.Path., F.R.S.E. D. N. WHEATLEY, B.Sc., Ph.D., 'MI.Biol. Department of Pathology, University Medical Buildings, Foresterhill, Aberdeen.

CILIA or flagella control and effect the move- ear (Gray, 1960), and in cells of Pecten ment of many unicellular organisms, for (Miller, 1958) and crab (Whitear, 1960). They example Paramecium; they may also cause have been more frequently reported, however, in movement of the medium surrounding cells vertebrate tissues-particularly mammalian- as in flame cells of Platyhelminuthes and in the but this may be due to the fact that these tissues epidielium of the and fallopian have been more intensively studied with the tu)bes in tthe subject. The fine structure electron microscope (Talble 1). of these cilia is well known and is essentially the same from the 'lowest ciliated creature to the highest mammals (for a brief review see Structure of 9 + 0 cilia Grimstone, 1962).

9 + 0 cilia in mammalian tissues differ from by copyright. The cilia -are characterized by a 9 + 2 fibre the 9 + 2 form in that they are associated with patern (Fig. '1) and a single ; the a 'diplosome that is a pasir of , one basal 'body, which has been referred to variously usually lying at right angles to the other. The as the , kinetosome, , fine structure of the cilium, 'in longitudinal and basal granulle, basal corpuscle etc., has a very transverse section, is illustrated diagrammatic- characteri'stic structure identical with that of the ally in Fig. 3. (Fig. 2). Our studies of these cilia in the zona glomer- Recent work on ciliary movement has led to ulosa of the rat adrenal cortex (Wheatley, the following hypotheses: the peripheral fi)bre 1966a) have confirmed much of the earlier http://pmj.bmj.com/ pairs are prObably contractile, whilst the central reports. The cilium ('Fig. 4) is a solitary organ- pair may be structural supports that determine elle; its basal body (referred to as the distal the plane in which a cilium moves (Gibbons, centriole by Barnes, 1961) and associated cen- 1961; Afzeliu's 1962,); secondary fiibres or side- triole (or proximal centriole) lie close to the arms may possess the contractile fibrous nucleus. The Golgi zone is seen nearby. The wall proteins whidh move a cilium (Andre, 1961). of the proximal centriole (in transverse section

From time to time brief reports on "aberrant" on September 27, 2021 by guest. Protected forms of cilia have been published (Pitelka, 1962; Satir, 1962). It is now establis1hed, how- ever, that there is a distinctive ciliary type with a fibre pattern of 9 + 0, in contrast to the usual 9 + 2 form, and it has lbeen found iin cells of many different organs. Wthen 9 + 0 cilia are found there is generally only one in a , whilst in mammaRiin such as the tracheal there are numerous 9 + 2 cilia in each cell. These cilia have been found in invertebrates, for example in Myzostomum (Afzelius, 1962), in the plate organs of the honey-bee antenna (Slifer and Sekhon, 1961), in the locust Fig. 1. Diagrammatic L.S. and T.S. of a 9 + 2 cilium Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from 404 POSTGRADUATE 'MEDICAL JOURNAL July, 1966

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Oot -___ PROXIMAL co CENTRIOLE the3rat adrenal zona glomerulosa. X 140,000. Fig. 3. Diagrammatic L.S. and T.S. of a 9 + 0,, A33electro3n are of lead3contra3tod u-Itra Fig.2T.S.ofmicrographsa centriole or basal body inof~~~~~~~~~~-Irii~~:.a cell r· ·· :·9diplosome-associated cilium

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~~~~33'~~~~~~~~~~~~~,,333~~iii';:.~i~:i 3 33 3~~~~~~~3¶33,'3333',33'33"'3" ""V).~~~~~~~~~~~~~~~~~~~~~~~~~3' "3.. ··::· in Fig. 4) consists of nine 'bundles, each of which -thinsecti3ons of OsO,-fixed, Eo 82m' de has three fibrous elements. Banded filaments i~333'333333333333ei~ 333 '3 ,;'"33';33,3' 3,~3'3333 radiate from the two bundles that lie closest to

3333 33 3 3 3~3 33333 3433'33333 : 3i"L333 ,3,3 issue the distal centriole: the bands are spaced atby copyright. Fi.the.Srato cnriole or baa od naelo All~~~~~~~~.eletro adrena'.l'rirogaphzona;:~ glmrloaar ofled cntrste1000ulra intervals of about 550 A. The distal centriole, thinsecin of 0s0-fied Epon 8:i1:~::'::2-embedded~'' :or basal body (in longitudinal section in Fig. t.issue.Rli,,,Iil 4), is about 330mu in length. From it paracen- trioles or satellites arise; cytoplasmic micro- tubules, or spindle fibres, are often attached to these processes. The basal body is linked to the by processes, similar in structure

