#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

STAT Is an Essential Activator of the Zygotic Genome in the Early
Embryo


In many organisms, transcription of the zygotic genome begins during the

maternal-to-zygotic transition (MZT), which is characterized by a dramatic

increase in global transcriptional activities and coincides with embryonic stem

cell differentiation. In Drosophila, it has been shown that

maternal morphogen gradients and ubiquitously distributed general transcription

factors may cooperate to upregulate zygotic genes that are essential for pattern

formation in the early embryo. Here, we show that Drosophila

STAT (STAT92E) functions as a general transcription factor that, together with

the transcription factor Zelda, induces transcription of a large number of

early-transcribed zygotic genes during the MZT. STAT92E is present in the early

embryo as a maternal product and is active around the MZT. DNA–binding

motifs for STAT and Zelda are highly enriched in promoters of early zygotic

genes but not in housekeeping genes. Loss of Stat92E in the

early embryo, similarly to loss of zelda, preferentially

down-regulates early zygotic genes important for pattern formation. We further

show that STAT92E and Zelda synergistically regulate transcription. We conclude

that STAT92E, in conjunction with Zelda, plays an important role in

transcription of the zygotic genome at the onset of embryonic development.


Vyšlo v časopise: STAT Is an Essential Activator of the Zygotic Genome in the Early Embryo. PLoS Genet 7(5): e32767. doi:10.1371/journal.pgen.1002086
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002086

Souhrn

In many organisms, transcription of the zygotic genome begins during the

maternal-to-zygotic transition (MZT), which is characterized by a dramatic

increase in global transcriptional activities and coincides with embryonic stem

cell differentiation. In Drosophila, it has been shown that

maternal morphogen gradients and ubiquitously distributed general transcription

factors may cooperate to upregulate zygotic genes that are essential for pattern

formation in the early embryo. Here, we show that Drosophila

STAT (STAT92E) functions as a general transcription factor that, together with

the transcription factor Zelda, induces transcription of a large number of

early-transcribed zygotic genes during the MZT. STAT92E is present in the early

embryo as a maternal product and is active around the MZT. DNA–binding

motifs for STAT and Zelda are highly enriched in promoters of early zygotic

genes but not in housekeeping genes. Loss of Stat92E in the

early embryo, similarly to loss of zelda, preferentially

down-regulates early zygotic genes important for pattern formation. We further

show that STAT92E and Zelda synergistically regulate transcription. We conclude

that STAT92E, in conjunction with Zelda, plays an important role in

transcription of the zygotic genome at the onset of embryonic development.


Zdroje

1. EphrussiASt JohnstonD

2004

Seeing is believing: the bicoid morphogen gradient

matures.

Cell

116

143

152

2. St JohnstonDNusslein-VolhardC

1992

The origin of pattern and polarity in the Drosophila

embryo.

Cell

68

201

219

3. Nusslein-VolhardC

1991

Determination of the embryonic axes of

Drosophila.

Dev

Suppl 1

1

10

4. WieschausE

1996

Embryonic transcription and the control of developmental

pathways.

Genetics

142

5

10

5. De RenzisSElementoOTavazoieSWieschausEF

2007

Unmasking activation of the zygotic genome using chromosomal

deletions in the Drosophila embryo.

PLoS Biol

5

e117

doi:10.1371/journal.pbio.0050117

6. LawrencePAStruhlG

1996

Morphogens, compartments, and pattern: lessons from

drosophila?

Cell

85

951

961

7. DrieverWNusslein-VolhardC

1988

The bicoid protein determines position in the Drosophila embryo

in a concentration-dependent manner.

Cell

54

95

104

8. RothSSteinDNusslein-VolhardC

1989

A gradient of nuclear localization of the dorsal protein

determines dorsoventral pattern in the Drosophila embryo.

Cell

59

1189

1202

9. LiangHLNienCYLiuHYMetzsteinMMKirovNRushlowC

2008

The zinc-finger protein Zelda is a key activator of the early

zygotic genome in Drosophila.

Nature

10. LibermanLMStathopoulosA

2009

Design flexibility in cis-regulatory control of gene expression:

synthetic and comparative evidence.

Dev Biol

327

578

589

11. GalloSMLiLHuZHalfonMS

2006

REDfly: a Regulatory Element Database for

Drosophila.

