Integrated metabolome, proteome, and transcriptome analysis explored the molecular mechanism of phosphoglycerate kinase 1 and pyruvate kinase M2 characterizing the postmortem meat quality
[en] Phosphoglycerate kinase 1 (PGK1) and pyruvate kinase M2 (PKM2) have been identified as the postmortem meat quality biomarkers. However, the precise molecular mechanism through which they affect and regulate the development of meat quality remains unclear. In this work, the high- and low-activity groups (n = 10) were selected from 60 lamb muscles at 24 h postmortem based on the activity levels of PGK1 and PKM2. The metabolomic, proteomic, and transcriptomic analyses combined with deeply integrated multi-omics analysis were used to elucidate the mechanisms by which PGK1 and PKM2 characterize meat quality. The results indicated that glycolysis played a crucial role in regulating PGK1 and PKM2 activity at the metabolome, proteome, and transcriptome levels. In glycolysis pathway, we identified several key components closely related to PGK1 and PKM2 activity, including differential metabolites (adenosine triphosphate, adenosine diphosphate, glucose-6-phosphate, nicotinamide adenine dinucleotide phosphate, fructose-6-phosphate, dihydroxyacetone phosphate, 3-phosphoglycerate, NAD+ nicotinamide adenine dinucleotide, lactate, and pyruvate), different abundance proteins (lactate dehydrogenase B and fructose bisphosphate aldolase B), and differentially expressed genes (hexokinase and fructose-1,6-bisphosphatase 1). It was concluded that PGK1 and PKM2 may affect the formation of meat quality by regulating these critical substrates. Additionally, PGK1 and PKM2 could also affect the tricarboxylic acid cycle, oxidative phosphorylation, and muscle contraction in postmortem and then influence meat quality. This integrative omics study offers valuable insight into unraveling the molecular mechanisms underlying postmortem meat quality development.
Disciplines :
Food science
Author, co-author :
Huang, Caiyan ; Université de Liège - ULiège > TERRA Research Centre ; Institute of Food Science and Technology, Chinese Academy of Agriculture Sciences, Key Laboratory of Agro-Products Quality & Safety Harvest, Storage, Transportation, Management and Control, Ministry of Agriculture and Rural Affairs, Beijing, China
Xiang, Can; Department of Flavor Chemistry, Institute of Food Science and Biotechnology, University of Hohenheim, Stuttgart, Germany
Wang, Fangzhou ; Université de Liège - ULiège > TERRA Research Centre
Blecker, Christophe ; Université de Liège - ULiège > TERRA Research Centre > Technologie Alimentaire (TA)
Wang, Zhenyu; Institute of Food Science and Technology, Chinese Academy of Agriculture Sciences, Key Laboratory of Agro-Products Quality & Safety Harvest, Storage, Transportation, Management and Control, Ministry of Agriculture and Rural Affairs, Beijing, China
Chen, Li; Institute of Food Science and Technology, Chinese Academy of Agriculture Sciences, Key Laboratory of Agro-Products Quality & Safety Harvest, Storage, Transportation, Management and Control, Ministry of Agriculture and Rural Affairs, Beijing, China
Zhang, Dequan ; Institute of Food Science and Technology, Chinese Academy of Agriculture Sciences, Key Laboratory of Agro-Products Quality & Safety Harvest, Storage, Transportation, Management and Control, Ministry of Agriculture and Rural Affairs, Beijing, China
Language :
English
Title :
Integrated metabolome, proteome, and transcriptome analysis explored the molecular mechanism of phosphoglycerate kinase 1 and pyruvate kinase M2 characterizing the postmortem meat quality
This study was financially supported by the National Natural Science Foundation of China (32072144), and the Agricultural Science and Technology Innovation Program, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences (CAAS\u2010ASTIP\u20102023\u2010IFST). Caiyan Huang's scholarship was sponsored by the China Scholarship Council (CSC).
