高氧气调包装贮藏牛排肉色稳定性的蛋白质组学
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摘要
为进一步了解高氧气调包装牛排贮藏过程中肉色稳定性变化的机理,本研究比较了腰背最长肌牛排在各贮藏时间点(0、5、10、15 d)的肉色指标变化以及蛋白质组学变化。结果发现高氧气调包装牛排的肉色稳定性随贮藏时间延长不断降低,这可能是贮藏期间牛排的高铁肌红蛋白还原能力和氧气消耗率显著下降所致;通过蛋白质组学分析,共发现了20个在贮藏过程中发生显著变化的差异蛋白,其中有15个蛋白与肉色密切相关,它们主要是一些参与糖酵解和能量代谢的酶类(丙酮酸激酶、3-磷酸甘油醛脱氢酶、果糖-二磷酸醛缩酶、果糖-1,6-二磷酸酶同工酶2、苹果酸脱氢酶和黄素还原酶),这些代谢酶的表达量随贮藏时间延长发生了不同程度的下调,减少了烟酰胺腺嘌呤二核苷酸和还原型烟酰胺腺嘌呤二核苷酸磷酸的产生,进而降低了肉色稳定性;另外,高氧气调包装贮藏过程中肉色稳定性的降低可能也与肌红蛋白的表达量下调有关;高氧环境还可能会促使抗氧化蛋白2、热休克蛋白以及DJ-1蛋白的表达量上调以抵御肉品的氧化应激反应,这些蛋白也都与肉色指标紧密相关。这些发现表明贮藏期间高氧气调包装对牛排蛋白质组的影响将直接决定其肉色稳定性的变化。
The objective of this study was to understand the mechanisms underlying changes in the color stability of high-oxygen modified atmosphere packaged(HiOx-MAP) steak during storage. The variations in meat color traits and sarcoplasmic proteome of longissimus dorsi steaks after different storage periods(0, 5, 10 and 15 days) were compared.The results suggested that the color stability of steaks decreased over time, which may be due to a significant decrease in metmyoglobin reducing activity(MRA) and oxygen consumption rate(OCR) during storage. The proteomic analysis revealed that a total of 20 differentially abundant proteins were identified during storage, 15 proteins of which were closely correlated with meat color traits and were identified as enzymes involved in glycolytic and energy metabolism(pyruvate kinase, glyceraldehyde-3-phosphate dehydrogenase, fructose-bisphosphate aldolase, fructose-1,6-bisphosphatase isozyme2, malate dehydrogenase, and flavin reductase). The expression levels of these metabolic enzymes were downregulated to different extents with increasing storage time, thereby reducing NADH and NADPH levels and consequently meat color stability. Moreover, the decrease in meat color stability also may be related to the down-regulation of myoglobin expression during storage. Oxidative environments could induce the expression of peroxiredoxin-2, heat shock protein and protein DJ-1 to resist oxidative stress, and these proteins were closely correlated with meat color parameters. These findings indicate that the influence of high-oxygen modified atmosphere packaging on meat proteome will directly determine changes in meat color stability throughout storage.
The objective of this study was to understand the mechanisms underlying changes in the color stability of high-oxygen modified atmosphere packaged(HiOx-MAP) steak during storage. The variations in meat color traits and sarcoplasmic proteome of longissimus dorsi steaks after different storage periods(0, 5, 10 and 15 days) were compared.The results suggested that the color stability of steaks decreased over time, which may be due to a significant decrease in metmyoglobin reducing activity(MRA) and oxygen consumption rate(OCR) during storage. The proteomic analysis revealed that a total of 20 differentially abundant proteins were identified during storage, 15 proteins of which were closely correlated with meat color traits and were identified as enzymes involved in glycolytic and energy metabolism(pyruvate kinase, glyceraldehyde-3-phosphate dehydrogenase, fructose-bisphosphate aldolase, fructose-1,6-bisphosphatase isozyme2, malate dehydrogenase, and flavin reductase). The expression levels of these metabolic enzymes were downregulated to different extents with increasing storage time, thereby reducing NADH and NADPH levels and consequently meat color stability. Moreover, the decrease in meat color stability also may be related to the down-regulation of myoglobin expression during storage. Oxidative environments could induce the expression of peroxiredoxin-2, heat shock protein and protein DJ-1 to resist oxidative stress, and these proteins were closely correlated with meat color parameters. These findings indicate that the influence of high-oxygen modified atmosphere packaging on meat proteome will directly determine changes in meat color stability throughout storage.
