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Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum

Yıl 2023, Cilt: 13 Sayı: 4, 2847 - 2860, 01.12.2023
https://doi.org/10.21597/jist.1312143

Öz

Angiotensin-converting enzyme (ACE, EC 3.4.15.1) is a physiological target for researching new antihypertensive drugs, as it is a substantial enzyme in the regulation of blood pressure. Herein, ACE was purified from human serum with affinity chromatography. Vmax and KM values were found as 60.98 (µmol/min)/mL and 0.34 mM, respectively. The effects of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) bioactive peptides on purified ACE were researched. Also, captopril, a specific ACE inhibitory, was used as a reference inhibitor. Bioactive peptides, GRGDS and RGD, demonstrated the inhibitory effect on purified ACE with IC50 values of 46.39 µM and 456.46 µM, respectively. Ki values and kind of inhibition for GRGDS and RGD by the Lineweaver-Burk chart were found. The kind of inhibitory for these bioactive peptides was calculated as reversible-competitive inhibitory. Ki values for GRGDS and RGD were obtained as 93.28 µM and 435.67 µM, respectively. The IC50 value of captopril was designated as 1.57 nM. The inhibitory kind of captopril was designated as reversible non-competitive inhibitory and the Ki value was 0.99 nM. In this study, it was concluded that RGD and GRGDS bioactive peptides have the potential to be utilized as ACE inhibitors.

