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The potential effects of sulforaphane hydrolyzed from glucosinolates and relationship between Nrf-2 Keap-1 signal pathway

Year 2021, Volume: 6 Issue: 3, 352 - 356, 28.09.2021

Deniz Karakcı

https://doi.org/10.35229/jaes.902598

Abstract

The glucosinolates (Gls) are economically important secondary plant metabolites which occur in all of Brassica vegetables. Glucosinolates and their hydrolysis products have many beneficial effects on humans and animals. Gls are hydrolyzed by myrosinase enzyme found in plant or produced in intestinal microflora, in this way it can appear their biological activities. One of breakdown products of Gls called isothiocyanates and they have an essential role in prevention some cancer types. The most studies on isothiocyanate, sulforaphane (SFN) was isolated from extracts of broccoli as a potent inducer of mammalian cytoprotective enzymes. It is reported that sulforaphane reduced the size of tumors in a rat mammary tumor model by acting as an indirect antioxidant. Nrf2 (NF-E2-related factor 2) is a transcription factor encoded by a specific gene that regulates the expression of antioxidant and detoxifying genes. Nrf2 controls the expression of many Phase I and Phase II drug-metabolizing enzymes. Also, Keap1 (Kelch-like ECH associating protein 1) is rich from amino acid cysteine and acts as a sensor that can work according to the existance of oxidative stress. Many of the genes encoding cytoprotective proteins share common transcriptional regulation through the Keap1-Nrf2-ARE pathway. According to increasing stress, Keap1 activates Nrf2 and induce the Antioxidant Response Element (ARE). Especially sulforaphane that is hydrolyzed from glucosinolates protects the body against oxidative damage and several cancer types by using this pathway.