引文
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[2]SEGRE A,FALASCONI L.Save food:global initiative on food loss and waste reduction[R].Italy:FAO,2016.
[3]YANG X Y,ZHANG Y M,ZHU L X,et al.Effect of packaging atmospheres on storage quality characteristics of heavily marbled beef longissimus steaks[J].Meat Science,2016,117:50-56.DOI:10.1016/j.meatsci.2016.02.030.
[4]ENGLISH A R,MAFI G G,VANOVERBEKE D L,et al.Effects of extended aging and modified atmospheric packaging on beef top loin steak color[J].Journal of Animal Science,2016,94(4):1727-1737.DOI:10.2527/jas.2015-0149.
[5]KIM Y H,HUNT M C,MANCINI R A,et al.Mechanism for lactate-color stabilization in injection-enhanced beef[J].Journal of Agricultural and Food Chemistry,2006,54(20):7856-7862.DOI:10.1021/jf061225h.
[6]WU Wei,YU Qianqian,FU Yu,et al.Towards muscle-specific meat color stability of Chinese Luxi yellow cattle:a proteomic insight into post-mortem storage[J].Journal of Proteomics,2016,147:108-118.DOI:10.1016/j.jprot.2015.10.027.
[7]NAIR M N,SUMAN S P,CHATLI M K,et al.Proteome basis for intramuscular variation in color stability of beef semimembranosus[J].Meat Science,2016,113:9-16.DOI:10.1016/j.meatsci.2015.11.003.
[8]JOSEPH P,SUMAN S P,RENTFROW G,et al.Proteomics of musclespecific beef color stability[J].Journal of Agricultural and Food Chemistry,2012,60(12):3196-3203.DOI:10.1021/jf204188v.
[9]American Meat Science Association(AMSA).Meat color measurement guidelines[EB/OL].(2012-12)[2017-11-01].https://meatscience.org/docs/default-source/publications-resources/Hot-Topics/downloadthe-ebook-format-pdf-of-the-meat-color-measurement-guidelines.pdf?sfvrsn=a218b8b3_0.
[10]SAMMEL L M,HUNT M C,KROPF D H,et al.Comparison of assays for metmyoglobin reducing ability in beef inside and outside semimembranosus muscle[J].Journal of Food Science,2002,67(3):978-984.DOI:10.1111/j.1365-2621.2002.tb09439.x.
[11]MADHAVI D L,CARPENTER C E.Aging and processing affect color,metmyoglobin reductase and oxygen consumption of beef muscles[J].Journal of Food Science,1993,58(5):939-942.DOI:10.1111/j.1365-2621.1993.tb06083.x.
[12]ESTéVEZ M.What’s new in meat oxidation?[M].PURSLOW P P.New aspects of meat quality:from genes to ethics.Sawston:Woodhead Publishing,2017:91-109.DOI:10.1016/B978-0-08-100593-4.00006-0.
[13]吴爽,罗欣,毛衍伟,等.线粒体对肉色及其稳定性影响的研究进展[J].食品科学,2018,39(15):247-253.DOI:10.7506/spkx1002-6630-201815036.
[14]RAMANATHAN R,MANCINI R A,SUMAN S P,et al.Effects of 4-hydroxy-2-nonenal on beef heart mitochondrial ultrastructure,oxygen consumption,and metmyoglobin reduction[J].Meat Science,2012,90(3):564-571.DOI:10.1016/j.meatsci.2011.09.017.
[15]CANTO A C V C S,SUMAN S P,NAIR M N,et al.Differential abundance of sarcoplasmic proteome explains animal effect on beef Longissimus lumborum color stability[J].Meat Science,2015,102:90-98.DOI:10.1016/j.meatsci.2014.11.011.
[16]BOULEY J,CHAMBON C,PICARD B.Mapping of bovine skeletal muscle proteins using two-dimensional gel electrophoresis and mass spectrometry[J].Proteomics,2004,4(6):1811-1824.DOI:10.1002/pmic.200300688.
