Skip to main content
SpringerLink
Log in

A Brief History of Eukaryotic Cell Cycle Research

  • Chapter
  • First Online:
Concepts in Cell Biology - History and Evolution

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 23))

Abstract

The extent of literature devoted to the eukaryotic cell cycle as well as the complexity of the underlying ideas, hypotheses, and models has become rather intimidating. However, our current understanding of the processes that produce (usually) two cells out of one is rooted in a relatively limited set of underlying concepts. Some of these originated in the second half of the twentieth century, whereas others can be traced back to the early days of cell theory. Rather than striving for exhaustive coverage of all existing relevant literature, a task probably far beyond the scope of any individual, I am attempting to map the origins and historical roots of the concepts and ideas that have formed our understanding of eukaryotic cell cycle regulation. The focus is mainly on the central regulatory circuit comprising cyclin-dependent kinases and cyclins, as well as on some remarkable contributions from plant studies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York

    Google Scholar 

  • Amon A, Tyers M, Futcher B, Nasmyth K (1993) Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74:993–1007

    Article  CAS  PubMed  Google Scholar 

  • Amon A, Irniger S, Nasmyth K (1994) Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 77:1037–1050

    Article  CAS  PubMed  Google Scholar 

  • Araujo AR, Gelens L, Sheriff RSM, Santos SDM (2016) Positive feedback keeps duration of mitosis temporally insulated from upstream cell-cycle events. Mol Cell 64:362–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asghar U, Witkiewicz AK, Turner NC, Knudsen ES (2015) The history and future of targeting cyclin-dependent kinases in cancer therapy. Nat Rev Drug Discov 14:130–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astbury WT (1961) Molecular biology or ultrastructural biology? Nature 190:1124

    Article  CAS  PubMed  Google Scholar 

  • Avery OT, MacLeod CM, McCarty M (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 79:137–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baluška F, Volkmann D, Menzel D, Barlow P (2012) Strasburger’s legacy to mitosis and cytokinesis and its relevance for the cell theory. Protoplasma 249:1151–1162

    Article  PubMed  Google Scholar 

  • Barker DG, White JH, Johnston LH (1987) Molecular characterisation of the DNA ligase gene, CDC17, from the fission yeast Schizosaccharomyces pombe. Eur J Biochem 162:659–667

    Article  CAS  PubMed  Google Scholar 

  • Baserga R (1985) The biology of cell reproduction. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Beach D, Durkacz B, Nurse P (1982) Functionally homologous cell cycle control genes in budding and fission yeast. Nature 300:706–709

    Article  CAS  PubMed  Google Scholar 

  • Benson KR (2001) T. H. Morgan’s resistance to the chromosome theory. Nat Rev Genet 2:469–474

    Article  CAS  PubMed  Google Scholar 

  • Bertoli C, Skotheim JM, de Bruin RA (2013) Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 14:518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bišová K, Zachleder V (2014) Cell-cycle regulation in green algae dividing by multiple fission. J Exp Bot 65:2585–2602

    Article  PubMed  CAS  Google Scholar 

  • Boettcher B, Barral Y (2013) The cell biology of open and closed mitosis. Nucleus 4:160–165

    Article  PubMed  PubMed Central  Google Scholar 

  • Booher R, Beach D (1988) Involvement of cdc13 + in mitotic control in Schizosaccharomyces pombe: possible interaction of the gene product with microtubules. EMBO J 7:2321–2327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boudolf V, Lammens T, Boruc J, Van Leene J, Van Den Daele H, Maes S, Van Isterdael G, Russinova E, Kondorosi E, Witters E, De Jaeger G, Inzé D, De Veylder L (2009) CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol 150:1482–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouldin CM, Kimelman D (2014) Cdc25 and the importance of G2 control: insights from developmental biology. Cell Cycle 13:2165–2171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bravo R, Fey SJ, Bellatin J, Larsen PM, Celis JE (1982) Identification of a nuclear polypeptide (“cyclin”) whose relative proportion is sensitive to changes in the rate of cell proliferation and to transformation. Prog Clin Biol Res 85:235–248

    CAS  PubMed  Google Scholar 

  • Cánepa ET, Scassa ME, Ceruti JM, Marazita MC, Carcagno AL, Sirkin PF, Ogara MF (2007) NK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 59:419–426