Keywords

glucosinolates sulforaphane oxidative stress cancer beneficial effect

References

  • Belenli, D., Polat,Ü., Berhow, M.A., Orman, A. &Yesilbag, D. (2016). Effects of glucosinolates and their hydrolysis products on biochemical and performance parameters in broiler chicken diets. Indian Journal of Animal Sciences, 86 (10), 72-78.
  • Belenli, D. & Polat, Ü. (2017). Sulforaphane acts as a cancer fighter.8 th BalkanAnimal Science Conference Balnimalcon 2017, 6-8 Eylül 2017, Prizren, Kosovo p.126.
  • Belenli, D. & Polat, Ü. (2018). Effects of dıetary cress seed (Lepidıum sativum) supplementation on biochemical, performance parameters and MDA levels in broilers. 1st International Veterinary Biochemistry and Clinical Biochemistry Congress, 12-15 Nisan 2018, Hatay, Turkey. p.196.
  • Bernardi, R.L., Finiguerra, M.G., Rossi, A.A. & Palmieri, S. (2003). Isolation and biochemical characterization of a basic myrosinase from ripe crambe abyssinica seeds, highly specific for epi-progoitrin. Journal of Agricultural and Food Chemistry, 51(9), 2737-44.
  • Chen, S. & Andreasson, E. (2001). Update of glucosinolate metabolism and transport. Plant Physiology and Biochemistry, 39, 743-758.
  • Chen, Y.Z., Lin, L., Wang, C.W., Yeh C.C. & Hwang, S.Y. (2004). Response of two pieris (Lepidoptera: Pieridae) species to fertilization of a host plant. Zoological Studies, 43(4), 778-786.
  • Cheng, D.L., Hashimoto, K. & Uda, Y. (2004). In vitro digestion ofsinigrin and glucotropaeolin by single strains ofBifido-bacteriumand identification of the digestive products. Food Chemical Toxicology, 42, 351-357.
  • Cartea, M.E. & Velasco, P. (2008). Glucosinolates in Brassica foods:bioavailability in food and significance for human health. Phytochemistry Reviews, 7, 213-229.
  • Devling, T.W., Lindsay C.D., McLellan L.I., McMahon M. & Hayes J.D. (2005). Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proceedings of the National Academy of Sciences USA, 102,7280-7285A.
  • Dinkova-Kostova, A.T., Holtzclaw, W.D. & Wakabayashi, N. (2005). Keap1, the sensor for electrophiles and oxidants that regulates the phase 2 response, is a zinc metalloprotein. Biochemistry, 44, 6889-6899.
  • Dinkova-Kostova, A.T. & Kostov R.V. (2012). Glucosinolates and isothiocyanates in health and disease. Trends in Molecular Medicine, 18(6), 337-347.
  • Doll, R. (1992). The lessons of life: keynote address to the nutrition and cancer conference. Cancer Research, 52, 2024-2029.
  • Fahey, J.W., Zhang, Y. & Talalay, P. (1997). Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proceedings of the National Academy of Sciences USA, 94,10367-10372.
  • Fahey, J.W. & Talalay, P. (1999). Antioxidant functions of sulforaphane: a potent inducer of Phase 2 detoxication enzymes. Food Chemical Toxicology, 37, 973-979.
  • Fahey, W.J., Amy, T., Zalcmann, L. & Talalay, P. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 5-51
  • Fenwick, G.R., Heaney ,R.K. & Mullin, W.J. (1983). Glucosinolates and their breakdown products in food and food plants. Critical Reviews in Food Science and Nutrition, 18, 123-201.
  • Finiguerra, M.G., Iori, R. & Palmieri, S. (2001). Soluble and total myrosinase activity in defatted Crambe abyssinica meal. Journal of Agricultural and Food Chemistry, 49(2), 840-845.
  • Gamet-Payrastre, L., Lumeau, S., Gasc, N., Cassar, G., Rollin, P. & Tulliez, J. (1998). Selective cytostatic and cytotoxic effects of glucosinolates hydrolysis products on human colon cancer cells in vitro. Anticancer Drug, 9, 141-148.
  • Gamet-Payrastre L, Li P, Lumeau S et al. (2000). Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Research, 60, 1426-1433.
  • Halkier BA, Du LC (1997). The biosynthesis of glucosinolates. Trends in Plant Science, 2, 425-431.
  • Hayes JD, Dinkova-Kostova AT (2014). The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends in Biochemical Sciences, 39(4), 199-217.