Kaynakça

  • Adelman B, Gennings C, Strony J, Hanners E, 1990. Synergistic inhibition of platelet aggregation by fibrinogen-related peptides. Circulation Research, 67(4): 941–947.
  • Arnaout MA, Mahalingam B, Xiong JP, 2005. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol., 21: 381-410.
  • Aydin F, Turkoglu V, Bas Z, 2021. Purification and characterization of angiotensin-converting enzyme (ACE) from sheep lung, Molecular Biology Reports 48: 4191-4199.
  • Balti R, Bougatef A, Guillochon D, Dhulster P, Nasri M, Nedjar-Arroume N, 2012. Changes in arterial blood pressure after single oral administration of cuttlefish (Sepia officinalis) muscle derived peptides in spontaneously hypertensive rats. Journal of Functional Foods, 4(3): 611-617.
  • Bas Z, 2021. Inhibition effect of nicotinamide (vitamin B3) and reduced glutathione (GSH) peptide on angiotensin-converting enzyme activity purified from sheep kidney. International Journal of Biological Macromolecules, 189: 65-71.
  • Bas Z, Turkoglu V, Goz Y, 2022. Investigation of inhibition effect of butanol and water extracts of Matricaria chamomilla L. on angiotensin-converting enzyme purified from human plasma. Biotechnology and Applied Biochemistry, 69: 273–280.
  • Basi Z, Turkoglu V, 2018. Purification of angiotensin-converting enzyme from human plasma and investigation of the effect of some active ingredients isolated from Nigella sativa L.extract on the enzyme activity. Biomedical Chromatography, 32: e4175.
  • Basi Z, Turkoglu V, 2019. In vitro effect of oxidized and reduced glutathione peptides on angiotensin converting enzyme purified from human plasma. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 1104: 190-195.
  • Baudin B, Bénéteau-Burnat B, 1999. Mixed-type inhibition of pulmonary angiotensin I-converting enzyme by captopril, enalaprilat and ramiprilat. Journal of Enzyme Inhibition, 14(6): 447–456.
  • Bernstein KE, Khan Z, Giani JF, Cao DY, Bernstein EA, Shen XZ, 2018. Angiotensin-converting enzyme in innate and adaptive immunity. Nature Reviews. Nephrology, 14(5): 325–336.
  • Bhaskar B, Ananthanarayan L, Jamdar S, 2019. Purification, identification, and characterization of novel angiotensin I-converting enzyme (ACE) inhibitory peptides from alcalase digested horse gram flour. LWT, 103: 155-161.
  • Bondre SV, Chavan RS, Raut, ID, Mohite SK, Magdum, CS, 2020. An overview of survey on antihypertensive drugs. Asian Journal of Pharmaceutical Research, 10 (3): 160–162.
  • Bradford MM, 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-54.
  • Chen J, Yu X, Chen Q, Wu Q, He Q, 2022. Screening and mechanisms of novel angiotensin-I-converting enzyme inhibitory peptides from rabbit meat proteins: A combined in silico and in vitro study. Food Chemistry, 370: 131070.
  • Colombo M, Bianchi A, 2010. Click chemistry for the synthesis of RGD-containing integrin ligands. Molecules (Basel, Switzerland), 15(1): 178–197.
  • Contreras MDM, Carrón R, Montero MJ, Ramos M, Recio I, 2009. Novel casein-derived peptides with antihypertensive activity. International Dairy Journal, 19(10): 566-573.
  • El-Dorry HA, Bull HG, Iwata K, Thornberry NA, Cordes EH, Soffer RL, 1982. Molecular and catalytic properties of rabbit testicular dipeptidyl carboxypeptidase. Journal of Biological Chemistry, 257(23): 14128-14133.
  • He R, Malomo SA, Girgih AT, Ju X, Aluko RE, 2013. Glycinyl-histidinyl-serine (GHS), a novel rapeseed protein-derived peptide has blood pressure-lowering effect in spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry, 61(35): 8396–8402.
  • Hermida, RC, Ayala, DE, Fernández JR, Portaluppi F, Fabbian F, Smolensky MH, 2011. Circadian rhythms in blood pressure regulation and optimization of hypertension treatment with ACE inhibitor and ARB medications. American Journal of Hypertension, 24(4): 383-391.
  • Holmquist B, Bünning P, Riordan JF, 1979. A continuous spectrophotometric assay for angiotensin converting enzyme. Analytical Biochemistry, 95 (2): 540-548.
  • Hooper NM, Turner AJ, 1987. Isolation of two differentially glycosylated forms of peptidyl-dipeptidase A (angiotensin converting enzyme) from pig brain: a re-evaluation of their role in neuropeptide metabolism. The Biochemical Journal, 241(3): 625–633.
  • Karahan F, Turkoglu V, 2021 Enhanced purification protocol for the angiotensin-converting enzyme from bovine systems and investigation of the in vitro effect of some active substances Chemico-Biological Interactions, 347: 109604.
