Troponin C in different insect muscle types: Identification of two isoforms in Lethocerus, Drosophila and Anopheles that are specific to asynchronous flight muscle in the adult insect

Feng Qiu, Anne Lakey, Bogos Agianian, Amanda Hutchings, Geoffrey W. Butcher, Siegfried Labeit, Kevin Leonard, Belinda Bullard

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

The indirect flight muscles (IFMs) of Lethocerus (giant water bug) and Drosophila (fruitfly) are asynchronous: oscillatory contractions are produced by periodic stretches in the presence of a Ca 2+ concentration that does not fully activate the muscle. The troponin complex on thin filaments regulates contraction in striated muscle. The complex in IFM has subunits that are specific to this muscle type, and stretch activation may act through troponin. Lethocerus and Drosophila have an unusual isoform of the Ca 2+-binding subunit of troponin, troponin C (TnC), with a single Ca 2+-binding site near the C-terminus (domain IV); this isoform is only in IFMs, together with a minor isoform with an additional Ca 2+-binding site in the N-terminal region (domain II). Lethocerus has another TnC isoform in leg muscle which also has two Ca 2+-binding sites. Ca 2+ binds more strongly to domain IV than to domain II in two-site isoforms. There are four isoforms in Drosophila and Anopheles (malarial mosquito), three of which are also in adult Lethocerus. A larval isoform has not been identified in Lethocerus. Different TnC isoforms are expressed in the embryonic, larval, pupal and adult stages of Drosophila; the expression of the two IFM isoforms is increased in the pupal stage. Immunoelectron microscopy shows the distribution of the major IFM isoform with one Ca 2+-binding site is uniform along Lethocerus thin filaments. We suggest that initial activation of IFM is by Ca 2+ binding to troponin with the two-site TnC, and full activation is through the action of stretch on the complex with the one-site isoform.

Original languageEnglish (US)
Pages (from-to)811-821
Number of pages11
JournalBiochemical Journal
Volume371
Issue number3
DOIs
StatePublished - May 1 2003
Externally publishedYes

Fingerprint

Troponin C
Anopheles
Drosophila
Insects
Muscle
Protein Isoforms
Muscles
Troponin
Binding Sites
Chemical activation
Striated Muscle
Immunoelectron Microscopy
Culicidae
Leg
Microscopic examination

Keywords

  • Ca binding
  • EF hand
  • Insect flight
  • Phylogeny
  • Stretch activation

ASJC Scopus subject areas

  • Biochemistry

Cite this

Troponin C in different insect muscle types : Identification of two isoforms in Lethocerus, Drosophila and Anopheles that are specific to asynchronous flight muscle in the adult insect. / Qiu, Feng; Lakey, Anne; Agianian, Bogos; Hutchings, Amanda; Butcher, Geoffrey W.; Labeit, Siegfried; Leonard, Kevin; Bullard, Belinda.

In: Biochemical Journal, Vol. 371, No. 3, 01.05.2003, p. 811-821.

Research output: Contribution to journalArticle

Qiu, Feng ; Lakey, Anne ; Agianian, Bogos ; Hutchings, Amanda ; Butcher, Geoffrey W. ; Labeit, Siegfried ; Leonard, Kevin ; Bullard, Belinda. / Troponin C in different insect muscle types : Identification of two isoforms in Lethocerus, Drosophila and Anopheles that are specific to asynchronous flight muscle in the adult insect. In: Biochemical Journal. 2003 ; Vol. 371, No. 3. pp. 811-821.
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abstract = "The indirect flight muscles (IFMs) of Lethocerus (giant water bug) and Drosophila (fruitfly) are asynchronous: oscillatory contractions are produced by periodic stretches in the presence of a Ca 2+ concentration that does not fully activate the muscle. The troponin complex on thin filaments regulates contraction in striated muscle. The complex in IFM has subunits that are specific to this muscle type, and stretch activation may act through troponin. Lethocerus and Drosophila have an unusual isoform of the Ca 2+-binding subunit of troponin, troponin C (TnC), with a single Ca 2+-binding site near the C-terminus (domain IV); this isoform is only in IFMs, together with a minor isoform with an additional Ca 2+-binding site in the N-terminal region (domain II). Lethocerus has another TnC isoform in leg muscle which also has two Ca 2+-binding sites. Ca 2+ binds more strongly to domain IV than to domain II in two-site isoforms. There are four isoforms in Drosophila and Anopheles (malarial mosquito), three of which are also in adult Lethocerus. A larval isoform has not been identified in Lethocerus. Different TnC isoforms are expressed in the embryonic, larval, pupal and adult stages of Drosophila; the expression of the two IFM isoforms is increased in the pupal stage. Immunoelectron microscopy shows the distribution of the major IFM isoform with one Ca 2+-binding site is uniform along Lethocerus thin filaments. We suggest that initial activation of IFM is by Ca 2+ binding to troponin with the two-site TnC, and full activation is through the action of stretch on the complex with the one-site isoform.",
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AB - The indirect flight muscles (IFMs) of Lethocerus (giant water bug) and Drosophila (fruitfly) are asynchronous: oscillatory contractions are produced by periodic stretches in the presence of a Ca 2+ concentration that does not fully activate the muscle. The troponin complex on thin filaments regulates contraction in striated muscle. The complex in IFM has subunits that are specific to this muscle type, and stretch activation may act through troponin. Lethocerus and Drosophila have an unusual isoform of the Ca 2+-binding subunit of troponin, troponin C (TnC), with a single Ca 2+-binding site near the C-terminus (domain IV); this isoform is only in IFMs, together with a minor isoform with an additional Ca 2+-binding site in the N-terminal region (domain II). Lethocerus has another TnC isoform in leg muscle which also has two Ca 2+-binding sites. Ca 2+ binds more strongly to domain IV than to domain II in two-site isoforms. There are four isoforms in Drosophila and Anopheles (malarial mosquito), three of which are also in adult Lethocerus. A larval isoform has not been identified in Lethocerus. Different TnC isoforms are expressed in the embryonic, larval, pupal and adult stages of Drosophila; the expression of the two IFM isoforms is increased in the pupal stage. Immunoelectron microscopy shows the distribution of the major IFM isoform with one Ca 2+-binding site is uniform along Lethocerus thin filaments. We suggest that initial activation of IFM is by Ca 2+ binding to troponin with the two-site TnC, and full activation is through the action of stretch on the complex with the one-site isoform.

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