    Article  PubMed  CAS  Google Scholar 

  • Carreño JE, Hansen F, Irarrázabal M, Philippi R, Correa M, Borja F, Adriasola C, Silva F, Serani A (2009) Some considerations about the theory of intelligent design. Biol Res 42:223–232

    Article  PubMed  Google Scholar 

  • Chen D, Dundr M, Wang C, Leung A, Lamond A, Misteli T, Huang S (2005) Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J Cell Biol 68:41–54

    Article  CAS  Google Scholar 

  • Clifford DM, Chen CT, Roberts RH, Feoktistova A, Wolfe BA, Chen JS, McCollum D, Gould KL (2008) The role of Cdc14 phosphatases in the control of cell division. Biochem Soc Trans 36:436–438

    Article  CAS  PubMed  Google Scholar 

  • Cromer L, Heyman J, Touati S, Harashima H, Araou E, Girard C, Horlow C, Wassmann K, Schnittger A, De Veylder L, Mercier R (2012) OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet 8(7):e1002865. https://doi.org/10.1371/journal.pgen.1002865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csikász-Nagy A (2009) Computational systems biology of the cell cycle. Brief Bioinform 10:424–434

    Article  PubMed  CAS  Google Scholar 

  • Cvrčková F, Nasmyth K (1993) Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J 12:5277–8526

    PubMed  PubMed Central  Google Scholar 

  • Day IS, Reddy AS (1994) Cloning of a family of cyclins from Arabidopsis thaliana. Biochim Biophys Acta 1218:115–118

    Article  CAS  PubMed  Google Scholar 

  • Ding DQ, Haraguchi T, Hiraoka Y (2016) A cohesin-based structural platform supporting homologous chromosome pairing in meiosis. Curr Genet 62:499–502

    Article  CAS  PubMed  Google Scholar 

  • Duesbery NS, Vande Woude GF (1988) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. Biol Cell 90:461–466

    Google Scholar 

  • Duncan RE, Persidsky MD (1958) The achromatic figure during mitosis in maize endosperm. Am J Bot 45:719–729

    Article  Google Scholar 

  • Duronio RJ, Xiong Y (2013) Signaling pathways that control cell proliferation. Cold Spring Harb Perspect Biol 5(3):a008904. https://doi.org/10.1101/cshperspect.a008904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edgar RS, Lielausis I (1964) Temperature-sensitive mutants of bacteriophage T4D: their isolation and genetic characterization. Genetics 49:649–662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans T, Rosenthal ET, Youngbloom J, Distel D, Hunt T (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33:389–396

    Article  CAS  PubMed  Google Scholar 

  • Fisher RP (2016) Getting to S: CDK functions and targets on the path to cell-cycle commitment. F1000 Res 5:2374. 10.12688/f1000research.9463.1

    Article  Google Scholar 

  • Fowke LC, Bech-Hansen CW, Gamborg OL, Constabel F (1975) Electron-microscope observations of mitosis and cytokinesis in multinucleate protoplasts of soybean. J Cell Sci 18:491–507

    CAS  PubMed  Google Scholar 

  • Fraenkel-Conrat H (1970) Reconstitution of viruses. Annu Rev Microbiol 24:463–478

    Article  CAS  PubMed  Google Scholar 

  • Fraenkel-Conrat H, Williams RC (1955) Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc Natl Acad Sci USA 41:690–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francis D (2011) A commentary on the G2/M transition of the plant cell cycle. Ann Bot 107:1065–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frawley LE, Orr-Weaver TL (2015) Polyploidy. Curr Biol 25:R353–R358

    Article  CAS  PubMed  Google Scholar 

  • Gautier J, Norbury C, Lohka M, Nurse P, Maller J (1988) Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2 +. Cell 54:433–439

    Article  CAS  PubMed  Google Scholar 

  • Gerhart J, Wu M, Kirschner M (1984) Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J Cell Biol 98:1247–1255

    Article  CAS  PubMed  Google Scholar 

  • Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:563–567

    Article  Google Scholar 

  • Goldbeter A (1997) Biochemical oscillations and cellular rhythms: the molecular bases of periodic and chaotic behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Groman NB (1962) Temperature and the reproduction of lambda-phage mutants. J Bacteriol 84:438–845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez C (2016) 25 years of cell cycle research: what’s ahead? Trends Plant Sci 21:823–833

