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Mitotic cell rounding

April 11, 2024

Mitotic cell rounding is a shape change that occurs in most animal cells that undergo mitosis. Cells abandon the spread or elongated shape characteristic of interphase and contract into a spherical morphology during mitosis. The phenomenon is seen both in artificial cultures in vitro and naturally forming tissue in vivo.

Cell shape changes as a function of mitotic phase. Shown is an example of a HeLa cell cultured on a glass surface. For visualization of DNA and mitotic phase assignment, the cell expresses Histone H2B-GFP to provide fluorescent labeling of chromosomes. Transmitted light (DIC), fluorescence (GFP), and merged images are shown every 4 minutes as the cell transitions from G2 phase through mitosis to telophase/G1 phase.

Early observations edit

In 1935, one of the first published accounts of mitotic rounding in live tissue described cell rounding in the pseudostratified epithelium of the mammalian neural tube.[1] Sauer noticed that cells in mitosis rounded up to the apical, or luminal, surface of the columnar epithelium before dividing and returning to their elongated morphology.

Significance edit

For a long time it was not clear why cells became round in mitosis. Recent studies in the epithelia and epidermis of various organisms, however, show that mitotic cell rounding might serve several important functions.[2]

  • Firstly, mitotic cell rounding in combination with maintenance of apical cell-cell junctions appears to be necessary for correct mitotic spindle alignment, so that daughter cells divide parallel to the tissue plane, thus sharing apical surface to maintain tissue homeostasis.[3][4][5] Failure to achieve this may result in mislocalization of one daughter cell to the basal region on the tissue layer and clearance via apoptotic cell death.[5]
  • Secondly, mitotic rounding has been proposed to be a driver for morphological events during tissue development. Examples include epithelial invagination of the Drosophila melanogaster tracheal placode[6] and the anisotropic shape and growth of the inner ear lumen in Zebrafish.[7]
  • Thirdly, mitotic rounding has been shown to be important to generate sufficient space and appropriate geometry for proper mitotic spindle function, which is necessary for timely and accurate progression through mitosis.[2][8][9]

Thus, mitotic cell rounding is involved in tissue organization and homeostasis.

Mechanisms edit

To understand the physical mechanisms of how cells round up in mitosis, researchers have conducted mechanical measurements with cultured cells in vitro. The forces that drive cell rounding have recently been characterized by researchers from the groups of Professors Tony Hyman and Daniel Muller, who used flat atomic force microscopy cantilevers to constrain mitotic cells and measure the response force.[10][11] More than 90% of the forces are generated by the collective activity of myosin II molecular motors in the actin cortex.[10][11] As a result, the surface tension and effective stiffness of the actin cortex increase as has been consistently observed in mitotic cells.[12][13][14] This in turn yields an increase in intracellular hydrostatic pressure due to the Law of Laplace, which relates surface tension of a fluid interface to the differential pressure sustained across that interface.[15] The increase in hydrostatic pressure is important because it produces the outward force necessary to push and rounds up against external objects or impediments, such as flexible cantilever,[10][11] soft gel[8] or micropillar[16] (in vitro examples), or surrounding extracellular matrix and neighboring cells[7] (in vivo examples). In HeLa cells in vitro, the force generated by a half-deformed mitotic cell is on the order of 50 to 100 nanonewtons.[10][11] Internal hydrostatic pressure has been measured to increase from below 100 pascals in interphase to 3 to 10 fold that in mitosis.[10][11][15]

In similar in vitro experiments, it was found that the threshold forces required to prevent mitosis are in excess of 100 nN.[9] At threshold forces the cell suffers a loss of cortical F-actin uniformity, which further amplifies the susceptibility to applied force. These effects potentiate distortion of cell dimensions and subsequent perturbation of mitotic progression via spindle defects.[8][9]

Release of stable focal adhesions is another important aspect of mitotic rounding. Cells that are genetically perturbed to manifest constitutively active adhesion regulators are unable to properly remodel their focal adhesions and facilitate the generation of a uniform actomyosin cortex.[8][17] Overall, the biochemical events governing the morphological and mechanical changes in mitotic cells are orchestrated by the mitotic master regulator Cdk1.[11][18]

Apart from actomyosin-related genes, several disease genes have recently been implicated in mitotic cell rounding. These include Parkinson’s disease associated DJ-1/Park7 and FAM134A/RETREG2.[19]


