How deregulated cell cycles (might) trigger cancer. Dan Fisher. Friday 27th October Lucie Fisher, 3 Eddie Fisher, 6.
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1 How deregulated cell cycles (might) trigger cancer Dan Fisher Friday 27th October 2017 Lucie Fisher, 3 Eddie Fisher, 6 1
2 transformed cells
3 transformed cells
4 Structure of this lecture Cancer and the cell cycle What causes cancer? The cell cycle vs growth DNA damage model 3
5 Structure of this lecture Cancer and the cell cycle What causes cancer? The cell cycle vs growth DNA damage model Principles of cell cycle control Phosphorylation and destruction Cyclin dependent kinases The APC/C Phosphates 3
6 Structure of this lecture Cancer and the cell cycle What causes cancer? The cell cycle vs growth DNA damage model Principles of cell cycle control Phosphorylation and destruction Cyclin dependent kinases The APC/C Phosphates Mitosis and genome stability DNA damage The centrosome cycle The spindle assembly checkpoint The Chromosomal Passenger complex 3
7 Structure of this lecture Cancer and the cell cycle What causes cancer? The cell cycle vs growth DNA damage model Principles of cell cycle control Phosphorylation and destruction Cyclin dependent kinases The APC/C Phosphates Mitosis and genome stability DNA damage The centrosome cycle The spindle assembly checkpoint The Chromosomal Passenger complex and finally How to target the cell cycle in cancer (maybe) 3
8 Structure of this lecture Cancer and the cell cycle What causes cancer? The cell cycle vs growth DNA damage model Principles of cell cycle control Phosphorylation and destruction Cyclin dependent kinases The APC/C Phosphates Mitosis and genome stability DNA damage The centrosome cycle The spindle assembly checkpoint The Chromosomal Passenger complex and finally How to target the cell cycle in cancer (maybe) 3
9 Cancer is just bad luck (due to excess cell division and defective cell death)
10 No it isn t
11
12
13 Cell proliferation is linked to growth Deregulation of the cell cycle Neufeld et al., (1998) Cell 8
14 Cell proliferation is linked to growth Deregulation of the cell cycle and of growth Neufeld et al., (1998) Cell Tapon et al., (2001) Cell 8
15 The cell cycle is not growth 9
16 The cell cycle is not growth 9
17 The cell cycle is not growth The cell cycle is a nuclear cycle 9
18 The first replicators: RNA polymers, formed on clay Cellular replication machines
19 The first replicators: RNA polymers, formed on clay Cellular replication machines
20 Emergence of heterogeneity requires cell division Sanchez Alvarado, Curr Biol 2012
21 Emergence of heterogeneity requires cell division Sanchez Alvarado, Curr Biol 2012
22 Oncogene-induced DNA damage model for cancer intiation and progression 12 Halazonetis et al (2008), Science
23 DNA damage in early stages of cancer 13 Bartkova et al (2006), Nature
24 How is the cell cycle controlled? 14
25 The complexity of cell proliferation Westra et al. (2011), BMC Systems Biol 5: 105
26 Cell cycle control by phosphorylation Physarum polycephalum 16
27 Cell cycle control by phosphorylation Physarum polycephalum Bradbury et al (1974) Control of cell division by very lysine rich histone (F1) phosphorylation Nature 247, Bradbury et al (1974) Molecular basis of control of mitotic cell division in eukaryotes. Nature 249,
28 Simplifying the cell cycle Walther Flemming, 1882
29 Simplifying the cell cycle The Nobel Prize in Physiology or Medicine 2001 "for their discoveries of key regulators of the cell cycle" Leland H. Hartwell R. Timothy (Tim) Hunt Sir Paul M. Nurse Cyclin Dependent Kinases (CDK)
30 Simplifying the cell cycle The Nobel Prize in Physiology or Medicine 2001 "for their discoveries of key regulators of the cell cycle" protéine Leland H. Hartwell R. Timothy (Tim) Hunt Sir Paul M. Nurse Cyclin Dependent Kinases (CDK)
31 Simplifying the cell cycle The Nobel Prize in Physiology or Medicine 2001 "for their discoveries of key regulators of the cell cycle" protéine Leland H. Hartwell R. Timothy (Tim) Hunt Sir Paul M. Nurse Cyclin Dependent Kinases (CDK)
32 Simplifying the cell cycle The Nobel Prize in Physiology or Medicine 2001 "for their discoveries of key regulators of the cell cycle" protéine Leland H. Hartwell R. Timothy (Tim) Hunt Sir Paul M. Nurse Cyclin Dependent Kinases (CDK)
