Susceptibility to heat stress and aberrant gene expression patterns in holocarboxylase synthetase-deficient Drosophila melanogaster are caused by decreased biotinylation of histones, not of carboxylases

Gabriela Camporeale, Janos Zempleni, Joel C. Eissenberg

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30 Citations (Scopus)

Abstract

Previously, we discovered that holocarboxylase synthetase (HCS) is a chromatin-associated protein in Drosophila melanogaster and that HCS deficiency alters chromatin structure and gene expression patterns, leading to decreased heat tolerance. The effects of HCS deficiency were attributed to decreased biotinylation of histones. However, HCS is known to mediate biotinylation of carboxylases in cytoplasm and mitochondria in addition to mediating biotinylation of histones. A challenge posed by the genetic analysis of HCS is to distinguish between the effects of decreased biotinylation of carboxylases from the effects of decreased histone biotinylation in the gene expression patterns and phenotypes observed in HCS-deficient flies. Here, we tested whether 3-methylcrotonyl-CoA carboxylase (MCC) mutant flies exhibit gene expression patterns and heat susceptibility similar to that in HCS-deficient Drosophila. Biotin transporter [sodium-dependent multivitamin transporter (SMVT)] mutants were used to investigate effects of cellular biotin depletion on gene expression and heat susceptibility. Deficiencies of MCC and SMVT in mutant flies were confirmed by real-time PCR, streptavidin blotting of holocarboxylases, and analysis of MCC activities; expression of HCS and biotinylation of histones were not altered in MCC and SMVT mutants. Gene expression patterns in MCC and SMVT mutants were different from that seen with HCS-deficient flies, as judged by the abundance of mRNA coding for defective chorion 1, chitin-binding peritrophin-A, dopamine receptor 2, and yolk protein 2. MCC mutants exhibited increased resistance to heat stress compared with wild-type flies. We conclude that gene expression patterns and phenotypes in HCS-deficient flies in previous studies are caused by decreased biotinylation of histones rather than MCC.

Original languageEnglish (US)
Pages (from-to)885-889
Number of pages5
JournalJournal of Nutrition
Volume137
Issue number4
StatePublished - Apr 1 2007

Fingerprint

methylcrotonoyl-CoA carboxylase
biotinylation
Biotinylation
Drosophila melanogaster
ligases
histones
Histones
heat stress
Hot Temperature
Diptera
Gene Expression
gene expression
Holocarboxylase Synthetase Deficiency
transporters
Sodium
mutants
sodium
Chromatin
biotin
chromatin

ASJC Scopus subject areas

  • Medicine (miscellaneous)
  • Nutrition and Dietetics

Cite this

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title = "Susceptibility to heat stress and aberrant gene expression patterns in holocarboxylase synthetase-deficient Drosophila melanogaster are caused by decreased biotinylation of histones, not of carboxylases",
abstract = "Previously, we discovered that holocarboxylase synthetase (HCS) is a chromatin-associated protein in Drosophila melanogaster and that HCS deficiency alters chromatin structure and gene expression patterns, leading to decreased heat tolerance. The effects of HCS deficiency were attributed to decreased biotinylation of histones. However, HCS is known to mediate biotinylation of carboxylases in cytoplasm and mitochondria in addition to mediating biotinylation of histones. A challenge posed by the genetic analysis of HCS is to distinguish between the effects of decreased biotinylation of carboxylases from the effects of decreased histone biotinylation in the gene expression patterns and phenotypes observed in HCS-deficient flies. Here, we tested whether 3-methylcrotonyl-CoA carboxylase (MCC) mutant flies exhibit gene expression patterns and heat susceptibility similar to that in HCS-deficient Drosophila. Biotin transporter [sodium-dependent multivitamin transporter (SMVT)] mutants were used to investigate effects of cellular biotin depletion on gene expression and heat susceptibility. Deficiencies of MCC and SMVT in mutant flies were confirmed by real-time PCR, streptavidin blotting of holocarboxylases, and analysis of MCC activities; expression of HCS and biotinylation of histones were not altered in MCC and SMVT mutants. Gene expression patterns in MCC and SMVT mutants were different from that seen with HCS-deficient flies, as judged by the abundance of mRNA coding for defective chorion 1, chitin-binding peritrophin-A, dopamine receptor 2, and yolk protein 2. MCC mutants exhibited increased resistance to heat stress compared with wild-type flies. We conclude that gene expression patterns and phenotypes in HCS-deficient flies in previous studies are caused by decreased biotinylation of histones rather than MCC.",
author = "Gabriela Camporeale and Janos Zempleni and Eissenberg, {Joel C.}",
year = "2007",
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language = "English (US)",
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TY - JOUR