    Article  CAS  PubMed  Google Scholar 

  • Hagan I, Hayles J, Nurse P (1988) Cloning and sequencing of the cyclin-related cdc13 + gene and a cytological study of its role in fission yeast mitosis. J Cell Sci 91:587–595

    CAS  PubMed  Google Scholar 

  • Hall MN, Linder P, Mortimer RK (1993) Carl C. Lindegren: iconoclastic father of Neurospora and yeast genetics. In: Hall MN, Linder P (eds) The early days of yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 17–38

    Google Scholar 

  • Hartwell LH (1991) Twenty-five years of cell cycle genetics. Genetics 129:975–980

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH (2002) Nobel lecture: yeast and cancer. Biosci Rep 22:373–394

    Article  CAS  PubMed  Google Scholar 

  • Hartwell LH, McLaughlin CS (1968) Temperature-sensitive mutants of yeast exhibiting a rapid inhibition of protein synthesis. J Bacteriol 96:1664–1671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, McLaughlin CS (1969) A mutant of yeast apparently defective in the initiation of protein synthesis. Proc Natl Acad Sci USA 62:468–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, Culotti J, Reid B (1970a) Genetic control of the cell-division cycle in yeast. I. Detection of mutants. Proc Natl Acad Sci USA 66:352–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, McLaughlin CS, Warner JR (1970b) Identification of ten genes that control ribosome formation in yeast. Mol Gen Genet 109:42–56

    Article  CAS  PubMed  Google Scholar 

  • Hartwell L, Mortimer RK, Culotti J, Culotti M (1973) Genetic control of the cell division cycle in yeast: V. Genetic analysis of cdc mutants. Genetics 74:267–286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, Culotti J, Pringle JR, Reid BJ (1974) Genetic control of the cell division cycle in yeast. Science 183:46–51

    Article  CAS  PubMed  Google Scholar 

  • Helmstetter CE (2015) A ten-year search for synchronous cells: obstacles, solutions, and practical applications. Front Microbiol 6:238. https://doi.org/10.3389/fmicb.2015.00238

    Article  PubMed  PubMed Central  Google Scholar 

  • Henderson L, Bortone DS, Lim C, Zambon AC (2013) Classic “broken cell” techniques and newer live cell methods for cell cycle assessment. Am J Physiol Cell Physiol 304:C927–C938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hindley J, Phear GA (1984) Sequence of the cell division gene CDC2 from Schizosaccharomyces pombe; patterns of splicing and homology to protein kinases. Gene 31:129–134

    Article  CAS  PubMed  Google Scholar 

  • Hooke R (1665) Micrographia: some physiological descriptions of minute bodies made by magnifying glasses with observations and inquiries thereupon. Martyn and Allestry, London

    Book  Google Scholar 

  • Howard A, Pelc SR (1951) Synthesis of nucleoprotein in bean root cells. Nature 167:599–600

    Article  CAS  PubMed  Google Scholar 

  • Hunt T (2002) Nobel Lecture: protein synthesis, proteolysis, and cell cycle transitions. Biosci Rep 22:465–486

    Article  CAS  PubMed  Google Scholar 

  • Hunt T (2015) Pursuing the impossible: an interview with Tim Hunt. BMC Biol 13:64. https://doi.org/10.1186/s12915-015-0164-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunt T, Nasmyth K, Novák B (2011) The cell cycle. Philos Trans R Soc B 366:3494–3497

    Article  Google Scholar 

  • Hurst LD, Nurse P (1991) A note on the evolution of meiosis. J Theor Biol 150:561–563

    Article  CAS  PubMed  Google Scholar 

  • Ingolia NT, Murray AW (2004) The ups and downs of modeling the cell cycle. Curr Biol 14:R771–R777

    Article  CAS  PubMed  Google Scholar 

  • Johnson RT, Rao PN (1971) Nucleo-cytoplasmic interactions in the acheivement of nuclear synchrony in DNA synthesis and mitosis in multinucleate cells. Biol Rev Camb Philos Soc 46:97–155

    Article  CAS  PubMed  Google Scholar 

  • Johnston LH, Nasmyth KA (1978) Saccharomyces cerevisiae cell cycle mutant cdc9 is defective in DNA ligase. Nature 274:891–893

