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| 研究生： |
周珮可 Chorpaka Thepthanee |
|---|---|
| 論文名稱： |
有色米及紫色稻葉生物活性物質分離純化及其功能特性 Isolation, purification and functional properties of bioactive substances from pigmented rice and black rice leaf |
| 指導教授： |
廖遠東
Liaw, Ean-Tun 劉展冏 Liu, Chan-Chiung |
| 學位類別： |
博士 Doctor |
| 系所名稱： |
農學院 - 食品科學系所 Department of Food Science |
| 畢業學年度： | 110 |
| 語文別： | 英文 |
| 論文頁數： | 161 |
| 中文關鍵詞： | 黑米稻葉 、抗氧化活性 、細胞週期 、細胞凋亡 |
| 外文關鍵詞： | Black rice leaf, Antioxidant activity, Cell cycle, Apoptosis |
| DOI URL： | http://doi.org/10.6346/NPUST202200028 |
| 相關次數： | 點閱：41 下載：0 |
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有色米 (Oryza sativa L.) 為水稻之特殊品種，其葉片與種子富含多種色素成分，可呈現黑色、紫色或紅色等不同顏色。文獻指出，有色米為一種良好之天然抗氧化劑來源。本研究將黑米稻葉與四種分別產自泰國與台灣之紅色及黑色有色米，以水與不同濃度乙醇（25%、50%、75%及95%）進行萃取，分析其生物活性成分及抗氧化能力，並且分離黑米稻葉中有助於抗氧化、抗發炎與抗癌活性之酚類化合物。首先測定黑米稻葉與有色米各種溶劑萃取物之總酚（TPC）、總類黃酮（TFC）、總花青素（TAC）與總原花青素（TPAC）含量及抗氧化活性（DPPH、ABTS自由基清除能力與還原力）。實驗結果顯示，可獲得最佳抗氧化活性與植物化學成分之最適萃取條件分別為50％（黑色米）與75％乙醇（紅色米與黑米稻葉），其中黑米稻葉之75％乙醇萃取物（BRLEE）具有最高之TPC與TFC值（分別為303.54 mg GAE/g與405.23 mg QE/g），黑米稻葉及黑色米萃取物皆含有花青素，而原花青素僅存在於紅色米中。此外，BRLEE也具有最佳之抗氧化能力，因此將BRLEE使用不同極性之溶劑進行分餾，包括正己烷（Hex）、乙酸乙酯（EtOAc）與正丁醇（n-BuOH），其中n-BuOH與EtOAc分餾組之TPC與TFC含量最高，而n-BuOH與水相分餾組富含花青素，於DPPH、ABTS自由基清除能力及還原力試驗中顯示強大之抗氧化能力。於LPS誘導RAW 264.7巨噬細胞之抗發炎活性試驗中，BRLEE與EtOAc分餾組雖然對細胞因子TNF-α釋放之影響較小，但具有降低NO及其它促發炎細胞因子（PGE2、IL-6及IL-1β）生成之能力，且顯著抑制iNOS與COX-2蛋白表現量。另外，EtOAc分餾組也可顯著降低HepG2肝癌細胞之存活率，增加Sub-G1期之細胞比例且透過粒線體依賴性途徑誘導細胞凋亡，並使用UV-LC-MS/MS 分析 EtOAc 分餾組之生物活性成分、酚酸及類黃酮化合物。進一步將富含酚類之EtOAc分餾組藉由Sephadex LH-20管柱層析，分離得到五種亞分餾組，接著測定其抗氧化及抗癌活性。結果顯示，所有亞分餾組中，亞分餾組5（Sub5）之TPC與TFC含量皆最高，且具有最佳DPPH、ABTS自由基清除能力與還原能力，IC50值分別為3.23、31.95及72.74 µg/mL。而於抗癌活性試驗中發現，Sub5之酚類化合物相較於其他亞分餾組，更能有效抑制肝癌（HepG2）、乳腺癌（MCF-7）及結腸癌（Caco-2）細胞之存活率，尤其是對HepG2肝癌細胞，Sub5顯著增加Sub-G1期之細胞比例，並可能透過粒線體及死亡受體依賴性途徑，伴隨著PI3K/AKT及Erk訊號路徑之抑制來誘導細胞凋亡。而UV-LC-MS/MS 之分析結果表明，由黑米稻葉分離而得之Sub5中主要化合物為木犀草素、木犀草素-8-C-葡萄糖苷與木犀草素-7-O-葡萄糖苷。綜上所述，黑米稻葉副產物有望作為一種具抗氧化、抗發炎與抗癌能力之生物活性成分之來源，可能有助於機能性食品與新穎藥劑之開發。
Pigmented rice (Oryza sativa L.) is a special type of rice with colors such as black, purple, and red in its seed or leaf. It has been reported to be a good source of natural antioxidants. The purposes of this study were to evaluate the effect of water and different concentrations of ethanol (25%, 50%, 75%, and 95%) extract on the phytochemical content and their antioxidant activity of four pigmented rice cultivars from Thailand and Taiwan and black rice leaf. Furthermore, isolated phenolic compounds from black rice leaf contribute strong antioxidant, anti-inflammatory and anticancer activities. Firstly, pigmented rice and black rice leaf were extracted with various solvents and then determined total phenolic (TPC), flavonoid (TFC), anthocyanins (TAC), and proanthocyanins (TPAC) contents, as well as antioxidant activities (DPPH and ABTS radicals scavenging activity and reducing power). The results showed that the optimal extraction condition for phytochemical contents and antioxidant activities recovery