References edit

  1. ^ Sauer, F.C. (October 1935). "Mitosis in the neural tube". Journal of Comparative Neurology. 62 (2): 377–405. doi:10.1002/cne.900620207. S2CID 84960254.
  2. ^ a b Cadart, Clotilde; Zlotek-Zlotkiewicz, Ewa; Le Berre, Mael; Piel, Matthieu; Matthews, Helen K (28 April 2014). "Exploring the function of cell shape and size during mitosis". Developmental Cell. 29 (2): 159–169. doi:10.1016/j.devcel.2014.04.009. PMID 24780736.
  3. ^ Meyer, Emily J; Ikmi, Aissam; Gibson, Matthew C (22 March 2011). "Interkinetic nuclear migration is a broadly conserved feature of cell division in pseudostratified epithelia". Current Biology. 21 (6): 485–491. doi:10.1016/j.cub.2011.02.002. PMID 21376598.
  4. ^ Luxenburg, Chen; Pasolli, H Amalia; Williams, Scott E; Fuchs, E (20 February 2011). "Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation". Nature Cell Biology. 13 (3): 203–214. doi:10.1038/ncb2163. PMC 3278337. PMID 21336301.
  5. ^ a b Nakajima, Yu-ichiro; Meyer, Emily J; Kroesen, Amanda; McKinney, Sean A; Gibson, Matthew C (21 July 2013). "Epithelial junctions maintain tissue architecture by directing planar spindle orientation". Nature. 500 (7462): 359–362. Bibcode:2013Natur.500..359N. doi:10.1038/nature12335. PMID 23873041. S2CID 4418619.
  6. ^ Kondo, Takefumi; Hayashi, Shigeo (13 January 2013). "Mitotic cell rounding accelerates epithelial invagination". Nature. 494 (7435): 125–129. Bibcode:2013Natur.494..125K. doi:10.1038/nature11792. PMID 23334416. S2CID 205232184.
  7. ^ a b Hoijman, Esteban; Rubbini, Davide; Colombelli, Julien; Alsina, Berta (16 June 2015). "Mitotic cell rounding and epithelial thinning regulate lumen growth and shape". Nature Communications. 6: 7355. Bibcode:2015NatCo...6.7355H. doi:10.1038/ncomms8355. hdl:10230/25942. PMID 26077034.
  8. ^ a b c d Lancaster, Oscar M; La Berre, Mael; Dimitracopoulos, Andrea; Bonazzi, Daria; Zlotek-Zlotkiewicz, Ewa; Picone, Remigio; Duke, Thomas; Piel, Matthieu; Baum, Buzz (13 May 2013). "Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation" (PDF). Developmental Cell. 25 (3): 270–283. doi:10.1016/j.devcel.2013.03.014. PMID 23623611.
  9. ^ a b c Cattin, Cedric J; Düggelin, Marcel; Martinez-Martin, David; Gerber, Christoph; Mueller, Daniel J; Stewart, Martin P (2015). "Mechanical control of mitotic progression in single animal cells". Proceedings of the National Academy of Sciences. 112 (36): 11258–11263. Bibcode:2015PNAS..11211258C. doi:10.1073/pnas.1502029112. PMC 4568679. PMID 26305930.
  10. ^ a b c d e Stewart, Martin P; Helenius, Jonne; Toyoda, Yusuke; Ramanathan, Subramanian P; Muller, Daniel J; Hyman, Anthony A (2 January 2011). "Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding". Nature. 469 (7329): 226–230. Bibcode:2011Natur.469..226S. doi:10.1038/nature09642. PMID 21196934. S2CID 4425308.