    Article  CAS  PubMed  Google Scholar 

  • Kerk D, Templeton G, Moorhead GB (2008) Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol 146:351–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch C, Nasmyth K (1994) Cell cycle regulated transcription in yeast. Curr Opin Cell Biol 6:451–459

    Article  CAS  PubMed  Google Scholar 

  • Koff A, Polyak K (1995) p27KIP1, an inhibitor of cyclin-dependent kinases. Prog Cell Cycle Res 1:141–147

    Article  CAS  PubMed  Google Scholar 

  • Komaki S, Schnittger A (2016) The spindle checkpoint in plants – a green variation over a conserved theme? Curr Opin Plant Biol 34:84–91

    Article  CAS  PubMed  Google Scholar 

  • Kuilman T, Maiolica A, Godfrey M, Scheidel N, Aebersold R, Uhlmann F (2015) Identification of Cdk targets that control cytokinesis. EMBO J 34:81–96

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Pushpa K, Mylavarapu SV (2015) Splitting the cell, building the organism: mechanisms of cell division in metazoan embryos. IUBMB Life 67:575–587

    Article  PubMed  CAS  Google Scholar 

  • Kushner DJ (1969) Self-assembly of biological structures. Bacteriol Rev 33:302–345

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MG, Nurse P (1987) Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature 327:31–35

    Article  CAS  PubMed  Google Scholar 

  • Lew DJ, Reed SI (1995) A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol 129:739–749

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Chang EC (2003) Schizosaccharomyces pombe Ras1 effector, Scd1, interacts with Klp5 and Klp6 kinesins to mediate cytokinesis. Genetics 165:477–488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lieberman HB, Yin Y (2004) A novel function for human Rad9 protein as a transcriptional activator of gene expression. Cell Cycle 3:1008–1010

    Article  CAS  PubMed  Google Scholar 

  • Lohka MJ, Hayes MK, Maller JL (1988) Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc Natl Acad Sci USA 85:3009–3013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorca T, Labbé JC, Devault A, Fesquet D, Capony JP, Cavadore JC, Le Bouffant F, Dorée M (1992) Dephosphorylation of cdc2 on threonine 161 is required for cdc2 kinase inactivation and normal anaphase. EMBO J 11:2381–2390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lörincz AT, Reed SI (1984) Primary structure homology between the product of yeast cell division control gene CDC28 and vertebrate oncogenes. Nature 307:183–185

    Article  PubMed  Google Scholar 

  • Loudon AS, Semikhodskii AG, Crosthwaite SK (2000) A brief history of circadian time. Trends Genet 16:477–481

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Wu Y, Jin J, Yan J, Kuang S, Zhou M, Zhang Y, Guo AY (2013) Phylogenetic analysis reveals the evolution and diversification of cyclins in eukaryotes. Mol Phylogenet Evol 66:1002–1010

    Article  CAS  PubMed  Google Scholar 

  • Magyar Z, Bögre L, Ito M (2016) DREAMs make plant cells to cycle or to become quiescent. Curr Opin Plant Biol 34:100–106

    Article  CAS  PubMed  Google Scholar 

  • Malumbres M (2014) Cyclin-dependent kinases. Genome Biol 15(6):122. https://doi.org/10.1186/gb4184

    Article  PubMed  PubMed Central  Google Scholar 

  • Markov AV, Kaznacheev IS (2016) Evolutionary consequences of polyploidy in prokaryotes and the origin of mitosis and meiosis. Biol Direct 11:28. https://doi.org/10.1186/s13062-016-0131-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masui Y (2001) From oocyte maturation to the in vitro cell cycle: the history of discoveries of Maturation-Promoting Factor (MPF) and Cytostatic Factor (CSF). Differentiation 69:1–17

    Article  CAS  PubMed  Google Scholar 

  • Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129–145

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto K, Moriuchi T, Koji T, Nakane PK (1987) Molecular cloning of cDNA coding for rat proliferating cell nuclear antigen (PCNA)/cyclin. EMBO J 6:637–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mazzarello P (1999) A unifying concept: the history of cell theory. Nat Cell Biol 1:E13–E15