  • Kitts DD, Weiler K, 2003. Bioactive proteins and peptides from food sources. Applications of bioprocesses used in isolation and recovery. Current Pharmaceutical Design, 9: 1309–1323.
  • Kiylik A, Turkoglu V, Bas Z, 2022. Purification of angiotensin-converting enzyme (ACE) from sheep kidney and inhibition effect of reduced nicotinamide adenine dinucleotide (NADH) on purified ACE activity. Cell Biochemistry and Biophysics, 80: 115-122.
  • Laemmli UK, 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685.
  • Lavoie JL, Sigmund, CD, 2003. Minireview: overview of the renin-angiotensin system—an endocrine and paracrine system. Endocrinology, 144(6): 2179-2183.
  • Liang F, Shi Y., Shi J, Zhang T, Zhang R, 2021. A novel Angiotensin-I-converting enzyme (ACE) inhibitory peptide IAF (Ile-Ala-Phe) from pumpkin seed proteins: in silico screening, inhibitory activity, and molecular mechanisms. European Food Research and Technology, 247(9): 2227-2237.
  • Lin Q, Liao W, Bai J, Wu W, Wu J, 2017. Soy protein-derived ACE-inhibitory peptide LSW (Leu-Ser-Trp) shows anti-inflammatory activity on vascular smooth muscle cells. Journal of Functional Foods, 34: 248-253.
  • Lineweaver H, Burk D, 1934. The determination of enzyme dissociation constants. Journal of the American Chemical Society, 56: 658–660.
  • Ma T, Fu Q, Mei Q, Tu Z, Zhang L, 2021. Extraction optimization and screening of angiotensin-converting enzyme inhibitory peptides from Channa striatus through bioaffinity ultrafiltration coupled with LC-Orbitrap-MS/MS and molecular docking. Food Chemistry, 354: 129589.
  • Majumder K, Chakrabarti S, Morton JS, Panahi S, Kaufman S, Davidge ST, Wu J, 2013. Egg-derived tri-peptide IRW exerts antihypertensive effects in spontaneously hypertensive rats. PloS One, 8(11): e82829.
  • Majumder K, Wu J, 2014. Molecular targets of antihypertensive peptides: understanding the mechanisms of action based on the pathophysiology of hypertension. International Journal of Molecular Sciences, 16(1): 256-283.
  • Miguel M, Gómez-Ruiz JÁ, Recio I, Aleixandre A, 2010. Changes in arterial blood pressure after single oral administration of milk-casein-derived peptides in spontaneously hypertensive rats. Molecular nutrition & food research, 54(10): 1422–1427.
  • Miyamoto S, Akiyama SK, Yamada, KM, 1995. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science (New York, N.Y.), 267(5199): 883–885.
  • Nicosia RF, Bonanno E, 1991. Inhibition of angiogenesis in vitro by Arg-Gly-Asp-containing synthetic peptide. The American Journal of Pathology, 138(4): 829–833.
  • Perazella MA, Setaro JF, 2003. Renin-angiotensin-aldosterone system: fundamental aspects and clinical implications in renal and cardiovascular disorders. Journal of Nuclear Cardiology: Official Publication of the American Society of Nuclear Cardiology, 10(2): 184–196.
  • Rezzani R, Porteri E, De Ciuceis C, Bonomini F, Rodella LF, Paiardi S, Boari GE, Platto C, Pilu A, Avanzi D, Rizzoni D, Agabiti Rosei E, 2010. Effects of melatonin and Pycnogenol on small artery structure and function in spontaneously hypertensive rats. Hypertension, 55 (6) : 1373–1380.
  • Sabeur K, Vo AT, Ball BA, 2001. Characterization of angiotensin-converting enzyme in canine testis. Reproduction (Cambridge, England), 122(1) : 139–146.
  • Sánchez A, Vázquez, A, 2017. Bioactive peptides: A review. Food Quality and Safety, 1: 29-46.
  • Thavasu PW, Longhurst S, Joel SP, Slevin ML, Balkwill FR, 1992. Measuring cytokine levels in blood. Importance of anticoagulants, processing, and storage conditions. Journal of Immunological Methods, 153(1-2) : 115–124.
  • Turpeinen AM, Järvenpää, S, Kautiainen H, Korpela R, Vapaatalo H, 2013. Antihypertensive effects of bioactive tripeptides - a random effects meta-analysis. Annals of Medicine, 45(1) : 51-56.
  • Wang F, Li Y, Shen Y, Wang A, Wang S, Xie, T, 2013. The functions and applications of RGD in tumor therapy and tissue engineering. International Journal of Molecular Sciences, 14(7) : 13447–13462.
  • Welschoff J, Matthey M, Wenzel D, 2014. RGD peptides induce relaxation of pulmonary arteries and airways via β3-integrins. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 28(5): 2281–2292.
  • Zhang N, Li F, Zhang T, Li, CY, Zhu L, Yan S, 2022. Isolation, identification, and molecular docking analysis of novel ACE inhibitory peptides from Spirulina platensis. European Food Research and Technology, 248(4): 1107-1115.
Yıl 2023, Cilt: 13 Sayı: 4, 2847 - 2860, 01.12.2023
https://doi.org/10.21597/jist.1312143