TABLE 1 http://pmj.bmj.com/ SUMMARY OF PREVIOUS REPORTS ON MAMMALIAM TISSUES WITH 9 + 0 OR DIPLOSOME-ASSOCIATED CILIA Tissue Species Reference Adenohypophysis Mouse Barnes (1961) Rabbit Salazar (1963) iRat Maillard (1963) Dog Kagayama (1965) Human foetus Ellis (1966) on September 27, 2021 by guest. Protected Adrenal medulla Rat de Robertis et al. (1960) Coupland (1965) Pancreas (endocrine) Mouse (a cells) Munger (1958) (/ cells) Eisterhuizen and Lever (1961) Parathyroids Man Munger and Roth (1963) Virginia Deer Rat Leeson (1962) Cerebral cortex Rat Dahl (1963) Retina Mouse de Robertis (1956) Various mammals Tok,ayasu and Yamada (1959) Guinea-pig Allen (1965) Autonomic nervous system Rat Grillo and Palay (1963) Kidney Rat Latta et al. (1961) Skin Man Wilson and MdWhorter (1963) Spleen Human foetus Zamboni and Westin (1964) 'Endothelial cells of Itrabeculum of eye Man Vegge (1963) Fibrobla,sts and smooth muscle cells iRat Sorokin (1962) Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from July, 1966 CURRIE and WHEATLEY: Cilia of a Distinctive Structure 405

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FIG. 4. L.S. of cilium in a zona glomerulosa cell. X50,000. to the satellites: these become wider towards the cell Imemlbrane and terminate in a row of very small particles. The membrane at the base of the cilium is unusually thick. We have con- by copyright. firmed Dahl's (1963) report that each of the nine triplets of the basal body sends out a processs to sl::. c the cell membrane. Sometimes a cluster of i:: ::LF"i...i%8Ps'88B.L II: vesicles is found around these processes and the same type of vesicle (about 200 A diameter) is not uncommonly scattered throughout the matrix of the whole diplosome region. The filbres of the cilium arise directly from .c;.:. :·rw~c:.p we:b:~~ .· .. :C: http://pmj.bmj.com/ the centriolar fibres: are but do .. they paired e~~··::*i·;1 X ,.· not usually appear to have side-arms like the 'X'''iz,: 9 + 2 cilium 'fibres. It ihas ,been suggested by Dahl l(1963) that connexions Imay be present between the filbre pairs and in our experience there is some evidence of Itheir presence (Fig. 5). We have also confirmed Dahl's report that there is a connexion ibetween the peripheral on September 27, 2021 by guest. Protected filbre pairs and the cell membrane. Afzelius (1962) has reported that secondary fibres may also be found, and our studies have sometimes suggested their presence. Dahl (1963) and Allen (1965) reported that filbre rearrangement takes place along the length of the cilium. By serial sectioning of cilia of the rat adrenal cortex we have established that (1) cilia taper considerably for most of their length '(Fig. 6a-c)-they can be over 2t/ long; (2) all nine peripheral pairs cannot be accommodated at the periphery as the cilium becomes narrower: a rearrangement FIG 5.- T.S. of cilium showing 9 + 0 fibre arrange- of fibres occurs to give patterns of eight or fewer ment. A connexion between fibre pairs is seen peripheral pairs with one or more pairs of fibres alt C and between a fibre pair and the cell mem- centrally placed to give, for example, an "8 + brane at I. X35,000. Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from 406 POSTGRADUATE MEDICAL JOURNAL July, 1966

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FIG. 6a-c.- T.S. at base (a), in distal region (b) and tip (c) of a serially sectioned cilium. All at same magnification :-Y 54 000

1" or "7 + 2" arrangement (Fig. 6b); and (3) Cilia in other tissues by copyright. all fibre pairs do not extend to the tip of a The tissues in which the 9 + 0 cilia with cilium and this probably explains the reports diplosome associations have been previously of cilia with less than 9 pairs of fibres (Steiner, reported are given ,in Table 1, and we have now Carruthers and Kalifat, 1962; Salazar, 1963; found them in the following cells: Coupland, 1965). 1. Rat zona glomerulosa ('Wheatley, 1966a) 2. Mouse zona glomerulosa (Wheatley, Cilia in rat zona glomerulosa 1966a) The electron micrographs here used to illus- 3. Rat adeno'hypophysis ,(Wheatley, 1966b) trate the structure of cilia and diplosomes are 4. Human foetal adenohypophysis (Ellis, http://pmj.bmj.com/ from the rat adrenal zona glomerulosa, in which 1966) they have not been described previously. They 5. Human foetal epidermis are particularly easy to detect When the adrenal 6. Human foetal cerebral cortex gland has been damaged by the action of dsime- 7. Rat duodenal smooth muscle thylbenz(a)anthracene (DMBA) (Huggins and Morii, 1961): this carcinogen causes necrosis of Function of 9 + 0 cilia the zona fasciculata and zona reticularis but not The extent to which a cilium into protrudes on September 27, 2021 by guest. Protected of the zona glomerulosa. Some of the zona the intercellular space varies from one to another glomerulosa cells do, however, seem to contain and it seems likely that it is not a rigid passive large cytoplasmic 'but iby serial section- structure which always Ibears the same relation- ing we have shown that in many cases these ship to its cell and the intercellular space: it is are continuous with and cilia probable that it can be protruded or retracted. frequently project into them (Fig. 7). Subjec- Its function is unknown but several hypotheses tively cilia seem to be more numerous in the will be briefly discussed. DMBA-treated rat adrenal than in the normal (1) Sensory function. It was suggested by gland, but this may be due to their tbeing more Munger 1(1958) and Barnes (1961), largely on easily detected. The zona fasciculata and zona the basis that these oilia are found in a number reticularis have been carefully searched for cilia of sensory cells, that they have a sensory but with negative results: centrioles, which function. appear to have the characteristics of basal (2) Motile function. Coupland (1965) sug- bodies are present but without the ciliary pro- gested that the cilia "stir up" the intercellular cesses (Fig. 8). fluid. Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from July, 1966 CURRIE and WHEATLEY: Cilia of a Distinctive Structure 407

