Extracts of <em>Musa basjoo</em> induce growth inhibition and changes in the protein expression of cell cycle control molecules in human colorectal cancer cell lines

Matsumoto,Harutoshi; Ando,Saeko; Yoshimoto,Eri; Numano,Takamasa; Sultana,Nahida; Fukamachi,Katsumi; Iinuma,Munekazu; Okuda,Kensuke; Kimura,Kazunori; Suzui,Masumi

doi:10.3892/ol.2022.13219

Extracts of Musa basjoo induce growth inhibition and changes in the protein expression of cell cycle control molecules in human colorectal cancer cell lines

Authors:
- Harutoshi Matsumoto
- Saeko Ando
- Eri Yoshimoto
- Takamasa Numano
- Nahida Sultana
- Katsumi Fukamachi
- Munekazu Iinuma
- Kensuke Okuda
- Kazunori Kimura
- Masumi Suzui
View Affiliations

Affiliations: Department of Neurotoxicology, Graduate School of Medical Sciences and Medical School, Nagoya City University, Nagoya, Aichi 467‑8601, Japan, Research and Development Division, DIMS Institute of Medical Science, Ichinomiya, Aichi 491‑0113, Japan, Laboratory of Pharmacognosy, Gifu Pharmaceutical University, Gifu-shi, Gifu 501‑1196, Japan, Laboratory of Bioorganic and Natural Products Chemistry, Kobe Pharmaceutical University, Kobe, Hyogo 658‑8558, Japan, Department of Clinical Pharmaceutics, Graduate School of Medical Sciences and Medical School, Nagoya City University, Nagoya, Aichi 467‑8601, Japan
Published online on: January 27, 2022 https://doi.org/10.3892/ol.2022.13219
Article Number: 99
Copyright: © Matsumoto et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Musa basjoo (MB) is a species of the banana plant belonging to the genus Musa that has been used as a folk medicine. However, evidence‑based biological activities and the molecular mechanism of action of MB are unknown. Thus, the aim of the present study was to examine whether the crude dried leaf extracts of MB inhibit the growth of colorectal (HT29 and HCT116) and other types (HepG2, MCF‑7 and PC‑3) of human cancer cell lines. Crude extracts of MB inhibited the growth of cells with IC₅₀ values of 136 µg/ml (acetone extract, HT29), 51 µg/ml (acetone extract, HCT116), 45 µg/ml (acetone extract, HepG2), 40 µg/ml (acetone extract, MCF‑7), 29 µg/ml (acetone extract, PC‑3), 175 µg/ml (methanol extract, HT29), 137 µg/ml (methanol extract, HCT116), 102 µg/ml (methanol extract, HepG2), 85 µg/ml (methanol extract, MCF‑7), and 85 µg/ml (methanol extract, PC‑3) in colony formation assays, and 126 µg/ml (acetone extract, HT29), 68 µg/ml (acetone extract, HCT116), 260 µg/ml (methanol extract, HT29), and 216 µg/ml (methanol extract, HCT116) in MTT assays. Thin layer chromatography analysis revealed the potential existence of aromatic compounds in the acetone extract of MB. Flow cytometric analysis indicated that the percentage of cells in G1 increased, and this was associated with a concomitant decrease of cells in the S and/or G2‑M phases of the cell cycle. When colorectal cancer cells were treated with acetone extract of MB, there was a marked decrease in the levels of expression of the cyclin D1, cyclin E, cdk2 and cdk4 proteins and a marked increase in the levels of the expression of the p21^CIP1, p27^KIP1, and p53 proteins, but those of apoptosis‑associated protein PARP did not change. There was a tendency for acetone extract of MB to inhibit xenograft tumor growth in mice. Collectively, the crude extracts of MB contain active components that exert growth inhibition of human cancer cells. This is the first systematic study of the anticancer activity of MB and may broaden insights into the possible clinical approach of specific herbal medicines.

