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Integration of Light Signals by the Retinoblastoma Pathway in the Control of S Phase Entry in the Picophytoplanktonic Cell


Although the decision to proceed through cell division depends largely on the metabolic status or the size of the cell, the timing of cell division is often set by internal clocks such as the circadian clock. Light is a major cue for circadian clock entrainment, and for photosynthetic organisms it is also the main source of energy supporting cell growth prior to cell division. Little is known about how light signals are integrated in the control of S phase entry. Here, we present an integrated study of light-dependent regulation of cell division in the marine green alga Ostreococcus. During early G1, the main genes of cell division were transcribed independently of the amount of light, and the timing of S phase did not occur prior to 6 hours after dawn. In contrast S phase commitment and the translation of a G1 A-type cyclin were dependent on the amount of light in a cAMP–dependent manner. CyclinA was shown to interact with the Retinoblastoma (Rb) protein during S phase. Down-regulating Rb bypassed the requirement for CyclinA and cAMP without altering the timing of S phase. Overexpression of CyclinA overrode the cAMP–dependent control of S phase entry and led to early cell division. Therefore, the Rb pathway appears to integrate light signals in the control of S phase entry in Ostreococcus, though differential transcriptional and posttranscriptional regulations of a G1 A-type cyclin. Furthermore, commitment to S phase depends on a cAMP pathway, which regulates the synthesis of CyclinA. We discuss the relative involvements of the metabolic and time/clock signals in the photoperiodic control of cell division.


Vyšlo v časopise: Integration of Light Signals by the Retinoblastoma Pathway in the Control of S Phase Entry in the Picophytoplanktonic Cell. PLoS Genet 6(5): e32767. doi:10.1371/journal.pgen.1000957
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000957

Souhrn

Although the decision to proceed through cell division depends largely on the metabolic status or the size of the cell, the timing of cell division is often set by internal clocks such as the circadian clock. Light is a major cue for circadian clock entrainment, and for photosynthetic organisms it is also the main source of energy supporting cell growth prior to cell division. Little is known about how light signals are integrated in the control of S phase entry. Here, we present an integrated study of light-dependent regulation of cell division in the marine green alga Ostreococcus. During early G1, the main genes of cell division were transcribed independently of the amount of light, and the timing of S phase did not occur prior to 6 hours after dawn. In contrast S phase commitment and the translation of a G1 A-type cyclin were dependent on the amount of light in a cAMP–dependent manner. CyclinA was shown to interact with the Retinoblastoma (Rb) protein during S phase. Down-regulating Rb bypassed the requirement for CyclinA and cAMP without altering the timing of S phase. Overexpression of CyclinA overrode the cAMP–dependent control of S phase entry and led to early cell division. Therefore, the Rb pathway appears to integrate light signals in the control of S phase entry in Ostreococcus, though differential transcriptional and posttranscriptional regulations of a G1 A-type cyclin. Furthermore, commitment to S phase depends on a cAMP pathway, which regulates the synthesis of CyclinA. We discuss the relative involvements of the metabolic and time/clock signals in the photoperiodic control of cell division.


Zdroje

1. SpudichJL

SagerR

1980 Regulation of the Chlamydomonas cell cycle by light and dark. J Cell Biol 85 136 145

2. OldenhofH

ZachlederV

Van den EndeH

2007 The cell cycle of Chlamydomonas reinhardtii: the role of the commitment point. Folia Microbiol (Praha) 52 53 60

3. KorolevaOA

TomlinsonM

ParinyapongP

SakvarelidzeL

LeaderD

2004 CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16 2364 2379

4. OakenfullEA

Riou-KhamlichiC

MurrayJA

2002 Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357 749 760

5. HullemanE

BoonstraJ

2001 Regulation of G1 phase progression by growth factors and the extracellular matrix. Cell Mol Life Sci 58 80 93

6. MoserBA

RussellP

2000 Cell cycle regulation in Schizosaccharomyces pombe. Curr Opin Microbiol 3 631 636

7. DonjerkovicD

ScottDW

2000 Regulation of the G1 phase of the mammalian cell cycle. Cell Res 10 1 16

8. HaylesJ

NurseP

1986 Cell cycle regulation in yeast. J Cell Sci Suppl 4 155 170

9. DolznigH

GrebienF

SauerT

BeugH

MullnerEW

2004 Evidence for a size-sensing mechanism in animal cells. Nat Cell Biol 6 899 905

10. EdmundsLNJr

Laval-MartinDL

GotoK

1987 Cell division cycles and circadian clocks. Modeling a metabolic oscillator in the algal flagellate Euglena. Ann N Y Acad Sci 503 459 475

11. MoriT

BinderB

JohnsonCH

1996 Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc Natl Acad Sci U S A 93 10183 10188

12. SchevingLE

1981 Circadian rhythms in cell proliferation: their importance when investigating the basic mechanism of normal versus abnormal growth. Prog Clin Biol Res 59C 39 79