  • Kavian, N., Mehlal, S., Jeljeli, M., Saidu, N.E.B., Nicco, C., Olivier, C., Chouzenoux S., Cauvet, A., Camus, C., Ait-Djoudi, M., Chéreau, C., Kerdine-Römer, S. Allanore, Y. & Batteux, F. (2018). The Nrf2-Antioxidant Response Element Signaling Pathway Controls Fibrosis and Autoimmunity in Scleroderma. Frontiers in Immunology, 9, 1-14.
  • Kobayashi, M. & Yamamoto, M. (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxidant & Redox Signaling, 7(3-4), 385-94.
  • Kore, A.M., Spencer, G.F. & Wallig, M.A. (1993). Purifcation of the (methylsulfnyl) alkyl glucosinolate hydrolysis products: 1-iso-thiocyanato-3-(methylsulfnyl) propane, 1-isothiocyanato-4-(methylsulfnyl) butane, 4-(methylsulfnyl) butanenitrile, and 5 (methylsulfnyl) pentanenitrile from broccoli and Lesquerella fendleri. Journal of Agricultural and Food Chemistry, 41, 89-95.
  • Maheao, K., Morel, F., Langouet, S., Kramer, H., Le Ferrec, E., Ketterer, B. & Guillouzo, A. (1997). Inhibition of cytochromes P-450 and induction of glutathione S-transferases by sulforaphane in primary human and rat hepatocytes. Cancer Research, 57, 3649-3652.
  • Michaud, D.S., Spiegelman, D., Clinton, S.K., Rimm, E.B., Willett, W.C. & Giovannucci, E.L. (1999). Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. Journal of the National Cancer Institute, 91, 605-613.
  • Mithen, R. (2001). Glucosinolates and their degradation products. Advances in Botanical Research, 35, 213-262.
  • Mitsuishi, Y., Motohashi, H. & Masayuki, Y. (2012). The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism. Frontier Oncology, 2, 1-13 Morel, F., Langouet, S., Maheao, K. & Guillouzo, A. (1997). The use of primary hepatocyte cultures for the evaluation of chemoprotective agents. Cell Biology and Toxicology, 13, 323-329.
  • Shapiro, T.A., Fahey, J.W., Wade, K.L., Stephenson, K.K. & Talalay, P. (2001). Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiology Biomarkers, 10, 501-508.
  • Sun, Y., Yang, T., Mao, L. & Zhang, F. (2018). Sulforaphane Protects against Brain Diseases: Roles of Cytoprotective Enzymes. Austin Journal of Cerebrovascular Disease & Stroke, 4(1),1-14.
  • Steinmetz, K.A. & Potter, J.D. (1991). Vegetables, fruit and cancer. I. Epidemiology. Cancer Cause Control, 2, 325-357.
  • Talalay, P., Dinkova-Kostova, A.T. & Holtzclaw, W.D. (2003). Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Advance in Enzyme Regulation, 43, 121-134.
  • Tripathi, M.K. & Mishra, A.S. (2007). Glucosinolates in animal nutrition: A review. Animal Feed Science and Technology, 132, 1-27.
  • Verhoeven, D.T., Goldbohm, R.A., Van Poppel, G., Verhagen, H. & Brandt, P.A. (1996). Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiology Biomarkers, 5, 733-748.
  • Vig, A.P., Rampal, G., Thind, T.S. & Arora, S. (2009). Bio-protective effects of glucosinolates-A review. Journal of Food Science and Technology, 42, 1561-1572.
  • Wakabayashi, N., Itoh, K., Wakabayashi, J. Motohashi H., Noda, S., Takahashi S., Imakado S., Kotsuji T., Otsuka F., Roop D.R., Harada, T., Engel J.D. & Yamamoto M. (2003). Keap-1 mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nature Genetics, 35, 238-245.
  • Yang, L., Palliyaguru, D.L. & Kenslera, T.W. (2016). Frugal chemoprevention: targeting Nrf2 with foods rich in sulforaphane. Seminers in Oncology, 43, 146-153.
  • Zhang, C.C.G., Posner, G.H. & Talalay, P. (1992). Spectroscopic quantitation of organic isothiocyanates by cyclocondensation with vicinal dithiols. Analytical Biochemistry, 205, 100-107.
  • Zhang, Y., Kensler, T.W., Cho, C.G., Posner, G.H. & Talalay, P. (1994). Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proceedings of the National Academy of Sciences USA, 91, 3147-3150.
  • Zhang, Y., Wade, K., Prestera, T., Talalay, P. (1996). Quantitative determination of isothiocyanates, dithiocarbamates, carbon disulfide, and related thiocarbonyl compounds by cyclocondensation with 1,2-benzenedithiol. Analytical Biochemistry, 239, 160-167.

