Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 1

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1 Outline Cell growth as the driver for cell cycle (in microbes): coordination of growth and division A basic principle organizing cell cycle control: why cyclin-dependent kinase activity must oscillate Very messy regulatory machinery that provides the oscillations: two potentially independent oscillatory mechanisms working in tandem Chemical-kinetic modeling (in collaboration with John Tyson) Coordination of growth and division: Hartwell and Unger 1977: The minimum time for the cell division cycle is significantly less than the mass doubling time. Note: mass increase (ribosomes, etc) is approximately exponential with increasing cell size. Thus the mass doubling time. Growth and division are entrained because small cells are significantly less likely to initiate the cell division cycle than larger cells. Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 1

2 Coordination of growth and division: Smaller cells are less likely to initiate the cell division cycle; the setpoint for the minimum size can be modulated by Cln3 (initiator cyclin) levels. The mechanism remains unsolved. Do cells measure nuclear/cytoplasmic ratios? Is nuclear Cln3 a part of this measurement ratio? Size Cln3 Cell division cycle Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 2

3 A good idea: Make a biochemical oscillator, so that some enzyme activity X goes up and down. Set up each bit of cell cycle machinery as two-step processes. Then, connect up the cell division cycle machinery in the following way: Step A X Step B X Steps A B A B Step A: fire loaded origins Step B: Reload origins Clb-Cdk1 B-type cyclin: the oscillating component (Tim Hunt) : Origins of DNA replication loaded : Origins of DNA replication in use : Origins of DNA replication unloaded Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 3

4 One part of regulation of origin loading by Cdk activity: removing Mcm proteins from the nucleus The Mcm complex is loaded at origins before firing. It is essential for origin function. Cdk phosphorylation of the Mcm complex results in its exclusion from the nucleus. See the movie: Note nuclear fluorescence only right after cell division. (Subtle point: fluorescence lasts a bit longer in daughter nuclei than in mother nuclei) Step A: assemble spindle Step B: dissassemble spindle Clb-Cdk1 B-type cyclin: the oscillating component Watch another movie! Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 4

5 Step A: Produce bud Step B: Split off bud (cytokinesis) Other cyclins Clb-Cdk1 B-type cyclin: the oscillating component Size Cln3 Cell division cycle Clb activity Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 5

6 A complication: 9 cyclins! Cell division cycle Cln3 Cln1,2 Clb3,4 Clb5,6 Clb1,2 The purpose of a Rube Goldberg Machine is to build the most complicated machine possible to perform a simple everyday task. Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 6

7 Origin loading Origin use (DNA replication) Spindle assembly Anaphase Telophase Cln1-3 Cell growth Cdh1 Sic1 Cdc14 Clb1-6 Pds1 Cdh1, : APC activators Oscillator components: cyclins Cyclins work by activating a kinase. Cyclin Inactive kinase Cyclin Active kinase Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 7

8 The kinase phosphorylates target proteins, and thereby regulates target activity. Active kinase ATP P ADP Events Oscillator components: APC (Ub)n Target APC The anaphase-promoting complex (APC) ubiquitin ligase complex Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 8

9 / Cdh1 db (Ub)n Target APC and Cdh1 are adapters that bring destruction-box-containing target proteins to the APC ubiquitin ligase complex db Target APC APC- activity is intrinsically LOW Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 9

10 Clb-Cdc28 P db (Ub)n Target APC Clb-Cdc28 ACTIVATES APC- Clb-Cdc28 db Cdh1 (Ub)n Target APC APC-Cdh1 is intrinsically HIGH Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 10

11 Clb-Cdc28 Cdh1 P db Target APC Clb-Cdc28 INACTIVATES APC-Cdh1 Replication, mitotic entry Cyclin Origin loading, mitotic exit Replicate Cyclin APC Segregate Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 11

12 Relaxation oscillator Negative feedback oscillator B-Cyclin Cdc14 Cdh1/Sic1 Cln B-Cyclin Circuitry for two different types of oscillators coexists in the wild-type budding yeast system. MEN Cdc14 Cdh1,Sic1 (Cdc6?) Cln Cell growth Mitotic entry Mitotic exit is the main mitotic cyclin. Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 12

13 GAL-SIC1 CLB2 or CLB2 db: turn off GAL-SIC1, elutriate mid-cell cycle, release into α-factor * WT db * CLB2 db Removing the destruction box prevents degradation CLB2 GAL-SIC1 or CLB2 db GAL-SIC1 : turn off GAL-SIC1 wt CLB2 db Removing the destruction box (exact endogenous gene replacement) blocks cells in late mitosis Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 13

