Preliminary investigation on the impact of salty and sugary former foods on pig liver and plasma profiles using OMICS approaches.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
21 08 2024
Historique:
received: 21 02 2024
accepted: 14 08 2024
medline: 22 8 2024
pubmed: 22 8 2024
entrez: 21 8 2024
Statut: epublish

Résumé

Replacing cereals with food leftovers could reduce feed-food competition and keep nutrients and energy in the food chain. Former food products (FFPs) are industrial food leftovers no more intended for human but still suitable as alternative and sustainable feedstuffs for monogastric. In this study, omics approaches were applied to evaluate the impact of dietary FFPs on pig liver proteome and plasma peptidome. Thirty-six Swiss Large White male castrated pigs were randomly assigned to three dietary treatments [control (CTR), 30% CTR replaced with salty FFP (SA), 30% CTR replaced with sugary FFP (SU)] from the start of the growing phase (22.4 ± 1.7 kg) until slaughtering (110 ± 3 kg). The low number of differentially regulated proteins in each comparison matrix (SA/SU vs. CTR) and the lack of metabolic interaction indicated a marginal impact on hepatic lipid metabolism. The plasma peptidomics investigation showed low variability between the peptidome of the three dietary groups and identified three possible bioactive peptides in the SA group associated with anti-hypertension and vascular homeostasis regulation. To conclude, the limited modulation of liver proteome and plasma peptidome by the SA and SU diets strenghtened the idea of reusing FFPs as feed ingredients to make pig production more sustainable.

Identifiants

pubmed: 39169123
doi: 10.1038/s41598-024-70310-z
pii: 10.1038/s41598-024-70310-z
doi:

Substances chimiques

Proteome 0
Peptides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

19386

Subventions

Organisme : Regione Lombardia
ID : D44I20002000002

Informations de copyright

© 2024. The Author(s).