for red rice cultivars and black rice leaf were 75% ethanol, while black rice cultivars were 50% ethanol. Black rice leaf extracted with 75% ethanol (BRLEE) presented the highest TPC and TFC values (303.54 mg GAE/g and 405.23 mg QE/g, respectively). Moreover, black rice leaf and black rice extracts contained anthocyanin, whereas proanthocyanin was found only in red rice cultivars. Interestingly, the BRLEE showed higher antioxidant abilities than other solvent extracts and pigmented rice. Therefore, the BRLEE was collected to sequentially fractionated according to solvent polarity, including hexane (Hex), ethyl acetate (EtOAc), and n-butanol (n-BuOH). Among all the fractions, the n-BuOH and EtOAc fractions demonstrated the highest contents of TPC and TFC, while anthocyanins were found to be abundant in the n-BuOH and aqueous fractions, which also exhibited powerful antioxidant capacities according to DPPH and ABTS radical-scavenging assays and a reducing power assay. Regarding anti-inflammatory activity, BRLEE and EtOAc inhibited the production of NO and cytokine secretion (PGE2, IL-6, and IL-1β) but displayed less effect on TNF-α release in LPS-induced RAW 264.7 cells. They also significantly reduced iNOS and COX-2 protein expression. Additionally, the EtOAc fraction demonstrated the most significant activity against HepG2 liver carcinoma cells, inhibited cell growth, increased the Sub-G1 population, and induced apoptosis via mitochondrion-dependent mechanisms. The bioactive components, phenolic acids, and flavonoids from EtOAc fraction were also investigated using UV-LC-MS/MS. The phenolic-rich EtOAc fraction was further separated into five subfractions by Sephadex LH-20 column chromatography, and their antioxidant and anticancer activities were investigated. The results revealed that among all the subfractions, subfraction 5 (Sub5) showed the lowest IC50 values, 3.23, 31.95, and 72.74 µg/mL for DPPH, ABTS, and reducing power assays, respectively. The TPC and TFC contents were also superior for Sub5 compared to the other subfractions. The phenolic substances obtained from Sub5 could reduce the cell viability of liver (HepG2), breast (MCF-7), and colon (Caco-2) cancer cells more than other subfraction. Notably, Sub5 significantly increased the accumulation of cells in the Sub-G1 phase in HepG2 cells. Furthermore, it could trigger apoptosis cell death through mitochondrial and death receptor pathways accompanying by the inhibition of PI3K/AKT and Erk signaling pathways. The UV-LC-MS/MS analysis demonstrated that the main compounds in the Sub5 derived from black rice leaf were luteolin, luteolin-8-C-glucoside, and luteolin-7-O-glucoside. These findings highlight the possibility of using black rice leaves, a rice by-product, as a potential source of bioactive compounds with antioxidant, anti-inflammatory, and anticancer properties. Thus, it may be beneficial for use in functional foods and the pharmaceutical industry.