    Article  CAS  PubMed  Google Scholar 

  • Minshull J, Pines J, Golsteyn R, Standart N, Mackie S, Colman A, Blow J, Ruderman JV, Wu M, Hunt T (1989) The role of cyclin synthesis, modification and destruction in the control of cell division. J Cell Sci Suppl 12:77–97

    Article  CAS  PubMed  Google Scholar 

  • Mitchison JM (1971) The biology of the cell cycle. Cambridge University Press, London

    Google Scholar 

  • Mitchison JM (1974) Sequences, pathways and timers in the cell cycle. In: Padilla GM, Cameron IL, Zimmerman A (eds) Cell cycle control. Academic, New York, pp 125–142

    Google Scholar 

  • Mitchison JM (2003) Growth during the cell cycle. Int Rev Cytol 226:165–258

    Article  CAS  PubMed  Google Scholar 

  • Murray AW, Kirschner MW (1989a) Cyclin synthesis drives the early embryonic cell cycle. Nature 339:275–280

    Article  CAS  PubMed  Google Scholar 

  • Murray AW, Kirschner MW (1989b) Dominoes and clocks: the union of two views of the cell cycle. Science 246:614–621

    Article  CAS  PubMed  Google Scholar 

  • Musacchio A (2015) The molecular biology of spindle assembly checkpoint signaling dynamics. Curr Biol 25:R1002–R1018

    Article  CAS  PubMed  Google Scholar 

  • Musiałek MW, Rybaczek D (2015) Behavior of replication origins in Eukaryota – spatio-temporal dynamics of licensing and firing. Cell Cycle 14:2251–2264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nasmyth KA, Reed SI (1980) Isolation of genes by complementation in yeast: molecular cloning of a cell-cycle gene. Proc Natl Acad Sci USA 77:2119–2123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasmyth K, Dirick L, Surana U, Amon A, Cvrčková F (1991) Some facts and thoughts on cell cycle control in yeast. Cold Spring Harb Symp Quant Biol 56:9–20

    Article  CAS  PubMed  Google Scholar 

  • Nobelprize.org (2001) The Nobel Prize in physiology or medicine 2001: Leland Hartwell, Tim Hunt, Sir Paul Nurse. http://www.nobelprize.org/nobel_prizes/medicine/laureates/2001/. Cited 20 Nov 2016

  • Novák B, Tyson JJ (2008) Design principles of biochemical oscillators. Nat Rev Mol Cell Biol 9:981–991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Novák B, Csikász-Nagy A, Gyorffy B, Nasmyth K, Tyson JJ (1998) Model scenarios for evolution of the eukaryotic cell cycle. Philos Trans R Soc Lond Ser B Biol Sci 353:2063–2076

    Article  Google Scholar 

  • Nurse P (1975) Genetic control of cell size at cell division in yeast. Nature 256:547–551

    Article  CAS  PubMed  Google Scholar 

  • Nurse P (2000) A long twentieth century of the cell cycle and beyond. Cell 100:71–78

    Article  CAS  PubMed  Google Scholar 

  • Nurse PM (2002) Nobel lecture: cyclin dependent kinases and cell cycle control. Biosci Rep 22:487–499

    Article  CAS  PubMed  Google Scholar 

  • Nurse P (2016) Learning from the uncontrollable. Cell 165:1301–1136

    Article  CAS  PubMed  Google Scholar 

  • Nurse P, Bissett Y (1981) Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature 292:558–560

    Article  CAS  PubMed  Google Scholar 

  • Nurse P, Thuriaux P, Nasmyth K (1976) Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 146:167–178

    Article  CAS  PubMed  Google Scholar 

  • Paweletz N (2001) Walther Flemming: pioneer of mitosis research. Nat Rev Mol Cell Biol 2:72–75

    Article  CAS  PubMed  Google Scholar 

  • Pedersen T (2003) Historical review: an energy reservoir for mitosis, and its productive wake. Trends Biochem Sci 28:125–129

    Article  CAS  Google Scholar 

  • Pesenti ME, Weir JR, Musacchio A (2016) Progress in the structural and functional characterization of kinetochores. Curr Opin Struct Biol 37:152–1563

    Article  CAS  PubMed  Google Scholar 

  • Peters JM (1999) Subunits and substrates of the anaphase-promoting complex. Exp Cell Res 248:339–349

    Article  CAS  PubMed  Google Scholar 

  • Peters JM (2005) Cyclin degradation: don’t mes(s) with meiosis. Curr Biol 15:R461–R463