Öz

Kaynakça

  • Adelman B, Gennings C, Strony J, Hanners E, 1990. Synergistic inhibition of platelet aggregation by fibrinogen-related peptides. Circulation Research, 67(4): 941–947.
  • Arnaout MA, Mahalingam B, Xiong JP, 2005. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol., 21: 381-410.
  • Aydin F, Turkoglu V, Bas Z, 2021. Purification and characterization of angiotensin-converting enzyme (ACE) from sheep lung, Molecular Biology Reports 48: 4191-4199.
  • Balti R, Bougatef A, Guillochon D, Dhulster P, Nasri M, Nedjar-Arroume N, 2012. Changes in arterial blood pressure after single oral administration of cuttlefish (Sepia officinalis) muscle derived peptides in spontaneously hypertensive rats. Journal of Functional Foods, 4(3): 611-617.
  • Bas Z, 2021. Inhibition effect of nicotinamide (vitamin B3) and reduced glutathione (GSH) peptide on angiotensin-converting enzyme activity purified from sheep kidney. International Journal of Biological Macromolecules, 189: 65-71.
  • Bas Z, Turkoglu V, Goz Y, 2022. Investigation of inhibition effect of butanol and water extracts of Matricaria chamomilla L. on angiotensin-converting enzyme purified from human plasma. Biotechnology and Applied Biochemistry, 69: 273–280.
  • Basi Z, Turkoglu V, 2018. Purification of angiotensin-converting enzyme from human plasma and investigation of the effect of some active ingredients isolated from Nigella sativa L.extract on the enzyme activity. Biomedical Chromatography, 32: e4175.
  • Basi Z, Turkoglu V, 2019. In vitro effect of oxidized and reduced glutathione peptides on angiotensin converting enzyme purified from human plasma. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 1104: 190-195.
  • Baudin B, Bénéteau-Burnat B, 1999. Mixed-type inhibition of pulmonary angiotensin I-converting enzyme by captopril, enalaprilat and ramiprilat. Journal of Enzyme Inhibition, 14(6): 447–456.
  • Bernstein KE, Khan Z, Giani JF, Cao DY, Bernstein EA, Shen XZ, 2018. Angiotensin-converting enzyme in innate and adaptive immunity. Nature Reviews. Nephrology, 14(5): 325–336.
  • Bhaskar B, Ananthanarayan L, Jamdar S, 2019. Purification, identification, and characterization of novel angiotensin I-converting enzyme (ACE) inhibitory peptides from alcalase digested horse gram flour. LWT, 103: 155-161.
  • Bondre SV, Chavan RS, Raut, ID, Mohite SK, Magdum, CS, 2020. An overview of survey on antihypertensive drugs. Asian Journal of Pharmaceutical Research, 10 (3): 160–162.
  • Bradford MM, 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-54.
  • Chen J, Yu X, Chen Q, Wu Q, He Q, 2022. Screening and mechanisms of novel angiotensin-I-converting enzyme inhibitory peptides from rabbit meat proteins: A combined in silico and in vitro study. Food Chemistry, 370: 131070.
  • Colombo M, Bianchi A, 2010. Click chemistry for the synthesis of RGD-containing integrin ligands. Molecules (Basel, Switzerland), 15(1): 178–197.
  • Contreras MDM, Carrón R, Montero MJ, Ramos M, Recio I, 2009. Novel casein-derived peptides with antihypertensive activity. International Dairy Journal, 19(10): 566-573.
  • El-Dorry HA, Bull HG, Iwata K, Thornberry NA, Cordes EH, Soffer RL, 1982. Molecular and catalytic properties of rabbit testicular dipeptidyl carboxypeptidase. Journal of Biological Chemistry, 257(23): 14128-14133.
  • He R, Malomo SA, Girgih AT, Ju X, Aluko RE, 2013. Glycinyl-histidinyl-serine (GHS), a novel rapeseed protein-derived peptide has blood pressure-lowering effect in spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry, 61(35): 8396–8402.
  • Hermida, RC, Ayala, DE, Fernández JR, Portaluppi F, Fabbian F, Smolensky MH, 2011. Circadian rhythms in blood pressure regulation and optimization of hypertension treatment with ACE inhibitor and ARB medications. American Journal of Hypertension, 24(4): 383-391.
  • Holmquist B, Bünning P, Riordan JF, 1979. A continuous spectrophotometric assay for angiotensin converting enzyme. Analytical Biochemistry, 95 (2): 540-548.
  • Hooper NM, Turner AJ, 1987. Isolation of two differentially glycosylated forms of peptidyl-dipeptidase A (angiotensin converting enzyme) from pig brain: a re-evaluation of their role in neuropeptide metabolism. The Biochemical Journal, 241(3): 625–633.
  • Karahan F, Turkoglu V, 2021 Enhanced purification protocol for the angiotensin-converting enzyme from bovine systems and investigation of the in vitro effect of some active substances Chemico-Biological Interactions, 347: 109604.