[17]ANDERSON M J,LONERGAN S M,HUFF-LONERGAN E.Differences in phosphorylation of phosphoglucomutase 1 in beef steaks from the longissimus dorsi with high or low star probe values[J].Meat Science,2014,96(1):379-384.DOI:10.1016/j.meatsci.2013.07.017.
[18]DI LUCA A,ELIA G,HAMILL R,et al.2D DIGE proteomic analysis of early post mortem muscle exudate highlights the importance of the stress response for improved water-holding capacity of fresh pork meat[J].Proteomics,2013,13(9):1528-1544.DOI:10.1002/pmic.201200145.
[19]WYTTENBACH A,SAUVAGEOT O,CARMICHAEL J,et al.Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin[J].Human Molecular Genetics,2002,11(9):1137-1151.DOI:10.1093/hmg/11.9.1137.
[20]BONIFATI V,OOSTRA B A,HEUTINK P.Linking DJ-1 to neurodegeneration offers novel insights for understanding the pathogenesis of Parkinson’s disease[J].Journal of Molecular Medicine,2004,82(3):163-174.DOI:10.1007/s00109-003-0512-1.
[21]RHEE S G,CHAE H Z,KIM K.Peroxiredoxins:a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling[J].Free Radical Biology and Medicine,2005,38(12):1543-1552.DOI:10.1016/j.freeradbiomed.2005.02.026.
[22]FONTANESI L,DAVOLI R,COSTA L N,et al.Investigation of candidate genes for glycolytic potential of porcine skeletal muscle:association with meat quality and production traits in Italian Large White pigs[J].Meat Science,2008,80(3):780-787.DOI:10.1016/j.meatsci.2008.03.022.
[23]ALVES R N,CORDEIRO O,SILVA T S,et al.Metabolic molecular indicators of chronic stress in gilthead seabream(Sparus aurata)using comparative proteomics[J].Aquaculture,2010,299(1/2/3/4):57-66.DOI:10.1016/j.aquaculture.2009.11.014.
[24]RAKUS D,PASEK M,KROTKIEWSKI H,et al.Interaction between muscle aldolase and muscle fructose 1,6-bisphosphatase results in the substrate channeling[J].Biochemistry,2004,43(47):14948-14957.DOI:10.1021/bi048886x.
[25]MARINO R,ALBENZIO M,DELLA MALVA A,et al.Changes in meat quality traits and sarcoplasmic proteins during aging in three different cattle breeds[J].Meat Science,2014,98(2):178-186.DOI:10.1016/j.meatsci.2014.05.024.
[26]YU Q Q,WU W,TIAN X J,et al.Unraveling proteome changes of Holstein beef M.semitendinosus and its relationship to meat discoloration during post-mortem storage analyzed by label-free mass spectrometry[J].Journal of Proteomics,2017,154:85-93.DOI:10.1016/j.jprot.2016.12.012.
[27]ATKINSON J L,FOLLETT M J.Biochemical studies on the discoloration of fresh meat[J].International Journal of Food Science&Technology,1973,8(1):51-58.DOI:10.1111/j.1365-2621.1973.tb01688.x.
[28]BEKHIT A E D A,HOPKINS D L,FAHRI F T,et al.Oxidative processes in muscle systems and fresh meat:sources,markers,and remedies[J].Comprehensive Reviews in Food Science and Food Safety,2013,12(5):565-597.DOI:10.1111/1541-4337.12027.
[29]SEKITO A,KOIDE-YOSHIDA S,NIKI T,et al.DJ-1 interacts with HIPK1 and affects H2O2-induced cell death[J].Free Radical Research,2006,40(2):155-165.DOI:10.1080/10715760500456847.
[30]WU Wei,GAO Xiaoguang,DAI Yan,et al.Post-mortem changes in sarcoplasmic proteome and its relationship to meat color traits in M.semitendinosus of Chinese Luxi yellow cattle[J].Food Research International,2015,72:98-105.DOI:10.1016/j.foodres.2015.03.030.
