Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)

Cristina Salmeron; Daniel Garcia de la Serrana Castillo; Vanesa Jimenez-Amilburu; Ramon Fontanillas; Isabel Navarro; Ian A. Johnston; Joaquim Gutierrez; Encarnacion Capilla

doi:10.1371/journal.pone.0075349

Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)

Cristina Salmeron, Daniel Garcia de la Serrana Castillo, Vanesa Jimenez-Amilburu, Ramon Fontanillas, Isabel Navarro, Ian A. Johnston, Joaquim Gutierrez, Encarnacion Capilla^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Calpains are non-lysosomal calcium-activated neutral proteases involved in a wide range of cellular processes including muscle proteolysis linked to post-mortem flesh softening. The aims of this study were (a) to characterise several members of the calpain system in gilthead sea bream and (b) to examine their expression in relation to nutritional status and muscle tenderisation. We identified the complete open reading frame of gilthead sea bream calpains1-3, sacapn1, sacapn2, sacapn3, and two paralogs of the calpain small subunit1, sacapns1a and sacapns1b. Proteins showed 63-90% sequence identity compared with sequences from mammals and other teleost fishes, and the characteristic domain structure of vertebrate calpains. Transcripts of sacapn1, sacapn2, sacapns1a and sacapns1b had a wide tissue distribution, whereas sacapn3 was almost exclusively detected in skeletal muscle. Next, we assessed transcript expression in skeletal muscle following alteration of nutritional status by (a) fasting and re-feeding or (b) feeding four experimental diets with different carbohydrate-to-protein ratios. Fasting significantly reduced plasma glucose and increased free fatty acids and triglycerides, together with a significant increase in sacapns1b expression. Following 7 days of re-feeding, plasma parameters returned to fed values and sacapn1, sacapn2, sacapns1a and sacapns1b expression was significantly reduced. Furthermore, an increase in dietary carbohydrate content (11 to 39%) diminished growth but increased muscle texture, which showed a significant correlation with decreased sacapn1 and sacapns1a expression, whilst the other calpains remained unaffected. This study has demonstrated that calpain expression is modulated by nutritional status and diet composition in gilthead sea bream, and that the expression of several calpain members is correlated with muscle texture, indicating their potential use as molecular markers for flesh quality in aquaculture production.

Original language	English
Article number	e75349
Number of pages	15
Journal	PLoS ONE
Volume	8
Issue number	9
DOIs	https://doi.org/10.1371/journal.pone.0075349
Publication status	Published - 25 Sept 2013

Keywords

Trout oncorhynchus-mykiss
Calcium-dependent protease
Bass dicentrarchus-labrax
Muscle-specific calpain
Skeletal-muscle
Atlantic salmon
Growth dynamics
Myofibril fragmentation
Longissimus muscle
Messenger-RNA

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Johnston_2013_PLOSone_Characterisation
Copyright: © 2013 Salmerón et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/4.0/
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Salmeron, C., Garcia de la Serrana Castillo, D., Jimenez-Amilburu, V., Fontanillas, R., Navarro, I., Johnston, I. A., Gutierrez, J., & Capilla, E. (2013). Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata). PLoS ONE, 8(9), Article e75349. https://doi.org/10.1371/journal.pone.0075349

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title = "Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)",

abstract = "Calpains are non-lysosomal calcium-activated neutral proteases involved in a wide range of cellular processes including muscle proteolysis linked to post-mortem flesh softening. The aims of this study were (a) to characterise several members of the calpain system in gilthead sea bream and (b) to examine their expression in relation to nutritional status and muscle tenderisation. We identified the complete open reading frame of gilthead sea bream calpains1-3, sacapn1, sacapn2, sacapn3, and two paralogs of the calpain small subunit1, sacapns1a and sacapns1b. Proteins showed 63-90% sequence identity compared with sequences from mammals and other teleost fishes, and the characteristic domain structure of vertebrate calpains. Transcripts of sacapn1, sacapn2, sacapns1a and sacapns1b had a wide tissue distribution, whereas sacapn3 was almost exclusively detected in skeletal muscle. Next, we assessed transcript expression in skeletal muscle following alteration of nutritional status by (a) fasting and re-feeding or (b) feeding four experimental diets with different carbohydrate-to-protein ratios. Fasting significantly reduced plasma glucose and increased free fatty acids and triglycerides, together with a significant increase in sacapns1b expression. Following 7 days of re-feeding, plasma parameters returned to fed values and sacapn1, sacapn2, sacapns1a and sacapns1b expression was significantly reduced. Furthermore, an increase in dietary carbohydrate content (11 to 39%) diminished growth but increased muscle texture, which showed a significant correlation with decreased sacapn1 and sacapns1a expression, whilst the other calpains remained unaffected. This study has demonstrated that calpain expression is modulated by nutritional status and diet composition in gilthead sea bream, and that the expression of several calpain members is correlated with muscle texture, indicating their potential use as molecular markers for flesh quality in aquaculture production.",

keywords = "Trout oncorhynchus-mykiss, Calcium-dependent protease, Bass dicentrarchus-labrax, Muscle-specific calpain, Skeletal-muscle, Atlantic salmon, Growth dynamics, Myofibril fragmentation, Longissimus muscle, Messenger-RNA",

author = "Cristina Salmeron and {Garcia de la Serrana Castillo}, Daniel and Vanesa Jimenez-Amilburu and Ramon Fontanillas and Isabel Navarro and Johnston, {Ian A.} and Joaquim Gutierrez and Encarnacion Capilla",

note = "EC is a Ram{\'o}n y Cajal researcher fellow from the “Ministerio de Ciencia e Innovaci” (MICINN). This work was supported by funds from the MICINN (AGL2009-12427 and AGL2010-17324), the Catalonian Government (2009SGR-00402) and the “Xarxa de Refer{\`e}ncia d{\textquoteright}R+D+I en Aq{\"u}icultura” and the European Union through the project LIFECYCLE (FP7-222719). ",

year = "2013",

month = sep,

day = "25",

doi = "10.1371/journal.pone.0075349",

language = "English",

volume = "8",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "9",

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Salmeron, C, Garcia de la Serrana Castillo, D, Jimenez-Amilburu, V, Fontanillas, R, Navarro, I, Johnston, IA, Gutierrez, J & Capilla, E 2013, 'Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)', PLoS ONE, vol. 8, no. 9, e75349. https://doi.org/10.1371/journal.pone.0075349

Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata). / Salmeron, Cristina; Garcia de la Serrana Castillo, Daniel; Jimenez-Amilburu, Vanesa et al.
In: PLoS ONE, Vol. 8, No. 9, e75349, 25.09.2013.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)

AU - Salmeron, Cristina

AU - Garcia de la Serrana Castillo, Daniel

AU - Jimenez-Amilburu, Vanesa

AU - Fontanillas, Ramon

AU - Navarro, Isabel

AU - Johnston, Ian A.

AU - Gutierrez, Joaquim

AU - Capilla, Encarnacion

N1 - EC is a Ramón y Cajal researcher fellow from the “Ministerio de Ciencia e Innovaci” (MICINN). This work was supported by funds from the MICINN (AGL2009-12427 and AGL2010-17324), the Catalonian Government (2009SGR-00402) and the “Xarxa de Referència d’R+D+I en Aqüicultura” and the European Union through the project LIFECYCLE (FP7-222719).

PY - 2013/9/25

Y1 - 2013/9/25

N2 - Calpains are non-lysosomal calcium-activated neutral proteases involved in a wide range of cellular processes including muscle proteolysis linked to post-mortem flesh softening. The aims of this study were (a) to characterise several members of the calpain system in gilthead sea bream and (b) to examine their expression in relation to nutritional status and muscle tenderisation. We identified the complete open reading frame of gilthead sea bream calpains1-3, sacapn1, sacapn2, sacapn3, and two paralogs of the calpain small subunit1, sacapns1a and sacapns1b. Proteins showed 63-90% sequence identity compared with sequences from mammals and other teleost fishes, and the characteristic domain structure of vertebrate calpains. Transcripts of sacapn1, sacapn2, sacapns1a and sacapns1b had a wide tissue distribution, whereas sacapn3 was almost exclusively detected in skeletal muscle. Next, we assessed transcript expression in skeletal muscle following alteration of nutritional status by (a) fasting and re-feeding or (b) feeding four experimental diets with different carbohydrate-to-protein ratios. Fasting significantly reduced plasma glucose and increased free fatty acids and triglycerides, together with a significant increase in sacapns1b expression. Following 7 days of re-feeding, plasma parameters returned to fed values and sacapn1, sacapn2, sacapns1a and sacapns1b expression was significantly reduced. Furthermore, an increase in dietary carbohydrate content (11 to 39%) diminished growth but increased muscle texture, which showed a significant correlation with decreased sacapn1 and sacapns1a expression, whilst the other calpains remained unaffected. This study has demonstrated that calpain expression is modulated by nutritional status and diet composition in gilthead sea bream, and that the expression of several calpain members is correlated with muscle texture, indicating their potential use as molecular markers for flesh quality in aquaculture production.

AB - Calpains are non-lysosomal calcium-activated neutral proteases involved in a wide range of cellular processes including muscle proteolysis linked to post-mortem flesh softening. The aims of this study were (a) to characterise several members of the calpain system in gilthead sea bream and (b) to examine their expression in relation to nutritional status and muscle tenderisation. We identified the complete open reading frame of gilthead sea bream calpains1-3, sacapn1, sacapn2, sacapn3, and two paralogs of the calpain small subunit1, sacapns1a and sacapns1b. Proteins showed 63-90% sequence identity compared with sequences from mammals and other teleost fishes, and the characteristic domain structure of vertebrate calpains. Transcripts of sacapn1, sacapn2, sacapns1a and sacapns1b had a wide tissue distribution, whereas sacapn3 was almost exclusively detected in skeletal muscle. Next, we assessed transcript expression in skeletal muscle following alteration of nutritional status by (a) fasting and re-feeding or (b) feeding four experimental diets with different carbohydrate-to-protein ratios. Fasting significantly reduced plasma glucose and increased free fatty acids and triglycerides, together with a significant increase in sacapns1b expression. Following 7 days of re-feeding, plasma parameters returned to fed values and sacapn1, sacapn2, sacapns1a and sacapns1b expression was significantly reduced. Furthermore, an increase in dietary carbohydrate content (11 to 39%) diminished growth but increased muscle texture, which showed a significant correlation with decreased sacapn1 and sacapns1a expression, whilst the other calpains remained unaffected. This study has demonstrated that calpain expression is modulated by nutritional status and diet composition in gilthead sea bream, and that the expression of several calpain members is correlated with muscle texture, indicating their potential use as molecular markers for flesh quality in aquaculture production.

KW - Trout oncorhynchus-mykiss

KW - Calcium-dependent protease

KW - Bass dicentrarchus-labrax

KW - Muscle-specific calpain

KW - Skeletal-muscle

KW - Atlantic salmon

KW - Growth dynamics

KW - Myofibril fragmentation

KW - Longissimus muscle

KW - Messenger-RNA

U2 - 10.1371/journal.pone.0075349

DO - 10.1371/journal.pone.0075349

M3 - Article

SN - 1932-6203

VL - 8

JO - PLoS ONE

JF - PLoS ONE

IS - 9

M1 - e75349

ER -

Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream (Sparus aurata)

Abstract

Keywords

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