  • Kitts DD, Weiler K, 2003. Bioactive proteins and peptides from food sources. Applications of bioprocesses used in isolation and recovery. Current Pharmaceutical Design, 9: 1309–1323.
  • Kiylik A, Turkoglu V, Bas Z, 2022. Purification of angiotensin-converting enzyme (ACE) from sheep kidney and inhibition effect of reduced nicotinamide adenine dinucleotide (NADH) on purified ACE activity. Cell Biochemistry and Biophysics, 80: 115-122.
  • Laemmli UK, 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685.
  • Lavoie JL, Sigmund, CD, 2003. Minireview: overview of the renin-angiotensin system—an endocrine and paracrine system. Endocrinology, 144(6): 2179-2183.
  • Liang F, Shi Y., Shi J, Zhang T, Zhang R, 2021. A novel Angiotensin-I-converting enzyme (ACE) inhibitory peptide IAF (Ile-Ala-Phe) from pumpkin seed proteins: in silico screening, inhibitory activity, and molecular mechanisms. European Food Research and Technology, 247(9): 2227-2237.
  • Lin Q, Liao W, Bai J, Wu W, Wu J, 2017. Soy protein-derived ACE-inhibitory peptide LSW (Leu-Ser-Trp) shows anti-inflammatory activity on vascular smooth muscle cells. Journal of Functional Foods, 34: 248-253.
  • Lineweaver H, Burk D, 1934. The determination of enzyme dissociation constants. Journal of the American Chemical Society, 56: 658–660.
  • Ma T, Fu Q, Mei Q, Tu Z, Zhang L, 2021. Extraction optimization and screening of angiotensin-converting enzyme inhibitory peptides from Channa striatus through bioaffinity ultrafiltration coupled with LC-Orbitrap-MS/MS and molecular docking. Food Chemistry, 354: 129589.
  • Majumder K, Chakrabarti S, Morton JS, Panahi S, Kaufman S, Davidge ST, Wu J, 2013. Egg-derived tri-peptide IRW exerts antihypertensive effects in spontaneously hypertensive rats. PloS One, 8(11): e82829.
  • Majumder K, Wu J, 2014. Molecular targets of antihypertensive peptides: understanding the mechanisms of action based on the pathophysiology of hypertension. International Journal of Molecular Sciences, 16(1): 256-283.
  • Miguel M, Gómez-Ruiz JÁ, Recio I, Aleixandre A, 2010. Changes in arterial blood pressure after single oral administration of milk-casein-derived peptides in spontaneously hypertensive rats. Molecular nutrition & food research, 54(10): 1422–1427.
  • Miyamoto S, Akiyama SK, Yamada, KM, 1995. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science (New York, N.Y.), 267(5199): 883–885.
  • Nicosia RF, Bonanno E, 1991. Inhibition of angiogenesis in vitro by Arg-Gly-Asp-containing synthetic peptide. The American Journal of Pathology, 138(4): 829–833.
  • Perazella MA, Setaro JF, 2003. Renin-angiotensin-aldosterone system: fundamental aspects and clinical implications in renal and cardiovascular disorders. Journal of Nuclear Cardiology: Official Publication of the American Society of Nuclear Cardiology, 10(2): 184–196.
  • Rezzani R, Porteri E, De Ciuceis C, Bonomini F, Rodella LF, Paiardi S, Boari GE, Platto C, Pilu A, Avanzi D, Rizzoni D, Agabiti Rosei E, 2010. Effects of melatonin and Pycnogenol on small artery structure and function in spontaneously hypertensive rats. Hypertension, 55 (6) : 1373–1380.
  • Sabeur K, Vo AT, Ball BA, 2001. Characterization of angiotensin-converting enzyme in canine testis. Reproduction (Cambridge, England), 122(1) : 139–146.
  • Sánchez A, Vázquez, A, 2017. Bioactive peptides: A review. Food Quality and Safety, 1: 29-46.
  • Thavasu PW, Longhurst S, Joel SP, Slevin ML, Balkwill FR, 1992. Measuring cytokine levels in blood. Importance of anticoagulants, processing, and storage conditions. Journal of Immunological Methods, 153(1-2) : 115–124.
  • Turpeinen AM, Järvenpää, S, Kautiainen H, Korpela R, Vapaatalo H, 2013. Antihypertensive effects of bioactive tripeptides - a random effects meta-analysis. Annals of Medicine, 45(1) : 51-56.
  • Wang F, Li Y, Shen Y, Wang A, Wang S, Xie, T, 2013. The functions and applications of RGD in tumor therapy and tissue engineering. International Journal of Molecular Sciences, 14(7) : 13447–13462.
  • Welschoff J, Matthey M, Wenzel D, 2014. RGD peptides induce relaxation of pulmonary arteries and airways via β3-integrins. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 28(5): 2281–2292.
  • Zhang N, Li F, Zhang T, Li, CY, Zhu L, Yan S, 2022. Isolation, identification, and molecular docking analysis of novel ACE inhibitory peptides from Spirulina platensis. European Food Research and Technology, 248(4): 1107-1115.
Toplam 44 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Organik Kimya (Diğer)
Bölüm Kimya / Chemistry
Yazarlar