    Article  CAS  PubMed  Google Scholar 

  • Piggott JR, Rai R, Carter BL (1982) A bifunctional gene product involved in two phases of the yeast cell cycle. Nature 298:391–393

    Article  CAS  PubMed  Google Scholar 

  • Pines J (2011) Cubism and the cell cycle: the many faces of the APC/C. Nat Rev Mol Cell Biol 12:427–438

    Article  CAS  PubMed  Google Scholar 

  • Pines J, Hunt T (1987) Molecular cloning and characterization of the mRNA for cyclin from sea urchin eggs. EMBO J 6:2987–2995

    CAS  PubMed  PubMed Central  Google Scholar 

  • PubMed (2016) National centre for biotechnology information, Bethesda. https://www.ncbi.nlm.nih.gov/pubmed. Cited 20 Dec 2016

  • Rankin S, Dawson DS (2016) Recent advances in cohesin biology. F1000 Res 5. 10.12688/f1000research.8881.1

  • Rao PN, Johnson RT (1970) Mammalian cell fusion: studies on the regulation of DNA synthesis and mitosis. Nature 225:159–164

    Article  CAS  PubMed  Google Scholar 

  • Rapoport Y (1991) Doctors’plot of 1953. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Reid BJ, Culotti JG, Nash RS, Pringle JR (2015) Forty-five years of cell-cycle genetics. Mol Biol Cell 26:4307–4312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remak R (1852) Ueber extracellulare Entstehung thierischer Zellen und über die Vermehrung derselben durch Theilung. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin 1852:47–57

    Google Scholar 

  • Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inzé D, Jacobs T, Kouchi H, Rouzé P, Sauter M, Savouré A, Sorrell DA, Sundaresan V, Murray JA (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 32:1003–1018

    Article  CAS  PubMed  Google Scholar 

  • Roberts JW, Steitz JE (1967) The reconstitution of infective bacteriophage R17. Proc Natl Acad Sci USA 58:1416–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubin SM (2013) Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem Sci 38:12–19

    Article  CAS  PubMed  Google Scholar 

  • Ruehle MD, Orias E, Pearson CG (2016) Tetrahymena as a unicellular model eukaryote: genetic and genomic tools. Genetics 203:649–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rusch HP, Sachsenmaier W, Behrens K, Gruter V (1966) Synchronization of mitosis by the fusion of the plasmodia of Physarum polycephalum. J Cell Biol 31:204–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sansó M, Fisher RP (2013) Pause, play, repeat: CDKs push RNAP II’s buttons. Transcription 4:146–152

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasabe M, Machida Y (2014) Signaling pathway that controls plant cytokinesis. Enzyme 35:145–165

    CAS  Google Scholar 

  • Schaechter M (2015) A brief history of bacterial growth physiology. Front Microbiol 6:289. https://doi.org/10.3389/fmicb.2015.00289

    Article  PubMed  PubMed Central  Google Scholar 

  • Schiestl RH, Reynolds P, Prakash S, Prakash L (1989) Cloning and sequence analysis of the Saccharomyces cerevisiae RAD9 gene and further evidence that its product is required for cell cycle arrest induced by DNA damage. Mol Cell Biol 9:1882–1896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler K, Winter E (2006) Phosphorylation of Ime2 regulates meiotic progression in Saccharomyces cerevisiae. J Biol Chem 281:18307–18316

    Article  CAS  PubMed  Google Scholar 

  • Schleiden M (1838) Beiträge zur Phytogenesis. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin 1838:137–176

    Google Scholar 

  • Segers G, Gadisseur I, Bergounioux C, de Almeida Engler J, Jacqmard A, Van Montagu M, Inzé D (1996) The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J 10:601–612

    Article  CAS  PubMed  Google Scholar 

  • Šetlík J, Zachleder V (1984) The multiple fission cell reproductive patterns in algae. In: Nurse P, Streiblová E (eds) The microbial cell cycle. CRC, Boca Raton, pp 253–279

    Google Scholar 

  • Sia RA, Herald HA, Lew DJ (1996) Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell 7:1657–1666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šimůnek M, Hossfeld U, Wissemann V (2011) ‘Rediscovery’ revised – the cooperation of Erich and Armin von Tschermak-Seysenegg in the context of the ‘rediscovery’ of Mendel’s laws in 1899–1901. Plant Biol (Stuttg) 13:835–841