Bai, Y., Li, X., Zhang, D., Chen, L., Hou, C., Zheng, X., Ren, C., & Ijaz, M. (2020). Role of phosphorylation on characteristics of glycogen phosphorylase in lamb with different glycolytic rates post-mortem. Meat Science, 164, 108096. https://doi.org/10.1016/j.meatsci.2020.108096
Briskey, E. J. (1964). Etiological status and associated studies of pale, soft, exudative porcine musculature. Advances in Food Research, 13, 89-178. https://pubmed.ncbi.nlm.nih.gov/14283271
Cai, R., Zhang, Y., Simmering, J. E., Schultz, J. L., Li, Y., Fernandez-Carasa, I., Consiglio, A., Raya, A., Polgreen, P. M., Narayanan, N. S., Yuan, Y., Chen, Z., Su, W., Han, Y., Zhao, C., Gao, L., Ji, X., Welsh, M. J., & Liu, L. (2019). Enhancing glycolysis attenuates Parkinson's disease progression in models and clinical databases. The Journal of Clinical Investigation, 129(10), 4539–4549. https://doi.org/10.1172/jci129987
Chauhan, S. S., & England, E. M. (2018). Postmortem glycolysis and glycogenolysis: Insights from species comparisons. Meat Science, 144, 118–126. https://doi.org/10.1016/j.meatsci.2018.06.021
Chen, D., Li, W., Du, M., & Cao, B. (2019). Adipogenesis, fibrogenesis and myogenesis related gene expression in longissimus muscle of high and low marbling beef cattle. Livestock Science, 229, 188–193. https://doi.org/10.1016/j.livsci.2019.09.032
Chen, L., Bai, Y., Everaert, N., Li, X., Tian, G., Hou, C., & Zhang, D. (2019). Effects of protein phosphorylation on glycolysis through the regulation of enzyme activity in ovine muscle. Food Chemistry, 293, 537–544. https://doi.org/10.1016/j.foodchem.2019.05.011
Chen, L., Li, Z., Everaert, N., Lametsch, R., & Zhang, D. (2019). Quantitative phosphoproteomic analysis of ovine muscle with different postmortem glycolytic rates. Food Chemistry, 280, 203–209. https://doi.org/10.1016/j.foodchem.2018.12.056
Creydt, M., & Fischer, M. (2018). Omics approaches for food authentication. Electrophoresis, 39(13), 1569–1581. https://doi.org/10.1002/elps.201800004
Gu, M., Li, C., Chen, L., Li, S., Xiao, N., Zhang, D., & Zheng, X. (2023). Insight from untargeted metabolomics: Revealing the potential marker compounds changes in refrigerated pork based on random forests machine learning algorithm. Food Chemistry, 424, 136341. https://doi.org/10.1016/j.foodchem.2023.136341
Hamm, R. (1977). Postmortem breakdown of ATP and glycogen in ground muscle: A review. Meat Science, 1(1), 15–39. https://doi.org/10.1016/0309-1740(77)90029-8
Honikel, K. O. (2014). Conversion of muscle to meat | Glycolysis. In M. Dikeman & C. Devine (Eds.), Encyclopedia of meat sciences (2nd ed., pp. 353–357). Academic Press. https://doi.org/10.1016/B978-0-12-384731-7.00095-7
Hopkins, D. L., Toohey, E. S., Warner, R. D., Kerr, M. J., & van de Ven, R. (2010). Measuring the shear force of lamb meat cooked from frozen samples: Comparison of two laboratories. Animal Production Science, 50(6), 382–385. https://doi.org/10.1071/AN09162
Huang, C., Blecker, C., Chen, L., Xiang, C., Zheng, X., Wang, Z., & Zhang, D. (2023). Integrating identification and targeted proteomics to discover the potential indicators of postmortem lamb meat quality. Meat Science, 199, 109126. https://doi.org/10.1016/j.meatsci.2023.109126
Huang, C., Hou, C., Ijaz, M., Yan, T., Li, X., Li, Y., & Zhang, D. (2020). Proteomics discovery of protein biomarkers linked to meat quality traits in post-mortem muscles: Current trends and future prospects: A review. Trends in Food Science & Technology, 105, 416–432. https://doi.org/10.1016/j.tifs.2020.09.030
Huang, C., Zhang, D., Wang, Z., Zhao, Y., Blecker, C., Li, S., Zheng, X., & Chen, L. (2023). Validation of protein biological markers of lamb meat quality characteristics based on the different muscle types. Food Chemistry, 427, 136739. https://doi.org/10.1016/j.foodchem.2023.136739