Resul Adanaş 0009-0007-4761-4930

Vedat Türkoğlu 0000-0002-0935-1195

Zehra Baş 0000-0002-4071-9744

Erken Görünüm Tarihi 30 Kasım 2023
Yayımlanma Tarihi 1 Aralık 2023
Gönderilme Tarihi 9 Haziran 2023
Kabul Tarihi 17 Ağustos 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 13 Sayı: 4

Kaynak Göster

APA Adanaş, R., Türkoğlu, V., & Baş, Z. (2023). Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum. Journal of the Institute of Science and Technology, 13(4), 2847-2860. https://doi.org/10.21597/jist.1312143
AMA Adanaş R, Türkoğlu V, Baş Z. Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum. Iğdır Üniv. Fen Bil Enst. Der. Aralık 2023;13(4):2847-2860. doi:10.21597/jist.1312143
Chicago Adanaş, Resul, Vedat Türkoğlu, ve Zehra Baş. “Inhibition Effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum”. Journal of the Institute of Science and Technology 13, sy. 4 (Aralık 2023): 2847-60. https://doi.org/10.21597/jist.1312143.
EndNote Adanaş R, Türkoğlu V, Baş Z (01 Aralık 2023) Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum. Journal of the Institute of Science and Technology 13 4 2847–2860.
IEEE R. Adanaş, V. Türkoğlu, ve Z. Baş, “Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum”, Iğdır Üniv. Fen Bil Enst. Der., c. 13, sy. 4, ss. 2847–2860, 2023, doi: 10.21597/jist.1312143.
ISNAD Adanaş, Resul vd. “Inhibition Effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum”. Journal of the Institute of Science and Technology 13/4 (Aralık 2023), 2847-2860. https://doi.org/10.21597/jist.1312143.
JAMA Adanaş R, Türkoğlu V, Baş Z. Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum. Iğdır Üniv. Fen Bil Enst. Der. 2023;13:2847–2860.
MLA Adanaş, Resul vd. “Inhibition Effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum”. Journal of the Institute of Science and Technology, c. 13, sy. 4, 2023, ss. 2847-60, doi:10.21597/jist.1312143.
Vancouver Adanaş R, Türkoğlu V, Baş Z. Inhibition effect of Gly-Arg-Gly-Asp-Ser (GRGDS) and Arg-Gly-Asp (RGD) Bioactive Peptides on Angiotensin-Converting Enzyme Activity Purified from Human Serum. Iğdır Üniv. Fen Bil Enst. Der. 2023;13(4):2847-60.