    Article  Google Scholar 

  • Speijer D, Lukeš J, Eliáš M (2015) Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci USA 112:8827–8834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sveiczer Á, Horváth A (2016) How do fission yeast cells grow and connect growth to the mitotic cycle? Curr Genet 63(2):165–173. https://doi.org/10.1007/s00294-016-0632-0

    Article  PubMed  CAS  Google Scholar 

  • Švorcová J, Markoš A, Das P (2018) Origins of the cellular biosphere. In: Baluška F, Sahi VP (eds) Concepts in cell biology – history and evolution. Plant cell monographs. Springer, Heidelberg

    Google Scholar 

  • Swenson KI, Farrell KM, Ruderman JV (1986) The clam embryo protein cyclin A induces entry into M phase and the resumption of meiosis in Xenopus oocytes. Cell 47:861–870

    Article  CAS  PubMed  Google Scholar 

  • Swift HH (1950) The desoxyribose nucleic acid content of animal nuclei. Physiol Zool 23:169–198

    Article  CAS  PubMed  Google Scholar 

  • Szabados L, Dudits D (1980) Fusion between interphase and mitotic plant protoplasts. Induction of premature chromosome condensation. Exp Cell Res 127:442–446

    Article  CAS  PubMed  Google Scholar 

  • Thomas JH (1993) Thinking about genetic redundancy. Trends Genet 9:395–399

    Article  CAS  PubMed  Google Scholar 

  • Thrasher JD (1966) Analysis of renewing epithelial cell populations. Methods Cell Biol 2:323–357

    Article  CAS  Google Scholar 

  • Toda T, Ochotorena I, Kominami K (1999) Two distinct ubiquitin-proteolysis pathways in the fission yeast cell cycle. Philos Trans R Soc Lond Ser B Biol Sci 354:1551–1557

    Article  CAS  Google Scholar 

  • Traub P, Nomura M (1968) Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc Natl Acad Sci USA 59:777–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traub P, Nomura M (1969) Structure and function of Escherichia coli ribosomes. VI. Mechanism of assembly of 30S ribosomes studied in vitro. J Mol Biol 40:391–413

    Article  CAS  PubMed  Google Scholar 

  • Trautmann S, Rajagopalan S, McCollum D (2004) The S. pombe Cdc14-like phosphatase Clp1p regulates chromosome biorientation and interacts with Aurora kinase. Dev Cell 7:755–762

    Article  CAS  PubMed  Google Scholar 

  • Tulin F, Cross FR (2014) A microbial avenue to cell cycle control in the plant superkingdom. Plant Cell 26:4019–4038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turing AM (1952) The chemical basis of morphogenesis. Philos Trans R Soc B 237:37–72

    Article  Google Scholar 

  • Tyson JJ, Novák B (2008) Temporal organization of the cell cycle. Curr Biol 18:R759–R768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyson JJ, Novák B (2015) Models in biology: lessons from modeling regulation of the eukaryotic cell cycle. BMC Biol 13:46. https://doi.org/10.1186/s12915-015-0158-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uhlmann F, Bouchoux C, López-Avilés S (2011) A quantitative model for cyclin-dependent kinase control of the cell cycle: revisited. Philos Trans R Soc Lond Ser B Biol Sci 366:3572–3583

    Article  CAS  Google Scholar 

  • Vidal A, Koff A (2000) Cell-cycle inhibitors: three families united by a common cause. Gene 247:1–15

    Article  CAS  PubMed  Google Scholar 

  • Mohl H von (1835) Ueber die Vermehrung der Pflanzen-Zellen durch Theilung: eine Inaug.-Dissertation. Winter, Tübingen

    Google Scholar 

  • von Nägeli KW (1842) Botanische Beitrage: 4. Zellenbildung in der Spitze der Wurzel Linnaea 16:252–256

    Google Scholar 

  • Walczak CE, Cai S, Khodjakov A (2010) Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 11:91–102. https://doi.org/10.1038/nrm2832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker PMB, Yates HB (1953) Nuclear components of dividing cells. Proc R Soc Lond B Biol Sci 140:274–299