Glukosinolatlardan hidrolize edilen sulforafanın potansiyel etkileri ve Nrf2-Keap-1 sinyal yolağı ile ilişkisi

Year 2021, Volume: 6 Issue: 3, 352 - 356, 28.09.2021

Deniz Karakcı

https://doi.org/10.35229/jaes.902598

Abstract

Glukosinolatlar (Gls), Brassica sebzelerinde bulunan ekonomik açıdan önemli olan ikincil bitki metabolitleridir. Glukosinolatlar ve bunların hidroliz ürünleri insanlar ve hayvanlar üzerinde birçok faydalı etkiye sahiptir. Gls, bitki içeriğinde ve bağırsak mikroflorasında bulunan myrosinaz enzimi ile hidrolize edilir ve bu şekilde biyolojik aktiviteleri ortaya çıkarabilmektedir. Glukosinolatların parçalanma ürünlerinden biri olan izotiyosiyanatlar bazı kanser türlerinin önlenmesinde önemli roller oynamaktadır. En çok incelenen izotiyosiyanat öncül maddesi sülforafan, memeli hücre koruyucu enzimlerinin güçlü bir uyarıcısı olarak brokoli özlerinden izole edilmektedir. Sülforafanın, bir sıçan memeli tümör modelinde, tümörlerin boyutunu indirekt bir antioksidan olarak çalışarak küçülttüğü bildirilmiştir. Nrf2 (NF-E2 ile ilişkili faktör 2), antioksidan ve detoksifiye eden genlerin ekspresyonunu düzenleyen, spesifik bir gen tarafından kodlanan bir transkripsiyon faktörüdür. Nrf2, birçok Faz I ve Faz II ilaç metabolize edici enzimlerin ekspresyonunu kontrol etmektedir. Aynı zamanda, Keap1 (Kelch-benzeri ECH birleştirici protein 1) sistein aminoasitlerce zengindir ve oksidatif stresin oluşmasına bağlı olarak çalışabilen bir sensör görevi yapmaktadır. Hücre koruyucu proteinleri kodlayan genlerin çoğu, Keap1-Nrf2-ARE sinyal yolu boyunca ortak transkripsiyonel düzenlemeyi sağlamaktadır. Artan strese göre, Keap1 Nrf2'yi aktive eder ve antioksidan tepki elementini (ARE) uyarmaktadır. Özellikle glukosinolatlardan hidrolize edilen sülforafan, bu yolu kullanarak oksidatif hasara ve çeşitli kanser türlerine karşı vücudu koruduğu düşünülmektedir.

