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Publication

A kinase-dependent feedforward loop affects CREBB stability and long term memory formation.

Pei-Tseng Lee | Guang Lin | Wen-Wen Lin | Fengqiu Diao | Benjamin H White | Hugo J Bellen
eLife | 2018

In Drosophila, long-term memory (LTM) requires the cAMP-dependent transcription factor CREBB, expressed in the mushroom bodies (MB) and phosphorylated by PKA. To identify other kinases required for memory formation, we integrated Trojan exons encoding T2A-GAL4 into genes encoding putative kinases and selected for genes expressed in MB. These lines were screened for learning/memory deficits using UAS-RNAi knockdown based on an olfactory aversive conditioning assay. We identified a novel, conserved kinase, Meng-Po (MP, CG11221, SBK1 in human), the loss of which severely affects 3 hr memory and 24 hr LTM, but not learning. Remarkably, memory is lost upon removal of the MP protein in adult MB but restored upon its reintroduction. Overexpression of MP in MB significantly increases LTM in wild-type flies showing that MP is a limiting factor for LTM. We show that PKA phosphorylates MP and that both proteins synergize in a feedforward loop to control CREBB levels and LTM. key words: Drosophila, Mushroom bodies, SBK1, deGradFP, T2A-GAL4, MiMIC.

Pubmed ID: 29473541

Research resources used in this publication

Additional research tools detected in this publication

Antibodies used in this publication

None found

Associated grants

  • Agency: NIGMS NIH HHS, United States
    Id: R01GM067858
  • Agency: NIH HHS, United States
    Id: P40 OD018537
  • Agency: NICHD NIH HHS, United States
    Id: U54 HD083092
  • Agency: NIGMS NIH HHS, United States
    Id: R01 GM067858
  • Agency: NICHD NIH HHS, United States
    Id: U54HD083092
  • Agency: Howard Hughes Medical Institute, United States

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03144}attP2 (organism)

RRID:BDSC_28717

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03144}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Pkc53E[MI05296] (organism)

RRID:BDSC_42309

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Pkc53E[MI05296] from BDSC.

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y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.GL00313}attP2 (organism)

RRID:BDSC_35393

Drosophila melanogaster with name y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.GL00313}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}PKD[MI09308]/TM3, Sb[1] Ser[1] (organism)

RRID:BDSC_52147

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}PKD[MI09308]/TM3, Sb[1] Ser[1] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Abl[MI00347]/TM6B, Tb[1] (organism)

RRID:BDSC_30964

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Abl[MI00347]/TM6B, Tb[1] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}PKD[MI09308]/TM3, Sb[1] Ser[1] (organism)

RRID:BDSC_52147

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}PKD[MI09308]/TM3, Sb[1] Ser[1] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Abl[MI00347]/TM6B, Tb[1] (organism)

RRID:BDSC_30964

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Abl[MI00347]/TM6B, Tb[1] from BDSC.

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y[1] w[*]; wg[Sp-1]/CyO, P{Wee-P.ph0}Bacc[Wee-P20]; P{y[+t7.7] w[+mC]=20XUAS-6XmCherry-HA}attP2 (organism)

RRID:BDSC_52268

Drosophila melanogaster with name y[1] w[*]; wg[Sp-1]/CyO, P{Wee-P.ph0}Bacc[Wee-P20]; P{y[+t7.7] w[+mC]=20XUAS-6XmCherry-HA}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}CG10702[MI15239] CG17343[MI15239] (organism)

RRID:BDSC_61003

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}CG10702[MI15239] CG17343[MI15239] from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03144}attP2 (organism)

RRID:BDSC_28717

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03144}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}CG44153[MI12160] CG4839[MI12160] (organism)

RRID:BDSC_56728

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}CG44153[MI12160] CG4839[MI12160] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Pvr[MI04181]/SM6a (organism)

RRID:BDSC_37275

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Pvr[MI04181]/SM6a from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}meng[MI03008] (organism)

RRID:BDSC_36177

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}meng[MI03008] from BDSC.

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w[1118]; P{w[+mC]=UAS-mCherry-AMPKalpha}3 (organism)

RRID:BDSC_32182

Drosophila melanogaster with name w[1118]; P{w[+mC]=UAS-mCherry-AMPKalpha}3 from BDSC.

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Pka-C1[H2]/CyO (organism)

RRID:BDSC_4101

Drosophila melanogaster with name Pka-C1[H2]/CyO from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}CG31145[MI00781] (organism)

RRID:BDSC_34108

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}CG31145[MI00781] from BDSC.

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w[*]; sna[Sco]/CyO; P{w[+mC]=tubP-GAL80[ts]}ncd[GAL80ts-7] (organism)

RRID:BDSC_7018

Drosophila melanogaster with name w[*]; sna[Sco]/CyO; P{w[+mC]=tubP-GAL80[ts]}ncd[GAL80ts-7] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}smal[MI06226]/CyO (organism)

RRID:BDSC_40801

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}smal[MI06226]/CyO from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03260}attP2 (organism)

RRID:BDSC_29581

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03260}attP2 from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03282}attP2 (organism)

RRID:BDSC_29603

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF03282}attP2 from BDSC.

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w[*]; P{w[+mC]=tubP-GAL80[ts]}20; TM2/TM6B, Tb[1] (organism)

RRID:BDSC_7019

Drosophila melanogaster with name w[*]; P{w[+mC]=tubP-GAL80[ts]}20; TM2/TM6B, Tb[1] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}PAN3[MI06674] (organism)

RRID:BDSC_41454

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}PAN3[MI06674] from BDSC.

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w[*]; P{w[+m*]=Mef2-GAL4.247}3 (organism)

RRID:BDSC_50742

Drosophila melanogaster with name w[*]; P{w[+m*]=Mef2-GAL4.247}3 from BDSC.

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P{y[+mDint2]=Crey}1b, y[1] M{vas-int.Dm}ZH-2A w[*] (organism)

RRID:BDSC_60299

Drosophila melanogaster with name P{y[+mDint2]=Crey}1b, y[1] M{vas-int.Dm}ZH-2A w[*] from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.HMS02330}attP40 (organism)

RRID:BDSC_41933

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.HMS02330}attP40 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Strn-Mlck[MI00830] (organism)

RRID:BDSC_33089

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Strn-Mlck[MI00830] from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.HMS02330}attP40 (organism)

RRID:BDSC_41933

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.HMS02330}attP40 from BDSC.

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y[1] w[*] Mi{y[+mDint2]=MIC}Pkcdelta[MI09597] (organism)

RRID:BDSC_54501

Drosophila melanogaster with name y[1] w[*] Mi{y[+mDint2]=MIC}Pkcdelta[MI09597] from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF02960}attP2 (organism)

RRID:BDSC_28325

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF02960}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Dyrk2[MI12124] (organism)

RRID:BDSC_56850

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Dyrk2[MI12124] from BDSC.

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w[*]; P{w[+mC]=UAS-FLP.D}JD2 (organism)

RRID:BDSC_4540

Drosophila melanogaster with name w[*]; P{w[+mC]=UAS-FLP.D}JD2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Pkc53E[MI05296] (organism)

RRID:BDSC_42309

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Pkc53E[MI05296] from BDSC.

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Pka-C1[B10] (organism)

RRID:BDSC_32018

Drosophila melanogaster with name Pka-C1[B10] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}CG10702[MI15239] CG17343[MI15239] (organism)

RRID:BDSC_61003

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}CG10702[MI15239] CG17343[MI15239] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Gprk2[MI01907] (organism)

RRID:BDSC_35954

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Gprk2[MI01907] from BDSC.

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y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.GL00313}attP2 (organism)

RRID:BDSC_35393

Drosophila melanogaster with name y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.GL00313}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Strn-Mlck[MI00830] (organism)

RRID:BDSC_33089

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Strn-Mlck[MI00830] from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}Mekk1[MI05281] (organism)

RRID:BDSC_41489

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}Mekk1[MI05281] from BDSC.

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y[1] w[*]; wg[Sp-1]/CyO; P{w[+mC]=lox(Trojan-GAL4)x3}11 (organism)

RRID:BDSC_60311

Drosophila melanogaster with name y[1] w[*]; wg[Sp-1]/CyO; P{w[+mC]=lox(Trojan-GAL4)x3}11 from BDSC.

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y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF01799}attP2 (organism)

RRID:BDSC_25793

Drosophila melanogaster with name y[1] v[1]; P{y[+t7.7] v[+t1.8]=TRiP.JF01799}attP2 from BDSC.

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y[1] w[*]; Mi{y[+mDint2]=MIC}PAN3[MI06674] (organism)

RRID:BDSC_41454

Drosophila melanogaster with name y[1] w[*]; Mi{y[+mDint2]=MIC}PAN3[MI06674] from BDSC.

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y[1] w[*]; P{w[+mC]=lox(Trojan-GAL4)x3}10; Dr[1]/TM3, Sb[1] Ser[1] (organism)

RRID:BDSC_60310

Drosophila melanogaster with name y[1] w[*]; P{w[+mC]=lox(Trojan-GAL4)x3}10; Dr[1]/TM3, Sb[1] Ser[1] from BDSC.

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About

The Stimulating Peripheral Activity to Relieve Conditions (SPARC) effort is the result of National Institutes of Health’s (NIH) drive to map out the neural circuitry responsible for visceral control in higher vertebrates. The SPARC Anatomy Working Group (SAWG) is responsible for the integrity of anatomical knowledge in SPARC

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Maryann Martone, Ph.D.

Department of Neurosciences, School of Medicine

University of California, San Diego

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