13. GeryS

KomatsuN

BaldjyanL

YuA

KooD

2006 The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol Cell 22 375 382

14. PregueiroAM

LiuQ

BakerCL

DunlapJC

LorosJJ

2006 The Neurospora checkpoint kinase 2: a regulatory link between the circadian and cell cycles. Science 313 644 649

15. Unsal-KacmazK

MullenTE

KaufmannWK

SancarA

2005 Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 25 3109 3116

16. HagiwaraS

TakahashiM

YamagishiA

ZhangY

GotoK

2001 Novel findings regarding photoinduced commitments of G1-, S- and G2-phase cells to cell-cycle transitions in darkness and dark-induced G1-, S- and G2-phase arrests in Euglena. Photochem Photobiol 74 726 733

17. GotoK

JohnsonCH

1995 Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii. J Cell Biol 129 1061 1069

18. CorellouF

SchwartzC

MottaJP

Djouani-Tahri elB

SanchezF

2009 Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote Ostreococcus. Plant Cell 21 3436 3449

19. DerelleE

FerrazC

RombautsS

RouzeP

WordenAZ

2006 Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103 11647 11652

20. RobbensS

KhadarooB

CamassesA

DerelleE

FerrazC

2005 Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri. Mol Biol Evol 22 589 597

21. CorellouF

CamassesA

LigatL

PeaucellierG

BougetFY

2005 Atypical regulation of a green lineage-specific B-type cyclin-dependent kinase. Plant Physiol 138 1627 1636

22. MoulagerM

MonnierA

JessonB

BouvetR

MosserJ

2007 Light-dependent regulation of cell division in Ostreococcus: evidence for a major transcriptional input. Plant Physiol 144 1360 1369

23. SoniR

CarmichaelJP

ShahZH

MurrayJA

1995 A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7 85 103

24. MadhyasthaHK

RadhaKS

NakajimaY

OmuraS

MaruyamaM

2008 uPA dependent and independent mechanisms of wound healing by C-phycocyanin. J Cell Mol Med 12 2691 2703

25. MohabirG

EdmundsLNJr

1999 Circadian clock regulation of the bimodal rhythm of cyclic AMP in wild-type Euglena. Cell Signal 11 143 147

26. HallDD

MarkwardtDD

ParvizF

HeidemanW

1998 Regulation of the Cln3-Cdc28 kinase by cAMP in Saccharomyces cerevisiae. Embo J 17 4370 4378

27. EhsanH

ReichheldJ-P

RoefL

WittersE

LardonF

1998 Effect of indomethacin on cell cycle dependent cyclic AMP fuxes in tobacco BY-2 cells. FEBS Letters 422 165 169

28. PasqualeSM

GoodenoughUW

1987 Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105 2279 2292

29. StarkGR

TaylorWR

2006 Control of the G2/M transition. Mol Biotechnol 32 227 248

30. MacalusoM

MontanariM

GiordanoA

2006 Rb family proteins as modulators of gene expression and new aspects regarding the interaction with chromatin remodeling enzymes. Oncogene 25 5263 5267

31. PlescaD

CrosbyME

GuptaD

AlmasanA

2007 E2F4 function in G2: maintaining G2-arrest to prevent mitotic entry with damaged DNA. Cell Cycle 6 1147 1152

32. SageJ

MulliganGJ

AttardiLD

MillerA

ChenS

2000 Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev 14 3037 3050

33. UmenJG

GoodenoughUW

2001 Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev 15 1652 1661

34. TayaY

1997 RB kinases and RB-binding proteins: new points of view. Trends Biochem Sci 22 14 17

35. DepoortereF

Van KeymeulenA

LukasJ

CostagliolaS

BartkovaJ

1998 A requirement for cyclin D3-cyclin-dependent kinase (cdk)-4 assembly in the cyclic adenosine monophosphate-dependent proliferation of thyrocytes. J Cell Biol 140 1427 1439

36. MatsuoT

2003 Control mechanism of the circadian clock for timing of cell division in vivo.[see comment]. Science 302 234 235

37. FuL

PatelMS

BradleyA

WagnerEF

KarsentyG

2005 The molecular clock mediates leptin-regulated bone formation. Cell 122 803 815

38. Grechez-CassiauA

RayetB

GuillaumondF

TeboulM

DelaunayF

2008 The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J Biol Chem 283 4535 4542

39. CourtiesC

VaquerA

TrousselierM

LautierJ

Chrétiennot-DinetM-J

1994 Smallest eukarotic organism. Nature 370 255

40. EvenY

DurieuxS

EscandeML

LozanoJC

PeaucellierG

2006 CDC2L5, a Cdk-like kinase with RS domain, interacts with the ASF/SF2-associated protein p32 and affects splicing in vivo. J Cell Biochem 99 890 904

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