Ji, S., Zhang, B., Liu, J., Qin, Y., Liang, C., Shi, S., Jin, K., Liang, D., Xu, W., Xu, H., Wang, W., Wu, C., Liu, L., Liu, C., Xu, J., Ni, Q., & Yu, X. (2016). ALDOA functions as an oncogene in the highly metastatic pancreatic cancer. Cancer Letters, 374(1), 127–135. https://doi.org/10.1016/j.canlet.2016.01.054
Jia, X., Hildrum, K. I., Westad, F., Kummen, E., Aass, L., & Hollung, K. (2006). Changes in enzymes associated with energy metabolism during the early post mortem period in Longissimus thoracis bovine muscle analyzed by proteomics. Journal of Proteome Research, 5(7), 1763–1769. https://doi.org/10.1021/pr060119s
Kim, G.-D., Jeong, J.-Y., Yang, H.-S., & Hur, S. J. (2019). Differential abundance of proteome associated with intramuscular variation of meat quality in porcine Longissimus thoracis et lumborum muscle. Meat Science, 149, 85–95. https://doi.org/10.1016/j.meatsci.2018.11.012
Li, Z., Li, X., Wang, Z., Shen, Q. W., & Zhang, D. (2016). Antemortem stress regulates protein acetylation and glycolysis in postmortem muscle. Food Chemistry, 202, 94–98. https://doi.org/10.1016/j.foodchem.2016.01.085
Liu, X., Zou, X., Zhou, Y., Chen, R., Peng, Y., & Qu, M. (2023). LDHA and LDHB overexpression promoted the Warburg effect in malignantly transformed GES-1 cells induced by N-nitroso compounds. Food and Chemical Toxicology, 180, 114007. https://doi.org/10.1016/j.fct.2023.114007
López-Pedrouso, M., Lorenzo, J. M., Cittadini, A., Sarries, M. V., Gagaoua, M., & Franco, D. (2023). A proteomic approach to identify biomarkers of foal meat quality: A focus on tenderness, color and intramuscular fat traits. Food Chemistry, 405, 134805. https://doi.org/10.1016/j.foodchem.2022.134805
Lu, W., Hou, Q., Zhang, J., & Zhang, W. (2023). Targeted energy metabolomics analysis of postmortem pork in an in vitro model as influenced by protein S-nitrosylation. Meat Science, 197, 109073. https://doi.org/10.1016/j.meatsci.2022.109073
Ma, Y., Han, L., Zhang, S., Zhang, X., Hou, S., Gui, L., Sun, S., Yuan, Z., Wang, Z., & Yang, B. (2023). Insight into the differences of meat quality between Qinghai white Tibetan sheep and black Tibetan sheep from the perspective of metabolomics and rumen microbiota. Food Chemistry: X, 19, 100843. https://doi.org/10.1016/j.fochx.2023.100843
Matarneh, S. K., Silva, S. L., & Gerrard, D. E. (2021). New insights in muscle biology that alter meat quality. Annual Review of Animal Biosciences, 9, 355–377. https://doi.org/10.1146/annurev-animal-021419-083902
Misra, B. B., Langefeld, C., Olivier, M., & Cox, L. A. (2019). Integrated omics: Tools, advances and future approaches. Journal of Molecular Endocrinology, 62(1), R21–R45. https://doi.org/10.1530/JME-18-0055
Muroya, S., Ohnishi-Kameyama, M., Oe, M., Nakajima, I., Shibata, M., & Chikuni, K. (2007). Double phosphorylation of the myosin regulatory light chain during rigor mortis of bovine longissimus muscle. Journal of Agricultural and Food Chemistry, 55(10), 3998–4004. https://doi.org/10.1021/jf063200o
Naba, A., Clauser, K. R., Ding, H., Whittaker, C. A., Carr, S. A., & Hynes, R. O. (2016). The extracellular matrix: Tools and insights for the “omics” era. Matrix Biology, 49, 10–24. https://doi.org/10.1016/j.matbio.2015.06.003
Nolfi-Donegan, D., Braganza, A., & Shiva, S. (2020). Mitochondrial electron transport chain: Oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biology, 37, 101674. https://doi.org/10.1016/j.redox.2020.101674
Picard, B., Lebret, B., Cassar-Malek, I., Liaubet, L., Berri, C., Le Bihan-Duval, E., Hocquette, J. F., & Renand, G. (2015). Recent advances in omic technologies for meat quality management. Meat Science, 109, 18–26. https://doi.org/10.1016/j.meatsci.2015.05.003
Reiche, A. M., Oberson, J. L., Silacci, P., Messadène-Chelali, J., Hess, H. D., Dohme-Meier, F., Dufey, P. A., & Terlouw, E. M. C. (2019). Pre-slaughter stress and horn status influence physiology and meat quality of young bulls. Meat Science, 158, 107892. https://doi.org/10.1016/j.meatsci.2019.107892