[31]SAYD T,MORZEL M,CHAMBON C,et al.Proteome analysis of the sarcoplasmic fraction of pig semimembranosus muscle:implications on meat color development[J].Journal of Agricultural and Food Chemistry,2006,54(7):2732-2737.DOI:10.1021/jf052569v.
[2]SEGRE A,FALASCONI L.Save food:global initiative on food loss and waste reduction[R].Italy:FAO,2016.
[3]YANG X Y,ZHANG Y M,ZHU L X,et al.Effect of packaging atmospheres on storage quality characteristics of heavily marbled beef longissimus steaks[J].Meat Science,2016,117:50-56.DOI:10.1016/j.meatsci.2016.02.030.
[4]ENGLISH A R,MAFI G G,VANOVERBEKE D L,et al.Effects of extended aging and modified atmospheric packaging on beef top loin steak color[J].Journal of Animal Science,2016,94(4):1727-1737.DOI:10.2527/jas.2015-0149.
[5]KIM Y H,HUNT M C,MANCINI R A,et al.Mechanism for lactate-color stabilization in injection-enhanced beef[J].Journal of Agricultural and Food Chemistry,2006,54(20):7856-7862.DOI:10.1021/jf061225h.
[6]WU Wei,YU Qianqian,FU Yu,et al.Towards muscle-specific meat color stability of Chinese Luxi yellow cattle:a proteomic insight into post-mortem storage[J].Journal of Proteomics,2016,147:108-118.DOI:10.1016/j.jprot.2015.10.027.
[7]NAIR M N,SUMAN S P,CHATLI M K,et al.Proteome basis for intramuscular variation in color stability of beef semimembranosus[J].Meat Science,2016,113:9-16.DOI:10.1016/j.meatsci.2015.11.003.
[8]JOSEPH P,SUMAN S P,RENTFROW G,et al.Proteomics of musclespecific beef color stability[J].Journal of Agricultural and Food Chemistry,2012,60(12):3196-3203.DOI:10.1021/jf204188v.
[9]American Meat Science Association(AMSA).Meat color measurement guidelines[EB/OL].(2012-12)[2017-11-01].https://meatscience.org/docs/default-source/publications-resources/Hot-Topics/downloadthe-ebook-format-pdf-of-the-meat-color-measurement-guidelines.pdf?sfvrsn=a218b8b3_0.
[10]SAMMEL L M,HUNT M C,KROPF D H,et al.Comparison of assays for metmyoglobin reducing ability in beef inside and outside semimembranosus muscle[J].Journal of Food Science,2002,67(3):978-984.DOI:10.1111/j.1365-2621.2002.tb09439.x.
[11]MADHAVI D L,CARPENTER C E.Aging and processing affect color,metmyoglobin reductase and oxygen consumption of beef muscles[J].Journal of Food Science,1993,58(5):939-942.DOI:10.1111/j.1365-2621.1993.tb06083.x.
[12]ESTéVEZ M.What’s new in meat oxidation?[M].PURSLOW P P.New aspects of meat quality:from genes to ethics.Sawston:Woodhead Publishing,2017:91-109.DOI:10.1016/B978-0-08-100593-4.00006-0.
[13]吴爽,罗欣,毛衍伟,等.线粒体对肉色及其稳定性影响的研究进展[J].食品科学,2018,39(15):247-253.DOI:10.7506/spkx1002-6630-201815036.
[14]RAMANATHAN R,MANCINI R A,SUMAN S P,et al.Effects of 4-hydroxy-2-nonenal on beef heart mitochondrial ultrastructure,oxygen consumption,and metmyoglobin reduction[J].Meat Science,2012,90(3):564-571.DOI:10.1016/j.meatsci.2011.09.017.
[15]CANTO A C V C S,SUMAN S P,NAIR M N,et al.Differential abundance of sarcoplasmic proteome explains animal effect on beef Longissimus lumborum color stability[J].Meat Science,2015,102:90-98.DOI:10.1016/j.meatsci.2014.11.011.
[16]BOULEY J,CHAMBON C,PICARD B.Mapping of bovine skeletal muscle proteins using two-dimensional gel electrophoresis and mass spectrometry[J].Proteomics,2004,4(6):1811-1824.DOI:10.1002/pmic.200300688.
