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CILIA of a DISTINCTIVE STRUCTURE (G + O) in ENDOCRINE and OTHER TISSUES

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CILIA of a DISTINCTIVE STRUCTURE (G + O) in ENDOCRINE and OTHER TISSUES 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 sense 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 respiratory tract and fallopian have been more intensively studied with the tu)bes in tthe human 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 1962). Grimstone, 9 + 0 cilia in mammalian tissues differ from The cilia -are characterized by a 9 + 2 fibre the 9 + 2 form in that they are associated with copyright. patern (Fig. '1) and a single basal body; the a 'diplosome that is a pasir of centrioles, one basal 'body, which has been referred to variously usually lying at right angles to the other. The as the kinetoplast, kinetosome, centrosome, 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. centriole (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 October 1, 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 cell, whilst in mammaRiin tissue such as the tracheal epithelium there are numerous 9 + 2 cilia in each cell. These cilia have been found in invertebrates, for example in Myzostomum sperms (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 t,434,'3 -3i~.'':'- 333 3?84:3'33333 33 FIBRES i-INVAGINATION 33: 333 ::·.·::· CELL MEMBRANE DISTAL CENTRIOLE o BASAL BODY iivl .....I''!·i·: ::. '... I 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 '¶3'33~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~il:iiiil:'3 3 3;333333'~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~,,33 ~~ ~ ~ ~ ~ ~ ~~, ~~~·i··i·.,33* ~~~~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 3433'33333 33 : 3i"L3333 ,3,3 issue3 3~3 33333 the distal centriole: the bands are spaced at Fi.the.Srato cnriole or baa od naelo copyright. 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 cell membrane 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) Ellis Human foetus (1966) on October 1, 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 Rete testis 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 ~iI ~~~4 ·~~~~~~~~~~~~~~~~~~~"~ ~i~i~? ~i~~... ~ii~~~~~~~~~~i......~~?i ~ ? ~i~i~iii~!~ i~ ~ 'i,~·''b , :* . ':· 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 thick. We have con- unusually 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: the centriolar fibres: are but do .. http://pmj.bmj.com/ 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 the ibetween peripheral on October 1, 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 -Ail 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 all fibre pairs do not extend to the tip of a The tissues in which the 9 + 0 cilia with copyright. 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.
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