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J Electron Microsc (Tokyo) 2011 Imoto S117 36

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  ........................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................ 60th Anniversary Issue: Biological The cell cycle, including the mitotic cycle and organelledivision cycles, as revealed by cytological observations YuutaImoto, YamatoYoshida, FumiYagisawa, HarukoKuroiwaand TsuneyoshiKuroiwa * Research Information Center for Extremophiles, Graduate School of Sciences, Rikkyo University,3-34-1 Nishiikebukuro, Toshimaku, Tokyo 171-0825, Japan * To whom correspondence should be addressed. E-mail: tsune@rikkyo.ne.jp, 09ld004f@rikkyo.ac.jp  Abstract  It is generally believed that the cell cycle consists essentially of themitotic cycle, which involves mitosis and cytokinesis. These processesare becoming increasingly well understood at the molecular level.However, successful cell reproduction requires duplication and segre-gation (inheritance) of all of the cellular contents, including not only thecell-nuclear genome but also intracellular organelles. Eukaryotic cellscontain at least three types of double membrane-bounded organelles (cellnucleus, mitochondria and plastids), four types of single membrane-bounded organelles (endoplasmic reticulum, Golgi apparatus, lysosomesand microbodies) and the cytoskeleton, which comprises tubulin-basedstructures (including microtubules, centrosome and spindle) and actinmicro 󿬁 laments. These membrane-bounded organelles cannot be formed de novo  and daughter organelles must be inherited from parent organellesduring cell cycle. Regulation of organelle division and its coordinationwith the progression of the cell cycle involves a sequence of events thatare subjected to precise spatio-temporal control. Considering that thecells of higher animals and plants contain many organelles which tend tobehave somewhat randomly, there is little information concerning the div-ision and inheritance of these double- and single-membrane-boundedorganelles during the cell cycle. Here, we summarize the current cytologi-cal and morphological knowledge of the cell cycle, including the divisioncycles of seven membrane-bounded and some non-membrane-boundedorganelles. The underlying mechanisms and the biological relevance of these processes are discussed, particularly with respect to cells of the primitive alga   Cyanidioschyzon merolae  that have a minimum of orga-nelles. We discuss unsolved problems and future perspectives opened byrecent studies. Keywords  cell cycle, organelle-division cycle, mitochondrial-division cycle,chloroplast-division cycle, microbody-division cycle, Golgi apparatus-div-ision cycle Received  17 January 2011, accepted 19 April 2011 Introduction Cells reproduce by duplication of their contentsand subsequent division. This cycle of duplicationand division is called the cell cycle, and the eventsof the cell cycle are generally understood to corre-spond to the mitotic cycle. Using autoradiography,Howard and Pelc [1]discovered that nuclear DNA issynthesized during a stage of interphase designated ........................................................................................................................................................................................................................................................  Journal of Electron Microscopy  60(Supplement 1) : S117 – S136 (2011)doi: 10.1093/jmicro/dfr034 ........................................................................................................................................................................................................................................................ © The Author 2011. Published by Oxford University Press [on behalf of Japanese Society of Microscopy]. All rights reserved.For permissions, please e-mail: journals.permissions@oup.com   b  y g u e  s  t   on O c  t   o b  e r 1  7  ,2  0 1 4 h  t   t   p :  /   /   j  mi   c r  o . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om   as S-phase. The S phase is followed by a gap (G2 phase), nuclear and cell division (M phase) and a second gap (G1 phase) before the next S phase.The functions of these phases have been identi 󿬁 edin many cells, including human and yeast cells [2,3]. It is generally believed that the structural and func-tional aspects of the cell cycle are primarily associ-ated with the cell nucleus. However, the cell alsocontains organelles enclosed by double membranes(mitochondria and plastids) and by a single mem-brane (endoplasmic reticulum (ER), dictyosomes of the Golgi apparatus and lysosomes or vacuoles).Clearly, successful cell reproduction requires faith-ful duplication and segregation of all of the cellular contents, which includes the intracellular organellesas well as the nuclear genome. Mitochondria and plastids are regarded as descendants