    Article  Google Scholar 

  • Wang JD, Levin PA (2009) Metabolism, cell growth and the bacterial cell cycle. Nat Rev Microbiol 7:822–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Liu Y, Chen X, Fan Z (2010) Amitosis-like nuclear division in erythrocytes of triploid rainbow trout Oncorhynchus mykiss. J Fish Biol 76:1205–1211

    Article  CAS  PubMed  Google Scholar 

  • Weinert TA (1992) Dual cell cycle checkpoints sensitive to chromosome replication and DNA damage in the budding yeast Saccharomyces cerevisiae. Radiat Res 132:141–143

    Article  CAS  PubMed  Google Scholar 

  • Weinert TA, Hartwell LH (1990) Characterization of RAD9 of Saccharomyces cerevisiae and evidence that its function acts posttranslationally in cell cycle arrest after DNA damage. Mol Cell Biol 10:6554–6564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen B, Nieuwland J, Murray JA (2013) The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication. J Exp Bot 64:1135–1144

    CAS  PubMed  Google Scholar 

  • Wilkins AS, Holliday R (2009) The evolution of meiosis from mitosis. Genetics 181:3–12

    Article  PubMed  PubMed Central  Google Scholar 

  • Willems AR, Goh T, Taylor L, Chernushevich I, Shevchenko A, Tyers M (1999) SCF ubiquitin protein ligases and phosphorylation-dependent proteolysis. Philos Trans R Soc Lond Ser B Biol Sci 354:1533–1550

    Article  CAS  Google Scholar 

  • Wilson EB (1902) The cell in development and inheritance. Macmillan, New York

    Google Scholar 

  • Winfree AT (1984) The prehistory of the Belousov-Zhabotinsky oscillator. J Chem Educ 61:661–663

    Article  Google Scholar 

  • Woollard A, Basi G, Nurse P (1996) A novel S phase inhibitor in fission yeast. EMBO J 15:4603–4612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright NA, Poulsom R (2012) Omnis cellula e cellula revisited: cell biology as the foundation of pathology. J Pathol 226:145–147

    Article  PubMed  Google Scholar 

  • Wu M, Gerhart JC (1980) Partial purification and characterization of the maturation-promoting factor from eggs of Xenopus laevis. Dev Biol 79:465–477

    Article  CAS  PubMed  Google Scholar 

  • Yanagida M (2005) Basic mechanism of eukaryotic chromosome segregation. Philos Trans R Soc Lond Ser B Biol Sci 360:609–621

    Article  CAS  Google Scholar 

  • Yanagida M (2014) The role of model organisms in the history of mitosis research. Cold Spring Harb Perspect Biol 6(9):a015768. https://doi.org/10.1101/cshperspect.a015768

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng T, Nibau C, Phillips DW, Jenkins G, Armstrong SJ, Doonan JH (2014) CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana. Proc Natl Acad Sci USA 111:2182–2187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I dedicate this essay to the memory of Zdeněk Neubauer (1942–2016), who taught me, among many other things, that stories make the difference between history and historiography. I thank the Ministry of Education, Youth and Sports of the Czech Republic for generous financial support from the NPUI LO 14017 project, and teams of The Biodiversity Heritage Library (www.biodiversitylibrary.org), Internet Archive (www.archive.org), Münchener Digitalisierungszentrum (www.digitale-sammlungen.de), and Project Gutenberg (www.gutenberg.org) for making the historical literature available on-line.

Author information

Authors and Affiliations

  1. Department of Experimental Plant Biology, Faculty of Science, Charles University, Praha 2, Czech Republic

    Fatima Cvrčková

Authors
  1. Fatima Cvrčková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatima Cvrčková .

Editor information

Editors and Affiliations

  1. Botanical Institute, Karlsruhe Institute of Technology, Karlsruhe, Germany

    Vaidurya Pratap Sahi

  2. IZMB, Department of Plant Cell Biology, University of Bonn, Bonn, Nordrhein-Westfalen, Germany

    František Baluška

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Cvrčková, F. (2018). A Brief History of Eukaryotic Cell Cycle Research. In: Sahi, V., Baluška, F. (eds) Concepts in Cell Biology - History and Evolution. Plant Cell Monographs, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-319-69944-8_4

Download citation

Publish with us

Policies and ethics

Search

Navigation