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(Jack) Ssp. Pruniflorum on Initial Stage Hepatocarcinogenesis in Rats

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(Jack) Ssp. Pruniflorum on Initial Stage Hepatocarcinogenesis in Rats molecules Article Chemopreventive Effect of Cratoxylum formosum (Jack) ssp. pruniflorum on Initial Stage Hepatocarcinogenesis in Rats Piman Pocasap 1,2, Natthida Weerapreeyakul 2,3,* and Rawiwan Wongpoomchai 4,5,* 1 Department of Pharmacology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand; [email protected] 2 Human High Performance and Health Promotion Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand 3 Division of Pharmaceutical Chemistry, Faculty of Pharmaceutical Sciences, Khon Kaen University, Khon Kaen 40002, Thailand 4 Department of Biochemistry, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 5 Research Center for Development of Local Lanna Rice and Rice Products, Chiang Mai University, Chiang Mai 50200, Thailand * Correspondence: [email protected] (N.W.); [email protected] (R.W.) Abstract: Cratoxylum formosum ssp. pruniflorum (Kurz) Gogelein (CP) is an indigenous plant found mainly in southeast Asia. Several in vitro studies have confirmed its activity against hepatocellular carcinoma; however, in vivo studies of the effect of CP on liver cancer are needed. This study investi- gated the effect of CP on early-stage hepatocarcinogenesis in rat liver when using diethylnitrosamine (DEN) as a carcinogen. Immunohistochemistry was used to detect (a) upregulation of glutathione S-transferase placental (GST-P) positive foci, (b) the proliferating cell nuclear antigen PCNA, and (c) apoptotic cells in the liver as indicators of early-stage carcinogenesis. Immunohistochemical pa- Citation: Pocasap, P.; rameters were observed in rats given CP orally following DEN injection. Rats given DEN presented Weerapreeyakul, N.; Wongpoomchai, overexpression of GST-P positive foci, PCNA, and apoptotic cells, indicating the formation of cancer- R. Chemopreventive Effect of ous tissues, and these effects were diminished by CP treatment. CP thus inhibited hepatocarcinogenic Cratoxylum formosum (Jack) ssp. effects in an animal model. These results could help plan further in vivo studies and support the use pruniflorum on Initial Stage of CP to prevent processes that promote the pathogenesis of hepatocellular carcinoma in humans. Hepatocarcinogenesis in Rats. Molecules 2021, 26, 4235. https:// Keywords: Cratoxylum formosum ssp. pruniflorum (Kurz) Gogelein; hepatocarcinogenesis; diethylni- doi.org/10.3390/molecules26144235 trosamine; rat; immunohistochemistry Academic Editor: Roberto Fabiani Received: 28 May 2021 Accepted: 8 July 2021 1. Introduction Published: 12 July 2021 Cratoxylum formosum ssp. pruniflorum (Kurz) Gogelein (CP) (“Tiew kon” in Thai) [1] is a plant in the Guttiferae family widely distributed in Southeast Asia [2]. The indigenous Publisher’s Note: MDPI stays neutral plant is used locally as an ingredient in traditional cuisines and remedies [3] and the main with regard to jurisdictional claims in ingredient in bitter nail tea in Yunnan province, China, and Vietnam [4]. Studies indicate published maps and institutional affil- that the phytochemical constituents—e.g., xanthones, flavonoids, and triterpenoids—in CP iations. could be used for therapeutic purposes [4–6]. Several related studies examined the potency of CP for various possible therapeutic uses such as antibacterials [7], anti-inflammatories [8], gastroprotective effects [9], and prevention of Alzheimer’s disease [10]. Another promising application of CP is its potential for anticancer activity. Copyright: © 2021 by the authors. Cancer is the leading cause of death worldwide. In 2020, 9.9 million people were Licensee MDPI, Basel, Switzerland. estimated to have died from cancer [11]. Hepatocellular carcinoma (HCC) is one of the most This article is an open access article pernicious cancers due to its high mortality, ranking as the fourth leading cause of cancer distributed under the terms and death and increasing [11]. In terms of geography, the prevalence and mortality rate of HCC conditions of the Creative Commons in southeast Asia is twice the worldwide values, ranking second among cancer-related Attribution (CC BY) license (https:// deaths in the region [12], requiring urgent countermeasures. The use of medicinal plants creativecommons.org/licenses/by/ that are easily found in the region with potential anticancer activity is a reasonable course 4.0/). Molecules 2021, 26, 4235. https://doi.org/10.3390/molecules26144235 https://www.mdpi.com/journal/molecules Molecules 2021, 26, 4235 2 of 12 of action, not as a definitive treatment but as an adjunct. The primary burden is not only the resistant nature of HCC—which is refractory to most currently available anticancer drugs [13]—but also lack of awareness is an important barrier to early diagnosis due to the absence of specific symptoms in the early stages [14], so a preventive