|
|
|
|
|
|
|
|
|||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
Journal of Cell Science, Vol 3, 207-230, Copyright © 1968 by Company of Biologists
Submitted on June 21, 1967
1 Department of Anatomy, Harvard Medical School Boston, Massachusetts 02115, U.S.A.
This study presents reconstructions of the processes of centriolar formation and ciliogenesis based on evidence found in electron micrographs of tissues and organ cultures obtained chiefly from the lungs of foetal rats. A few observations on living cultures supplement the major findings.
In this material, centrioles are generated by two pathways. Those centrioles that are destined to participate in forming the achromatic figure, or to sprout transitory, rudimentary (primary) cilia, arise directly off the walls of pre-existing centrioles. In pulmonary cells of all types this direct pathway operates during interphase. The daughter centrioles are first recognizable as annular structures (procentrioles) which lengthen into cylinders through acropetal deposition of osmiophilic material in the procentriolar walls. Triplet fibres develop in these walls from singlet and doublet fibres that first appear near the procentriolar bases and thereafter extend apically. When little more than half grown, the daughter centrioles are released into the cytoplasm, where they complete their maturation. A parent centriole usually produces one daughter at a time. Exceptionally, up to 8 have been observed to develop simultaneously about 1 parent centriole. Primary cilia arise from directly produced centrioles in differentiating pulmonary cells of all types throughout the foetal period. In the bronchial epithelium they appear before the time when the ciliated border is generated.
Fairly late in foetal life, centrioles destined to become kinetosomes in ciliated cells of the epithelium become assembled from masses of fibrogranular material located in the apical cytoplasm. Formation of these centrioles may be under the remote influence of the diplosomal centrioles. More certainly, the precursor material accumulates in close proximity to Golgi elements. Within the fibrogranular areas, osmiophilic granules (400-800Å) increase in size and eventually become consolidated into dense spheroidal bodies (deuterosomes), which organize the growth of procentrioles around them. When mature, the newly formed centrioles become aligned in rows beneath the apical plasma membrane. There each centriole produces satellites from its sides, a root from its base, and a cilium from its apex. Early stages in the formation of both primary cilia and those of the ciliated border are similar. In developing cilia of the ciliated border, however, the outer ciliary fibres rapidly reach the tips of the elongating shafts, and a central pair of fibres is formed (9 + 2 arrangement). In primary cilia, development of the fibres seems to lag behind the elongation of the shafts, and only the outer ciliary fibres appear (9 + 0 arrangement). The strengths and weaknesses of the proposed reconstructions of centriolar formation and ciliogenesis are discussed, and the occurrence in other living forms of similar pathways for centriolar formation is noted. Further discussion leads to an interpretation of the centriole as a semi-autonomous organelle whose replicative capacity is separable from the characteristic triplet fibre structure of its wall.
Submitted on June 21, 1967
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  S. Blachon, X. Cai, K. A. Roberts, K. Yang, A. Polyanovsky, A. Church, and T. Avidor-Reiss A Proximal Centriole-Like Structure Is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication Genetics, May 1, 2009; 182(1): 133 - 144. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. Prosser, K. R. Straatman, and A. M. Fry Molecular Dissection of the Centrosome Overduplication Pathway in S-Phase-Arrested Cells Mol. Cell. Biol., April 1, 2009; 29(7): 1760 - 1773. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Yin, F. Bangs, I. R. Paton, A. Prescott, J. James, M. G. Davey, P. Whitley, G. Genikhovich, U. Technau, D. W. Burt, et al. The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation Development, February 15, 2009; 136(4): 655 - 664. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. C. Keller, S. Geimer, E. Romijn, J. Yates III, I. Zamora, and W. F. Marshall Molecular Architecture of the Centriole Proteome: The Conserved WD40 Domain Protein POC1 Is Required for Centriole Duplication and Length Control Mol. Biol. Cell, February 1, 2009; 20(4): 1150 - 1166. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Absalon, T. Blisnick, M. Bonhivers, L. Kohl, N. Cayet, G. Toutirais, J. Buisson, D. Robinson, and P. Bastin Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei J. Cell Sci., November 15, 2008; 121(22): 3704 - 3716. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. A. Barr Cilia the masterplan J. Cell Sci., January 1, 2008; 121(1): 5 - 6. [Full Text] [PDF]
|
|
|
|
 |
|