CONTENTS
摘要 I
ABSTRACT III
ACKNOWLEDGEMENTS VI
CONTENTS VII
LIST OF TABLES XII
LIST OF FIGURES XIV
CHAPTER I INTRODUCTION 1
1.1 Background 1
1.2 Objectives of the research 3
CHAPTER II LITERATURE REVIEW 4
2.1 Pigmented rice 4
2.1.1 Black rice 4
2.2.2 Red rice 5
2.2 Bioactive constituents in pigmented rice 5
2.2.1 Anthocyanins 5
2.2.2 Proanthocyanidins 6
2.2.3 Phenolic acids 7
2.2.4 Flavonoids 8
2.2.5 γ-Oryzanol 8
2.2.6 Vitamin E 9
2.3 Biological activities and health benefits of pigmented rice 10
2.3.1 Antioxidant activities 10
2.3.2 Anti-atherosclerosis activities 11
2.3.3 Anti-diabetic activities 11
2.3.4 Anti-inflammatory 12
2.3.5 Anticancer activity 12
2.4 Rice leaf 13
2.5 Free radicals and oxidative stress 14
2.6 Antioxidant 17
2.6.1 Polyphenols 17
2.6.1.1 Phenolic acids 18
2.6.1.2 Flavonoids 19
2.7 Inflammation 23
2.7.1 Macrophage and LPS 24
2.7.2 Cytokines 25
2.7.2.1 Tumor necrosis factor-alpha (TNF-α) 25
2.7.2.2 Interleukin 6 (IL-6) 26
2.7.2.2 Interleukin 1 beta (IL-1β) 26
2.7.3 NO and iNOS 26
2.7.4 PGE2 and COX-2 27
2.8 Cancer 27
2.8.1 Liver cancer 28
2.8.2 Breast cancer 29
2.8.3 Colon cancer 29
2.9 Cell cycle 30
2.10 Apoptosis 32
2.10.1 Morphology of Apoptosis 32
2.10.2 Mechanisms of Apoptosis 33
2.10.2.1 Apoptosis pathway 33
2.10.2.2 p53-induced apoptosis pathway 35
2.10.2.3 ERK pathway 38
2.10.2.4 PI3K/Akt pathway 38
CHAPTER III RESEARCH METHODOLOGY 40
3.1 Experimental design 40
3.2 Analytical methods 41
3.2.1 Part I: Effect of different concentrations of ethanol on the phytochemical contents and antioxidant activities of extracts from pigmented rice and black rice leaf. 41
3.2.2 Part II: Effect of different solvent polarity fractions on the phytochemical contents and their biological activities of black rice leaf. 41
3.2.3 Part III: Isolation, phytochemical contents, antioxidant, and anticancer activities of ethyl acetate subfractions derived from black rice leaf. 41
3.3 Material 41
3.3.1 Plant materials and sample preparation 41
3.3.2 Cells 41
3.4 Chemical reagents 42
3.5 Equipment 43
3.6 Assays 45
3.6.1 Extraction and fractionation of samples 45
3.6.2 Fractionation of phenolic compounds using Sephadex LH-20 column chromatography 46
3.6.3 Determination of total phenolic content (TPC) 46
3.6.4 Determination of total flavonoid content (TFC) 47
3.6.6 Determination of total proanthocyanidins content (TPAC) 48
3.6.7 Antioxidant activities 48
3.6.7.1 DPPH radical scavenging assay 48
3.6.7.2 ABTS radical scavenging assay 49
3.6.7.3 Reducing power assay 49
3.6.8 Cells experiment 50
3.6.8.1 Preparation of cell culture medium 50
3.6.8.2 Cell subculture 51
3.6.9 Anti-inflammatory activities 53
3.6.9.1 Cell viability 53
3.6.9.2 Nitric oxide (NO) determination 53
3.6.9.3 Cytokine productions 54
3.6.9.4 Western blotting assay 54
3.6.10 Anticancer activities 57
3.6.10.1 Cell proliferation 57
3.6.10.3 Apoptosis 58
3.6.10.4 Apoptosis protein 59