of endosym-biotic prokaryotes. They have their own DNA and proliferate by division. Regulation of organelle div-ision and its coordination with the progression of the cell cycle involves a sequence of events that aresubjected to a precise spatio-temporal control. Tounderstand the cell cycle, we need to recognizecoordination between the mitotic cycle and orga-nelle division cycles. Therefore, it is important tosurvey the division cycle of double- andsingle-membrane-bounded organelles and thedynamics of cytoskeleton during the cell cycle.We have proposed the concept of the  ‘ mitochon-drial division (MD) cycle ’  analogous to the mitoticcycle [4 – 6]. In the plasmodium of the slime mold  Physarum polycephalum,  mitosis and the mitoticcycle are naturally synchronized and, in addition,the mitochondria contain large rod-shaped com- plexes of DNA and proteins, termed nucleoids. Themitotic and MD cycles were precisely examinedusing  3 H-thymidine autoradiography and it wasshown that mitochondrial phases of the divisioncycle, i.e. mt-S, mt-G2, mt-M and mt-G1 lasted 7.7,2, 1.5 and 3 h, respectively, while the mitotic S, G2and M phases lasted 6, 7 and 1 h, respectively. G1lasted for a very short time. Although the timing of the phases of the mitotic and MD cycles differedmarkedly, the total generation time of the mitoticcycle (14 h) was the same as that of mitochondria (Fig. 1).The plastid division (PD) cycle was examined intobacco Bright Yellow 2 (BY-2) cells usingcytological techniques. The plastid DNA synthesis phase (pt-S) during the cell cycle of cultured BY-2cells was examined by  3 H-thymidine autoradiog-raphy following medium renewal. The timing of the pt-S phase differed from that of the mitotic S phase.These observations suggest that the PD cycle pro-ceeded independently from the mitotic cycle [7].Plastid and mitochondrial DNA syntheses were alsoobserved in root meristem and cultured BY-2 cellsby immuno 󿬂 uorescence microscopy of Technovitsections using an antibody against 5-bromodeoxyuridine (BrdU) and co- 󿬂 uorescent staining withDAPI and quantitative Southern hybridization [8]. Itwas shown that large quantities of both mitochon-drial and plastid DNA were preferentially syn-thesized prior to S-phase. However, in plants,animals and fungi, it has been dif  󿬁 cult to determinethe timing of each phase of the division cycle of double-membrane-bounded organelles. However,the difference in the timing of the organelle S-phaseand mitotic S-phase has been established.Partitioning or division (inheritance) of single-mem-brane-bounded organelles occurs in manyorganisms. Additionally, the dynamics of cyto-skeletal proteins and of centrosomes, which playmajor roles in the cell transport system and in celldivision during the mitotic cycle, must be examinedduring the cell cycle [2,3].During G1 phase, the two Fig. 1  Diagram of the mitotic cycle of   P. polycephalum . The cycle proceeds clockwise. The outer circle represents mitochondrial eventsand the inner circle depicts cell nuclear events. The duration of each phase is shownin hours. This  󿬁 gurewas adapted fromRef. [5]. S118  JOURNAL OF ELECTRON MICROSCOPY, Vol. 60, Supplement 1, 2011   b  y g u e  s  t   on O c  t   o b  e r 1  7  ,2  0 1 4 h  t   t   p :  /   /   j  mi   c r  o . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om   orthogonal centrosomes separate. In general, inthese multi-organelle organisms, it has been dif  󿬁 cultto demonstrate each division or partitioning of double-and single-membrane-bounded organellesbecause the cells contain large numbers of theseorganelles and divisions or partitioning occur moreor less randomly (mitochondrial and plastid fusionmay also occur).The unicellular red alga   Cyanidioschyzon merolae  is a very small organism (1.5 – 2.0  μ m diam-eter), whose cells offer unique advantages for studies of double- and single-membrane-boundedorganelle division cycles. They contain a minimalset of organelles; i.e. a cell nucleus, a mitochon-drion, a chloroplast, a microbody, an outer nuclear membrane/ER, a single Golgi apparatus and a fewlysosomes [9 – 11]. Its organelle divisions can behighly synchronized with the light/dark cycle. Thegenome of   C. merolae  has been completelysequenced and it is one of the smallest genomes(16.5 Mb), with the lowest number of genes amongfree-living eukaryotes [9,12]. Because most of the genes are present in low copy numbers and lackintrons, they are suitable for identifying functioninggenes by proteome and transcriptome analysis.Moreover, microarray analysis of its geneexpression pro 󿬁 le during organelle division andinheritance was recently reported [13].Besides studies of the mitotic cycle, MD and PDcycles have been examined by genome analysis[9,12], matrix assisted laser desorption ionization time of   󿬂 ight mass spectrometry (MALDI-TOF-MS)[14 – 17]and gene targeting [15 – 19].The myosin genewas absent from the genome [9,12] and actin genes were not expressed. Therefore, micro 󿬁 laments andintermediate  󿬁 laments could not be identi 󿬁 edthroughout cell cycle by transcriptome and pro-teome analyses [9,13]. In addition, during G1 phase, cytoskeletal microtubules are absent [20].Miyagishima   et al.  [21] presented time-lapse videoimages of   C. merolae  during the M phase under  phase contrast light microscopy. The images weretaken at 20 min intervals for the  󿬁 rst 220 min after the onset of the chloroplast division, and at 10 minintervals, starting 340 min after the onset of thechloroplast division [21]. The temporal sequence of electron microscopic images of the division processof double- and single-membrane-boundedorganelles, and of non-membrane-bounded orga-nelles, during cell cycle could be inferred from theimages of the chloroplasts in living cells.Here, we review the current cytological and mor- phological knowledge concerning the cell cycle,including the division cycles of sevenmembrane-bounded-organelles (cell nucleus,mitochondria, chloroplasts, microbodies, lysosomes,the Golgi apparatus and ER) and non-memb-rane-bounded organelles (centrosomes and spindle). Wediscuss the underlying mechanisms and the biologi-cal relevance of this process, particularly in  C. merolae  cells in comparison with other organisms(Fig. 2). Furthermore, we discuss unsolved funda-mental problems of the cell cycle related to themitotic and organelle division cycles and future per-spectives opened up by recent studies. Division cycle and inheritance of double-membrane-bounded organelles(cell nuclei, mitochondria and plastids) Mitotic cycle The typical eukaryotic cell cycle is divided into G1,S, G2 and M phases [2,3]. The generation times and the durations of each phase have been determinedin many organisms, for example, the generationtime of the plant  Crepis capillaries  is 10.4 h, com- prising the DNA synthesis phase (S phase 5.1 h),the gap between S phase and M phase (G2 phase2.2 h), mitosis (M phase 1.5 h) and the gap betweenM and S phases (G1 phase 1.6 h) [22,23]. The con- densed mitotic chromosomes are readily visible inalmost all cells of Bikonta, Opisthokonta and Amoebozoa [2,3]. In the case of budding yeasts, the 16 condensed meiotic chromosomes are readily visible [24], but are less easily seen in mitosis [2,3]. The cytological mechanisms for condensation of chromosomes from interphase to mitosis have beenexamined in detail in plants using high-resolutionelectron microautoradiography [24 – 27] and the mol-ecular mechanism of chromosome condensation inanimals have been summarized by Hirano [28]. Thecell divides by forming a partition and splitting intwo. Cytokinesis occurs by actin contractile rings[2,3]. In contrast to the situation in higher eukary- otic cells, the nuclear envelop of the yeast cell doesnot break down during M phase. The microtubules Y. Imoto  et al. Cell cycle and organelle division cycles  S119   b  y g u e  s  t   on O c  t   o b  e r 1  7  ,2  0 1 4 h  t   t   p :  /   /   j  mi   c r  o . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om   Fig. 2  Summary of the division cycles and the temporal relationships of the three double-membrane-bounded organelles (cell nucleus,mitochondrion and chloroplast (plastid)) and the four single-membrane-bounded organelles (ER, Golgi apparatus, lysosome and microbody)and centrosome in  Cyanidioschyzon merolae  cells. Each  C. merolae  cell has a minimum set of organelles comprising one cell nucleus, onemitochondrion and one chloroplast, simple ER, one Golgi apparatus, one microbody and a few lysosomes. The organelle divisions can behighly synchronized by the light/dark cycle. Chloroplast, mitochondrion and cell nucleus divisions occur in that order. Mitotic chromosomesare not organized at M phase. Chloroplast and mitochondrion divide using the chloroplast (PD ring) and MD machineries (MD ring),respectively. Microbody and lysosome are inherited using the mitochondrion as a carrier. Tubulins are absent in G1 phase, synthesized as a monomer in S and organized into mitochondrial spindle and mitotic spindles in M phase. Mitotic cycle: G1, S, G2, M; MD cycle:mitochondrial G1 phase (mt-G1), mitochondrial S phase (mt-S), mitochondrial mitotic phase (mt-M); and plastid cell cycle: plastidG1 phase(pt-G1), plastid S phase (pt-S), plastid division phase (pt-M), the division cycles of the ER, Golgi apparatus, lysosome, microbody, and thenon-membrane-bounded organelle (centrosome). Double arrowheads indicate the time point of the organelle replication and singlearrowheads indicate the time point of the organelle division. Time shows hours after the second cell cycle. S120  JOURNAL OF ELECTRON MICROSCOPY, Vol. 60, Supplement 1, 2011   b  y g u e  s  t   on O c  t   o b  e r 1  7  ,2  0 1 4 h  t   t   p :  /   /   j  mi   c r  o . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om 
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