Références

Pinotti, L. et al. Recycling food leftovers in feed as opportunity to increase the sustainability of livestock production. J. Clean Prod. 294, 126290 (2021).
doi: 10.1016/j.jclepro.2021.126290
Pinotti, L., Mazzoleni, S., Moradei, A., Lin, P. & Luciano, A. Effects of alternative feed ingredients on red meat quality: A review of algae, insects, agro-industrial by-products and former food products. It. J. Anim. Sci. 22, 695–710 (2023).
doi: 10.1080/1828051X.2023.2238784
Govoni, C., Chiarelli, D. D., Luciano, A., Pinotti, L. & Rulli, M. C. Global assessment of land and water resource demand for pork supply. Environ. Res. Lett. 17, 074003–074015 (2022).
doi: 10.1088/1748-9326/ac74d7
Andretta, I. et al. Environmental impacts of pig and poultry production: Insights from a systematic review. Front. Vet. Sci. 8, 750733 (2021).
pubmed: 34778435 pmcid: 8578682 doi: 10.3389/fvets.2021.750733
European Food Safety Authority (EFSA). Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on theobromine as undesirable substances in animal feed. EFSA J. 725, 1–66 (2008).
Pinotti, L. et al. Review: pig-based bioconversion: The use of former food products to keep nutrient in the food chain. Animal 17, 100918 (2023).
pubmed: 37544840 doi: 10.1016/j.animal.2023.100918
Tretola, M., Luciano, A., Ottoboni, M., Baldi, A. & Pinotti, L. Influence of traditional vs alternative dietary carbohydrates sources on the large intestinal microbiota in post-weaning piglets. Animals 9, 516 (2019).
pubmed: 31374923 pmcid: 6719221 doi: 10.3390/ani9080516
Luciano, A., Espinosa, C. D., Pinotti, L. & Stein, H. H. Standardized total tract digestibility of phosphorus in bakery meal fed to pigs and effects of bakery meal on growth performance of weanling pigs. Anim. Feed Sci. Technol. 284, 115148–115157 (2022).
doi: 10.1016/j.anifeedsci.2021.115148
Luciano, A. et al. Sweet vs. salty former food products in post-weaning piglets: Effects on growth, apparent total tract digestibility and blood metabolites. Animals 11, 3315 (2021).
pubmed: 34828047 pmcid: 8614654 doi: 10.3390/ani11113315
Pinotti, L. et al. PSXI-21 inclusion of former food products in post-weaning diet of piglets: Impact on the fatty acid profile of subcutaneous adipose tissue and on serum metabolites. J. Anim. Sci. 101, 563–564 (2023).
doi: 10.1093/jas/skad281.660
Su, D. et al. Metabolomic markers of ultra-processed food and incident CKD. Clin. J. Am. Soc. Nephrol. 18, 327–336 (2023).
pubmed: 36735499 pmcid: 10103271 doi: 10.2215/CJN.0000000000000062
Mazzoleni, S. et al. Sugary and salty former food products in pig diets affect energy and nutrient digestibility, feeding behavior but not the growth performance and carcass composition. Animal 17, 101019 (2023).
pubmed: 37967497 doi: 10.1016/j.animal.2023.101019
Tretola, M. et al. Sustainable pig diets: Partial grain replacement with former food products and its impact on meat quality. J. Anim. Sci. 102, skae070 (2024).
pubmed: 38490265 doi: 10.1093/jas/skae070
Roche, M., Rondeau, P., Singh, N. R., Tarnus, E. & Bourdon, E. The antioxidant properties of serum albumin. FEBS Lett. 582, 1783–1787 (2008).
pubmed: 18474236 doi: 10.1016/j.febslet.2008.04.057
Eugenio, F. A., van Milgen, J., Duperray, J., Sergheraert, R. & Le Floc’h, N. Feeding pigs amino acids as protein-bound or in free form influences postprandial concentrations of amino acids, metabolites, and insulin. Animal 17, 100684 (2023).
pubmed: 36542911 doi: 10.1016/j.animal.2022.100684
Szostak, A. et al. Effect of a diet enriched with omega-6 and omega-3 fatty acids on the pig liver transcriptome. Genes Nutr. 11, 9 (2016).
pubmed: 27482299 pmcid: 4959555 doi: 10.1186/s12263-016-0517-4
Hodson, L., Rosqvist, F. & Parry, S. The influence of dietary fatty acids on liver fat content and metabolism. Proc Nutr. Soc. 79, 30–41 (2020).
pubmed: 30942685 doi: 10.1017/S0029665119000569
Bovo, S. et al. Metabolomics evidences plasma and serum biomarkers differentiating two heavy pig breeds. Animal. 10, 1741–1748 (2016).
pubmed: 27055632 doi: 10.1017/S1751731116000483
Dallas, D. C. et al. Current peptidomics: Applications, purification, identification, quantification, and functional analysis. Proteomics. 15, 1026–1038 (2015).
pubmed: 25429922 pmcid: 4371869 doi: 10.1002/pmic.201400310
Dupont, D. Peptidomic as a tool for assessing protein digestion. Curr. Opin. Food Sci. 16, 53–58 (2017).
doi: 10.1016/j.cofs.2017.08.001
Cunningham, R., Ma, D. & Li, L. Mass spectrometry-based proteomics and peptidomics for systems biology and biomarker discovery. Front. Biol. 7, 313–335 (2012).
doi: 10.1007/s11515-012-1218-y
Di Meo, A., Pasic, M. D. & Yousef, G. M. Proteomics and peptidomics: Moving toward precision medicine in urological malignancies. Oncotarget 7, 52460–52474 (2016).