View Figures

View References

1	Surh YJ: Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer. 3:768–780. 2003. View Article : Google Scholar : PubMed/NCBI
2	Lee KW, Bode AM and Dong Z: Molecular targets of phytochemicals for cancer prevention. Nat Rev Cancer. 11:211–218. 2011. View Article : Google Scholar : PubMed/NCBI
3	Kennedy J: Bananas and people in the homeland of genus Musa: Not just pretty fruit. Ethnobot Res Appl. 7:179–197. 2009. View Article : Google Scholar
4	Zhang XW, Park YJ, Choe YH and Kim BS: Effect of anti-inflamentation extracts from Korean traditional medicinal herb. Int J Pharm Res. 4:122–125. 2014.
5	Imam MZ and Akter S: Musa paradisiaca L. and Musa sapientum L.: A phytochemical and pharmacological review. J Appl Pharm Sci. 1:14–20. 2011.
6	Nishino H, Tokuda H, Satomi Y, Masuda M, Onozuka M, Yamaguchi S, Takayasu J, Tsuruta J, Takemura M, Ii T, et al: Cancer chemoprevention by phytochemicals and their related compounds. Asian Pac J Cancer Prev. 1:49–55. 2000.PubMed/NCBI
7	Jiao L, Bi L, Lu Y, Wang Q, Gong Y, Shi J and Xu L: Cancer chemoprevention and therapy using Chinese herbal medicine. Biol Proced Online. 20:12018. View Article : Google Scholar : PubMed/NCBI
8	Morioka T, Suzui M, Nabandith V, Inamine M, Aniya Y, Nakayama T, Ichiba T, Mori H and Yoshimi N: The modifying effect of Peucedanum japonicum, a herb in the Ryukyu Islands, on azoxymethane-induced colon preneoplastic lesions in male F344 rats. Cancer Lett. 205:133–141. 2004. View Article : Google Scholar : PubMed/NCBI
9	Morioka T, Suzui M, Nabandith V, Inamine M, Aniya Y, Nakayama T, Ichiba T and Yoshimi N: Modifying effects of Terminalia catappa on azoxymethane-induced colon carcinogenesis in male F344 rats. Eur J Cancer Prev. 14:101–105. 2005. View Article : Google Scholar : PubMed/NCBI
10	Kaneshiro T, Suzui M, Takamatsu R, Murakami A, Ohigashi H, Fujino T and Yoshimi N: Growth inhibitory activities of crude extracts obtained from herbal plants in the Ryukyu Islands on several human colon carcinoma cell lines. Asian Pac J Cancer Prev. 6:353–358. 2005.PubMed/NCBI
11	Ishihara M, Naoi K, Hashita M, Itoh Y and Suzui M: Growth inhibitory activity of ethanol extracts of Chinese and Brazilian propolis in four human colon carcinoma cell lines. Oncol Rep. 22:349–354. 2009.PubMed/NCBI
12	Suzui M, Masuda M, Lim JTE, Albanese C, Pestell RG and Weinstein IB: Growth inhibition of human hepatoma cells by acyclic retinoid is associated with induction of p21CIP1 and inhibition of expression of cyclin D1. Cancer Res. 62:3997–4006. 2002.PubMed/NCBI
13	Ando S, Fukamachi K, Yoshimoto E, Matsumoto H, Iinuma M and Suzui M: Palmitoyl piperidinopiperidine, a novel derivative of 10-hydroxy-2-decenoic acid, as a potent and selective anticancer agent against human colon carcinoma cell lines. Int J Oncol. 58:251–265. 2021. View Article : Google Scholar : PubMed/NCBI
14	Suzui M, Inamine M, Kaneshiro T, Morioka T, Yoshimi N, Suzuki R, Kohno H and Tanaka T: Indole-3-carbinol inhibits the growth of human colon carcinoma cells but enhances the tumor multiplicity and volume of azoxymethane-induced rat colon carcinogenesis. Int J Oncol. 27:1391–1399. 2005.PubMed/NCBI
15	Suzui M, Sunagawa N, Chiba I, Moriwaki H and Yoshimi N: Acyclic retinoid, a novel synthetic retinoid, induces growth inhibition, apoptosis, and changes in mRNA expression of cell cycle- and differentiation-related molecules in human colon carcinoma cells. Int J Oncol. 28:1193–1199. 2006.PubMed/NCBI