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FIG. 7.- Cilium of a zona glomerulosa cell in a , from an adrenal gland of a rat treated with dimethylbenz(a)anthracene. X12,500. (3) Role in . The association of cilia the other hand, it may be that the cilium deter- with the centriolar apparatus raises the possi- mines one pole of a cell before mitosis, the cen- bility that they may Ibe involved in some way by copyright. in the Iprocess of cell division. (4) Vestigial. The 9 + 0 oiliary figure arrange- ment may be due to incom'plete morphogenesis of the 9 + 2 form (Sorokin, 1962). It seems unlikely that the cilia are vestigial and non-functioning since they are present in a numlber of foetal tissues and their morphology is consistent from cell to cell and from tissue to tissue. Nor does it seem likely that one cilium http://pmj.bmj.com/ plays an -important motile role. Several questions must be answered before their Ipossible function is defined: for example, it is of importance to determine whether every cell of a tissue possesses a cilium and whether each cell has only one cilium. Dalhl (1963) presented some evidence that most of the cells of the fascia dentata in the rat cerebral cortex possess a on September 27, 2021 by guest. Protected cilium. Barnes (1961) found an indication of two cilia in a single cell of the mouse adeno- hypophysis. Some cells of the rat adenohypo- physis (Wheatley, 1966b) and of the trabecular endothelium in the human eye (Vegge, 1963) possess two cilia. We are more inclined to the view that the cilium may have a sensory function. It certainly orovides a direct means of communication between the extracellular enviroment and the centriolar apparatus. In view of the latter's role in cell division, the associated ciliuum may be some delicate control mechanism through which FIG. 8.- Centriole with characteristics of a basal a cell may receive the to divide. On body in a zona reticularis cell. X35,000. Postgrad Med J: first published as 10.1136/pgmj.42.489.403 on 1 July 1966. Downloaded from 408 POSTGRADUATE MEDICAL JOURNAL July, 1966 triole not associated with a cilium (the proximal LEESON, T. S. (1962): Electron Microscopy of the centriole) migrating into a diametrically oppo- Rete Testis of the Rat, Anat. Rec., 144, 57. site position. MAILLARD, M. (1963): Origine des Grains de S&cretion We acknowledge the Scottish Hospital Endow- dans les Cellules de 1' ant6hypophyse Embryonnaire ments Research Trust for a grant in part support of du Rat; R6le de l'appareil de Golgi, J. de Mikro- this work. scopie, 2, 81. Figs. 2, 4, 5, 6a, 6b and 8 are reproduced by MILLER, W. H. (1958): iDerivatives of Cilia in the permission of the Editor of J. 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med. Bull., 18, 238. WHITEAR, M. (1960): Chordotonal Organs in Crus- on September 27, 2021 by guest. Protected HUGGINS, C., and MORII, S. (1961): Selective Adrenal tacea, Nature, (Loud.) 187, 522. Necrosis and Apoplexy induced by 7, 12-dimethyl- WILSON, R. B., and MCWHORTER, C. A. (1963): benz(a)anthracene, J. Exp. Med., 114, 741. Isolated Flagella in Human Skin. Electron Micro- KAGAYAMA, M. (1965): The 'Follicular Cells in the Lab. Invest., 12, 242. Pars Distalis of the Dog Pituitary Gland: an Elec- scopic Observations, 'tron Microscope Study, Endocrinology, 77, 1053. ZAMBONI, L., and WESTIN, B. (1964): The Ultrastruc- LATTA, H., MAUNSBACH, A. B., and MADDEN, S. C. ture of the Human Foetal Spleen. I. One Type of (1961): Cilia in Different Segments of the Rat Mesenchymal Cell in the Early Stages of Develop- , J. biophys. biochem. Cytol., 11, 248. ment of the Spleen, J. Ultrastruct. Res., 11, 469.