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Journal of Food Science and Technology logoLink to Journal of Food Science and Technology
. 2021 Feb 4;58(9):3465–3472. doi: 10.1007/s13197-021-04990-0

Using BAMLET complex in a functional spreadable cheese elaborated with bovine colostrum

Karen Argelia Reyes-Portillo 1, Aurora Quintero-Lira 1, Javier Piloni-Martini 1, Fernanda Sarahí Fajardo-Espinoza 2, Humberto Hernández-Sánchez 3, Sergio Soto-Simental 1,
PMCID: PMC8292466  PMID: 34366463

Abstract

BAMLET is a bioactive complex formed by the interaction between α-Lactoalbumin (α-LA) and oleic acid which exhibits cytotoxic activity against cancer cells. BAMLET is selectively cytotoxic to malignant cells while sparing the healthy ones. There are, however, no reports about its application in a food matrix. The objective of this work was to synthetize the BAMLET complex from oleic acid and bovine colostrum from the second and third milkings which naturally contain α-LA to prepare two functional spreadable cheeses. The complex was successfully formed and retained in the cheeses as verified through SDS-PAGE applied to the whey obtained. The spreadable cheese from the second milking had a higher protein content (13.56 ± 0.02%) and a higher yield (40%) than the product obtained from the third milking. Even though the cheeses did not show any significant differences (p > 0.05) in the inhibition of the angiotensin-converting enzyme 1, their inhibitory activities were good, as a 0.5 g portion of the cheese from the second milking was sufficient to inhibit 57.52 ± 9.17%, while the cheese from the third milking inhibited 51.48 ± 1.07% of the enzyme. The sensory analysis showed a good acceptance for both spreadable cheeses.

Keywords: BAMLET complex, Bovine colostrum, Spreadable cheese, Formation

Introduction

A complex formed with human α-Lactoalbumin (α-LA) and oleic acid was discovered in 1995 and was named HAMLET (Human Alpha-Lactoalbumin Made Lethal for Tumor cells), presenting tumoricidal action (Hoque et al. 2017). Later, similar complexes were created, one of which was BAMLET (Bovine Alpha-Lactalbumin Made Lethal for Tumor cells) using bovine α-LA that showed cytotoxic activity against more than 40 different lymphomas and carcinomas, differentiating healthy cells without affecting them (Puthia et al. 2014). This cytotoxic effect has been attributed to oleic acid as it disturbs the structure of biological membranes and therefore the function of membrane-bound proteins (Fontana et al. 2013). However, no studies have been published that report that the complex has been created in a food matrix. Furthermore, with regard to bovine milk, α-LA is present at a concentration of 1.2 g L−1, while in bovine colostrum it is found at a concentration of 3.0 g L−1 (Borad and Singh 2018). Over the past few years, the use of bovine colostrum has been investigated due to its functional properties presented by the so-called "first milk". This is the secretion produced by mammals within the first 48 h after farrowing, which is richer in fat, minerals, proteins, bioactive peptides, immunological components, growth factors and vitamins than mature milk (Abdel-Salam et al. 2018; Dzik et al. 2017). Based on the above, the following work was proposed with the objective of forming the BAMLET complex in bovine colostrum from second and third milkings to obtain a spreadable cheese from each milking. It was necessary to verify that the complex was maintained in the cheeses and then characterize them physically and chemically. Moreover, the cheeses containing the complex were evaluated for their ability to inhibit the angiotensin-converting enzyme 1 (ACE1) in order to determine its potential as an antihypertensive product. Finally, a sensory analysis of the products was applied to determine their acceptability among consumers.

Materials and methods

Bovine colostrum from the second and third milkings following calving of clinically healthy third calving Holstein cows was obtained from a dairy farm in Tulancingo de Bravo, Hidalgo, Mexico. The samples were stored under deep freezing conditions (-50 °C) until use.

BAMLET complex preparation

The BAMLET complex in bovine colostrum was prepared according to the methodology described by Delgado et al. (2015). Colostrum samples from second and third milkings were adjusting to pH 5.5 using lactic acid (85%, v/v). Subsequently, the colostrum was heated until to 85 °C in a 5L digital general-purpose water bath (Fisher Scientific Co, Niles, Illinois, USA), after which oleic acid was added (0.36 g in 1 mL of ethanol, w/v). The mix was ultrasonicated for 2 min at 30 °C using an ultrasonic processor model CPX-130 (Cole-Parmer, Vernon Hills, Illinois, USA). The reaction was completed with constant stirring for 30 min at 85 °C, then the BAMLET complex reaction was stopped by cooling under running water and stirred for 24 h at 4 °C. The samples were neutralized to pH 7 with 5 M NaOH and finally ultrasonicated for 1 min at 130 W with pulsations of 10 s at 85% opening (Cole-Parmer, Vernon Hills, Illinois, USA) to finally obtain the BAMLET enriched bovine colostrum ready to make the spreadable cheese.

Spreadable cheese production

The production of spreadable cheese was carried out according to the following methodology. Colostrum from the second and third milking was heated to 38 °C, adding calcium chloride (0.25 g L−1 of colostrum) and stirred until it was completely dissolved to carry out the coagulation process. Next, 4 mL of rennet was added per liter of colostrum, homogenizing the mixture until flocculation and then left for 30 min. The curd was cut gently for 30 min at 38 °C, and was then stored at 4 °C for 12 h, after which the cheese was centrifuged using a Sorvall Legend RT centrifuge (Thermo Scientific, Mundelein, Illinois, USA) at 2980 rpm for 30 min to remove the whey. The mixture was then filtered with # 5 Whatman filter paper with the help of a vacuum pump (Air Admiral 79,202–00, Cole-Parmer, Vernon Hills, Illinois, USA) and stored under refrigeration conditions until use.

SDS-PAGE

To verify that the BAMLET complex was correctly formed and retained in the spreadable cheese, a polyacrylamide gel electrophoresis was performed using the methodology proposed by Laemmli (1970). The bands obtained were compared with a Broad Range 61-0317 (BIO-RAD) wide-range ladder.

Chemical and physicochemical analysis

The pH measurement in the bovine colostrum was performed with a H1 2211 pH/ORP meter (Hanna Instruments, Mexico City, Mexico), with the electrode directly inserted into the spreadable cheese according to the methodology used by Frau, Font de Valdez and Pece (2014). Titratable acidity in colostrum was determined using 10 mL of the sample and titrated with 0.1 N NaOH using phenolphthalein as an indicator, with the results expressed in Dornic degrees (°D) as recommended by Alves et al. (2015). Colostrum density was measured by employing the pycnometer method (Rudosvsky et al. 2008). Lactose content was determined with phenol–sulfuric acid reagent as reported by Dubois et al. (1956). Proximal chemical analysis was determined according to AOAC (2019), moisture (927.05), ash (33.5.05), protein (991.20) and fat (2000.18, 33.7.02) parameters.

Texture analysis

Samples of the cheeses (two spreadable cheeses with BAMLET complex and one commercial spreadable cheese) were analyzed for texture. The test was carried out according to the methodology described by Ghorbel et al. (2016). Samples were placed into containers of 70-mm diameter and 60-mm height, with a completely smooth and uniform surfaces. Furthermore, a TA15/100 cone probe fitted with a 45°, clear acrylic cylinder measuring 30 mm in diameter was employed, which was attached to a Brookfield CT3 texture analyzer (Brookfield, Middleboro, Massachusetts, USA) equipped with a 4.5 kg load cell. Hardness and adhesiveness were calculated using the Texture Pro CT Software, version 1.4 (Brookfield, Middleboro, Massachusetts, USA).

Angiotensin-converting enzyme 1 inhibition

To evaluate the in vitro antihypertensive activity of BAMLET cheeses, the inhibition of the ACE1 was measured through a modification of the spectrophotometric assay of Cushman and Cheung (1971) as described by Fajardo-Espinoza et al. (2020). The colostrum (0.5 mL) and cheese (0.5 g) samples were dissolved in 10 mL distilled water, adjusting their pH to 8.3 and mixing 80 µL of the samples with 200 µL of buffer substrate which consisted of hippuryl histidyl leucine (Sigma Aldrich) dissolved in borate buffer (0.1 M pH 8.3) with 0.3 M NaCl. The mixture was pre-incubated at 37 °C for 3 min and the reaction started with the addition of 20 µL of ACE1 (0.20 U mL−1), with the reaction mixture stirred for 30 s in a vortex agitator and incubated at 37 °C for 30 min. The reaction was stopped with the addition of 250 µL of 1 N HCl, while to extract the hippuric acid, 1.7 mL of ethyl acetate was added to the reaction tubes, mixed and then centrifuged at 1750×g at 4 °C for 5 min using a Sorvall Legend RT centrifuge (Thermo Scientific, Mundelein, Illinois, USA). Once the centrifugation was completed, 800 µL of the organic phase were taken and heated in a bath at 92 °C for 30 min to remove the ethyl acetate. The contents of the tubes were then resuspended in 1 mL of distilled water, shaking each tube for 1 min to resuspension and read at 230 nm in the GENESYS 10S Vis spectrophotometer (Thermo Scientific, Madison, USA). Inhibition percentage was calculated following the next equation:

AI(%)=B-AB-C100

where, AI is inhibitory activity; A, absorbance of sample with inhibitor compound and angiotensin-converting enzyme 1; B, absorbance of angiotensin-converting enzyme 1 without sample (100% activity of angiotensin-converting enzyme 1; C, absorbance of mix of reaction without angiotensin-converting enzyme 1 (0% of activity of angiotensin-converting enzyme 1) and 0% of activity is equal to 20 µL of distilled water instead of enzyme.

Sensory analysis

A sensory evaluation was conducted to compare flavor in spreadable cheeses elaborated with BAMLET colostrum from second and third milkings, with the test performed according to the methodology described by Lucera et al. (2018). A total of 100 untrained panelists aged between 17 and 51 years old tested spreadable cheese samples (3 g each) using a 7-point hedonic scale. Samples were randomly encoded and placed on a natural flavorless cracker. Cheeses were elaborated a day before the analysis and stored at room temperature until 1 h before the evaluation.

Statistical analysis

Results were expressed as the mean ± standard deviation and the experiments were performed in triplicate. For the analysis of the physicochemical composition and texture of the samples, a completely randomized design was applied and analyzed for differences using a one-way Analysis of Variance (ANOVA). The marginal means were compared using a Tukey’s HSD test. The results of the antihypertensive capacity were analyzed with a paired sample means comparison t-test (α = 0.05). A non-parametric Wilcoxon test was applied to verify the panelists’ preferences regarding the flavor of the processed cheeses in the sensory analysis. All data was analyzed using the SPSS software (IBM SPSS Statistics, version 20, USA). A significance level of α = 0.05 was established for all tests.

Results and discussion

Formation of the BAMLET complex in native bovine colostrum

The formation of the BAMLET complex in the second and third milkings of native bovine colostrum indicates that 23.85 µmol of oleic acid bonded to 1 µmol α-LA. This obtained ratio is within the range reported by Dopierała et al. (2019) for the formation of complexes such as HAMLET and BAMLET, as they describe a binding of 8.5 to 48 µmol of oleic acid for each µmol of α-LA. Therefore, it is concluded that the adapted methodology is suitable for directly forming the BAMLET complex in bovine colostrum after the addition of oleic acid under the necessary conditions of pH, heating and agitation (Permyakov et al. 2011).

Spreadable cheeses with BAMLET complex of bovine colostrum (SC)

Two spreadable cheeses were obtained with a bovine colostrum BAMLET complex from the second (SC2) and third milkings (SC3). Both presented a yellow coloration and a thicker consistency compared to a cheese made from mature milk. These physical characteristics can be mainly attributed to the fat content as well as the carotenoids present in bovine colostrum (McGrath et al. 2016) that differentiate it from milk with regard to color (Abdel-Salam et al. 2018). In addition, cheeses containing the BAMLET complex made with the binding of oleic acid to α-LA, have a long shelf life in the gastrointestinal tract, as reported by Dopierała et al. (2019). This is because it is relatively resistant to digestive proteases such as pepsin and trypsin due to their compact and globular structure, indicating that this complex would remain stable until carrying out its cytotoxic action. Moreover, a yield of 40% was obtained in the SC2 and 30% for SC3, which are higher than the yield obtained for mature milk, mainly due to the proportion of the constituents of colostrum, such as a higher concentration of solids, proteins, fat and ash (Borad and Singh 2018).

BAMLET complex retention in the spreadable cheese

Figure 1 shows the electrophoretic profiles performed for verifying the retention of the complex in the spreadable cheese. In gel (a), the presence of α-LA is observed in lanes 3 and 6 at 14,200 Da, where whey from native colostrum of second milking was introduced. In contrast, it is absent in lanes 4 and 5 into which the whey of the second milking SC was placed. The third milking samples were placed in gel (b) where it can also be seen that the α-LA band is present in the NC whey (lanes 3 and 6) but absent in the spreadable cheeses made from colostrum with BAMLET (lanes 4 and 5). The absence of the α-LA band indicates that the protein bound with oleic acid and remained as a complex in the cheese, which does not occur in a conventional cheese making process with mature milk, since most of the α-LA is lost in the whey fraction and is normally a protein of cheese whey (Lappa et al. 2019).

Fig. 1.

Fig. 1

Changes in protein profile during the preparation of spreadable cheese using second (a) and third (b) milking bovine colostrum

Physicochemical profile of native bovine colostrum and bovine colostrum with BAMLET complex

The physicochemical profile of native bovine colostrum (NB) and bovine colostrum (BC) with the BAMLET complex is presented in Table 1. The data obtained indicates that there are significant differences (p < 0.05) in the NB and the BC protein content between the second and third milkings. It is important to highlight that the protein content in the BC increased (8.01% and 5.17% for the second and third milkings, respectively) compared to the NC (6.60% and 4.08% for the second and third milkings, respectively). The differences between the milkings are attributed to the fact that the colostrum with the best quality and the highest concentration of components is obtained in the first milking and as the lactation cycle progresses, its components are diluted until the colostrum turns into milk. Meanwhile, the parameters for humidity and lactose increased until reaching the standard values for mature milk, although some variations may occur due mainly to the physiological factors of the cows such as the calving number, age and feed (Borad and Singh 2018). The increase in the protein observed in the BC samples can be attributed to the heat treatment used to form the complex, which concentrated the proteins through partial evaporation. However, the differences between NC and BC from the same milkings were not significant (p > 0.05). On the other hand, the NaOH used to neutralize the bovine colostrum generated some salts as well as the lactic acid that was used to lower the pH at the beginning of the reaction, which also caused a slight increase in ash content in the BC. Various methodologies described for the preparation for BAMLET complexes (Brinkmann et al. 2011; Delgado et al. 2015; Fang et al. 2014) state that for the formation of the cytotoxic complex, a low pH and heat treatment are required. This in turn leads to a better coupling of the oleic acid caused by denaturation and the new conformation of α-LA to its apo form, exposing its hydrophobic nucleus where fatty acid binds, in addition to the fact that this denaturation is the key to the antitumor effect of BAMLET complex.

Table 1.

Physicochemical properties of native bovine colostrum and bovine colostrum with BAMLET complex

Treatmentse
NC2 NC3 BC2 BC3
Dry extract (%) 16.48 ± 0.05b 14.18 ± 0.24a 16.61 ± 0.45b 15.39 ± 0.30a
Moisture (%) 83.52 ± 0.05a 85.82 ± 0.24b 83.39 ± 0.45a 84.61 ± 031b
Ash (%) 1.01 ± 0.00b 0.89 ± 0.01a 1.20 ± 0.03b 1.06 ± 0.00a
Protein (%) 6.60 ± 0.29b 4.08 ± 0.28a 8.01 ± 0.21b 5.17 ± 0.00a
Fat (%) 4.98 ± 0.02b 4.55 ± 0.15a 12.00 ± 0.00b 4.82 ± 0.05a
Lactose (%) 3.15 ± 0.20a 4.20 ± 0.24b 3.37 ± 0.70a 3.54 ± 0.28a
Acidity (%) 0.42 ± 0.00b 0.38 ± 0.00a 0.72 ± 0.02d 0.52 ± 0.07c
pH 6.19 ± 0.01b 6.17 ± 0.00a 7.00 ± 0.00c 7.00 ± 0.00c
Density (g/mL) 1.038 ± 0.001c 1.036 ± 0.001b 1.046 ± 0.001d 1.033 ± 0.000a

a,b,c,dMeans ± standard deviation (SD) in the same row with different superscripts differ significantly (p < 0.05)

eNC2 = native bovine colostrum of second milking, NC3 = native bovine colostrum of third milking, BC2 = bovine colostrum of second milking with BAMLET complex, BC3 = bovine colostrum of third milking with BAMLET complex

Physicochemical profile of spreadable cheeses with BAMLET complex of bovine colostrum

The physicochemical characteristics of the SC are summarized in Table 2, with the obtained protein and fat values revealing that the cheeses differ significantly from each other (p < 0.05). SC have a higher protein content compared to a cheese reported with mature milk (Ghorbel et al. 2016) due to the substantial composition of colostrum and the formation of the complex. However, through the combination of α-LA with oleic acid, the protein remained in the cheese without being lost in the whey as happens with more conventional processes. Furthermore, SC were also characterized by a lower fat content (6.75% and 9.5%, second and third milkings, respectively) and acidity (0.23% and 0.26%, second and third milkings, respectively) compared to a cream cheese made from mature milk reported by Brighenti et al. (2018), characteristics which were attributed to the methodology used for the formation of the complex.

Table 2.

Physical and chemical properties of spreadable cheeses of bovine colostrum with BAMLET complex

Treatmentsc
SC2 SC3
Dry extract (%) 25.44 ± 0.50a 24.00 ± 1.45a
Humidity (%) 74.56 ± 0.50a 76.00 ± 1.45a
Ash (%) 1.81 ± 0.01a 1.80 ± 0.04a
Protein (%) 13.56 ± 0.02a 11.00 ± 0.11b
Fat (%) 6.75 ± 0.25a 9.5 ± 0.00b
Lactose (%) 6.71 ± 0.81a 7.05 ± 0.48a
Acidity (%) 0.23 ± 0.00a 0.26 ± 0.00a
pH 6.77 ± 0.05a 6.79 ± 0.01a

a,b Means ± standard deviation (SD) in the same row with different superscripts significantly differ (p < 0.05)

cSC2 = spreadable cheese with BAMLET complex of bovine colostrum second milking, SC3 = spreadable cheese with BAMLET complex of bovine colostrum third milking

Texture analysis

The results obtained from the texture analysis carried out in SC and a commercial spreadable cheese (CS) are presented in Table 3. It can be observed that the SC did not show significant differences (p > 0.05) for hardness parameters, as it was softer and less adhesive than the commercial product. There are several factors that influence the texture properties of spreadable cheeses, including protein and fat content, the latter providing lubricity and softness (Hussein and Shalaby 2014). In addition, Korish and Abd Elhamid (2012) report that higher humidity leads to lower hardness values in products, with the BAMLET cheeses recording high humidity percentages (74.56% and 76%, second and third milkings, respectively). Lee and Klostermeyer (2001) state that the hardness has little to do with high pH values, and the pH of the BAMLET in this study oscillated between 6.77 and 6.79 (second and third milkings, respectively). Furthermore, SC had higher alkaline content than the commercial product as well as being less salty, both of which are factors that contribute to softness according to Kaminarides et al. (2006). Regarding adhesiveness, this parameter increases with lower protein content (Zheng et al. 2016). According to a study carried out by Bayarri et al. (2012) on 8 commercial spreadable cheese samples, lower protein content was found compared with the spreadable cheeses of the BAMLET complex which was attributed to the composition of colostrum and complex formation, contributing to the low adhesiveness values.

Table 3.

Textural properties of spreadable cheeses with BAMLET complex of bovine colostrum and commercial spreadable cheese

Treatmentsc
SC2 SC3 CS
Hardness (N) 1.64 ± 0.40a 0.87 ± 0.22a 13.40 ± 2.26b
Adhesiveness (N) 0.28 ± 0.08ab 0.17 ± 0.04a 0.40 ± 0.01b

a,b Means ± standard deviation (SD) in the same row with different superscripts significantly differ (p < 0.05)

cSC2 = spreadable cheese with BAMLET complex of bovine colostrum second milking, SC3 = spreadable cheese with BAMLET complex of bovine colostrum third milking, CS = commercial spreadable cheese

Antihypertensive property of BAMLET spreadable cheese

Figure 2 shows the percentages of inhibition of the ACE1 to evaluate its functionality as a possible food and to determine its antihypertensive capacity. While there are no significant differences (p > 0.05) between the second milking samples, the second milking NC had the highest percentage of inhibition (72.27 ± 8.82%), and the third milking BC had the lowest percentage of inhibition (50.11 ± 12.83%). The highest activity observed in the second milking NC can be attributed to the release of bioactive peptides (Layman et al. 2018). The decreased activity in third milking BC suggests that a high temperature heat treatment (similar to the one that was carried out for the generation of the complex) as well as a change in pH deteriorates the stability of ACE inhibitor peptides. However, this bioactivity was not lost and only decreased as it is known that these peptides can resist pH ranges of 1.0–8.0 and temperatures of up to 110 °C (Wu et al. 2014). Even so, there were no significant differences (p > 0.05) in all treatments from the second milking samples. Furthermore, the synthetic inhibitor captopril was used as a control, which showed that 21.79 mg inhibited 66.19 ± 17.35% of the ACE compared with SC. A 0.5 g portion of the second milking was sufficient to inhibit 57.52 ± 9.17%, while the cheese from the third milking inhibited 51.48 ± 1.07%. However, synthetic inhibitors have the disadvantage of presenting side effects such as coughs, taste disorders and skin rash (Chen et al. 2013). Therefore, spreadable cheeses obtained with the BAMLET complex of bovine colostrum could be a natural alternative for the treatment of blood pressure, as it contains a cytotoxic complex.

Fig. 2.

Fig. 2

Inhibition of ACE by spreadable cheese with BAMLET complex. a,bMeans ± standard deviation (SD) with different letters differ significantly (p ≤ 0.05). NC native bovine colostrum, BC BOVINE colostrum with BAMLET complex, SC spreadable cheese with BAMLET complex of bovine colostrum (n = 2)

Sensory analysis

Figure 3 shows the degree of taste satisfaction for the SC, with no significant differences found according to the Wilcoxon non-parametric test (p > 0.05). However, it can be observed that the highest frequencies for cheeses were located at the "I like" and “I do not like or dislike” points, which can be attributed to the composition of the bovine colostrum. Colostrum contains a higher fat content than mature milk, resulting in a product with more smoothness which is pleasing to the palate of consumers, while the use of oleic acid suggests an improvement in the sensory characteristics of the cheeses. The average age of the consumers who applied the analysis was 24.8 years, Markey et al. (2017) reported that this consumer is more sensitive to the changes in the profile of the cheese compositions. The results from this study indicate that panelist accept the cheeses obtained from bovine colostrum either SC2 and SC3, which would imply potential consumer acceptance in the functional food market.

Fig. 3.

Fig. 3

Sensorial analysis of the spreadable cheeses with BAMLET complex of bovine colostrum. 1 = I like it extremely, 2 = I like very much, 3 = I like, 4 = I do not like or dislike, 5 = I do not like, 6 = I really dislike, 7 = I dislike extremely. SC2 = spreadable cheese with BAMLET complex of bovine colostrum second milking, SC3 = spreadable cheese with BAMLET complex of bovine colostrum third milking

Conclusions

The findings of the present study indicate that the methodology developed for the formation of the BAMLET complex in bovine colostrum was effective and that it is possible to successfully obtain a spreadable cheese with its use. This was corroborated by means of an SDS-PAGE performed in the whey of the cheese obtained, indicating that the complex was retained in the food matrix as the α-LA band was absent, leading to the assumption that this protein was completely bound to oleic acid in the form of the complex. This could also explain the increase in protein content in the colostrum spreadable cheeses. In addition, it was shown that the spreadable cheeses with the complex have an adequate antihypertensive capacity, while the texture characteristic is improved for spreadable products as they are softer and less adhesive than commercial spreadable cheese. In addition, the results obtained from the sensory analysis suggest a good acceptance by the consumer towards the spreadable cheeses with the BAMLET complex.

Acknowledgements

Reyes-Portillo K.A. received 928777 grant number from Consejo Nacional de Ciencia y Tecnología, Mexico.

Author contributions

MSc Karen Argelia Reyes-Portillo carried out the work and wrote of the manuscript, Dr Aurora Quintero-Lira supervised the work and contribute to wrote the manuscript, Dr Fernanda Sarahí Fajardo-Espinoza carried out some experiments and wrote the manuscript, Dr Javier Piloni-Martini conceiving the study, supervised the work and wrote the manuscript, Dr Humberto Hernández-Sánchez conceiving the study, supervised the work, edited and corrected the manuscript, Sergio Soto-Simental conceiving the study, supervised the work, wrote, edit and corrected the manuscript.

Funding

A grant number 928777 was obtained from Consejo Nacional de Ciencia y Tecnología, Mexico.

Availability of data and material

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no competing interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Abdel-Salam ZA, Abdel-Salam SAM, Abdel-Mageed II, Harith MA. Evaluation of proteins in sheep colostrum via laser-induced breakdown spectroscopy and multivariate analysis. J Adv Res. 2018;15:19–25. doi: 10.1016/j.jare.2018.07.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alves AC, Alves NG, Ascari IJ, Junqueira FB, Coutinho AS, Lima RR, Pérez JRO, De Paula SO, Furusho-Garcia IF, Abreu LR. Colostrum composition of Santa Inês sheep and passive transfer of immunity to lambs. J Dairy Sci. 2015;98:3706–3716. doi: 10.3168/jds.2014-7992. [DOI] [PubMed] [Google Scholar]
  3. Bayarri S, Carbonell I, Costell E. Viscoelasticity and texture of spreadable cheeses with different fat contents at refrigeration and room temperatures. J Dairy Sci. 2012;95:6926–6936. doi: 10.3168/jds.2012-5711. [DOI] [PubMed] [Google Scholar]
  4. Borad SG, Singh AK. Colostrum immunoglobulins: Processing, preservation and application aspects. Int Dairy J. 2018;85:201–210. doi: 10.1016/j.idairyj.2018.05.016. [DOI] [Google Scholar]
  5. Brighenti M, Govindasamy-Lucey S, Jaeggi JJ, Johnson ME, Lucey JA. Effects of processing conditions on the texture and rheological properties of model acid gels and cream cheese. J Dairy Sci. 2018;101:6762–6775. doi: 10.3168/jds.2018-14391. [DOI] [PubMed] [Google Scholar]
  6. Brinkmann CR, Thiel S, Larsen MK, Petersen TE, Jensenius JC, Heegaard CW. Preparation and comparison of cytotoxic complexes formed between oleic acid and either bovine or human α-lactalbumin. J Dairy Sci. 2011;94:2159–2170. doi: 10.3168/jds.2010-3622. [DOI] [PubMed] [Google Scholar]
  7. Chen J, Wang Y, Ye R, Wu Y, Xia W. Comparison of analytical methods to assay inhibitors of angiotensin I-converting enzyme. Food Chem. 2013;141:3329–3334. doi: 10.1016/j.foodchem.2013.06.048. [DOI] [PubMed] [Google Scholar]
  8. Cushman DW, Cheung HS. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem Pharmacol. 1971;20:1637–1648. doi: 10.1016/0006-2952(71)90292-9. [DOI] [PubMed] [Google Scholar]
  9. Delgado Y, Morales-Cruz M, Figueroa CM, Hernández-Román J, Hernández G, Griebenow K. The cytotoxicity of BAMLET complexes is due to oleic acid and independent of the α-lactalbumin component. FEBS Open Bio. 2015;5:397–404. doi: 10.1016/j.fob.2015.04.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dopierała K, Krajewska M, Prochaska K. Binding of α-lactalbumin to oleic acid monolayer and its relevance to formation of HAMLET-like complexes. Int Dairy J. 2019;89:96–104. doi: 10.1016/j.idairyj.2018.08.017. [DOI] [Google Scholar]
  11. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method of determination of sugars and related substances. Anal Chem. 1956;28:350–356. doi: 10.1021/ac60111a017. [DOI] [Google Scholar]
  12. Dzik S, Miciński B, Aitzhanova I, Miciński J, Pogorzelska J, Beisenov A, Kowalski IM. Properties of bovine colostrum and the possibilities of use. Pol Ann Med. 2017;24:295–299. doi: 10.1016/j.poamed.2017.03.004. [DOI] [Google Scholar]
  13. Fajardo-Espinoza FS, Romero-Rojas A, Hernández-Sánchez H. Production of bioactive peptides from bovine colostrum whey using enzymatic hydrolysis. Rev Mex Ing Quim. 2020;19:1–9. doi: 10.24275/rmiq/Alim525. [DOI] [Google Scholar]
  14. Fang B, Zhang M, Tian M, Jiang L, Guo HY, Ren FZ. Bovine lactoferrin binds oleic acid to form an anti-tumor complex similar to HAMLET. BBA Mol Cel Biol L. 2014;1841:535–543. doi: 10.1016/j.bbalip.2013.12.008. [DOI] [PubMed] [Google Scholar]
  15. Fontana A, Spolaore B, Polverino de Laureto P. The biological activities of protein/oleic acid complexes reside in the fatty acid. Biochim Biophys Acta. 2013;1834:1125–1143. doi: 10.1016/j.bbapap.2013.02.041. [DOI] [PubMed] [Google Scholar]
  16. Frau F, Font de Valdez G, Pece N. Effect of pasteurization temperature, starter culture, and incubation temperature on the physicochemical properties, yield, rheology, and sensory characteristics of spreadable goat cheese. J Food Process. 2014;2014:1–8. doi: 10.1155/2014/705746. [DOI] [Google Scholar]
  17. Ghorbel D, Bettaïeb NB, Ghrib F, Slema MB, Attia H. Textural properties of commercial processed cheese spreads: instrumental and sensory evaluations. Int J Food Prop. 2016;19:1513–1521. doi: 10.1080/10942912.2015.1065425. [DOI] [Google Scholar]
  18. Hoque M, Gupta J, Saleemuddin M. Augmenting the cytotoxicity of oleic acid-protein complexes: potential of target-specific antibodies. Biochimie. 2017;137:139–146. doi: 10.1016/j.biochi.2017.03.013. [DOI] [PubMed] [Google Scholar]
  19. Hussein GAM, Shalaby SM. Microstructure and textural properties of Kareish cheese manufactured by various ways. Ann Agric Sci. 2014;59:25–31. doi: 10.1016/j.aoas.2014.06.004. [DOI] [Google Scholar]
  20. Kaminarides S, Kalogridis D, Massouras T. Creation and quality characterization of processed cheeses derived mainly from Halloumi cheese. Lait. 2006;86:333–343. doi: 10.1051/lait:2006009. [DOI] [Google Scholar]
  21. Korish M, Abd Elhamid AM. Improving the textural properties of Egyptian kariesh cheese by addition of hydrocolloids. Int J Dairy Technol. 2012;65:237–242. doi: 10.1111/j.1471-0307.2011.00818.x. [DOI] [Google Scholar]
  22. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lappa IK, Papadaki A, Kachrimanidou V, Terpou A, Koulougliotis D, Eriotou E, Kopsahelis N. Cheese whey processing: integrated biorefinery concepts and emerging food applications. Foods. 2019;8:347. doi: 10.3390/foods8080347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Layman DK, Lönnerdal B, Fernstrom JD. Applications for α-lactalbumin in human nutrition. Nutr Rev. 2018;76:444–460. doi: 10.1093/nutrit/nuy004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lee SK, Klostermeyer H. The effect of ph on the rheological properties of reduced-fat model processed cheese spreads. LWT-Food Sci Technol. 2001;34:288–292. doi: 10.1006/fstl.2001.0761. [DOI] [Google Scholar]
  26. Lucera A, Costa C, Marinelli V, Saccotelli MA, Del Nobile MA, Conte A. Fruit and vegetable by-products to fortify spreadable cheese. Antioxidants. 2018;7:61. doi: 10.3390/antiox7050061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McGrath BA, Fox PF, McSweeney PLH, Kelly AL. Composition and properties of bovine colostrum: a review. Dairy Sci Technol. 2016;96:133–158. doi: 10.1007/s13594-015-0258-x. [DOI] [Google Scholar]
  28. Markey O, Souroullas K, Fagan CC, Kliem KE, Vasilopoulou D, Jackson KG, Humphries DJ, Grandison AS, Givens DI, Lovegrove JA, Methven L. Consumer acceptance of dairy products with a saturated fatty acid–reduced, monounsaturated fatty acid–enriched content. J Dairy Sci. 2017;100:7953–7966. doi: 10.3168/jds.2016-12057. [DOI] [PubMed] [Google Scholar]
  29. Permyakov SE, Knyazeva EL, Leonteva MV, Fadeev RS, Chekanov AV, Zhadan AP, Håkanssond AP, Akatov VS, Permyakov EA. A novel method for preparation of HAMLET-like protein complexes. Biochimie. 2011;93:1495–1501. doi: 10.1016/j.biochi.2011.05.002. [DOI] [PubMed] [Google Scholar]
  30. Official Methods of Analysis of AOAC INTERNATIONAL (2019) 21th, AOAC International, Gaitherburg, MD, USA, Official methods 927.05; 33.5.05; 991.20 and 2000.18.33.7.02
  31. Puthia M, Storm P, Nadeem A, Hsiung S, Svanborg C. Prevention and treatment of colon cancer by peroral administration of HAMLET (human α-lactalbumin made lethal to tumour cells) Gut. 2014;63:131–142. doi: 10.1136/gutjnl-2012-303715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rudovsky A, Locher L, Zeynerc A, Sobiraj A, Wittek T. Measurement of immunoglobulin concentration in goat colostrum. Small Rumin Res. 2008;74:265–269. doi: 10.1016/j.smallrumres.2007.06.003. [DOI] [Google Scholar]
  33. Wu W, Yu P, Zhang F, Che H, Jiang Z. Stability and cytotoxicity of angiotensin-I-converting enzyme inhibitory peptides derived from bovine casein. J Biomed Biotechnol. 2014;15:143–152. doi: 10.1631/jzus.B1300239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zheng Y, Liu Z, Mo B. Texture profile analysis of sliced cheese in relation to chemical composition and storage temperature. J Chem. 2016;2016:1–10. doi: 10.1155/2016/8690380. [DOI] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.


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