strategy should be prioritized. We previously reported the chemotherapeutic property of CP against HCC in vitro. CP exerts an anticancer activity through several mechanisms, including DNA alkylation, sup- pressing DNA supercoil relaxation, and overexpression of the death receptor TRAILR5 [15]. These triggers lead to apoptotic cell death in extrinsic and intrinsic pathways, as indi- cated by various caspase cascade activations [15,16]. Our previous phytochemical analysis indicated that the hydroethanolic extract contained several phytochemical constituents, including xanthones, phenolic compounds (e.g., gallic acid, chlorogenic acid, and caffeic acid), and fatty acids (e.g., palmitic acid and oleic acid) [10,15]. Those results agreed with other studies in which the group of compounds (including xanthones and pheno- lics) represents the major phytoconstituents of CP, so could contribute to the observed chemotherapeutic properties [17–19]. Several studies have used different cell lines exhibit- ing the anticancer capability of CP [17,20]. To our knowledge, there has been no study using an animal model to determine the potency of CP against cancer. This study was, therefore, conducted to examine the efficacy of CP in carcinogen-induced rats. While our previous study demonstrated CP’s chemotherapeutic properties (as a suppressing agent) to eradicate cancer in vitro, the present study focused on its chemopreventive activity (as a blocking agent) to prevent the initial steps of hepatocarcinogenesis in vivo. The outcome of the study could support the use of CP as an herbal adjuvant of anticancer therapeutics and be a baseline for further study and use in humans. 2. Results 2.1. Effects of CP on Body/Internal Organ Weights and Food/Water Consumption Results show no significant effect of CP on body growth as observed among each treatment group. The body weights, as well as food/water consumption in the CP-treated groups, were not significantly different from the initial DEN-induced (Group 1) or the NSS (normal saline)-injected group (Group 5) (Table1). A significant difference was also not detected in the relative weight of the livers, kidneys, or spleens in each treatment group (Figure1), implying there was no effect of the CP extract at the treatment regimen on the observed vital organs. Table 1. Effect of CP on male Wistar rat body weight (BW) and food/water consumption. Treatment * Food Consumption Water Consumption Group Initial Weight (g) Final Weight (g) Initiator Test Compound (g/rat/day) (g/rat/day) 1 DEN DW 206 ± 12 434 ± 52 22 ± 1 32 ± 4 2 DEN CP 20 mg/kg 209 ± 7 438 ± 41 21 ± 2 27 ± 2 3 DEN CP 100 mg/kg 205 ± 8 394 ± 43 22 ± 2 28 ± 3 4 DEN CP 500 mg/kg 205 ± 9 393 ± 24 21 ± 2 26 ± 3 5 NSS DW 211 ± 7 446 ± 21 23 ± 4 29 ± 9 6 NSS CP 20 mg/kg 203 ± 8 447 ± 35 23 ± 4 31 ± 3 7 NSS CP 100 mg/kg 208 ± 8 448 ± 33 21 ± 1 30 ± 3 8 NSS CP 500 mg/kg 204 ± 10 465 ± 32 25 ± 3 30 ± 7 * DEN (10 mg/kg BW) or NSS (4 mL/kg BW) initially administered at weeks 0 and 1 then either DW (distilled water, 4 mL) or CP (20, 100, and 200 mg/kg BW) fed weekly starting from week 2 until the end of the experiment (week 12). 2.2. Effects of CP on ALT and AST Levels The rat serum ALT and AST were monitored (Figure2). No significant difference in ALT serum level was observed amongst the treatment groups, except CP extract at 100 mg/kg BW, which lowered the ALT level compared to the NSS-injected group (Figure2a) . The AST serum levels were decreased in the CP extract treatment groups (20 and 500 mg/kg) compared to NSS injected group. The CP extract at 500 mg/kg BW Molecules 2021, 26, 4235 3 of 12 reduced the elevated AST serum level induced by DEN (Figure2b). Overall, the data indicate no hepatoxicity of CP at the regimen used. Figure 1. The effect of CP on relative vital organ weight. DEN or NSS were initially administered at week 0 and 1. Then either DW (for groups 1 and 5) or CP were fed weekly starting from week 2 till the end of the experiment. Data was distributed normally (Shapiro-Wilk and Levene’s test: p ≥ 0.05) and was analyzed for statistically significance using one-way ANOVA with LSD’s post hoc test: F(Liver) = 1.577 (p = 0.159), F(Spleen) = 1.992 (p = 0.070), and F(Renal) = 0.549 (p = 0.794). * CP dosage unit; mg/kg BW. Figure 2. The effect of CP on the serum level of ALT (a) and AST (b). DEN or NSS were initially administered at week 0 and 1. Then either DW (for groups 1 and 5) or CP were fed weekly starting from week 2 till the end of the experiment. Data was distributed normally (Shapiro–Wilk and Levene’s tests: p ≥ 0.05) and was analyzed for statistically significant using one-way ANOVA with LSD’s post hoc test: F(ALT) = 2.243 (p = 0.048) and F(AST) = 5.061 (p < 0.001). * CP dosage unit; mg/kg BW. 2.3. Effect of CP on GST-P Positive Foci The initial administration of DEN induced hepatocarcinogenesis, as indicated by the GST-P positive foci, whereas no positive trait was observed in the NSS-injected group.
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