Parvalbumin isotypes in white muscle from three teleost fish: Characterization and their expression during development

doi:10.1016/0305-0491(95)02066-7

Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology

Volume 113, Issue 3, March 1996, Pages 475-484

https://doi.org/10.1016/0305-0491(95)02066-7 Get rights and content

Abstract

Parvalbumin isotypes were isolated by chromatography from trunk white muscle of rainbow trout (Oncorhynchus mykiss W.), brown trout (Salmo trutta L.), and sea bass (Dicentrarchus labrax L.). Five, four and two components were respectively purified and physico-chemically characterized. Expression of the various isotypes was followed in the course of the fish development and, in adult fish, from the anterior to the posterior myotomes. Isotype distribution varies both chronologically and spatially. In trout, parvalbumins occur around hatching; as the fish develop, transitions occur in isotype expression, PA II appearing as the predominant larval form and PA III, IV, or V as the main adult form, as previously observed in Barbus barbus (L.). In the sea bass, the developmental expression pattern is more unexpected: the synthesis of both isotypes (PA II and PA V) is delayed and the larval form PA II remains the principal isotype in adult fish. These observations indicate that the polymorphism of parvalbumins in fish constitutes a subtle mechanism modulating the speed and power of muscle contraction. Our results support the view that each isotype plays a specific role in relation to the muscle activity required in fish at a given developmental stage or a given trunk level in the adult.

References (26)

M.M. Bradford
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Analyt. Biochem.
(1976)
I. Dubois et al.
Soluble calcium-binding proteins: parvalbumins and calmodulin from eel skeletal muscle
Comp. Biochem. Physiol.
(1990)
G.L. Ellman
Tissue sulfhydryl groups
Arch. Biochem. Biophys.
(1959)
A.F.S.A. Habeeb
A sensitive method for localization of disulfide containing peptides in column effluents
Analyt. Biochem.
(1973)
F. Huriaux et al.
Electrophoretic comparison of myosin light chains and parvalbumins of trunk and head muscles from two barbel (Barbus barbus) populations
Comp. Biochem. Physiol
(1990)
L.M. Schwartz et al.
Differential expression of the Ca²⁺-binding protein parvalbumin during myogenesis in Xenopus laevis
Devel. Biol.
(1988)
W.W. Ballard
Normal embryonic stages for salmonid fishes, based on Salmo gairdneri Richardson and Salvelinus fontinalis (Mitchill)
J. Exp. Zool.
(1973)
M.R. Celio et al.
Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres
Nature
(1982)
B. Focant et al.
Myosin, parvalbumin and myofibril expression in barbel (Barbus barbus L.) lateral white muscle during development
Fish Physiol. Biochem.
(1992)
B. Focant et al.
Electrophoretic comparison of the proteins of some perch (Perca fluviatilis L.) head muscles
J. Muscle Res. Cell Motil.
(1981)

B. Focant et al.

Parvalbumin and myosin expression in the teleost Dicentrarchus labrax (L.) white muscle during development

Rapp. Comm. Int. Mer Médit.

(1995)

B. Focant et al.

Biochemical analysis of parvalbumins and myosin light chains from Mediterranean Serranids: first application to the systematic

Rapp. Comm. Int. Mer Médit

(1988)

C. Gerday

Soluble calcium-binding proteins from fish and invertebrate muscle

Molec. Physiol.

(1982)

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Parvalbumin expression in trout swimming muscle correlates with relaxation rate
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Rainbow trout (Oncorhynchus mykiss) display longitudinal and developmental shifts in muscle relaxation rate. This study aimed to determine the role of variations in parvalbumin content in modulating muscle relaxation. Parvalbumin is a low molecular weight protein that buffers myoplasmic Ca²⁺ and enhances muscle relaxation. In some fish, longitudinal variations in muscle relaxation have been linked to variations in the total amount of parvalbumin present in muscle and in the relative expression of two parvalbumin isoforms. We have demonstrated previously that anterior slow-twitch or red myotomal muscle relaxes more rapidly than that from the posterior for both rainbow and brook trout. Further, younger rainbow trout parr have faster red muscle relaxation rates than older smolts. Here we report similar results for fast-twitch or white muscle. We quantified the parvalbumin expression in red and white muscle from different body positions of rainbow trout parr and smolts and for brook trout (Salvelinus fontinalis) adults. There was a significant shift in total parvalbumin content of muscle: the faster muscle from the anterior myotome contained greater amounts of parvalbumin. For brook trout, longitudinal variation in relaxation rate was also associated with shifts in the relative expression of the two parvalbumin isoforms. The faster muscle of parr contained more parvalbumin. Lastly, trout white muscle tended to have higher levels of parvalbumin and greater levels of the Parv2 (relative to Parv1) isoform as compared to red muscle. Parvalbumin expression correlated with muscle relaxation rate in trout, although there were species-specific differences in the importance of altering total parvalbumin content versus shifts in relative parvalbumin isoform expression.
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^☆: This work was supported by research grant 3.4514.93 from the Belgian Fonds de la Recherche Scientifique Médicale and collaborative research grant 870447 from NATO. P. V. and B. F. are Research Associate of the Fonds National de la Recherche Scientifique of Belgium.

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Parvalbumin isotypes in white muscle from three teleost fish: Characterization and their expression during development☆

Abstract

Analyt. Biochem.

Comp. Biochem. Physiol.

Arch. Biochem. Biophys.

Analyt. Biochem.

Comp. Biochem. Physiol

Devel. Biol.

Normal embryonic stages for salmonid fishes, based on Salmo gairdneri Richardson and Salvelinus fontinalis (Mitchill)

J. Exp. Zool.

Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres

Nature

Myosin, parvalbumin and myofibril expression in barbel (Barbus barbus L.) lateral white muscle during development

Fish Physiol. Biochem.

Electrophoretic comparison of the proteins of some perch (Perca fluviatilis L.) head muscles