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Effect of Fresh Soy Milk and Its Compounds on Apoptosis in Human Leukemic Cells and Peripheral Blood Mononuclear Cells

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Effect of Fresh Soy Milk and Its Compounds on Apoptosis in Human Leukemic Cells and Peripheral Blood Mononuclear Cells Ali et al Tropical Journal of Pharmaceutical Research March 2021; 20 (3): 511-517 ISSN: 1596-5996 (print); 1596-9827 (electronic) © Pharmacotherapy Group, Faculty of Pharmacy, University of Benin, Benin City, 300001 Nigeria. Available online at http://www.tjpr.org http://dx.doi.org/10.4314/tjpr.v20i3.10 Original Research Article Effect of fresh soy milk and its compounds on apoptosis in human leukemic cells and peripheral blood mononuclear cells Qalidah Mohamad Ali1, Endang Kumolosasi1*, Mohd Makmor Bakry2 1Drug and Herbal Research Centre, 2Centre of Quality Management of Medicine, Faculty of Pharmacy, University Kebangsaan Malaysia, Kuala Lumpur, Malaysia *For correspondence: Email: [email protected]; [email protected]; Tel: +60392898054; HP: +60149208598; Fax: +60326983271 Sent for review: 25 April 2020 Revised accepted: 26 February 2021 Abstract Purpose: To determine the effect of fresh soy milk and its compounds (coumestrol, daidzein and genistein) on apoptosis in human leukemic cells and peripheral blood mononuclear cells (PBMC). Methods: The apoptotic effect of fresh soy milk and its compounds on human leukemic cells (K562, Jurkat, U937) and PBMC was determined by flow cytometry. The PBMC from healthy donors were isolated by conducting density gradient centrifugation principle. Lymphoprep and cytotoxicity of the compounds was evaluated by 3-(4,5- ‘;1dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) MTT) assay. Results: PBMC treatment of daidzein and genistein had a significantly higher half-maximal inhibitory concentration (IC50) value (p < 0.01) and (p < 0.0001), compared to the leukemia cells. In addition, soy milk had a significantly higher IC50 value (p < 0.05) in PBMC than the leukemia cells. Coumestrol induced a significantly increased apoptotic cells in K562, U937 cells (p < 0.01) and Jurkat cells (p < 0.05). However, daidzein only increased apoptosis (p < 0.05) in K562 and U937. Genistein reported a significantly increased apoptotic cell in K562, Jurkat (p < 0.01) and U937 cells (p < 0.001). Nonetheless, in PBMC, significant apoptosis by the compounds did not occur. However, only soy milk induced a significantly increased apoptosis in PBMC (p < 0.05). Conclusion: The findings indicate that coumestrol, daidzein, genistein and soy milk inhibits the viability of leukemia cells by apoptosis induction, but they are non-toxic toward normal cells. Therefore, the results suggest that the compound alone, and thus, soy milk might have a therapeutic effect in leukemia. Keyword: Fresh soy milk, Phytoestrogen, Apoptosis, Human leukemic cells, Peripheral blood mononuclear cell This is an Open Access article that uses a fund-ing model which does not charge readers or their institutions for access and distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0) and the Budapest Open Access Initiative (http://www.budapestopenaccessinitiative.org/read), which permit unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Tropical Journal of Pharmaceutical Research is indexed by Science Citation Index (SciSearch), Scopus, International Pharmaceutical Abstract, Chemical Abstracts, Embase, Index Copernicus, EBSCO, African Index Medicus, JournalSeek, Journal Citation Reports/Science Edition, Directory of Open Access Journals (DOAJ), African Journal Online, Bioline International, Open-J-Gate and Pharmacy Abstracts INTRODUCTION marrow. According to the Global Cancer Statistics of 2018, leukemia represented 437,033 Leukemia is a type of blood cancer that occurs in (2.4%) new cases and 309,006 (3.2%) deaths, adults and children, and characterized as an and thus, was ranked 15th place from all 36 abnormal growth of white blood cells in the bone cancer sites [1]. This hematogenic disease is ----------------------------------------------------------------------------------------------------------------------------------------------------- © 2021 The authors. This work is licensed under the Creative CommonsTrop Attribution J Pharm 4.0Res, International March 2021; License 20(3): 511 Ali et al caused by genetic changes in the normal stem EXPERIMENTAL cells, which causes an alteration in the normal cell division and an uncontrolled multiplication of Materials immature leukemia cells [2]. Phytoestrogens are divided into three major groups, which are Coumestrol was purchased from Carbosynhth, isoflavone (daidzein, genistein, formononetin, China, while daidzein and genistein were glycetein, biochanin A), coumestans (coumestrol, purchased from ChromaDex, Los Angeles. The plicadin, wedelolactone), and lignin which compounds