The AKAP Yu is required for olfactory long-term memory formation in Drosophila

Yubing Lu, Yi Sheng Lu, Yichun Shuai, Chunhua Feng, Tim Tully, Zuoping Xie, Yi Zhong, Hai Meng Zhou

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Extensive neurogenetic analysis has shown that memory formation depends critically on cAMP-protein kinase A (PKA) signaling. Details of how this pathway is involved in memory formation, however, remain to be fully elucidated. From a large-scale behavioral screen in Drosophila, we identified the yu mutant to be defective in one-day memory after spaced training. The yu mutation disrupts a gene encoding an A-kinase anchoring protein (AKAP). AKAPs comprise a family of proteins, which determine the subcellular localization of PKAs and thereby critically restrict cAMP signaling within a cell. Further behavioral characterizations revealed that long-term memory (LTM) was disrupted specifically in the yu mutant, whereas learning, short-term memory and anesthesia-resistant memory all appeared normal. Another independently isolated mutation of the yu gene failed to complement the LTM defect associated with the yu mutation, and this phenotypic defect could be rescued by induced acute expression of a yu + transgene, suggesting that yu functions physiologically during memory formation. AKAP Yu is expressed preferentially in the mushroom body (MB) neuroanatomical structure, and expression of a yu + transgene to the MB, but not to other brain regions, is sufficient to rescue the LTM defect of the yu mutant. These observations lead us to conclude that proper localization of PKA by Yu AKAP in MB neurons is required for the formation of LTM.

Original languageEnglish (US)
Pages (from-to)13792-13797
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume104
Issue number34
DOIs
StatePublished - Aug 21 2007

Fingerprint

Long-Term Memory
Protein Kinases
Drosophila
Mushroom Bodies
Cyclic AMP-Dependent Protein Kinases
Transgenes
Mutation
Short-Term Memory
Genes
Anesthesia
Learning
Neurons
Brain
Proteins

Keywords

  • A-kinase anchoring protein
  • Mushroom body
  • Olfactory memory
  • cAMP pathway

ASJC Scopus subject areas

  • General

Cite this

The AKAP Yu is required for olfactory long-term memory formation in Drosophila. / Lu, Yubing; Lu, Yi Sheng; Shuai, Yichun; Feng, Chunhua; Tully, Tim; Xie, Zuoping; Zhong, Yi; Zhou, Hai Meng.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 34, 21.08.2007, p. 13792-13797.

Research output: Contribution to journalArticle

Lu, Yubing ; Lu, Yi Sheng ; Shuai, Yichun ; Feng, Chunhua ; Tully, Tim ; Xie, Zuoping ; Zhong, Yi ; Zhou, Hai Meng. / The AKAP Yu is required for olfactory long-term memory formation in Drosophila. In: Proceedings of the National Academy of Sciences of the United States of America. 2007 ; Vol. 104, No. 34. pp. 13792-13797.
@article{0605e69119784637b33b29e5212cb742,
title = "The AKAP Yu is required for olfactory long-term memory formation in Drosophila",
abstract = "Extensive neurogenetic analysis has shown that memory formation depends critically on cAMP-protein kinase A (PKA) signaling. Details of how this pathway is involved in memory formation, however, remain to be fully elucidated. From a large-scale behavioral screen in Drosophila, we identified the yu mutant to be defective in one-day memory after spaced training. The yu mutation disrupts a gene encoding an A-kinase anchoring protein (AKAP). AKAPs comprise a family of proteins, which determine the subcellular localization of PKAs and thereby critically restrict cAMP signaling within a cell. Further behavioral characterizations revealed that long-term memory (LTM) was disrupted specifically in the yu mutant, whereas learning, short-term memory and anesthesia-resistant memory all appeared normal. Another independently isolated mutation of the yu gene failed to complement the LTM defect associated with the yu mutation, and this phenotypic defect could be rescued by induced acute expression of a yu + transgene, suggesting that yu functions physiologically during memory formation. AKAP Yu is expressed preferentially in the mushroom body (MB) neuroanatomical structure, and expression of a yu + transgene to the MB, but not to other brain regions, is sufficient to rescue the LTM defect of the yu mutant. These observations lead us to conclude that proper localization of PKA by Yu AKAP in MB neurons is required for the formation of LTM.",
keywords = "A-kinase anchoring protein, Mushroom body, Olfactory memory, cAMP pathway",
author = "Yubing Lu and Lu, {Yi Sheng} and Yichun Shuai and Chunhua Feng and Tim Tully and Zuoping Xie and Yi Zhong and Zhou, {Hai Meng}",
year = "2007",
month = "8",
day = "21",
doi = "10.1073/pnas.0700439104",
language = "English (US)",
volume = "104",
pages = "13792--13797",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "34",