T1 - Susceptibility to heat stress and aberrant gene expression patterns in holocarboxylase synthetase-deficient Drosophila melanogaster are caused by decreased biotinylation of histones, not of carboxylases

AU - Camporeale, Gabriela

AU - Zempleni, Janos

AU - Eissenberg, Joel C.

PY - 2007/4/1

Y1 - 2007/4/1

N2 - Previously, we discovered that holocarboxylase synthetase (HCS) is a chromatin-associated protein in Drosophila melanogaster and that HCS deficiency alters chromatin structure and gene expression patterns, leading to decreased heat tolerance. The effects of HCS deficiency were attributed to decreased biotinylation of histones. However, HCS is known to mediate biotinylation of carboxylases in cytoplasm and mitochondria in addition to mediating biotinylation of histones. A challenge posed by the genetic analysis of HCS is to distinguish between the effects of decreased biotinylation of carboxylases from the effects of decreased histone biotinylation in the gene expression patterns and phenotypes observed in HCS-deficient flies. Here, we tested whether 3-methylcrotonyl-CoA carboxylase (MCC) mutant flies exhibit gene expression patterns and heat susceptibility similar to that in HCS-deficient Drosophila. Biotin transporter [sodium-dependent multivitamin transporter (SMVT)] mutants were used to investigate effects of cellular biotin depletion on gene expression and heat susceptibility. Deficiencies of MCC and SMVT in mutant flies were confirmed by real-time PCR, streptavidin blotting of holocarboxylases, and analysis of MCC activities; expression of HCS and biotinylation of histones were not altered in MCC and SMVT mutants. Gene expression patterns in MCC and SMVT mutants were different from that seen with HCS-deficient flies, as judged by the abundance of mRNA coding for defective chorion 1, chitin-binding peritrophin-A, dopamine receptor 2, and yolk protein 2. MCC mutants exhibited increased resistance to heat stress compared with wild-type flies. We conclude that gene expression patterns and phenotypes in HCS-deficient flies in previous studies are caused by decreased biotinylation of histones rather than MCC.

AB - Previously, we discovered that holocarboxylase synthetase (HCS) is a chromatin-associated protein in Drosophila melanogaster and that HCS deficiency alters chromatin structure and gene expression patterns, leading to decreased heat tolerance. The effects of HCS deficiency were attributed to decreased biotinylation of histones. However, HCS is known to mediate biotinylation of carboxylases in cytoplasm and mitochondria in addition to mediating biotinylation of histones. A challenge posed by the genetic analysis of HCS is to distinguish between the effects of decreased biotinylation of carboxylases from the effects of decreased histone biotinylation in the gene expression patterns and phenotypes observed in HCS-deficient flies. Here, we tested whether 3-methylcrotonyl-CoA carboxylase (MCC) mutant flies exhibit gene expression patterns and heat susceptibility similar to that in HCS-deficient Drosophila. Biotin transporter [sodium-dependent multivitamin transporter (SMVT)] mutants were used to investigate effects of cellular biotin depletion on gene expression and heat susceptibility. Deficiencies of MCC and SMVT in mutant flies were confirmed by real-time PCR, streptavidin blotting of holocarboxylases, and analysis of MCC activities; expression of HCS and biotinylation of histones were not altered in MCC and SMVT mutants. Gene expression patterns in MCC and SMVT mutants were different from that seen with HCS-deficient flies, as judged by the abundance of mRNA coding for defective chorion 1, chitin-binding peritrophin-A, dopamine receptor 2, and yolk protein 2. MCC mutants exhibited increased resistance to heat stress compared with wild-type flies. We conclude that gene expression patterns and phenotypes in HCS-deficient flies in previous studies are caused by decreased biotinylation of histones rather than MCC.

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