Keywords

glukosinolatlar sulforafan oksidatif stres kanser yararlı etki

References

  • Belenli, D., Polat,Ü., Berhow, M.A., Orman, A. &Yesilbag, D. (2016). Effects of glucosinolates and their hydrolysis products on biochemical and performance parameters in broiler chicken diets. Indian Journal of Animal Sciences, 86 (10), 72-78.
  • Belenli, D. & Polat, Ü. (2017). Sulforaphane acts as a cancer fighter.8 th BalkanAnimal Science Conference Balnimalcon 2017, 6-8 Eylül 2017, Prizren, Kosovo p.126.
  • Belenli, D. & Polat, Ü. (2018). Effects of dıetary cress seed (Lepidıum sativum) supplementation on biochemical, performance parameters and MDA levels in broilers. 1st International Veterinary Biochemistry and Clinical Biochemistry Congress, 12-15 Nisan 2018, Hatay, Turkey. p.196.
  • Bernardi, R.L., Finiguerra, M.G., Rossi, A.A. & Palmieri, S. (2003). Isolation and biochemical characterization of a basic myrosinase from ripe crambe abyssinica seeds, highly specific for epi-progoitrin. Journal of Agricultural and Food Chemistry, 51(9), 2737-44.
  • Chen, S. & Andreasson, E. (2001). Update of glucosinolate metabolism and transport. Plant Physiology and Biochemistry, 39, 743-758.
  • Chen, Y.Z., Lin, L., Wang, C.W., Yeh C.C. & Hwang, S.Y. (2004). Response of two pieris (Lepidoptera: Pieridae) species to fertilization of a host plant. Zoological Studies, 43(4), 778-786.
  • Cheng, D.L., Hashimoto, K. & Uda, Y. (2004). In vitro digestion ofsinigrin and glucotropaeolin by single strains ofBifido-bacteriumand identification of the digestive products. Food Chemical Toxicology, 42, 351-357.
  • Cartea, M.E. & Velasco, P. (2008). Glucosinolates in Brassica foods:bioavailability in food and significance for human health. Phytochemistry Reviews, 7, 213-229.
  • Devling, T.W., Lindsay C.D., McLellan L.I., McMahon M. & Hayes J.D. (2005). Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proceedings of the National Academy of Sciences USA, 102,7280-7285A.
  • Dinkova-Kostova, A.T., Holtzclaw, W.D. & Wakabayashi, N. (2005). Keap1, the sensor for electrophiles and oxidants that regulates the phase 2 response, is a zinc metalloprotein. Biochemistry, 44, 6889-6899.
  • Dinkova-Kostova, A.T. & Kostov R.V. (2012). Glucosinolates and isothiocyanates in health and disease. Trends in Molecular Medicine, 18(6), 337-347.
  • Doll, R. (1992). The lessons of life: keynote address to the nutrition and cancer conference. Cancer Research, 52, 2024-2029.
  • Fahey, J.W., Zhang, Y. & Talalay, P. (1997). Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proceedings of the National Academy of Sciences USA, 94,10367-10372.
  • Fahey, J.W. & Talalay, P. (1999). Antioxidant functions of sulforaphane: a potent inducer of Phase 2 detoxication enzymes. Food Chemical Toxicology, 37, 973-979.
  • Fahey, W.J., Amy, T., Zalcmann, L. & Talalay, P. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 5-51
  • Fenwick, G.R., Heaney ,R.K. & Mullin, W.J. (1983). Glucosinolates and their breakdown products in food and food plants. Critical Reviews in Food Science and Nutrition, 18, 123-201.
  • Finiguerra, M.G., Iori, R. & Palmieri, S. (2001). Soluble and total myrosinase activity in defatted Crambe abyssinica meal. Journal of Agricultural and Food Chemistry, 49(2), 840-845.
  • Gamet-Payrastre, L., Lumeau, S., Gasc, N., Cassar, G., Rollin, P. & Tulliez, J. (1998). Selective cytostatic and cytotoxic effects of glucosinolates hydrolysis products on human colon cancer cells in vitro. Anticancer Drug, 9, 141-148.
  • Gamet-Payrastre L, Li P, Lumeau S et al. (2000). Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Research, 60, 1426-1433.
  • Halkier BA, Du LC (1997). The biosynthesis of glucosinolates. Trends in Plant Science, 2, 425-431.
  • Hayes JD, Dinkova-Kostova AT (2014). The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends in Biochemical Sciences, 39(4), 199-217.
  • Kavian, N., Mehlal, S., Jeljeli, M., Saidu, N.E.B., Nicco, C., Olivier, C., Chouzenoux S., Cauvet, A., Camus, C., Ait-Djoudi, M., Chéreau, C., Kerdine-Römer, S. Allanore, Y. & Batteux, F. (2018). The Nrf2-Antioxidant Response Element Signaling Pathway Controls Fibrosis and Autoimmunity in Scleroderma. Frontiers in Immunology, 9, 1-14.