pubmed: 27119500 pmcid: 5239567 doi: 10.18632/oncotarget.8931
Jun, H., Daiwen, C. & Bing, Y. Metabolic and transcriptomic responses of weaned pigs induced by different dietary amylose and amylopectin ratio. PLoS ONE 5, e15110 (2010).
pubmed: 21152049 pmcid: 2994909 doi: 10.1371/journal.pone.0015110
Yin, F. et al. Digestion rate of dietary starch affects the systemic circulation of lipid profiles and lipid metabolism-related gene expression in weaned pigs. Br. J. Nutr. 106, 369–377 (2021).
doi: 10.1017/S0007114511000213
Sejersen, H., Sørensen, M. T., Larsen, T., Bendixen, E. & Ingvartsen, K. L. Liver protein expression in young pigs in response to a high-fat diet and diet restriction. J. Anim. Sci. 91, 147–158 (2013).
pubmed: 23048158 doi: 10.2527/jas.2012-5303
Duran-Montgé, P., Theil, P. K., Lauridsen, C. & Esteve-Garcia, E. Dietary fat source affects metabolism of fatty acids in pigs as evaluated by altered expression of lipogenic genes in liver and adipose tissues. Animal 3, 535–542 (2009).
pubmed: 22444377 doi: 10.1017/S1751731108003686
Sinha, R. A. et al. Caffeine stimulates hepatic lipid metabolism by the autophagy-lysosomal pathway in mice. Hepatology 59, 1366–1380 (2014).
pubmed: 23929677 doi: 10.1002/hep.26667
Wei, D. et al. Theobromine ameliorates nonalcoholic fatty liver disease by regulating hepatic lipid metabolism via mTOR signaling pathway in vivo and in vitro. Can. J. Physiol. Pharmacol. 99, 775–785 (2021).
pubmed: 33290156 doi: 10.1139/cjpp-2020-0259
Lafarga, T. & Hayes, M. Bioactive peptides from meat muscle and by-products: Generation, functionality and application as functional ingredients. Meat Sci. 98, 227–239 (2014).
pubmed: 24971811 doi: 10.1016/j.meatsci.2014.05.036
Nongonierma, A. B. & Fitzgerald, R. J. The scientific evidence for the role of milk protein-derived bioactive peptides in humans: A review. J. Funct. Foods. 17, 640–656 (2015).
doi: 10.1016/j.jff.2015.06.021
Cerrato, A. et al. Comprehensive identification of native medium-sized and short bioactive peptides in sea bass muscle. Food Chem. 343, 128443 (2021).
pubmed: 33129615 doi: 10.1016/j.foodchem.2020.128443
Caira, S. et al. Recent developments in peptidomics for the quali-quantitative analysis of food-derived peptides in human body fluids and tissues. Trends Food Sci. Technol. 126, 41–60 (2022).
doi: 10.1016/j.tifs.2022.06.014
Chakrabarti, S., Guha, S. & Majumder, K. Food-derived bioactive peptides in human health: Challenges and opportunities. Nutrients 10, 1738 (2018).
pubmed: 30424533 pmcid: 6265732 doi: 10.3390/nu10111738
Mora, L., Aristoy, M.-C. & Toldrá, F. Bioactive peptides. In Encyclopedia of Food Chemistry 381–389 (Elsevier, 2019). https://doi.org/10.1016/B978-0-08-100596-5.22397-4 .
Dave, L. A., Hayes, M., Montoya, C. A., Rutherfurd, S. M. & Moughan, P. J. Human gut endogenous proteins as a potential source of angiotensin-I-converting enzyme (ACE-I)-, renin inhibitory and antioxidant peptides. Peptides 76, 30–44 (2016).
pubmed: 26617077 doi: 10.1016/j.peptides.2015.11.003
Souffrant, W. B. et al. Exogenous and endogenous contributions to nitrogen fluxes in the digestive tract of pigs fed a casein diet. III. Recycling of endogenous nitrogen. Reprod. Nutr. Dev. 33, 373–382 (1993).
pubmed: 8240681 doi: 10.1051/rnd:19930406
Dave, L. A., Montoya, C. A., Rutherfurd, S. M. & Moughan, P. J. Gastrointestinal endogenous proteins as a source of bioactive peptides - An in silico study. PLoS ONE 9, e98922 (2014).
pubmed: 24901416 pmcid: 4047039 doi: 10.1371/journal.pone.0098922
Meisel, H. Biochemical properties of bioactive peptides derived from milk proteins: Potential nutraceuticals for food and pharmaceutical applications. Livest. Prod. Sci. 50, 125–138 (1997).
doi: 10.1016/S0301-6226(97)00083-3
Rutherfurd-Markwick, K. J. & Moughan, P. J. Bioactive peptides derived from food. J. AOAC Int. 88, 955–966 (2005).
pubmed: 16001873 doi: 10.1093/jaoac/88.3.955
Shahidi, F. & Zhong, Y. Bioactive peptides. J. AOAC Int. 91, 914–931 (2008).
pubmed: 18727554 doi: 10.1093/jaoac/91.4.914
Liang, G. et al. Nicotinamide N-methyltransferase and liver diseases. Genes Dis. 10, 1883–1893 (2023).
pubmed: 37492717 doi: 10.1016/j.gendis.2022.03.019
Asif, S. et al. Hmgcs2-mediated ketogenesis modulates high-fat diet-induced hepatosteatosis. Mol. Metab. 61, 101494 (2022).
pubmed: 35421611 pmcid: 9039870 doi: 10.1016/j.molmet.2022.101494
Luciano, A. et al. O121 Former food products in post-weaning piglets: Effects on subcutaneous adipose tissue and on selected metabolites. Anim. Sci. Proc. 13, 392–394 (2022).
doi: 10.1016/j.anscip.2022.07.131
Wood, J. D. et al. Fat deposition, fatty acid composition and meat quality: A review. Meat Sci. 78, 343–358 (2008).
