Sasa quelpaertensis Nakai extract induces p53‑independent apoptosis via the elevation of nitric oxide production in human HCT116 colon cancer cells

Kim,Min  Young

doi:10.3892/ol.2020.11379

Sasa quelpaertensis Nakai extract induces p53‑independent apoptosis via the elevation of nitric oxide production in human HCT116 colon cancer cells

Authors:
- Min Young Kim
View Affiliations

Affiliations: Toxicology Laboratory, Faculty of Biotechnology (Biomaterials), College of Applied Science, Jeju National University, Jeju 63243, Republic of Korea
Published online on: February 10, 2020 https://doi.org/10.3892/ol.2020.11379
Pages: 3027-3034

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

Induction of apoptosis in human cancer cells by Sasa quelpaertensis Nakai has been considered to be a potential therapeutic target for cancer treatment; however, the underlying mechanisms of action are not well understood. The present study investigated the role of nitric oxide (NO•) and inhibitors of apoptosis (IAPs) during apoptosis induced by Sasa quelpaertensis Nakai extracts (SQE) in p53‑wild type (WT) and p53‑null HCT116 colon carcinoma cells. Trypan blue exclusion and Annexin V/propidium iodide assays were used to test for antiproliferation, and apoptosis and cell cycle. Griess and reverse transcription‑polymerase chain reaction and western blotting assays were carried out to assay NO• production, and to detect the mRNA and protein levels of Bcl‑2, PARP and IAPs. A colorimetric assay was utilized to measure the time‑dependent increase in caspase‑3 activity. SQE inhibited cell growth and promoted apoptosis by the elevation of NO• in a dose‑ and time‑dependent manner. In addition, both cell types underwent a reduction in mRNA and protein levels of IAPs (survivin, CIAP‑1 and ‑2, and X‑linked inhibitor of apoptosis) as well as anti‑apoptotic Bcl‑2, whereas an increase in protein expression of poly (ADP‑ribose) polymerase 1 and caspase 3 activity was observed; however, an equivalent cytotoxic and apoptotic effect by SQE was observed in p53‑WT and p53‑null cells. Collectively, the results indicated that SQE‑induced apoptosis was independent of p53 status and associated with modulation of endogenous NO• and IAP family gene expression.