  • Kobayashi, M. & Yamamoto, M. (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxidant & Redox Signaling, 7(3-4), 385-94.
  • Kore, A.M., Spencer, G.F. & Wallig, M.A. (1993). Purifcation of the (methylsulfnyl) alkyl glucosinolate hydrolysis products: 1-iso-thiocyanato-3-(methylsulfnyl) propane, 1-isothiocyanato-4-(methylsulfnyl) butane, 4-(methylsulfnyl) butanenitrile, and 5 (methylsulfnyl) pentanenitrile from broccoli and Lesquerella fendleri. Journal of Agricultural and Food Chemistry, 41, 89-95.
  • Maheao, K., Morel, F., Langouet, S., Kramer, H., Le Ferrec, E., Ketterer, B. & Guillouzo, A. (1997). Inhibition of cytochromes P-450 and induction of glutathione S-transferases by sulforaphane in primary human and rat hepatocytes. Cancer Research, 57, 3649-3652.
  • Michaud, D.S., Spiegelman, D., Clinton, S.K., Rimm, E.B., Willett, W.C. & Giovannucci, E.L. (1999). Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. Journal of the National Cancer Institute, 91, 605-613.
  • Mithen, R. (2001). Glucosinolates and their degradation products. Advances in Botanical Research, 35, 213-262.
  • Mitsuishi, Y., Motohashi, H. & Masayuki, Y. (2012). The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism. Frontier Oncology, 2, 1-13 Morel, F., Langouet, S., Maheao, K. & Guillouzo, A. (1997). The use of primary hepatocyte cultures for the evaluation of chemoprotective agents. Cell Biology and Toxicology, 13, 323-329.
  • Shapiro, T.A., Fahey, J.W., Wade, K.L., Stephenson, K.K. & Talalay, P. (2001). Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiology Biomarkers, 10, 501-508.
  • Sun, Y., Yang, T., Mao, L. & Zhang, F. (2018). Sulforaphane Protects against Brain Diseases: Roles of Cytoprotective Enzymes. Austin Journal of Cerebrovascular Disease & Stroke, 4(1),1-14.
  • Steinmetz, K.A. & Potter, J.D. (1991). Vegetables, fruit and cancer. I. Epidemiology. Cancer Cause Control, 2, 325-357.
  • Talalay, P., Dinkova-Kostova, A.T. & Holtzclaw, W.D. (2003). Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Advance in Enzyme Regulation, 43, 121-134.
  • Tripathi, M.K. & Mishra, A.S. (2007). Glucosinolates in animal nutrition: A review. Animal Feed Science and Technology, 132, 1-27.
  • Verhoeven, D.T., Goldbohm, R.A., Van Poppel, G., Verhagen, H. & Brandt, P.A. (1996). Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiology Biomarkers, 5, 733-748.
  • Vig, A.P., Rampal, G., Thind, T.S. & Arora, S. (2009). Bio-protective effects of glucosinolates-A review. Journal of Food Science and Technology, 42, 1561-1572.
  • Wakabayashi, N., Itoh, K., Wakabayashi, J. Motohashi H., Noda, S., Takahashi S., Imakado S., Kotsuji T., Otsuka F., Roop D.R., Harada, T., Engel J.D. & Yamamoto M. (2003). Keap-1 mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nature Genetics, 35, 238-245.
  • Yang, L., Palliyaguru, D.L. & Kenslera, T.W. (2016). Frugal chemoprevention: targeting Nrf2 with foods rich in sulforaphane. Seminers in Oncology, 43, 146-153.
  • Zhang, C.C.G., Posner, G.H. & Talalay, P. (1992). Spectroscopic quantitation of organic isothiocyanates by cyclocondensation with vicinal dithiols. Analytical Biochemistry, 205, 100-107.
  • Zhang, Y., Kensler, T.W., Cho, C.G., Posner, G.H. & Talalay, P. (1994). Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proceedings of the National Academy of Sciences USA, 91, 3147-3150.
  • Zhang, Y., Wade, K., Prestera, T., Talalay, P. (1996). Quantitative determination of isothiocyanates, dithiocarbamates, carbon disulfide, and related thiocarbonyl compounds by cyclocondensation with 1,2-benzenedithiol. Analytical Biochemistry, 239, 160-167.
There are 40 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Deniz Karakcı 0000-0002-1884-1874

Publication Date September 28, 2021
Submission Date March 29, 2021
Acceptance Date May 8, 2021
Published in Issue Year 2021 Volume: 6 Issue: 3

Cite

APA Karakcı, D. (2021). Glukosinolatlardan hidrolize edilen sulforafanın potansiyel etkileri ve Nrf2-Keap-1 sinyal yolağı ile ilişkisi. Journal of Anatolian Environmental and Animal Sciences, 6(3), 352-356. https://doi.org/10.35229/jaes.902598
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