  11. ^ a b c d e f Ramanathan, Subramanian P; Helenius, Jonne; Stewart, Martin P; Cattin, Cedric J; Hyman, Anthony A; Muller, Daniel J (26 January 2015). "Cdk1-dependent mitotic enrichment of cortical myosin II promotes cell rounding against confinement". Nature Cell Biology. 17 (2): 148–159. doi:10.1038/ncb3098. PMID 25621953. S2CID 5208968.
  12. ^ Maddox, Amy S; Burridge, Keith (20 January 2003). "RhoA is required for cortical retraction and rigidity during mitotic cell rounding". Journal of Cell Biology. 160 (2): 255–265. doi:10.1083/jcb.200207130. PMC 2172639. PMID 12538643.
  13. ^ Kunda, Patricia; Pelling, Andrew E; Liu, Tao; Baum, Buzz (22 January 2008). "Moesin Controls Cortical Rigidity, Cell Rounding, and Spindle Morphogenesis during Mitosis". Current Biology. 18 (2): 91–101. doi:10.1016/j.cub.2007.12.051. PMID 18207738.
  14. ^ Matthews, Helen K; Delabre, Ulysse; Rohn, Jennifer L; Guck, Jochen; Kunda, Patricia; Baum, Buzz (14 August 2012). "Changes in Ect2 localization couple actomyosin-dependent cell shape changes to mitotic progression". Developmental Cell. 23 (2): 371–383. doi:10.1016/j.devcel.2012.06.003. PMC 3763371. PMID 22898780.
  15. ^ a b Fischer-Friedrich, Elisabeth; Hyman, Anthony A; Jülicher, Frank; Müller, Daniel J; Helenius, Jonne (29 August 2014). "Quantification of surface tension and internal pressure generated by single mitotic cells". Scientific Reports. 4: 6213. Bibcode:2014NatSR...4E6213F. doi:10.1038/srep06213. PMC 4148660. PMID 25169063.
  16. ^ Sorce, B (2015). "Mitotic cells contract actomyosin cortex and generate pressure to round against or escape epithelial confinement". Nature Communications. 6: 8872. Bibcode:2015NatCo...6.8872S. doi:10.1038/ncomms9872. hdl:1721.1/100828. PMID 26602832. S2CID 3175608.
  17. ^ Dao, Vi Thuy; Dupuy, Aurélien Guy; Gavet, Olivier; Caron, Emmanuelle; de Gunzburg, Jean (15 August 2009). "Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis". Journal of Cell Science. 122 (16): 2996–3004. doi:10.1242/jcs.041301. PMID 19638416.
  18. ^ Clark, Andrew G; Paluch, Ewa (21 April 2011). "Mechanics and Regulation of Cell Shape During the Cell Cycle". Cell Cycle in Development. Results and Problems in Cell Differentiation. 53: 31–77. doi:10.1007/978-3-642-19065-0_3. ISBN 978-3-642-19064-3. PMID 21630140.
  19. ^ Toyoda*, Yusuke; Cattin*, Cedric J.; Stewart*, Martin P.; Poser, Ina; Theis, Mirko; Kurzchalia, Teymuras V.; Buchholz, Frank; Hyman, Anthony A.; Müller, Daniel J. (2 November 2017). "Genome-scale single-cell mechanical phenotyping reveals disease-related genes involved in mitotic rounding". Nature Communications. 8 (1): 1266. Bibcode:2017NatCo...8.1266T. doi:10.1038/s41467-017-01147-6. PMC 5668354. PMID 29097687.