33 The essential cell cycle G1 M-phase CDK Mitosis M S-phase S DNA Replication CDK G2 18
34 The essential cell cycle M-phase CDK Mitosis CDK S-phase DNA Replication 18
35 The essential cell cycle M-phase CDK Mitosis CDK S-phase DNA Replication 18
36 Regulation of cell proliferation Environmental signals Signalling pathways Changes in gene expression (transcription, translation, etc) CDKs Checkpoint kinases S-Phase: replication M-Phase: mitosis
37 Regulation of cell proliferation Environmental signals Signalling pathways Changes in gene expression (transcription, translation, etc) CDKs Checkpoint kinases S-Phase: replication M-Phase: mitosis
38 20 Cyclin dependent kinases: structure and function
39 20 Cyclin dependent kinases: structure and function
40 20 Cyclin dependent kinases: structure and function
41 20 Cyclin dependent kinases: structure and function
42 Every act of creation is, first of all, an act of destruction (Pablo Picasso) Evans et al (1983) Cell 21
43 Every act of creation is, first of all, an act of destruction (Pablo Picasso) Evans et al (1983) Cell 21
44 The ubiquitin E3 ligase complex, APC/C, targets cyclins and securin for destruction 22 Pines, J. (2011) Nat Rev Mol Cell Biol
45 The ubiquitin E3 ligase complex, APC/C, targets cyclins and securin for destruction 22 Pines, J. (2011) Nat Rev Mol Cell Biol
46 The ubiquitin E3 ligase complex, APC/C, targets cyclins and securin for destruction D-box recognition site 22 Pines, J. (2011) Nat Rev Mol Cell Biol
47 CDKs control DNA replication by triggering Pre-IC formation Licensing: formation of Prereplication complex CDK DDK Pre-Initiation complexes with the replisome 23
48 Mitosis CDKs phosphorylate many substrates 24
49 Mitosis CDKs phosphorylate many substrates Biotin dutp To switch off replication 24
50 Mitosis CDKs phosphorylate many substrates Biotin dutp To switch off replication To condense DNA Interphase Mitosis 24
51 Mitosis CDKs phosphorylate many substrates Biotin dutp To switch off replication To condense DNA Interphase Mitosis To disassemble the nuclear envelope and pores 24
52 Mitosis CDKs phosphorylate many substrates Biotin dutp To switch off replication To condense DNA Interphase Mitosis To promote selfactivation To disassemble the nuclear envelope and pores 24
53 Mitosis CDKs phosphorylate many substrates To form spindles and a metaphase plate 24
54 A single enzyme complex can control the cell cycle GROWTH! COMMITMENT! S! G2! cdc2! +! cyclin! G1! M! CHECKPOINT! CHECKPOINT! cdc2! + cyclin! Fisher and Nurse (1996) 25
55 A single enzyme complex can control the cell cycle GROWTH! COMMITMENT! S! G2! cdc2! +! cyclin! G1! M! CHECKPOINT! CHECKPOINT! cdc2! + cyclin! Fisher and Nurse (1996) 25
56 Cdk1 activity levels drive the cell cycle Min( Mitosis( Min( S"phase( Max( Licensing( 26
57 27 *Power is nothing without control
58 Inhibition of phosphatases counteracting CDKs shortcircuits the cell cycle G1 control depletion M S G2 28
59 Inhibition of phosphatases counteracting CDKs shortcircuits the cell cycle G1 control depletion M S Mitotic substrate phosphorylation G2 Decreasing PP2A activity Relative cyclin concentration 28
60 Cdk1 network: An extended symmetrical kinase-phosphatase network generating ultrasensitive behaviour PP1. $ PP1?$ PP2A.$ A/E. $ *$ Gwll. $ Gwll$?! PP2A$ S$ S. $ *$ Wee1. $ Wee1$ Cdk1$ Cdc25. $ Cdc25$ Cdk1. $ 29 Fisher, D. (2012)
61 Coffee break 10 minutes! 30
62 Cancer heterogeneity 31 Pereira et al., Nat Commun 2016
63 Chromothripsis: acute chromosome shattering in cancer 32 Forment et al (2012), Nat Rev Canc
64 The DNA damage checkpoint controls the cell cycle to maintain genomic stability 33
65 From replication to mitosis: the source of DNA damage? 34
66 How does deregulated growth or cell cycle cause DNA damage? Environmental signals Signalling pathways Changes in gene expression (transcription, translation, etc) CDKs Checkpoint kinases S-Phase: replication M-Phase: mitosis
67 How does deregulated growth or cell cycle cause DNA damage? Environmental signals Signalling pathways Changes in gene expression (transcription, translation, etc) CDKs Checkpoint kinases S-Phase: replication M-Phase: mitosis
68 The cell cycle and cancer progression 36 Forment et al (2012), Nat Rev Canc
69 Mitosis with non-replicated DNA is a source of genomic instability Fragile sites 37 Debatisse, M. et al. (2012) Trends Genet