[17]ANDERSON M J,LONERGAN S M,HUFF-LONERGAN E.Differences in phosphorylation of phosphoglucomutase 1 in beef steaks from the longissimus dorsi with high or low star probe values[J].Meat Science,2014,96(1):379-384.DOI:10.1016/j.meatsci.2013.07.017.
[18]DI LUCA A,ELIA G,HAMILL R,et al.2D DIGE proteomic analysis of early post mortem muscle exudate highlights the importance of the stress response for improved water-holding capacity of fresh pork meat[J].Proteomics,2013,13(9):1528-1544.DOI:10.1002/pmic.201200145.
[19]WYTTENBACH A,SAUVAGEOT O,CARMICHAEL J,et al.Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin[J].Human Molecular Genetics,2002,11(9):1137-1151.DOI:10.1093/hmg/11.9.1137.
[20]BONIFATI V,OOSTRA B A,HEUTINK P.Linking DJ-1 to neurodegeneration offers novel insights for understanding the pathogenesis of Parkinson’s disease[J].Journal of Molecular Medicine,2004,82(3):163-174.DOI:10.1007/s00109-003-0512-1.
[21]RHEE S G,CHAE H Z,KIM K.Peroxiredoxins:a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling[J].Free Radical Biology and Medicine,2005,38(12):1543-1552.DOI:10.1016/j.freeradbiomed.2005.02.026.
[22]FONTANESI L,DAVOLI R,COSTA L N,et al.Investigation of candidate genes for glycolytic potential of porcine skeletal muscle:association with meat quality and production traits in Italian Large White pigs[J].Meat Science,2008,80(3):780-787.DOI:10.1016/j.meatsci.2008.03.022.
[23]ALVES R N,CORDEIRO O,SILVA T S,et al.Metabolic molecular indicators of chronic stress in gilthead seabream(Sparus aurata)using comparative proteomics[J].Aquaculture,2010,299(1/2/3/4):57-66.DOI:10.1016/j.aquaculture.2009.11.014.
[24]RAKUS D,PASEK M,KROTKIEWSKI H,et al.Interaction between muscle aldolase and muscle fructose 1,6-bisphosphatase results in the substrate channeling[J].Biochemistry,2004,43(47):14948-14957.DOI:10.1021/bi048886x.
[25]MARINO R,ALBENZIO M,DELLA MALVA A,et al.Changes in meat quality traits and sarcoplasmic proteins during aging in three different cattle breeds[J].Meat Science,2014,98(2):178-186.DOI:10.1016/j.meatsci.2014.05.024.
[26]YU Q Q,WU W,TIAN X J,et al.Unraveling proteome changes of Holstein beef M.semitendinosus and its relationship to meat discoloration during post-mortem storage analyzed by label-free mass spectrometry[J].Journal of Proteomics,2017,154:85-93.DOI:10.1016/j.jprot.2016.12.012.
[27]ATKINSON J L,FOLLETT M J.Biochemical studies on the discoloration of fresh meat[J].International Journal of Food Science&Technology,1973,8(1):51-58.DOI:10.1111/j.1365-2621.1973.tb01688.x.
[28]BEKHIT A E D A,HOPKINS D L,FAHRI F T,et al.Oxidative processes in muscle systems and fresh meat:sources,markers,and remedies[J].Comprehensive Reviews in Food Science and Food Safety,2013,12(5):565-597.DOI:10.1111/1541-4337.12027.
[29]SEKITO A,KOIDE-YOSHIDA S,NIKI T,et al.DJ-1 interacts with HIPK1 and affects H2O2-induced cell death[J].Free Radical Research,2006,40(2):155-165.DOI:10.1080/10715760500456847.
[30]WU Wei,GAO Xiaoguang,DAI Yan,et al.Post-mortem changes in sarcoplasmic proteome and its relationship to meat color traits in M.semitendinosus of Chinese Luxi yellow cattle[J].Food Research International,2015,72:98-105.DOI:10.1016/j.foodres.2015.03.030.
[31]SAYD T,MORZEL M,CHAMBON C,et al.Proteome analysis of the sarcoplasmic fraction of pig semimembranosus muscle:implications on meat color development[J].Journal of Agricultural and Food Chemistry,2006,54(7):2732-2737.DOI:10.1021/jf052569v.
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