External links edit

  • . qucosa.de. Archived from the original on 2015-09-24. Retrieved 2015-07-04.
  • "ETH ETH E-Collection: The Mechanism of Mitotic Rounding: Role of the Actomyosin Cortex — ETH". e-collection.library.ethz.ch. Retrieved 2015-07-04.
  • "Two Minute Talk: Mitotic Cell Rounding — YouTube". youtube.com. Retrieved 2015-07-04.

April 11, 2024
mitotic, cell, rounding, shape, change, that, occurs, most, animal, cells, that, undergo, mitosis, cells, abandon, spread, elongated, shape, characteristic, interphase, contract, into, spherical, morphology, during, mitosis, phenomenon, seen, both, artificial,. Mitotic cell rounding is a shape change that occurs in most animal cells that undergo mitosis Cells abandon the spread or elongated shape characteristic of interphase and contract into a spherical morphology during mitosis The phenomenon is seen both in artificial cultures in vitro and naturally forming tissue in vivo Cell shape changes as a function of mitotic phase Shown is an example of a HeLa cell cultured on a glass surface For visualization of DNA and mitotic phase assignment the cell expresses Histone H2B GFP to provide fluorescent labeling of chromosomes Transmitted light DIC fluorescence GFP and merged images are shown every 4 minutes as the cell transitions from G2 phase through mitosis to telophase G1 phase Contents 1 Early observations 2 Significance 3 Mechanisms 4 References 5 External linksEarly observations editIn 1935 one of the first published accounts of mitotic rounding in live tissue described cell rounding in the pseudostratified epithelium of the mammalian neural tube 1 Sauer noticed that cells in mitosis rounded up to the apical or luminal surface of the columnar epithelium before dividing and returning to their elongated morphology Significance editFor a long time it was not clear why cells became round in mitosis Recent studies in the epithelia and epidermis of various organisms however show that mitotic cell rounding might serve several important functions 2 Firstly mitotic cell rounding in combination with maintenance of apical cell cell junctions appears to be necessary for correct mitotic spindle alignment so that daughter cells divide parallel to the tissue plane thus sharing apical surface to maintain tissue homeostasis 3 4 5 Failure to achieve this may result in mislocalization of one daughter cell to the basal region on the tissue layer and clearance via apoptotic cell death 5 Secondly mitotic rounding has been proposed to be a driver for morphological events during tissue development Examples include epithelial invagination of the Drosophila melanogaster tracheal placode 6 and the anisotropic shape and growth of the inner ear lumen in Zebrafish 7 Thirdly mitotic rounding has been shown to be important to generate sufficient space and appropriate geometry for proper mitotic spindle function which is necessary for timely and accurate progression through mitosis 2 8 9 Thus mitotic cell rounding is involved in tissue organization and homeostasis Mechanisms editTo understand the physical mechanisms of how cells round up in mitosis researchers have conducted mechanical measurements with cultured cells in vitro The forces that drive cell rounding have recently been characterized by researchers from the groups of Professors Tony Hyman and Daniel Muller who used flat atomic force microscopy cantilevers to constrain mitotic cells and measure the response force 10 11 More than 90 of the forces are generated by the collective activity of myosin II molecular motors in the actin cortex 10 11 As a result the surface tension and effective stiffness of the actin cortex increase as has been consistently observed in mitotic cells 12 13 14 This in turn yields an increase in intracellular hydrostatic pressure due to the Law of Laplace which relates surface tension of a fluid interface to the differential pressure sustained across that interface 15 The increase in hydrostatic pressure is important because it produces the outward force necessary to push and rounds up against external objects or impediments such as flexible cantilever 10 11 soft gel 8 or micropillar 16 in vitro examples or surrounding extracellular matrix and neighboring cells 7 in vivo examples In HeLa cells in vitro the force generated by a half deformed mitotic cell is on the order of 50 to 100 nanonewtons 10 11 Internal hydrostatic pressure has been measured to increase from below 100 pascals in interphase to 3 to 10 fold that in mitosis 10 11 15 In similar in vitro experiments it was found that the threshold forces required to prevent mitosis are in excess of 100 nN 9 At threshold forces the cell suffers a loss of cortical F actin uniformity which further amplifies the susceptibility to applied force These effects potentiate distortion of cell dimensions and subsequent perturbation of mitotic progression via spindle defects 8 9 Release of stable focal adhesions is another important aspect of mitotic rounding Cells that are genetically perturbed to manifest constitutively active adhesion regulators are unable to properly remodel their focal adhesions and facilitate the generation of a uniform actomyosin cortex 8 17 Overall the biochemical events governing the morphological and mechanical changes in mitotic cells are orchestrated by the mitotic master regulator Cdk1 11 18 Apart from actomyosin related genes several disease genes have recently been implicated in mitotic cell rounding These include Parkinson s disease associated DJ 1 Park7 and FAM134A RETREG2 19 References