Ren, C., Li, X., Bai, Y., Schroyen, M., & Zhang, D. (2022). Phosphorylation and acetylation of glycolytic enzymes cooperatively regulate their activity and lamb meat quality. Food Chemistry, 397, 133739. https://doi.org/10.1016/j.foodchem.2022.133739
Santiago, B., Baldassini, W., Neto, O. M., Chardulo, L. A., Torres, R., Pereira, G., Curi, R., Chiaratti, M. R., Padilha, P., Alessandroni, L., & Gagaoua, M. (2023). Post-mortem muscle proteome of crossbred bulls and steers: Relationships with carcass and meat quality. Journal of Proteomics, 278, 104871. https://doi.org/10.1016/j.jprot.2023.104871
Setyabrata, D., Ma, D., Xie, S., Thimmapuram, J., Cooper, B. R., Aryal, U. K., & Kim, Y. H. B. (2023). Proteomics and metabolomics profiling of meat exudate to determine the impact of postmortem aging on oxidative stability of beef muscles. Food Chemistry: X, 18, 100660. https://doi.org/10.1016/j.fochx.2023.100660
Wang, C., Matarneh, S. K., Gerrard, D., & Tan, J. (2022). Contributions of energy pathways to ATP production and pH variations in postmortem muscles. Meat Science, 189, 108828. https://doi.org/10.1016/j.meatsci.2022.108828
Xu, L., He, Y., Yuan, X., Liu, K., Cui, Y., Ma, H., Ma, C., & Yu, X. (2023). iTRAQ-based proteomic analysis reveals the underlying mechanism of postmortem tenderization of refrigerated porcine Longissimus thoracis et lumborum muscle. Meat Science, 197, 109068. https://doi.org/10.1016/j.meatsci.2022.109068
Yu, Q., Tian, X., Shao, L., Li, X., & Dai, R. (2019). Targeted metabolomics to reveal muscle-specific energy metabolism between bovine Longissimus lumborum and psoas major during early postmortem periods. Meat Science, 156, 166–173. https://doi.org/10.1016/j.meatsci.2019.05.029
Zequan, X., Yonggang, S., Guangjuan, L., Shijun, X., Li, Z., Mingrui, Z., Yanli, X., & Zirong, W. (2021). Proteomics analysis as an approach to understand the formation of pale, soft, and exudative (PSE) pork. Meat Science, 177, 108353. https://doi.org/10.1016/j.meatsci.2020.108353
Zequan, X., Yonggang, S., Heng, X., Yaodong, W., Xin, M., Dan, L., Li, Z., Tingting, D., & Zirong, W. (2022). Transcriptome-based analysis of early post-mortem formation of pale, soft, and exudative (PSE) pork. Meat Science, 194, 108962. https://doi.org/10.1016/j.meatsci.2022.108962
Zhan, H., Xiong, Y., Wang, Z., Dong, W., Zhou, Q., Xie, S., Li, X., Zhao, S., & Ma, Y. (2022). Integrative analysis of transcriptomic and metabolomic profiles reveal the complex molecular regulatory network of meat quality in Enshi black pigs. Meat Science, 183, 108642. https://doi.org/10.1016/j.meatsci.2021.108642
Zhang, M., Guo, Y., Su, R., Corazzin, M., Hou, R., Xie, J., Zhang, Y., Zhao, L., Su, L., & Jin, Y. (2022). Transcriptome analysis reveals the molecular regulatory network of muscle development and meat quality in Sunit lamb supplemented with dietary probiotic. Meat Science, 194, 108996. https://doi.org/10.1016/j.meatsci.2022.108996
Zhang, P., Shao, Y., Quan, F., Liu, L., & Yang, J. (2021). FBP1 enhances the radiosensitivity by suppressing glycolysis via the FBXW7/mTOR axis in nasopharyngeal carcinoma cells. Life Sciences, 283, 119840. https://doi.org/10.1016/j.lfs.2021.119840
Zheng, P., Zhang, N., Ren, D., Yu, C., Zhao, B., & Zhang, Y. (2023). Integrated spatial transcriptome and metabolism study reveals metabolic heterogeneity in human injured brain. Cell Reports Medicine, 4(6), 101057. https://doi.org/10.1016/j.xcrm.2023.101057
Zhu, Y., Zhang, Y., Li, Y., Guo, C., Fan, Z., Li, Y., Yang, M., Zhou, X., Sun, Z., & Wang, J. (2022). Integrative proteomics and metabolomics approach to elucidate metabolic dysfunction induced by silica nanoparticles in hepatocytes. Journal of Hazardous Materials, 434, 128820. https://doi.org/10.1016/j.jhazmat.2022.128820