Bioinformatics

22

381

383

12. MarksteinMMarksteinPMarksteinVLevineMS

2002

Genome-wide analysis of clustered Dorsal binding sites identifies

putative target genes in the Drosophila embryo.

Proc Natl Acad Sci U S A

99

763

768

13. MacdonaldPMStruhlG

1986

A molecular gradient in early Drosophila embryos and its role in

specifying the body pattern.

Nature

324

537

545

14. MlodzikMGehringWJ

1987

Expression of the caudal gene in the germ line of Drosophila:

formation of an RNA and protein gradient during early

embryogenesis.

Cell

48

465

478

15. SprengerFStevensLMNusslein-VolhardC

1989

The Drosophila gene torso encodes a putative receptor tyrosine

kinase.

Nature

338

478

483

16. CasanovaJStruhlG

1989

Localized surface activity of torso, a receptor tyrosine kinase,

specifies terminal body pattern in Drosophila.

Genes Dev

3

2025

2038

17. LiWX

2005

Functions and mechanisms of receptor tyrosine kinase Torso

signaling: Lessons from Drosophila embryonic terminal

development.

Dev Dyn

232

656

672

18. StathopoulosALevineM

2002

Dorsal gradient networks in the Drosophila

embryo.

Dev Biol

246

57

67

19. HouXSMelnickMBPerrimonN

1996

Marelle acts downstream of the Drosophila HOP/JAK kinase and

encodes a protein similar to the mammalian STATs [published erratum

appears in Cell 1996 Apr 19;85(2):following 290].

Cell

84

411

419

20. LiJLiWCalhounHCXiaFGaoFBLiWX

2003

Patterns and functions of STAT activation during Drosophila

embryogenesis.

Mech Dev

120

1455

1468

21. YanRSmallSDesplanCDearolfCRDarnellJEJr

1996

Identification of a Stat gene that functions in Drosophila

development.

Cell

84

421

430

22. LiWX

2008

Canonical and non-canonical JAK-STAT signaling.

Trends Cell Biol

18

545

551

23. LiJLiWX

2003

Drosophila gain-of-function mutant RTK torso triggers ectopic Dpp

and STAT signaling.

Genetics

164

247

258

24. LiJXiaFLiWX

2003

Coactivation of STAT and Ras is required for germ cell

proliferation and invasive migration in Drosophila.

Dev Cell

5

787

798

25. LiWXAgaisseHMathey-PrevotBPerrimonN

2002

Differential requirement for STAT by gain-of-function and

wild-type receptor tyrosine kinase Torso in Drosophila.

Development

129

4241

4248

26. JinksTMPolydoridesADCalhounGSchedlP

2000

The JAK/STAT signaling pathway is required for the initial choice

of sexual identity in Drosophila melanogaster.

Molecular Cell

5

581

587

27. ten BoschJRBenavidesJAClineTW

2006

The TAGteam DNA motif controls the timing of Drosophila

pre-blastoderm transcription.

Development

133

1967

1977

28. SubramanianATamayoPMoothaVKMukherjeeSEbertBLGilletteMAPaulovichAPomeroySLGolubTRLanderESMesirovJP

2005

Gene set enrichment analysis: a knowledge-based approach for

interpreting genome-wide expression profiles.

Proc Natl Acad Sci U S A

102

15545

15550

29. HarrisonDABinariRNahreiniTSGilmanMPerrimonN

1995

Activation of a Drosophila Janus kinase (JAK) causes

hematopoietic neoplasia and developmental defects.

Embo J

14

2857

2865

30. LuoHHanrattyWPDearolfCR

1995

An amino acid substitution in the Drosophila hopTum-l Jak kinase

causes leukemia-like hematopoietic defects.

Embo J

14

1412

1420

31. ShiSCalhounHCXiaFLiJLeLLiWX

2006

JAK signaling globally counteracts heterochromatic gene

silencing.

Nat Genet

38

1071

1076

32. SweitzerSMCalvoSKrausMHFinbloomDSLarnerAC

1995

Characterization of a Stat-like DNA binding activity in

Drosophila melanogaster.