edit Sauer F C October 1935 Mitosis in the neural tube Journal of Comparative Neurology 62 2 377 405 doi 10 1002 cne 900620207 S2CID 84960254 a b Cadart Clotilde Zlotek Zlotkiewicz Ewa Le Berre Mael Piel Matthieu Matthews Helen K 28 April 2014 Exploring the function of cell shape and size during mitosis Developmental Cell 29 2 159 169 doi 10 1016 j devcel 2014 04 009 PMID 24780736 Meyer Emily J Ikmi Aissam Gibson Matthew C 22 March 2011 Interkinetic nuclear migration is a broadly conserved feature of cell division in pseudostratified epithelia Current Biology 21 6 485 491 doi 10 1016 j cub 2011 02 002 PMID 21376598 Luxenburg Chen Pasolli H Amalia Williams Scott E Fuchs E 20 February 2011 Developmental roles for Srf cortical cytoskeleton and cell shape in epidermal spindle orientation Nature Cell Biology 13 3 203 214 doi 10 1038 ncb2163 PMC 3278337 PMID 21336301 a b Nakajima Yu ichiro Meyer Emily J Kroesen Amanda McKinney Sean A Gibson Matthew C 21 July 2013 Epithelial junctions maintain tissue architecture by directing planar spindle orientation Nature 500 7462 359 362 Bibcode 2013Natur 500 359N doi 10 1038 nature12335 PMID 23873041 S2CID 4418619 Kondo Takefumi Hayashi Shigeo 13 January 2013 Mitotic cell rounding accelerates epithelial invagination Nature 494 7435 125 129 Bibcode 2013Natur 494 125K doi 10 1038 nature11792 PMID 23334416 S2CID 205232184 a b Hoijman Esteban Rubbini Davide Colombelli Julien Alsina Berta 16 June 2015 Mitotic cell rounding and epithelial thinning regulate lumen growth and shape Nature Communications 6 7355 Bibcode 2015NatCo 6 7355H doi 10 1038 ncomms8355 hdl 10230 25942 PMID 26077034 a b c d Lancaster Oscar M La Berre Mael Dimitracopoulos Andrea Bonazzi Daria Zlotek Zlotkiewicz Ewa Picone Remigio Duke Thomas Piel Matthieu Baum Buzz 13 May 2013 Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation PDF Developmental Cell 25 3 270 283 doi 10 1016 j devcel 2013 03 014 PMID 23623611 a b c Cattin Cedric J Duggelin Marcel Martinez Martin David Gerber Christoph Mueller Daniel J Stewart Martin P 2015 Mechanical control of mitotic progression in single animal cells Proceedings of the National Academy of Sciences 112 36 11258 11263 Bibcode 2015PNAS 11211258C doi 10 1073 pnas 1502029112 PMC 4568679 PMID 26305930 a b c d e Stewart Martin P Helenius Jonne Toyoda Yusuke Ramanathan Subramanian P Muller Daniel J Hyman Anthony A 2 January 2011 Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding Nature 469 7329 226 230 Bibcode 2011Natur 469 226S doi 10 1038 nature09642 PMID 21196934 S2CID 4425308 a b c d e f Ramanathan Subramanian P Helenius Jonne Stewart Martin P Cattin Cedric J Hyman Anthony A Muller Daniel J 26 January 2015 Cdk1 dependent mitotic enrichment of cortical myosin II promotes cell rounding against confinement Nature Cell Biology 17 2 148 159 doi 10 1038 ncb3098 PMID 25621953 S2CID 5208968 Maddox Amy S Burridge Keith 20 January 2003 RhoA is required for cortical retraction and rigidity during mitotic cell rounding Journal of Cell Biology 160 2 255 265 doi 10 1083 jcb 200207130 PMC 2172639 PMID 12538643 Kunda Patricia Pelling Andrew E Liu Tao Baum Buzz 22 January 2008 Moesin Controls Cortical Rigidity Cell Rounding and Spindle Morphogenesis during Mitosis Current Biology 18 2 91 101 doi 10 1016 j cub 2007 12 051 PMID 18207738 Matthews Helen K Delabre Ulysse Rohn Jennifer L Guck Jochen Kunda Patricia Baum Buzz 14 August 2012 Changes in Ect2 localization couple actomyosin dependent cell shape changes to mitotic progression Developmental Cell 23 2 371 383 doi 10 1016 j devcel 2012 06 003 PMC 3763371 PMID 22898780 a b Fischer Friedrich Elisabeth Hyman Anthony A Julicher Frank Muller Daniel J Helenius Jonne 29 August 2014 Quantification of surface tension and internal pressure generated by single mitotic cells Scientific Reports 4 6213 Bibcode 2014NatSR 4E6213F doi 10 1038 srep06213 PMC 4148660 PMID 25169063 Sorce B 2015 Mitotic cells contract actomyosin cortex and generate pressure to round against or escape epithelial confinement Nature Communications 6 8872 Bibcode 2015NatCo 6 8872S doi 10 1038 ncomms9872 hdl 1721 1 100828 PMID 26602832 S2CID 3175608 Dao Vi Thuy Dupuy Aurelien Guy Gavet Olivier Caron Emmanuelle de Gunzburg Jean 15 August 2009 Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis Journal of Cell Science 122 16 2996 3004 doi 10 1242 jcs 041301 PMID 19638416 Clark Andrew G Paluch Ewa 21 April 2011 Mechanics and Regulation of Cell Shape During the Cell Cycle Cell Cycle in Development Results and Problems in Cell Differentiation 53 31 77 doi 10 1007 978 3 642 19065 0 3 ISBN 978 3 642 19064 3 PMID 21630140 Toyoda Yusuke Cattin Cedric J Stewart Martin P Poser Ina Theis Mirko Kurzchalia Teymuras V Buchholz Frank Hyman Anthony A Muller Daniel J 2 November 2017 Genome scale single cell mechanical phenotyping reveals disease related genes involved in mitotic rounding Nature Communications 8 1 1266 Bibcode 2017NatCo 8 1266T doi 10 1038 s41467 017 01147 6 PMC 5668354 PMID 29097687 External links edit Qucosa The Mechanics of Mitotic Cell Rounding qucosa de Archived from the original on 2015 09 24 Retrieved 2015 07 04 ETH ETH E Collection The Mechanism of Mitotic Rounding Role of the Actomyosin Cortex ETH e collection library ethz ch Retrieved 2015 07 04 Two Minute Talk Mitotic Cell Rounding YouTube youtube com Retrieved 2015 07 04 Retrieved from https en wikipedia org w index php title Mitotic cell rounding amp oldid 1193778132, wikipedia, wiki, book, books, library,

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