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. 2020 Jul 16;9(7):170.
doi: 10.3390/biology9070170.

Peptide Profiling and Biological Activities of 12-Month Ripened Parmigiano Reggiano Cheese

Lisa Solieri  1 , Andrea Baldaccini  1 , Serena Martini  1 , Aldo Bianchi  2 , Valentina Pizzamiglio  2 , Davide Tagliazucchi  1
Affiliations

Peptide Profiling and Biological Activities of 12-Month Ripened Parmigiano Reggiano Cheese

Lisa Solieri et al. Biology (Basel). .

Abstract

Proteolysis degree, biological activities, and water-soluble peptide patterns were evaluated in 12 month-ripened Parmigiano Reggiano (PR) cheeses collected in different dairy farms and showing different salt and fat content. Samples classified in high-salt and high-fat group (HH) generally showed lower proteolysis degree than samples having low-salt and low-fat content (LL). This positive correlation between salt/fat reduction and proteolysis was also confirmed by the analysis of biological activities, as the LL group showed higher average values of angiotensin-converting enzyme (ACE)-inhibitory and antioxidant activities. UHPLC/HR-MS allowed the identification of 805 unique peptides: LL and HH groups shared 59.3% of these peptides, while 20.9% and 19.9% were LL and HH specific, respectively. Frequency analysis of peptides identified a core of 183 peptides typical of 12-month ripened PR cheeses (corresponding to the 22.7% of total peptides), but no significant differences were detected in peptide patterns between LL and HH groups. Forty bioactive peptides, including 18 ACE-inhibitors and 12 anti-microbial peptides, were identified, of which 25 firstly found in PR cheese. Globally, this work contributed to unraveling the potentially healthy benefits of peptides fraction in PR cheese and provided prior evidence that PR with reduced fat/salt content showed the highest antihypertensive and antioxidant activities.

Keywords: bioactive peptides; fermented food; lactobacilli; peptidomic; proteomic.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. V.P. and A.B. (Aldo Bianchi) are employed by the Consorzio del Formaggio Parmigiano Reggiano. This does not alter the authors’ adherence to all the journal’s policies on sharing data and materials.

Figures

Figure 1
Figure 1
Total peptides concentration and biological activities of 12-month ripened Parmigiano-Reggiano (PR) peptide fractions. (A) Total peptides concentration. (B) Angiotensin-converting enzyme inhibitory activity. (C) Dipeptidyl-peptidase IV-inhibitory activity. (D) Antioxidant activity. Light grey bars represent PR samples belonging to the high-salt and high-fat group (HH). Dark grey bars represent PR samples belonging to the low-salt and low-fat group (LL). HH represents the average values, considering the samples belonging to the high-salt and high-fat group. LL represents the average values, considering the samples belonging to the low-salt and low-fat group. Average represents the mean values considering all of the 12 PR samples. The x-axis reports the code number of PR samples. Values are means of three assay replications ± standard deviation (SD). Different letters indicate significantly different values (p < 0.05).
Figure 2
Figure 2
Venn diagrams of peptides obtained from Parmigiano-Reggiano (PR) peptide fractions. (A) Venn diagram created with all the identified peptides in the 12 PR peptide fractions (see online supplementary material Table S1 for the peptide sequences). (B) Venn diagram created with bioactive peptides identified in the 12 PR peptide fractions (see Table 1 for the peptide sequences). HH represents the samples belonging to the high-salt and high-fat group. LL represents the samples belonging to the low-salt and low-fat group.
Figure 3
Figure 3
Frequency of identification of the peptides in the Parmigiano-Reggiano (PR) peptide fractions. (A) Frequency of identification of the peptides considering all of the 12 PR samples. (B) Frequency of identification of the peptides in the 6 PR samples belonging to the high-salt and high-fat group. (C) Frequency of identification of the peptides in the 6 PR samples belonging to the low-salt and low-fat group. (D) Frequency of identification of the bioactive peptides considering all of the 12 PR samples. The numbers from 1 to 12 or from 1 to 6 indicate the number of PR samples in which the peptides were identified. The percentage values are referred to the % of peptides found in the PR samples. For example, in Figure 3A, 31.9% of single peptides were found in an individual PR sample, whereas the 10.3% of peptides were common in all of the 12 PR samples.
Figure 4
Figure 4
Distribution of peptides characterized by angiotensin-converting enzyme (ACE) inhibitory IC50 values lower than 300 µmol/L along with principal components 1 (PC1) and 2 (PC2). IC50 represent the concentration of peptide able to inhibit the enzymatic activity by 50%. Yellow diamonds represent LL class samples, red diamonds represent HH class samples, green circle represents the biological activity (ACE-inhibition), and blue triangles represent the bioactive peptides.
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References

    1. Godos J., Tieri M., Ghelfi F., Titta L., Marventano S., Lafranconi A., Gambera A., Alonzo E., Sciacca S., Buscemi S., et al. Dairy foods and health: An umbrella review of observational studies. Int. J. Food Sci. Nutr. 2019;71:138–151. doi: 10.1080/09637486.2019.1625035. - DOI - PubMed
    1. Guo J., Givens D.I., Astrup A., Bakker S.J.L., Goossens G.H., Kratz M., Marette A., Pijl H., Soedamah-Muthu S.S. The impact of dairy products in the development of type 2 diabetes: Where does the evidence stand in 2019? Adv. Nutr. 2019;10:1066–1075. doi: 10.1093/advances/nmz050. - DOI - PMC - PubMed
    1. Tagliazucchi D., Martini S., Solieri L. Bioprospecting for bioactive peptide production by lactic acid bacteria isolated from fermented dairy food. Fermentation. 2019;5:96. doi: 10.3390/fermentation5040096. - DOI
    1. Summer A., Formaggioni P., Franceschi P., Di Frangia F., Righi F., Malacarne M. Cheese as functional food: The example of Parmigiano-Reggiano and Grana Padano. Food Technol. Biotech. 2017;55:277–289. doi: 10.17113/ftb.55.03.17.5233. - DOI - PMC - PubMed
    1. Sforza S., Galaverna G., Neviani E., Pinelli C., Dossena A., Marchelli M. Study of the oligopeptide fraction in Grana Padano and Parmigiano-Reggiano cheeses by liquid chromatography-electrospray ionization mass spectrometry. Eur. J. Mass Spectrom. 2004;10:421–427. doi: 10.1255/ejms.603. - DOI - PubMed