Atpase Activity in the Ciliary Rootlet of Human Retinal Rods

Matsusaka, Toshihiko

doi:10.1083/jcb.33.1.203

Cited by 42 publications

(21 citation statements)

References 12 publications

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“…Chlamydomonas Mutant with Altered Rotational Orientation contractile proteins and ATPase activity are associated with the striated fibers ofmany organisms (2,18,21,42).…”

Section: Discussionmentioning

confidence: 99%

Flagellar waveform and rotational orientation in a Chlamydomonas mutant lacking normal striated fibers.

Hoops¹,

Wright²,

Jarvik³

et al. 1984

The Journal of Cell Biology

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The Chlamydomonas mutant vfl-3 lacks normal striated fibers and microtubular rootlets. Although the flagella beat vigorously, the cells rarely display effective forward swimming . High speed cinephotomicrography reveals that flagellar waveform, frequency, and beat synchrony are similar to those of wild-type cells, indicating that neither striated fibers nor microtubular rootlets are required for initiation or synchronization of flagellar motion . However, in contrast to wild type, the effective strokes of the flagella of vfl-3 may occur in virtually any direction . Although the direction of beat varies between cells, it was not observed to vary for a given flagellum during periods of filming lasting up to several thousand beat cycles, indicating that the flagella are not free to rotate in the mature cell. Structural polarity markers in the proximal portion of each flagellum show that the flagella of the mutant have an altered rotational orientation consistent with their altered direction of beat. This implies that the variable direction of beat is not due to a defect in the intrinsic polarity of the axoneme, and that in wild-type cells the striated fibers and/or associated structures are important in establishing or maintaining the correct rotational orientation of the basal bodies to ensure that the inherent functional polarity of the flagellum results in effective cellular movement . As in wild type, the flagella of vfl-3 coordinately switch to a symmetrical, flagellar-type waveform during the shock response (induced by a sudden increase in illumination), indicating that the striated fibers are not directly involved in this process .Striated fibers are associated with most cilia and flagella (26,36), including the modified cilia of sense organs (3) . Their ubiquitous presence suggests that these fibers play an important role or roles in flagellar and ciliary morphogenesis or function. Several possible functions have been proposed for the striated fibers, including (a) an active role in the initiation or coordination of flagellar movement (7, 15,19,31,32,42), (b) a passive role in anchoring the cilia and flagella to resist the forces and moments resulting from ciliary or flagellar beating (1,25,26,37,38), and (c) a role in the development or maintenance of the proper positioning of the basal bodies (9, 11,25,26). However, there has previously been no experimental evidence for any of these functions.Recently, a mutant of Chlamydomonas was described that is defective in striated fibers and microtubular rootlets (43). This mutant provides an opportunity for learning more about the roles of these structures. We studied flagellar waveform and orientation in forward and reverse swimming cells ofthis $~s mutant; the flagella have a waveform similar to that of wild type in both forward and reverse beating modes. However, the direction of beat is highly variable, and thin-section analysis shows that the mutant's flagella are present in abnormal rotational orientations . These results suggest that the striated f...

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“…Chlamydomonas Mutant with Altered Rotational Orientation contractile proteins and ATPase activity are associated with the striated fibers ofmany organisms (2,18,21,42).…”

Section: Discussionmentioning

confidence: 99%

Flagellar waveform and rotational orientation in a Chlamydomonas mutant lacking normal striated fibers.

Hoops¹,

Wright²,

Jarvik³

et al. 1984

The Journal of Cell Biology

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“…In primates these fibrillar structures frequently have an intimate association with other cellular organelles, such as mitochondria (Orzalesy and Bairati, 1964;Matsusaka, 1967;Uga et aI., 1970;Murray et aI., 1973). In primates these fibrillar structures frequently have an intimate association with other cellular organelles, such as mitochondria (Orzalesy and Bairati, 1964;Matsusaka, 1967;Uga et aI., 1970;Murray et aI., 1973).…”

Section: Discussionmentioning

confidence: 99%

Comparative Retinal Pigment Epithelium and Photoreceptor Ultrastructure in Nocturnal and Fossorial Rodents: The Eastern Woodrat, Neotoma floridana, and the Plains Pocket Gopher, Geomys bursarius

Feldman

Phillips

1984

Journal of Mammalogy

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In fossorial plains pocket gophers (Geomys bursarius) the eyes are extremely small and the cells of the retinal pigment epithelium (RPE) have extensive, highly developed apical microvilli and numerous melanolysosomes. The neural retina consists of both cone (up to 25%) and rod photoreceptor cells. The cones often are clustered and surrounded by rods. Ultrastructurally, the cones differ from rods in position and appearance of nuclei, overall shape of cell body, disc membrane, and presence of pedicle-type synaptic terminals. By way of comparison, in nocturnal eastern woodrats (Neotoma floridana) the RPE cells have poorly developed apical microvilli and relatively few melanolysosomes. The neural retina consists almost entirely (99%) of abundant and densely packed rod photoreceptors characterized by unusually long outer segments with a high number of discs. Numerous significant quantitative differences between RPE and photoreceptors of Neotoma and Geomys serve to underscore further the dissimilarities of the retinas of these rodents. Although G. bursarius and other species of gophers live in dark or semi-dark burrow systems and have eyes that are reduced in size, the RPE and neural retina is characterized by an intermediate (diurnal-nocturnal) structural pattern suggestive of good visual acuity. The lack of any obvious specialization in RPE or photoreceptor morphology is striking and could imply that the generalized eye in gophers is representative of the eyes found in their ancestors. If so, gophers probably evolved from ground-dwelling diurnal species.J. Mamm., 65 (2):231-245, 1984 231 at University of Nebraska-Lincoln Libraries on June 9, 2016 http://jmammal.oxfordjournals.org/ Downloaded from 232 JOURNAL OF MAMMALOGY Vol. 65, No.2morphology. The neural retina in Neotoma is vascularized; capillaries are particularly prominent in the inner nuclear layer where they seem to lie in a plane parallel to the retinal layers. Capillaries, arterioles, and venules also are common in the ganglion cell layer, bordering on the