pubmed: 22062452 doi: 10.1016/j.meatsci.2007.07.019
Song, Q. et al. Nicotinamide N-methyltransferase upregulation contributes to palmitate-elicited peroxisome proliferator-activated receptor transactivation in hepatocytes. Am. J. Physiol. Cell. Physiol. 325, C29–C41 (2023).
pubmed: 37212549 pmcid: 10259858 doi: 10.1152/ajpcell.00010.2023
Ali, A. et al. Ferritin heavy chain (FTH1) exerts significant antigrowth effects in breast cancer cells by inhibiting the expression of c-MYC. FEBS Open Bio 11, 3101–3114 (2021).
pubmed: 34551213 pmcid: 8564339 doi: 10.1002/2211-5463.13303
Nebert, D. W. & Vasiliou, V. Analysis of the glutathione S-transferase (GST) gene family. Hum. Genom. 1, 460 (2004).
doi: 10.1186/1479-7364-1-6-460
Wu, X. et al. Involvement of kynurenine pathway between inflammation and glutamate in the underlying etiopathology of CUMS-induced depression mouse model. BMC Neurosci. 23, 62 (2022).
pubmed: 36357867 pmcid: 9650798 doi: 10.1186/s12868-022-00746-4
Lindquist, C. et al. Increased fatty acid oxidation and mitochondrial proliferation in liver are associated with increased plasma kynurenine metabolites and nicotinamide levels in normolipidemic and carnitine-depleted rats. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 186, 158543 (2020).
doi: 10.1016/j.bbalip.2019.158543
Pretorius, D., Richter, R. P., Anand, T., Cardenas, J. C. & Richter, J. R. Alterations in heparan sulfate proteoglycan synthesis and sulfation and the impact on vascular endothelial function. Matrix Biol. Plus. 16, 100121 (2022).
pubmed: 36160687 pmcid: 9494232 doi: 10.1016/j.mbplus.2022.100121
Jansen, P. A. et al. Expression of the vanin gene family in normal and inflamed human skin: Induction by proinflammatory cytokines. J. Invest. Dermatol. 129, 2167–2174 (2009).
pubmed: 19322213 doi: 10.1038/jid.2009.67
Mariani, F. & Roncucci, L. Role of the vanins-myeloperoxidase axis in colorectal carcinogenesis. Int. J. Mol. Sci. 18, 918 (2017).
pubmed: 28448444 pmcid: 5454831 doi: 10.3390/ijms18050918
Kaskow, B. J., Proffitt, J. M., Blangero, J., Moses, E. K. & Abraham, L. J. Diverse biological activities of the vascular non-inflammatory molecules - the Vanin pantetheinases. Biochem. Biophys. Res. Commun. 417, 653–8 (2012).
pubmed: 22155241 doi: 10.1016/j.bbrc.2011.11.099
Solberg, R. et al. The mammalian cysteine protease legumain in health and disease. Int. J. Mol. Sci. 23, 15983 (2022).
pubmed: 36555634 pmcid: 9788469 doi: 10.3390/ijms232415983
Foltz, M., van der Pijl, P. C. & Duchateau, G. S. Current in vitro testing of bioactive peptides is not valuable. J. Nutr. 140, 117–118 (2010).
pubmed: 19906810 doi: 10.3945/jn.109.116228
Miner-Williams, W. M., Stevens, B. R. & Moughan, P. J. Are intact peptides absorbed from the healthy gut in the adult human?. Nutr. Res. Rev. 27, 308–329 (2014).
pubmed: 25623084 doi: 10.1017/S0954422414000225
Haahr, M. Random.org: True random number service. Website ( http://www.random.org ). 10 (2010).
Ferrario, G. et al. Polyphenols from thinned young apples: HPLC-HRMS profile and evaluation of their anti-oxidant and anti-inflammatory activities by proteomic studies. Antioxidants 11, 1577 (2022).
pubmed: 36009298 pmcid: 9405250 doi: 10.3390/antiox11081577
Aletti, F. et al. Peptidomic analysis of rat plasma: Proteolysis in hemorrhagic shock. Shock 45, 540–554 (2016).
pubmed: 26863123 pmcid: 4833562 doi: 10.1097/SHK.0000000000000532
Giromini, C. et al. In vitro-digested milk proteins: Evaluation of angiotensin-1-converting enzyme inhibitory and antioxidant activities, peptidomic profile, and mucin gene expression in HT29-MTX cells. J. Dairy Sci. 102, 10760–10771 (2019).
pubmed: 31521344 doi: 10.3168/jds.2019-16833
Maffioli, E. et al. High-resolution mass spectrometry-based approaches for the detection and quantification of peptidase activity in plasma. Molecules 25, 4071 (2020).
pubmed: 32899982 pmcid: 7571063 doi: 10.3390/molecules25184071
Coccetti, P. et al. The CK2 phosphorylation of catalytic domain of Cdc34 modulates its activity at the G1 to S transition in Saccharomyces cerevisiae. Cell Cycle 7, 1391–1401 (2008).
pubmed: 18418079 doi: 10.4161/cc.7.10.5825
Toni, M. et al. Environmental temperature variation affects brain protein expression and cognitive abilities in adult zebrafish (Danio rerio): A proteomic and behavioural study. J. Proteom. 204, 103396 (2019).
doi: 10.1016/j.jprot.2019.103396
Singh, S. et al. SATPdb: A database of structurally annotated therapeutic peptides. Nucleic Acids Res. 44, D1119–D1126 (2016).
pubmed: 26527728 doi: 10.1093/nar/gkv1114
Qin, D. et al. DFBP: A comprehensive database of food-derived bioactive peptides for peptidomics research. Bioinformatics 38, 3275–3280 (2020).
doi: 10.1093/bioinformatics/btac323