View Figures

View References

1	Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI
2	Palma S, Zwenger AO, Croce MV, Abba MC and Lacunza E: From molecular biology to clinical trials: Toward personalized colorectal cancer therapy. Clin Colorectal Cancer. 15:104–115. 2016. View Article : Google Scholar : PubMed/NCBI
3	Janne PA and Mayer RJ: Chemoprevention of colorectal cancer. N Engl J Med. 342:1960–1968. 2000. View Article : Google Scholar : PubMed/NCBI
4	de Gramont A, Figer A, Seymour M, Homerin M, Hmissi A, Cassidy J, Boni C, Cortes-Funes H, Cervantes A, Freyer G, et al: Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol. 18:2938–2947. 2000. View Article : Google Scholar : PubMed/NCBI
5	Rejhová A, Opattová A, Čumová A, Slíva D and Vodička P: Natural compounds and combination therapy in colorectal cancer treatment. Eur J Med Chem. 144:582–594. 2018. View Article : Google Scholar : PubMed/NCBI
6	Lichota A and Gwozdzinski K: Anticancer activity of natural compounds from plant and marine environment. Int J Mol Sci. 19(pii): E35332018. View Article : Google Scholar : PubMed/NCBI
7	Hu C, Zhang Y and Kitts DD: Evaluation of antioxidant and prooxidant activities of bamboo Phyllostachys nigra var. Henonis leaf extract in vitro. J Agric Food Chem. 48:3170–3176. 2000. View Article : Google Scholar : PubMed/NCBI
8	Kweon MH, Hwang HJ and Sung HC: Identification and antioxidant activity of novel chlorogenic acid derivatives from bamboo (Phyllostachys edulis). J Agric Food Chem. 49:4646–4655. 2001. View Article : Google Scholar : PubMed/NCBI
9	Ra JH, Nakamura M, Herath KHINM, Jee Y and Kim JS: Antioxidant and hepatoprotective effects of different ethanol concentrations in extraction from leaves of Sasa quelpaertensis Nakai. South African J Botany. 112:376–382. 2017. View Article : Google Scholar
10	Seki T and Maeda H: Cancer preventive effect of Kumaizasa bamboo leaf extracts administered prior to carcinogenesis or cancer inoculation. Anticancer Res. 30:111–118. 2010.PubMed/NCBI
11	Sakai S, Saito G, Sugayama J, Kamasuka T, Takano T and Takada S: Anticancer effect of polysaccharide fraction prepared from bamboo grass. Gan. 55:197–203. 1964.PubMed/NCBI
12	Yoon SA, Kang SI, Shin SH, Ko HC and Kim SJ: Anti-diabetic potential of a Sasa quelpaertensis Nakai extract in L6 skeletal muscle cells. Food Sci Biotechnol. 23:1335–1339. 2014. View Article : Google Scholar
13	An SM, Lee SI, Choi SW, Moon SW and Boo YC: p-Coumaric acid, a constituent of Sasa quelpaertensis Nakai, inhibits cellular melanogenesis stimulated by alpha-melanocyte stimulating hormone. Br J Dermatol. 159:292–299. 2008. View Article : Google Scholar : PubMed/NCBI
14	Madushani Herath KHIN, Bing SJ, Cho J, Kim A, Kim G, Kim JS, Kim JB, Doh YH and Jee Y: Sasa quelpaertensis leaves ameliorate alcohol-induced liver injury by attenuating oxidative stress in HepG2 cells and mice. Acta Histochem. 120:477–489. 2018. View Article : Google Scholar : PubMed/NCBI
15	Ryou SH, Kang MS, Kim KI, Kang YH and Kang JS: Effects of green tea or Sasa quelpaertensis bamboo leaves on plasma and liver lipids, erythrocyte Na efflux, and platelet aggregation in ovariectomized rats. Nutr Res Pract. 6:106–112. 2012. View Article : Google Scholar : PubMed/NCBI
16	Jang MG, Park SY, Lee SR, Choi SY, Hwang JH, Ko HC, Park JG, Chung WS and Kim SJ: Sasa quelpaertensis leaf extracts induce apoptosis in human leukemia HL-60 cells. Food Sci Biotechnol. 17:188–190. 2008.
17	Jang MG, Ko HC and Kim SJ: Effect of Sasa quelpaertensis Nakai extracts and its constituent p-coumaric acid on the apoptosis of human cancer cell lines. J Food Biochem. 24:293–297. 2018.
18	Byun JH and Kim MY: Apoptotic effect of Sasa quelpaertensis Nakai in human colon cancer HT-29 cells. J Life Sci. 24:1012–1018. 2014. View Article : Google Scholar