70 Mitosis with non-replicated DNA is a source of genomic instability Fragile sites Replication forks 37 Debatisse, M. et al. (2012) Trends Genet
71 Mitosis and cancer 38 Flemming, 1882 Von Hansemann, 1890
72 Aneuploidy in cancer initiation and progression Theodor Boveri, 1914 Abnormal centrosome number as a source of aneuploidy 39
73 Phases of Mitosis Pro Pro-Meta Meta Ana Telo 40
74 Cohesin keeps sister chromatids together S-phase 41
75 Cohesin keeps sister chromatids together S-phase 41
76 Cohesin keeps sister chromatids together S-phase 41
77 Cohesin keeps sister chromatids together S-phase 41
78 41 Cohesin keeps sister chromatids together
79 Cohesin keeps sister chromatids together Mitosis 41
80 Cohesin keeps sister chromatids together Separase Securin APC/C SAC Mitosis 41
81 Cohesin keeps sister chromatids together Mitosis 41
82 Mitotic spindles are composed of dynamic microtubules 42
83 Centrosomes nucleate the mitotic spindle Mahoney et al., (2006) Curr Biol. 43
84 Centrosomes nucleate the mitotic spindle Mahoney et al., (2006) Curr Biol. 43
85 Centrosomes nucleate the mitotic spindle Mahoney et al., (2006) Curr Biol. 43
86 Kinetochore-mediated spindle formation Spindle without centrosomes 44
87 Kinetochore-mediated spindle formation Spindle without centrosomes 44
88 45 Gonczy, P. (2015) Nat Rev Cancer The centrosome cycle
89 The centrosome cycle Kinesin 5 CDK1-CycB2 AurA Plk1 NEK2 Separase APC/C- CDH1 CDK2-CycE Mps1 Plk4 45 Gonczy, P. (2015) Nat Rev Cancer
90 The centrosome cycle Multipolar spindles in cancer cells 45 Gonczy, P. (2015) Nat Rev Cancer
91 The centrosome cycle and cancer Multipolar mitoses kill cells Ganem et al., 2009, Nature, 460,
92 The centrosome cycle and cancer Multipolar mitoses kill cells Merotelic attachments often occur Ganem et al., 2009, Nature, 460,
93 The centrosome cycle and cancer clustered centrosomes with merotelic attachments lagging chromosomes Ganem et al., 2009, Nature, 460,
94 The centrosome cycle and cancer clustered centrosomes with merotelic attachments lagging chromosomes Ganem et al., 2009, Nature, 460,
95 The spindle assembly checkpoint: halting mitosis Unattached kinetochores activate the SAC inhibitors SAC inactivated 47
96 The spindle assembly checkpoint: halting mitosis Unattached kinetochores activate the SAC SAC activation inhibitors SAC inactivated 47
97 The spindle assembly checkpoint: halting mitosis Unattached kinetochores activate the SAC SAC activation Mitotic kinases (Plk1, Aur B) inhibitors SAC inactivated 47
98 The spindle assembly checkpoint: halting mitosis Unattached kinetochores activate the SAC Mitotic kinases (Plk1, Aur B) inhibitors kinetochore-mt binding SAC inactivated 47
99 The spindle assembly checkpoint: halting mitosis Unattached kinetochores activate the SAC Mitotic kinases (Plk1, Aur B) inhibitors kinetochore-mt binding SAC inactivated Alkaloid drugs (taxol) Sustained SAC 47 Apoptosis
100 Cancer cells can proliferate without centrosomes Centrinone: Plk4 inhibitor 48 Wong et al., 2015, Science 348, 1155
101 Cancer cells can proliferate without centrosomes Centrinone: Plk4 inhibitor 48 Wong et al., 2015, Science 348, 1155
102 chromosomes cytokinesis: the CPC 49 Carmena, M. et al. (2012) Nat Rev Mol Cell Biol
103 chromosomes cytokinesis: the CPC 49 Carmena, M. et al. (2012) Nat Rev Mol Cell Biol
104 chromosomes cytokinesis: the CPC 49 Carmena, M. et al. (2012) Nat Rev Mol Cell Biol
105 chromosomes cytokinesis: the CPC 49 Carmena, M. et al. (2012) Nat Rev Mol Cell Biol
106 50 Cytokinesis
107 50 Cytokinesis
108 Targeting the cell cycle? 51
109 52 Targeting DNA replication and repair
110 Targeting cell growth and proliferation 53 Hanahan and Weinberg (2011) Cell
111 Targeting cell growth and proliferation 53 Hanahan and Weinberg (2011) Cell
112 Cell cycle kinase inhibitors as potential therapeutic agents Cdk 54
113 Cell cycle kinase inhibitors as potential therapeutic agents Aurora 54
114 Cell cycle kinase inhibitors as potential therapeutic agents Plk 54
115 Controlling cell proliferation and resistance using adaptive therapy approaches Using CDK inhibitors 100% sensitive cells + 1% resistant cells 100% resistant cells Bacevic, Noble et al., 2017, Nature communications, in press 55
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