16	Suzui M, Shimizu M, Masuda M, Lim JTE, Yoshimi N and Weinstein IB: Acyclic retinoid activates retinoic acid receptor β and induces transcriptional activation of p21CIP1 in HepG2 human hepatoma cells. Mol Cancer Ther. 3:309–316. 2004.PubMed/NCBI
17	Suzui M, Okuno M, Tanaka T, Nakagama H and Moriwaki H: Enhanced colon carcinogenesis induced by azoxymethane in min mice occurs via a mechanism independent of beta-catenin mutation. Cancer Lett. 183:31–41. 2002. View Article : Google Scholar : PubMed/NCBI
18	Weinstein IB: Disorders in cell circuitry during multistage carcinogenesis: The role of homeostasis. Carcinogenesis. 21:857–864. 2000. View Article : Google Scholar : PubMed/NCBI
19	Freed-Pastor WA and Prives C: Mutant p53: One name, many proteins. Genes Dev. 26:1268–1286. 2012. View Article : Google Scholar : PubMed/NCBI
20	Amelio I and Melino G: The p53 family and the hypoxia-inducible factors (HIFs): Determinants of cancer progression. Trends Biochem Sci. 40:425–434. 2015. View Article : Google Scholar : PubMed/NCBI
21	Tomasini R, Tsuchihara K, Wilhelm M, Fujitani M, Rufini A, Cheung CC, Khan F, Itie-Youten A, Wakeham A, Tsao MS, et al: TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev. 22:2677–2691. 2008. View Article : Google Scholar : PubMed/NCBI
22	Guo X, Keyes WM, Papazoglu C, Zuber J, Li W, Lowe SW, Vogel H and Mills AA: TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat Cell Biol. 11:1451–1457. 2009. View Article : Google Scholar : PubMed/NCBI
23	Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dötsch V, Andrews NC, Caput D and McKeon F: p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell. 2:305–316. 1998. View Article : Google Scholar : PubMed/NCBI
24	Huang B, Ban X, He J, Tong J, Tian J and Wang Y: Comparative analysis of essential oil components and antioxidant activity of extracts of Nelumbo nucifera from various areas of China. J Agric Food Chem. 58:441–448. 2010. View Article : Google Scholar : PubMed/NCBI
25	Wang Q, Yang Y, Zhao X, Zhu B, Nan P, Zhao J, Wang L, Chen F, Liu Z and Zhong Y: Chemical variation in the essential oil of Ephedra sinica from Northeastern China. Food Chem. 98:52–58. 2006. View Article : Google Scholar
26	Sefidkon F, Jamzad Z and Mirza M: Chemical variation in the essential oil of Satureja sahendica from Iran. Food Chem. 88:325–328. 2004. View Article : Google Scholar
27	Wang YH and Zhang YR: Variations in compositions and antioxidant activities of essential oils from leaves of Luodian Blumea balsamifera from different harvest times in China. PLoS One. 15:e02346612020. View Article : Google Scholar : PubMed/NCBI
28	Tan XJ, Li Q, Chen XH, Wang ZW, Shi ZY, Bi KS and Jia Y: Simultaneous determination of 13 bioactive compounds in Herba Artemisiae Scopariae (Yin Chen) from different harvest seasons by HPLC-DAD. J Pharm Biomed Anal. 47:847–853. 2008. View Article : Google Scholar : PubMed/NCBI
29	Jiang L, Zhang B, Wang Y, Sun J, Ma X, Wang G, Fu S, Lin C and Li Y: Three new acenaphthene derivatives from rhizomes of Musa basjoo and their cytotoxic activity. Nat Prod Res. 35:1307–1312. 2021. View Article : Google Scholar : PubMed/NCBI
30	Uchikura T, Sugiwaki H, Yoshimura M, Mitsuhashi H, Fuchino H, Kawahara N, Hakamatsuka T and Amakura Y: Characterization of UV-sensitive marker constituents of Polygala root for TLC: Applications in quality control of single crude drug extract preparations. Chem Pharm Bull (Tokyo). 66:1174–1180. 2018. View Article : Google Scholar : PubMed/NCBI
31	Patil S, Nivsarkar M and Anandajiwala S: Isolation and TLC densitometric quantification of Lysergol from the seeds of Ipomoea muricata (Linn.) Jacq. ISRN Chromatogr. 2013:1345862013. View Article : Google Scholar
32	Kaya B, Menemen Y and Saltan FZ: Flavonoid compounds identified in Alchemilla L. species collected in the north-eastern Black Sea region of Turkey. Afr J Tradit Complement Altern Med. 9:418–425. 2012. View Article : Google Scholar : PubMed/NCBI
33	Hemmalakshmi S, Priyanga S and Devaki K: Phytochemical screening and HPTLC fingerprinting analysis of ethanolic extract of Erythrina variegate L. flowers. Int J Pharm Pharm Sci. 8:210–217. 2016.
34	Bhat A and Raveesha KA: Antifungal activity of Pimenta dioica (L.) merril an aromatic medicinal tree. Int J Pharm Pharm Sci. 8:92–95. 2016. View Article : Google Scholar
35	Wang X, Wang D, Huo Y, Dai D, Li C and Liu G: Identification of isoliquiritigenin as an activator that stimulates the enzymatic production of glycyrrhetinic acid monoglucuronide. Sci Rep. 7:125032017. View Article : Google Scholar : PubMed/NCBI
36	Lv GP, Aoli M, Zhou B and Zhao J: Development of a rapid and simple non-derivatization method to determine constituents and antioxidative capacity of camellia oils by HPTLC. Food Nutr Sci. 4:204–210. 2013.
37	Sobstyl E, Szopa A, Ekiert H, Gnat S, Typek R and Choma IM: Effect directed analysis and TLC screening of Schisandra chinensis fruits. J Chromatogr A. 1618:4609422020. View Article : Google Scholar : PubMed/NCBI
38	Usia T, Banskota AH, Tezuka Y, Midorikawa K, Matsushige K and Kadota S: Constituents of Chinese propolis and their antiproliferative activities. J Nat Prod. 65:673–676. 2002. View Article : Google Scholar : PubMed/NCBI
39	Sun LP, Xu X, Hwang HH, Wang X, Su KY and Chen YL: Dichloromethane extracts of propolis protect cell from oxygen-glucose deprivation-induced oxidative stress via reducing apoptosis. Food Nutr Res. 60:300812016. View Article : Google Scholar : PubMed/NCBI
40	Xuan H, Wang Y, Li A, Fu C, Wang Y and Peng W: Bioactive components of Chinese propolis water extract on antitumor activity and quality control. Evid Based Complement Alternat Med. 2016:96419652016. View Article : Google Scholar : PubMed/NCBI
41	Ito T, Furusawa M, Tanaka T, Ali Z, Iliya I, Nakaya K, Murata J, Darnaedi D and Iinuma M: Resveratrol derivatives from Upuna borneensis. Chem Pharm Bull (Tokyo). 53:219–224. 2005. View Article : Google Scholar : PubMed/NCBI
42	Hattori H, Okuda K, Murase T, Shigetsura Y, Narise K, Semenza GL and Nagasawa H: Isolation, identification, and biological evaluation of HIF-1-modulating compounds from Brazilian green propolis. Bioorg Med Chem. 19:5392–5401. 2011. View Article : Google Scholar : PubMed/NCBI
43	Robles AJ, McCowen S, Cai S, Glassman M, Ruiz F II, Cichewicz RH, McHardy SF and Mooberry SL: Structure-activity relationships of new natural product-based diaryloxazoles with selective activity against androgen receptor-positive breast cancer cells. J Med Chem. 60:9275–9289. 2017. View Article : Google Scholar : PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI PubMed/NCBI