Auteurs

Michele Manoni (M)

Department of Veterinary Medicine and Animal Science (DIVAS), University of Milan, Via dell'Università 6, 26900, Lodi, Italy. michele.manoni@unimi.it.

Alessandra Altomare (A)

Department of Pharmaceutical Sciences (DISFARM), University of Milan, Via Mangiagalli 25, 20133, Milan, Italy.

Simona Nonnis (S)

Department of Veterinary Medicine and Animal Science (DIVAS), University of Milan, Via dell'Università 6, 26900, Lodi, Italy.
CRC I-WE, Coordinating Research Centre: Innovation for Well-Being and Environment, University of Milan, Via Festa del Perdono 7, 20122, Milan, Italy.

Giulio Ferrario (G)

Department of Pharmaceutical Sciences (DISFARM), University of Milan, Via Mangiagalli 25, 20133, Milan, Italy.

Sharon Mazzoleni (S)

Department of Veterinary Medicine and Animal Science (DIVAS), University of Milan, Via dell'Università 6, 26900, Lodi, Italy.

Marco Tretola (M)

Agroscope, Institute for Livestock Sciences, Rte de la Tioleyre 4, 1725, Posieux, Switzerland.

Giuseppe Bee (G)

Agroscope, Institute for Livestock Sciences, Rte de la Tioleyre 4, 1725, Posieux, Switzerland.

Gabriella Tedeschi (G)

Department of Veterinary Medicine and Animal Science (DIVAS), University of Milan, Via dell'Università 6, 26900, Lodi, Italy.
CRC I-WE, Coordinating Research Centre: Innovation for Well-Being and Environment, University of Milan, Via Festa del Perdono 7, 20122, Milan, Italy.

Giancarlo Aldini (G)

Department of Pharmaceutical Sciences (DISFARM), University of Milan, Via Mangiagalli 25, 20133, Milan, Italy.

Luciano Pinotti (L)

Department of Veterinary Medicine and Animal Science (DIVAS), University of Milan, Via dell'Università 6, 26900, Lodi, Italy.
CRC I-WE, Coordinating Research Centre: Innovation for Well-Being and Environment, University of Milan, Via Festa del Perdono 7, 20122, Milan, Italy.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH