Increased Inhibition of Angiotensin Converting Enzyme (ACE) Obtained from Indonesian Buffalo Meat Protein Using SEP-PAK Plus C18

Authors

  • Rio Olympias Sujarwanta Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Jamhari Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Edi Suryanto Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Rusman Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Setiyono Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Endy Triyannanto Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Yuny Erwanto Department of Animal Product Technology, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia
  • Ragil Yuliatmo Department of Leather Processing Technology, Politeknik ATK, Bantul, Yogyakarta, Indonesia

DOI:

https://doi.org/10.3923/pjn.2018.434.440

Keywords:

ACE-I, buffalo meat, enzymes, hydrolysis, SEP-PAK plus C18

Abstract

Objective: This study aimed to investigate angiotensin converting enzyme (ACE) inhibitory activity derived from Indonesian native buffalo meat and its purified protein using SEP-PAK Plus C18. Methodology: Buffalo meat was hydrolyzed with pepsin, trypsin and a combination of pepsin and trypsin. These hydrolysates were assessed for dissolved protein, the molecular weight of proteins and ACE inhibitory activity. The hydrolysate with the highest ACE inhibitory activity was subsequently purified using SEP-PAK Plus C18. The molecular weight of the proteins was analyzed using descriptive statistics and the dissolved protein content and ACE inhibitory activity were evaluated in a complete randomized design. Results: Buffalo meat contained protein (22.66±0.2%) and dissolved protein (3.67±0.59 mg mL–1). Enzymatic hydrolysis significantly elevated the level of dissolved protein and decreased the molecular weight of the proteins. The dissolved protein content following hydrolysis by pepsin, trypsin and a combination of pepsin and trypsin was 10.91±0.4, 8.09±0.8 and 10.90±0.4 mg mL–1, respectively. The molecular weight of proteins in the buffalo meat homogenate ranged from 40-70 kDa, whereas, the hydrolysates were generally less than 40 kDa. The ACE inhibitory activity of the purified hydrolysate (IC50 = 75.8±20 μg mL–1) was approximately twice that of the hydrolysate (IC50 = 133±18 μg mL–1). Purification using SEP-PAK Plus C18 increased ACE inhibitory activity. Conclusion: Buffalo meat hydrolyzed by pepsin had the highest ACE inhibitory activity compared with other hydrolysates. Purification using SEP-PAK Plus C18 almost doubled the ACE inhibitory activity.

References

Copley, J.B. and R. Rosario, 2005. Hypertension: A review and rationale of treatment. Disease-a-Month, 51: 548-614.

Forouzanfar, M.H., P. Liu, G.A. Roth, M. Ng and S. Biryukov et al., 2017. Global burden of hypertension and systolic blood pressure of at least 110 to 115 mm Hg, 1990-2015. JAMA, 317: 165-182.

Hanif, K., H.K. Bid and R. Konwar, 2010. Reinventing the ACE inhibitors: Some old and new implications of ACE inhibition. Hypertens. Res., 33: 11-21.

Ondetti, M.A., N.J. Williams, E. Sabo, J. Pluscec, E.R. Weaver and O. Kocy, 1971. Angiotensin-converting enzyme inhibitors from the venom of Bothrops jararaca. Isolation, elucidation of structure and synthesis. Biochemistry, 10: 4033-4039.

Cheng, F., T. Wan, Y. Liu, K. Lai, L. Lin and R. Sakata, 2008. Attenuating development of cardiovascular hypertrophy with hydrolysate of chicken leg bone protein in spontaneously hypertensive rats. Asian Aust. J. Anim. Sci., 21: 732-737.

Katayama, K., H. Fuchu, M. Sugiyama, S. Kawahara, K. Yamauchi, Y. Kawamura and M. Muguruma, 2003. Peptic hydrolysate of porcine crude myosin has many active fractions inhibiting angiotensin I-converting enzyme. Asian Aust. J. Anim. Sci., 16: 1384-1389.

Arihara, K., Y. Nakashima, T. Mukai, S. Ishikawa and M. Itoh, 2001. Peptide inhibitors for angiotensin I-converting enzyme from enzymatic hydrolysates of porcine skeletal muscle proteins. Meat Sci., 57: 319-324.

Nakashima, Y., K. Arihara, A. Sasaki, H. Mio, S. Ishikawa and M. Itoh, 2002. Antihypertensive activities of peptides derived from porcine skeletal muscle myosin in spontaneously hypertensive rats. J. Food Sci., 67: 434-437.

Katayama, K., M. Tomatsu, S. Kawahara, K. Yamauchi and H. Fuchu et al., 2004. Inhibitory profile of nonapeptide derived from porcine troponin C against angiotensin I-converting enzyme. J. Agric. Food Chem., 52: 771-775.

Katayama, K., T. Mori, S. Kawahara, K. Miake and Y. Kodama et al., 2007. Angiotensinâ€I converting enzyme inhibitory peptide derived from porcine skeletal muscle myosin and its antihypertensive activity in spontaneously hypertensive rats. J. Food Sci., 72: S702-S706.

Katayama, K., H.E. Anggraeni, T. Mori, A.M. Ahhmed and S. Kawahara et al., 2007. Porcine skeletal muscle troponin is a good source of peptides with angiotensin-I converting enzyme inhibitory activity and antihypertensive effects in spontaneously hypertensive rats. J. Agric. Food Chem., 56: 355-360.

Darewicz, M., J. Borawska, G.E. Vegarud, P. Minkiewicz and A. Iwaniak, 2014. Angiotensin I-converting enzyme (ACE) inhibitory activity and ACE inhibitory peptides of salmon (Salmo salar) protein hydrolysates obtained by human and porcine gastrointestinal enzymes. Int. J. Mol. Sci., 15: 14077-14101.

Nahariah, N., A.M. Legowo, E. Abustam and A. Hintono, 2015. Angiotensin I-Converting enzyme inhibitor activity on egg albumen fermentation. Asian-Aust. J. Anim. Sci., 28: 855-861.

Yuliatmo, R., N.A. Z. Fitriyanto, B. Jamhari and Y. Erwanto, 2016. Increasing of angiotensin converting enzyme inhibitory derived from Indonesian native chicken leg protein using Bacillus cereus protease enzyme. Int. Food Res. J., 24: 1799-1804.

Lee, K.J., S.B. Kim, J.S. Ryu, H.S. Shin and J.W. Lim, 2005. Separation and purification of angiotensin converting enzyme inhibitory peptides derived from goat's milk casein hydrolysates. Asian-Aust. J. Anim. Sci., 18: 741-746.

Liepke, C., H.D. Zucht, W.G. Forssmann and L. Standker, 2001. Purification of novel peptide antibiotics from human milk. J. Chromatogr. B: Biomed. Sci. Applic., 752: 369-377.

Yust, M.M., J. Pedroche, J. Giron-Calle, M. Alaiz, F. Millan and J. Vioque, 2003. Production of ace inhibitory peptides by digestion of chickpea legumin with alcalase. Food Chem., 81: 363-369.

Jamhari, J., L.M. Yusiati, E. Suryanto, M.N. Cahyanto, Y. Erwanto and M. Muguruma, 2013. Purification of angiotensin converting enzyme inhibitory peptide derived from Kacang goat meat protein hydrolysate. J. Indonesian Trop. Anim. Agric., 38: 239-246.

Mohammad, N.P., M.K. Chatli, D.K. Sharma and J. Sahoo, 2010. Effect of cooking methods and fat levels on the physico-chemical, processing, sensory and microbial quality of buffalo meat patties. Asian-Aust. J. Anim. Sci., 23: 1380-1385.

Baco, S., M. Yusuf, B. Wello and M. Hatta, 2013. Current status of reproductive management in Bali cows in South Sulawesi Province, Indonesia. Open J. For., 3: 2-6.

AOACI, 2012. Official Methods of Analysis of AOAC International. 19th Edn., AOAC International, Gaithersburg, Maryland, ISBN: 9780935584837.

Gornall, A.G., C.J. Bardawill and M.M. David, 1949. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem., 177: 751-766.

Laemmli, U.K., 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685.

Cushman, D.W. and H.S. Cheung, 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol., 20: 1637-1648.

Steel, R.G.D., J.H. Torrie and D.A. Dickey, 1997. Principles and Procedures of Statistics: A Biometrical Approach. 3rd Edn., McGraw-Hill Co., New York, USA., ISBN: 9780070610286, Pages: 666.

Kandeepan, G., S.K. Mendiratta, V. Shukla and M.R. Vishnuraj, 2013. Processing characteristics of buffalo meat: A review. J. Meat Sci. Technol., 1: 1-11.

Muhlisin, P., S.J. Lee, J.K. Lee and S.K. Lee, 2014. Effects of crossbreeding and gender on the carcass traits and meat quality of Korean native black pig and Duroc crossbred. Asian-Aust. J. Anim. Sci., 27: 1019-1025.

Muhlisin, C.S.S., Y.J. Rhee, Y.H. Song and S.K. Lee, 2016. Effects of direct-fed microbial and pine cone extract on carcass traits and meat quality of Hanwoo (Korean native cattle). Asian-Aust. J. Anim. Sci., 29: 722-730.

Wells, L., K.A. Edwards and S.I. Bernstein, 1996. Myosin heavy chain isoforms regulate muscle function but not myofibril assembly. EMBO J., 15: 4454-4459.

Martinez, I., R. Slizyte and E. Dauksas, 2007. High resolution two-dimensional electrophoresis as a tool to differentiate wild from farmed cod (Gadus morhua) and to assess the protein composition of klipfish. Food Chem., 102: 504-510.

Lin, W.F., Y.C. Lyu, Y.J. Wu, C.H. Lu and D.F. Hwang, 2012. Species identification of snapper: A food poisoning incident in Taiwan. Food Control, 25: 511-515.

Saiga, A.I., K. Iwai, T. Hayakawa, Y. Takahata, S. Kitamura, T. Nishimura and F. Morimatsu, 2008. Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. J. Agric. Food Chem., 56: 9586-9591.

Iwaniak, A., P. Minkiewicz and M. Darewicz, 2014. Food-originating ACE inhibitors, including antihypertensive peptides, as preventive food components in blood pressure reduction. Compr. Rev. Food Sci. Food Safety, 13: 114-134.

Akillioglu, H.G. and S. Karakaya, 2009. Effects of heat treatment and in vitro digestion on the angiotensin converting enzyme inhibitory activity of some legume species. Eur. Food Res. Technol., 229: 915-921.

Park, Y.W. and M.S. Nam, 2015. Bioactive peptides in milk and dairy products: A review. Korean J. Food Sci. Anim. Resour., 35: 831-840.

Downloads

Published

15.08.2018

Issue

Section

Research Article

How to Cite

Sujarwanta, R. O., Jamhari, Suryanto, E., Rusman, Setiyono, Triyannanto, E., Erwanto, Y., & Yuliatmo, R. (2018). Increased Inhibition of Angiotensin Converting Enzyme (ACE) Obtained from Indonesian Buffalo Meat Protein Using SEP-PAK Plus C18. Pakistan Journal of Nutrition, 17(9), 434–440. https://doi.org/10.3923/pjn.2018.434.440