}

TY - JOUR

T1 - The AKAP Yu is required for olfactory long-term memory formation in Drosophila

AU - Lu, Yubing

AU - Lu, Yi Sheng

AU - Shuai, Yichun

AU - Feng, Chunhua

AU - Tully, Tim

AU - Xie, Zuoping

AU - Zhong, Yi

AU - Zhou, Hai Meng

PY - 2007/8/21

Y1 - 2007/8/21

N2 - Extensive neurogenetic analysis has shown that memory formation depends critically on cAMP-protein kinase A (PKA) signaling. Details of how this pathway is involved in memory formation, however, remain to be fully elucidated. From a large-scale behavioral screen in Drosophila, we identified the yu mutant to be defective in one-day memory after spaced training. The yu mutation disrupts a gene encoding an A-kinase anchoring protein (AKAP). AKAPs comprise a family of proteins, which determine the subcellular localization of PKAs and thereby critically restrict cAMP signaling within a cell. Further behavioral characterizations revealed that long-term memory (LTM) was disrupted specifically in the yu mutant, whereas learning, short-term memory and anesthesia-resistant memory all appeared normal. Another independently isolated mutation of the yu gene failed to complement the LTM defect associated with the yu mutation, and this phenotypic defect could be rescued by induced acute expression of a yu + transgene, suggesting that yu functions physiologically during memory formation. AKAP Yu is expressed preferentially in the mushroom body (MB) neuroanatomical structure, and expression of a yu + transgene to the MB, but not to other brain regions, is sufficient to rescue the LTM defect of the yu mutant. These observations lead us to conclude that proper localization of PKA by Yu AKAP in MB neurons is required for the formation of LTM.

AB - Extensive neurogenetic analysis has shown that memory formation depends critically on cAMP-protein kinase A (PKA) signaling. Details of how this pathway is involved in memory formation, however, remain to be fully elucidated. From a large-scale behavioral screen in Drosophila, we identified the yu mutant to be defective in one-day memory after spaced training. The yu mutation disrupts a gene encoding an A-kinase anchoring protein (AKAP). AKAPs comprise a family of proteins, which determine the subcellular localization of PKAs and thereby critically restrict cAMP signaling within a cell. Further behavioral characterizations revealed that long-term memory (LTM) was disrupted specifically in the yu mutant, whereas learning, short-term memory and anesthesia-resistant memory all appeared normal. Another independently isolated mutation of the yu gene failed to complement the LTM defect associated with the yu mutation, and this phenotypic defect could be rescued by induced acute expression of a yu + transgene, suggesting that yu functions physiologically during memory formation. AKAP Yu is expressed preferentially in the mushroom body (MB) neuroanatomical structure, and expression of a yu + transgene to the MB, but not to other brain regions, is sufficient to rescue the LTM defect of the yu mutant. These observations lead us to conclude that proper localization of PKA by Yu AKAP in MB neurons is required for the formation of LTM.

KW - A-kinase anchoring protein

KW - Mushroom body

KW - Olfactory memory

KW - cAMP pathway

UR - http://www.scopus.com/inward/record.url?scp=35348852458&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=35348852458&partnerID=8YFLogxK

U2 - 10.1073/pnas.0700439104

DO - 10.1073/pnas.0700439104

M3 - Article

C2 - 17690248

AN - SCOPUS:35348852458

VL - 104

SP - 13792

EP - 13797

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 34

ER -