were dissolved in 0.1 % dimethyl consists of plant lignans and enterolignans [3]. sulfoxide (DMSO) purchased from Merck, These plant dietary estrogens are mainly found Germany, to obtain the stock solutions. Fresh in soy products, nuts, legumes, flax seed oil and Soy Milk was prepared by soaking washed cereals [4]. Phytoestrogens are believed to be soybeans in distilled water for 10 h, and then the involved in the prevention and inhibition of beans were drained, rinsed and blended with cancer cell growth, such as bladder, breast, distilled water. The blended soybeans were colorectal and prostate cancers, by having cloth-filtered and pressed into a beaker. The similar structures as estrogen and the potential to obtained fresh soy milk was boiled for 30 min bind with the estrogen receptor. For example, and stored in a fridge at 4 ºC. It was considered consumption of soy milk product is linked to as 100% fresh soy milk (Unpublished paper). reduced cancer risk [5]. The compound concentrations used in the Major components of isoflavones are daidzein assays were obtained from the stock solutions, and genistein, which are widely found in and diluted with complete media. Acute soybeans, and can suppress the growth and lymphocytic leukemia (Jurkat) and acute division of cancer cells [6]. Therefore, myelogenous leukemia (U937), along with constituents of soybeans have been widely chronic myelogenous leukemia (K562) cell lines studied for anticancer properties. Fermented were purchased from the American Type Culture fresh soy milk was shown to induce apoptosis Collection (ATCC, USA). The Jurkat and U937 and suppress chemically induced mammary cell lines were cultured in RPMI-160 (Gibco, cancer in vivo. In addition, the risk of getting USA), and K562 cell line in Iscove’s Modified breast cancer in pre menopause and post Dulbecco’s Medium IMDM, (Gibco, USA), which menopause Asian women were reduced after contained penicillin, streptomycin (100U/ml), and prior exposure to soy-based products, hence the 10% fetal bovine serum (FBS). BD association of the anticancer properties of soy PharmingenTM Annexin V-FITC was obtained milk in lessening the risk of getting cancer [7]. from BD Bioscience, USA. Propidium Iodide, (PI), methylthiazolytetrazolium, and MTT were Apoptosis is normally known as a programmed obtained from Sigma, USA, while Hydroquinone cell death, which usually occurs to preserve was from Merck, Germany. homeostasis, growth of embryonic, and division of lymphoid and hematopoietic cells [8] . As a Purification of peripheral blood mononuclear regulated programmed cell death, apoptosis cells (PBMCs) occurs by intrinsic and extrinsic pathways that cause some alterations, such as the bulge of a Blood was taken from healthy participant who membrane, chromatin rupture and mitochondria volunteered to participate in the study and impairment [9]. In the extrinsic pathway, fulfilled the required criteria: aged between 18 activation of a specific ligand, such as tumor and 50 years old, a non-smoker who did not take necrosis factor related apoptosis inducing ligand any supplements or medication, and had fasted (TRAIL), initiates caspase-8 and subsequently overnight. A consent form was gained from each activates caspase-3, causing permanent donor before blood collection. This study biological and morphological changes. procedures received approval from the UKM Meanwhile, the intrinsic pathway is stimulated by Human Ethical Committee (approval no. mitochondria dysfunction and impairment of UKM.PPI.800-1/1/5/JEP-2019-383) and aligned plasma membrane, which causes permeability with principles outlined by the Helsinki and the release of certain proteins such as Declaration [11]. Cytochrome C through supramolecular pore, thus activating caspase-9 [10]. Therefore, the Blood was collected in EDTA tubes and diluted purpose of the current study is to determine the with the equal amount of plain RPMI-1640 media effect of fresh soy milk and its compounds on in 1:1 ratio. The diluted sample was slowly apoptosis in human leukemic cells and peripheral layered above density gradient medium blood mononuclear cells. LymphoprepTM (Axis-Shield, Norway), and further centrifuged by using density gradient Trop J Pharm Res, March 2021; 20(3): 512 Ali et al centrifugation at 600x g for 20 min at 20ºC. most cells. In Figure 1A, coumestrol caused a PBMC layer was slowly removed, washed twice significantly lower viability of K562 (74.33% ± and re-suspended in RPMI-1640. 4.49%, p<0.01), Jurkat (68.33 ± 7.22%, p<0.05), U937 (52.33 ± 2.33%, p<0.0001), and PBMC Cell viability assay (92.66 ± 2.18%, p<0.05) compared to the negative control. Daidzein in Figure 1B, only To determine the viability of cells, MTT assay showed a significantly lowered viability in K562 was carried out as stated by established (67.33 ± 9.9%, p<0.05), Jurkat (60.33
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