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“…Though most authors describe a constant banding pattern, at least three reports have commented upon the variations in rootlet period-424 icity (15,32,34) and have inferred a possible physiological role for the altered states . The idea that the rootlet is a contractile element of the flagellar apparatus which may play an active role in modifying the flagellar beat is supported by the following : the recent demonstration of cyclic contraction and extension of an algal rhizoplast mediated by calcium and adenosine triphosphate (32); the isolation and reactivation of the flagellar apparatus from Chlamydomonas reinhardii by adenosine triphosphate (18) ; and reports of adenosine triphosphatase activity in the striated rootlets of algae (32), flagellates (1), and of vertebrate oviduct (2) and retinal rod cells (25) .A satisfactory understanding of their nature and function awaits the isolation and characterization of the major constituents of rootlets from diverse sources . To date, rootlet proteins have been described from only three sources : the molluscan gill epithelium rootlet, 230,000 and 250,000 daltons (37); the Tetrahymena kinetodesmal fiber, 250,000 daltons (40) ; and the giant costa of the flagellate Trichomonas, 90,000 daltons (1) .…”

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confidence: 94%

Isolation, ultrastructure, and protein composition of the flagellar rootlet of Naegleria gruberi.

Larson¹,

Dingle²

1981

The Journal of Cell Biology

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Attached to the basal bodies of Naegleria gruberi flagellates is a striated rootlet or rhizoplast . The rootlet-basal body complex has been isolated by Triton X-100 lysis of deflagellated cells and differential centrifugation through a 25% glycerol medium . Rootlets isolated from mature flagellates are -13 p,m long but vary from 8 to 15 ftm in length : they taper at both ends from a maximum width of -0 .25 p,m in the vicinity of the basal bodies . They are highly stable during isolation but can be solubilized by urea, high salt, low pH, or detergent (Sarkosyl) . Partial dissociation of rootlets with 1 M urea reveals that they are composed of filaments, -5 nm diameter, associated in linear fashion to yield the characteristic 21-nm cross-banded appearance . Differential solubilization of rootlets and their associated contaminants allowed identification of a major rootlet protein, comprising at least 50% of any purified rootlet preparation, with an apparent subunit molecular weight of 170,000. The localization of rootlets in situ by indirect immunofluorescence using a specific antibody directed against the purified rootlet protein demonstrated unequivocally that this 170,000-dalton protein is an organelle component.The flagella of eukaryotic cells are generally found as part of a flagellar apparatus-an interconnected assemblage of basal body, flagellum, and a striated rootlet fiber or rhizoplast . Likewise, cilia, basal bodies, and one or more rootlets often combine to constitute what could be called a "ciliary apparatus" in ciliated cells . Although flagellated and ciliated cells lacking rootlets are known, and even common (e .g., sperm cells, certain mammalian ciliated epithelia), some form of rootlet structure is attached to the basal bodies of most cilia and flagella (7,8,30) . Despite intense current interest in the structure, function, and morphogenesis of flagella and their basal bodies, virtually no attention has been paid to the other major component of the flagellar or ciliary apparatus, the rootlet. References to flagellar rootlets have most often been restricted to ultrastructural descriptions and to speculation about possible roles in motility (5,9,15,16,19,26,28,34,38) .Electron micrographs of rootlets generally reveal bundles of 4-to 5-nm-diameter filaments aggregated in a paracrystalline array to produce fibrous, cross-striated organelles reminiscent of collagen fibrils (9, 26, 28, 37) . The cross-striations form one major repeating unit that may be further divided into -13 intraperiod sub-bands (28, 38) . Reported widths for this major repeat unit range from 12 to 78 nm (34,35) . Though most authors describe a constant banding pattern, at least three reports have commented upon the variations in rootlet period-424 icity (15,32,34) and have inferred a possible physiological role for the altered states . The idea that the rootlet is a contractile element of the flagellar apparatus which may play an active role in modifying the flagellar beat is supported by the following : the recent demonst...

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Atpase Activity in the Ciliary Rootlet of Human Retinal Rods

Cited by 42 publications

References 12 publications

Flagellar waveform and rotational orientation in a Chlamydomonas mutant lacking normal striated fibers.

Flagellar waveform and rotational orientation in a Chlamydomonas mutant lacking normal striated fibers.

Comparative Retinal Pigment Epithelium and Photoreceptor Ultrastructure in Nocturnal and Fossorial Rodents: The Eastern Woodrat, Neotoma floridana, and the Plains Pocket Gopher, Geomys bursarius

Isolation, ultrastructure, and protein composition of the flagellar rootlet of Naegleria gruberi.

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