19	Kim JH and Kim MY: Antiproliferative and apoptotic effects of Sasa quelpaertensis Nakai in human cancer cells. J Life Sci. 24:903–909. 2014. View Article : Google Scholar
20	Redza-Dutordoir M and Averill-Bates DA: Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 1863:2977–2992. 2016. View Article : Google Scholar : PubMed/NCBI
21	Tang D, Kang R, Berghe TV, Vandenabeele P and Kroemer G: The molecular machinery of regulated cell death. Cell Res. 29:347–364. 2019. View Article : Google Scholar : PubMed/NCBI
22	Moon SH, Cho MH and Kim MY: Cellular inactivation of nitric oxide induces p53-dependent apoptosis in human melanoma cells. Trop J Pharm Res. 15:1595–1603. 2016. View Article : Google Scholar
23	Kim JY, Kim JH, Byun JH, Lee YJ, Im SJ, Lee D, Moon SH and Kim MY: Antioxidant and anticancer activities of water and ethanol extracts obtained from Sasa quelpaertensis Nakai. Life Sci J. 10:1250–1254. 2013.
24	Kim M, Kim YS, Kim KM, Ko HC, Kim SJ, Kim JH and Kim Y: Combination of Sasa quelpaertensis Nakai leaf extract and cisplatin suppresses the cancer stemness and invasion of human lung cancer cells. Integr Cancer Ther. 13:529–540. 2014. View Article : Google Scholar : PubMed/NCBI
25	Xu W, Liu LZ, Loizidou M, Ahmed M and Charles IG: The role of nitric oxide in cancer. Cell Res. 12:311–320. 2002. View Article : Google Scholar : PubMed/NCBI
26	Wink DA, Ridnour LA, Hussain SP and Harris CC: The reemergence of nitric oxide and cancer. Nitric Oxide. 19:65–67. 2008. View Article : Google Scholar : PubMed/NCBI
27	Rao CV: Nitric oxide signaling in colon cancer chemoprevention. Mutat Res. 555:107–119. 2004. View Article : Google Scholar : PubMed/NCBI
28	Li CQ and Wogan GN: Nitric oxide as a modulator of apoptosis. Cancer Lett. 226:1–15. 2005. View Article : Google Scholar : PubMed/NCBI
29	Karin M and Lin A: NF-kappaB at the crossroads of life and death. Nat Immunol. 3:221–227. 2002. View Article : Google Scholar : PubMed/NCBI
30	Salvesen GS and Duckett CS: IAP proteins: Blocking the road to death's door. Nat Rev Mol Cell Biol. 3:401–410. 2002. View Article : Google Scholar : PubMed/NCBI
31	Fiandalo MV and Kyprianou N: Caspase control: Protagonists of cancer cell apoptosis. Exp Oncol. 34:165–175. 2012.PubMed/NCBI
32	Jin SJ, Yang Y, Ma L, Ma BH, Ren LP, Guo LC, Wang WB, Zhang YX, Zhao ZJ and Cui M: In vivo and in vitro induction of the apoptotic effects of oxysophoridine on colorectal cancer cells via the Bcl-2/Bax/caspase-3 signaling pathway. Oncol Lett. 14:8000–8006. 2017.PubMed/NCBI
33	Zhao Y, Jing Z, Lv J, Zhang Z, Lin J, Cao X, Zhao Z, Liu P and Mao W: Berberine activates caspase-9/cytochrome c-mediated apoptosis to suppress triple-negative breast cancer cells in vitro and in vivo. Biomed Pharmacother. 95:18–24. 2017. View Article : Google Scholar : PubMed/NCBI
34	Koh DW, Dawson TM and Dawson VL: Mediation of cell death by poly(ADP-ribose) polymerase-1. Pharmacol Res. 52:5–14. 2005. View Article : Google Scholar : PubMed/NCBI
35	Ozaki T and Nakagawara A: p53: The attractive tumor suppressor in the cancer research field. J Biomed Biotechnol. 2011:6039252011. View Article : Google Scholar : PubMed/NCBI
36	Levine AJ, Momand J and Finlay CA: The p53 tumour suppressor gene. Nature. 351:453–456. 1991. View Article : Google Scholar : PubMed/NCBI
37	Zilfou JT and Lowe SW: Tumor suppressive functions of p53. Cold Spring Harb Perspect Biol. 1:a0018832009. View Article : Google Scholar : PubMed/NCBI
38	Chen L, Jiang J, Cheng C, Yang A, He Q, Li D and Wang Z: P53 dependent and independent apoptosis induced by lidamycin in human colorectal cancer cells. Cancer Biol Ther. 6:965–973. 2007. View Article : Google Scholar : PubMed/NCBI
39	Mahyar-Roemer M and Roemer K: p21 Waf1/Cip1 can protect human colon carcinoma cells against p53-dependent and p53-independent apoptosis induced by natural chemopreventive and therapeutic agents. Oncogene. 20:3387–3398. 2001. View Article : Google Scholar : PubMed/NCBI