 E. K. Vladar and T. Stearns Molecular characterization of centriole assembly in ciliated epithelial cells J. Cell Biol., October 3, 2007; 178(1): 31 - 42. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Fan, V. Fogg, Q. Wang, X.-W. Chen, C.-J. Liu, and B. Margolis A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin {beta} interactions J. Cell Biol., July 24, 2007; 178(3): 387 - 398. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-i. Yoshimura, J. Egerer, E. Fuchs, A. K. Haas, and F. A. Barr Functional dissection of Rab GTPases involved in primary cilium formation J. Cell Biol., July 24, 2007; 178(3): 363 - 369. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Kuriyama, Y. Terada, K. S. Lee, and C. L. C. Wang Centrosome replication in hydroxyurea-arrested CHO cells expressing GFP-tagged centrin2 J. Cell Sci., July 15, 2007; 120(14): 2444 - 2453. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Pan, Y. You, T. Huang, and S. L. Brody RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1 J. Cell Sci., June 1, 2007; 120(11): 1868 - 1876. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Dubreuil, A.-M. Marzesco, D. Corbeil, W. B. Huttner, and M. Wilsch-Brauninger Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1 J. Cell Biol., February 12, 2007; 176(4): 483 - 495. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. R. Dawe, H. Farr, and K. Gull Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells J. Cell Sci., January 1, 2007; 120(1): 7 - 15. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. R. Davenport and B. K. Yoder An incredible decade for the primary cilium: a look at a once-forgotten organelle Am J Physiol Renal Physiol, December 1, 2005; 289(6): F1159 - F1169. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Manandhar, H. Schatten, and P. Sutovsky Centrosome Reduction During Gametogenesis and Its Significance Biol Reprod, January 1, 2005; 72(1): 2 - 13. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Jurczyk, A. Gromley, S. Redick, J. S. Agustin, G. Witman, G. J. Pazour, D. J.M. Peters, and S. Doxsey Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly J. Cell Biol., August 30, 2004; 166(5): 637 - 643. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. Brody Genetic Regulation of Cilia Assembly and the Relationship to Human Disease Am. J. Respir. Cell Mol. Biol., April 1, 2004; 30(4): 435 - 437. [Full Text] [PDF]
|
|
|
|
 |
|
 Y. You, T. Huang, E. J. Richer, J.-E. H. Schmidt, J. Zabner, Z. Borok, and S. L. Brody Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells Am J Physiol Lung Cell Mol Physiol, April 1, 2004; 286(4): L650 - L657. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. N. Gomperts, X. Gong-Cooper, and B. P. Hackett Foxj1 regulates basal body anchoring to the cytoskeleton of ciliated pulmonary epithelial cells J. Cell Sci., March 15, 2004; 117(8): 1329 - 1337. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Kubo and S. Tsukita Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly J. Cell Sci., March 1, 2003; 116(5): 919 - 928. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. C. Look, M. J. Walter, M. R. Williamson, L. Pang, Y. You, J. N. Sreshta, J. E. Johnson, D. S. Zander, and S. L. Brody Effects of Paramyxoviral Infection on Airway Epithelial Cell Foxj1 Expression, Ciliogenesis, and Mucociliary Function Am. J. Pathol., December 1, 2001; 159(6): 2055 - 2069. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. H. Hinchcliffe and G. Sluder "It Takes Two to Tango": understanding how centrosome duplication is regulated throughout the cell cycle Genes & Dev., May 15, 2001; 15(10): 1167 - 1181. [Full Text]
|
|
|
|
 |
|
 E. T. O’Brien, X.-o. Ren, and Y. Wang Localization of Myocilin to the Golgi Apparatus in Schlemm's Canal Cells Invest. Ophthalmol. Vis. Sci., November 1, 2000; 41(12): 3842 - 3849. [Abstract] [Full Text]
|
|
|
|
|
|
S. L. Brody, X. H. Yan, M. K. Wuerffel, S.-K. Song, and S. D. Shapiro Ciliogenesis and Left-Right Axis Defects in Forkhead Factor HFH-4-Null Mice Am. J. Respir. Cell Mol. Biol., July 1, 2000; 23(1): 45 - 51. [Abstract] [Full Text]
|
|
|
|
|
|
J Laoukili, E Perret, S Middendorp, O Houcine, C Guennou, F Marano, M Bornens, and F Tournier Differential expression and cellular distribution of centrin isoforms during human ciliated cell differentiation in vitro J. Cell Sci., January 4, 2000; 113(8): 1355 - 1364. [Abstract] [PDF]
|
|
|
|
|
|
W. L. Lingle and J. L. Salisbury Altered Centrosome Structure Is Associated with Abnormal Mitoses in Human Breast Tumors Am. J. Pathol., December 1, 1999; 155(6): 1941 - 1951. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Kubo, H. Sasaki, A. Yuba-Kubo, S. Tsukita, and N. Shiina Centriolar Satellites: Molecular Characterization, Atp-Dependent Movement toward Centrioles and Possible Involvement in Ciliogenesis J. Cell Biol., November 29, 1999; 147(5): 969 - 980. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. N. Blatt, X. H. Yan, M. K. Wuerffel, D. L. Hamilos, and S. L. Brody Forkhead Transcription Factor HFH-4 Expression Is Temporally Related to Ciliogenesis Am. J. Respir. Cell Mol. Biol., August 1, 1999; 21(2): 168 - 176. [Abstract] [Full Text]
|
|
|
|
|
|
I. R. Adams and J. V. Kilmartin Localization of Core Spindle Pole Body (SPB) Components during SPB Duplication in Saccharomyces cerevisiae J. Cell Biol., May 17, 1999; 145(4): 809 - 823. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Lechtreck, A Teltenkotter, and A Grunow A 210 kDa protein is located in a membrane-microtubule linker at the distal end of mature and nascent basal bodies J. Cell Sci., January 6, 1999; 112(11): 1633 - 1644. [Abstract] [PDF]
|
|
|
|
|
|
Y. Bobinnec, A. Khodjakov, L.M. Mir, C.L. Rieder, B. Edde, and M. Bornens Centriole Disassembly In Vivo and Its Effect on Centrosome Structure and Function in Vertebrate Cells J. Cell Biol., December 14, 1998; 143(6): 1575 - 1589. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. Morris and J. M. Scholey Heterotrimeric Kinesin-II Is Required for the Assembly of Motile 9+2 Ciliary Axonemes on Sea Urchin Embryos J. Cell Biol., September 8, 1997; 138(5): 1009 - 1022. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. K. JEFFERY The Development of Large and Small Airways Am. J. Respir. Crit. Care Med., May 1, 1997; 157(5): 174 - 180. [Full Text]
|
|