14 MEN Cdc14 APC-P APC Cdh1,Sic1 (Cdc6?) Cln Cell growth Mitotic entry Mitotic exit Cyclin Phosphorylation of APC subunits Cdc16, Cdc23, Cdc27 by kinase may provide an essential component for the negative feedback oscillator MEN Cdc14 APC Cdh1,Sic1 (Cdc6?) Cln Cell growth Mitotic entry Mitotic exit A tool: the APC-A mutant, in which the APC subunits cannot be phosphorylated due to S/T A mutations Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 14

15 Cyclin Cdh1/Sic1 Cyclin APC-A: Unphosphorylatable APC subunits. Negative feedback oscillator disabled x cdh1 Relaxation oscillator disabled. Tetrad analysis APC-A cdh1 Cannot complete mitosis YEPGal GAL-SIC1 ON YEPD GAL-SIC1 OFF RS425 RS415-cdh1 RS415-CDH1 RS415-CDC20 RS425-CDC20 CDC16-A CDC23-A CDC27-A cdh1 ura3::ura3::gal-sic1 SIC1 or CDC20 overexpression can restore cdh1 APC-A viability Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 15

16 Disabling both oscillators blocks the cell cycle; either one alone may be sufficient. S/M Cdc14 G1 Cdh1/Sic1 Cln MEN Conceptual model Cdc14 Cdh1,Sic1 (Cdc6?) Mitotic entry Mitotic exit Rate equations Computer simulations d/dt = ksynth kdeg**(cdh1+) d/dt=ka**(1-) kd* dcdh1/dt=ka*(1-cdh1) ki**cdh1 predictions Genetic/biochemical tests; revise rate equations and/or conceptual model Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 16

17 Realistic computational analysis* shows that a double-oscillator system can account for cell cycle regulation, in wild-type and in many mutant situations Cln2 Activity * MASS Clb5 Cdc6 Sic1 Cdh1 Time * K. Chen, J. Tyson wt MASS Cycles Clb5 CLB2-db MASS Mitotic arrest Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 17

18 wt APC-A cdh1 APC-A cdh1 The wild-type model is reasonably robust; some viable mutants are very fragile Log 2 Maximum parameter change >= DOWN 1 0 >= UP Fraction of parameters wt cdh1 APC-A sic1 Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 18

19 APC-A cdh1 APC-A cdh1 + multi-copy SIC1 APC-A cdh1 + GAL-CDC20 Parameter kdb2p ks20 ks20 kd20 ka20 ksc1 ksc1 kaswi Jiswi Effect of change Increase -dependent degradation Increase constitutive CDC20 transcription Increase -regulated CDC20 transcription Decrease degradation Increase Phospho-APCindependent activity Increase constitutive SIC1 transcription Increase Swi5-regulated SIC1 transcription Increase Swi5-regulated SIC1 transcription Increase Swi5-regulated SIC1 transcription Change Up 10X Up 20X Up 4X Down 8X Up 7X Up 8X Up 90X Up 10X Up 90X cdh1 APC-A model: test systematic parameter variations for suppression of inviability Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 19

20 Experiment Computation CLB2-db cdh1 sic1 GAL-CDC20 APC-A APC-A cdh1 APC-A cdh1+ CDC20,SIC1 overexpression Why would cells have two functional oscillators? Maybe they function at different times Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 20

21 Clb/: for running a minimal cell cycle? M Sic1/Cdh1: for maintaining G1? Sic1/Cdh1 Clb (G1) G1 Sic1/Cdh1 Clb S G1 Sic1/Cdh1 Clb M G1 Sic1/Cdh1 Frog p27/p21/cdh1 G1 p27/p21/cdh1 S/M Cyclin G1/S CycE, CycA CycB G2/M Frog Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 21

22 S/M Cdc14 G1 Cdh1/Sic1 Cln Low nutrients, inhibitory extracellular factors S/M G1 Cdh1/Kip1 Cyclin B Cyclin D,E,A Inhibitory extracellular factors Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 22

23 Ralph Wäsch (CLB2-db) Vincent Archambault (model testing) Jamie Bean (movies) John Tyson, Kathy Chen (Virginia Tech) Dr. Fred Cross, Rockefeller (KITP Bio Networks 3/26/2003) 23

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