J Biol Chem

270

16510

16513

33. ShiSLarsonKGuoDLimSJDuttaPYanSJLiWX

2008

Drosophila STAT is required for directly maintaining HP1

localization and heterochromatin stability.

Nat Cell Biol

10

489

496

34. PadgettRWSt JohnstonRDGelbartWM

1987

A transcript from a Drosophila pattern gene predicts a protein

homologous to the transforming growth factor-beta family.

Nature

325

81

84

35. St JohnstonRDGelbartWM

1987

Decapentaplegic transcripts are localized along the

dorsal-ventral axis of the Drosophila embryo.

Embo J

6

2785

2791

36. RayRPAroraKNusslein-VolhardCGelbartWM

1991

The control of cell fate along the dorsal-ventral axis of the

Drosophila embryo.

Development

113

35

54

37. WhartonKARayRPGelbartWM

1993

An activity gradient of decapentaplegic is necessary for the

specification of dorsal pattern elements in the Drosophila

embryo.

Development

117

807

822

38. HuangJDSchwyterDHShirokawaJMCoureyAJ

1993

The interplay between multiple enhancer and silencer elements

defines the pattern of decapentaplegic expression.

Genes Dev

7

694

704

39. Lopez-OnievaLFernandez-MinanAGonzalez-ReyesA

2008

Jak/Stat signalling in niche support cells regulates dpp

transcription to control germline stem cell maintenance in the Drosophila

ovary.

Development

135

533

540

40. WangLLiZCaiY

2008

The JAK/STAT pathway positively regulates DPP signaling in the

Drosophila germline stem cell niche.

J Cell Biol

180

721

728

41. HulskampMPfeifleCTautzD

1990

A morphogenetic gradient of hunchback protein organizes the

expression of the gap genes Kruppel and knirps in the early Drosophila

embryo.

Nature

346

577

580

42. PignoniFBaldarelliRMSteingrimssonEDiazRJPatapoutianAMerriamJRLengyelJA

1990

The Drosophila gene tailless is expressed at the embryonic

termini and is a member of the steroid receptor superfamily.

Cell

62

151

163

43. ParoushZWainwrightSMIsh-HorowiczD

1997

Torso signalling regulates terminal patterning in Drosophila by

antagonising Groucho-mediated repression.

Development

124

3827

3834

44. CarrollSBScottMP

1986

Zygotically active genes that affect the spatial expression of

the fushi tarazu segmentation gene during early Drosophila

embryogenesis.

Cell

45

113

126

45. SeftonLTimmerJRZhangYBerangerFClineTW

2000

An extracellular activator of the Drosophila JAK/STAT pathway is

a sex- determination signal element.

Nature

405

970

973

46. AvilaFWEricksonJW

2007

Drosophila JAK/STAT pathway reveals distinct initiation and

reinforcement steps in early transcription of Sxl.

Curr Biol

17

643

648

47. GilchristDADos SantosGFargoDCXieBGaoYLiLAdelmanK

2010

Pausing of RNA polymerase II disrupts DNA-specified nucleosome

organization to enable precise gene regulation.

Cell

143

540

551

48. ChouTBNollEPerrimonN

1993

Autosomal P[ovoD1] dominant female-sterile insertions

in Drosophila and their use in generating germ-line

chimeras.

Development

119

1359

1369

49. PignoniFSteingrimssonELengyelJA

1992

bicoid and the terminal system activate tailless expression in

the early Drosophila embryo.

Development

115

239

251

50. ChenHWChenXOhSWMarinissenMJGutkindJSHouSX

2002

mom identifies a receptor for the Drosophila JAK/STAT signal

transduction pathway and encodes a protein distantly related to the

mammalian cytokine receptor family.

Genes Dev

16

388

398

51. CapovillaMBrandtMBotasJ

1994

Direct regulation of decapentaplegic by Ultrabithorax and its

role in Drosophila midgut morphogenesis.

Cell

76

461

475

52. ImmergluckKLawrencePABienzM

1990

Induction across germ layers in Drosophila mediated by a genetic

cascade.

Cell

62

261

268

53. PanganibanGEReuterRScottMPHoffmannFM

1990

A Drosophila growth factor homolog, decapentaplegic, regulates

homeotic gene expression within and across germ layers during midgut

morphogenesis.

Development

110

1041

1050

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#