3.6.11 Bioactive compounds analysis by liquid chromatography tandem mass spectrometry (UV-LC-MS/MS) 60
3.7 Statistical analysis 61
CHAPTER IV RESULTS AND DISCUSSION 62
14.1 Part I: Effect of different concentrations of ethanol extract on the phytochemical contents and antioxidant activities of pigmented rice and black rice leaf. 62
4.1.1 Extraction yield, TPC, and TFC of pigmented rice grains and black rice leaf 63
4.1.2 TAC and TPAC of pigmented rice grains and black rice leaf 68
4.1.3 Antioxidant activities in extracts of pigmented rice grains and black rice leaf. 72
4.2 Part II: Effect of different solvent polarity fractions on the phytochemical contents and their biological activities of black rice leaf. 77
4.2.1 Extraction yields, TPC, TFC, and TAC of different fractions derived from BRLEE 78
4.2.2 Antioxidant activities of different fractions derived from BRLEE 81
4.2.3 Anti-inflammatory activities of BRLEE and its fractions in RAW 264.7 macrophage cells 84
4.2.5. Effect of BRLEE and EtOAc on LPS-induced iNOS and COX-2 expression in RAW 264.7 macrophage cells 88
4.2.6 Antiproliferative activity of BRLEE and its fractions on HepG2 cells 90
4.2.7 The effect of EtOAc on Sub-G1 phase accumulation and cell-cycle arrest in HepG2 cells 94
4.2.8 The effect of EtOAc on HepG2 cell apoptosis 96
4.2.9 Key proteins in apoptotic pathways regulated by EtOAc fraction 99
4.2.10 Composition of bioactive compounds of EtOAc fraction 102
4.3 Part III: Isolation, phytochemical contents, antioxidant, and anticancer activities of ethyl acetate subfractions derived from black rice leaf 107
4.3.1 Extraction yield, TPC, and TFC of ethyl acetate subfractions derived from black rice leaf 108
4.3.2 Antioxidant activities of ethyl acetate subfractions derived from black rice leaf 110
4.3.3 Antiproliferative activity of ethyl acetate subfractions derived from black rice leaf against several human cancer cell lines 112
4.3.4 Morphological changes of HepG2 cells following treatment with Sub5 115
4.3.5 Effect of Sub5 on Sub-G1 phase accumulation and cell-cycle arrest in HepG2 cells 117
4.3.6 Effect of Sub5 on HepG2 cell apoptosis 119
4.3.7 Effect of Sub5 on the expression of proteins from intrinsic and extrinsic apoptotic pathways in HepG2 cells 122
4.3.8 Effect of Sub5 on the expression of proteins from PI3K/Akt and Erk signaling pathway in HepG2 cells 126
4.3.9 Composition of bioactive compounds of Sub5 128
CHAPTER V CONCLUSIONS 131
REFERENCES 133
BIO-SKETCH OF AUTHOR 160
LIST OF TABLES
Table 1. Biologically relevant free radicals and reactive. 16
Table 2. Common buffer in Western blotting. 56
Table 3. Extraction yields of pigmented rice grains and black rice leaf. 65
Table 4. Total phenolic contents in extracts of pigmented rice grains and black rice leaf. 66
Table 5. Total flavonoid content in extracts of pigmented rice grains and black rice leaf. 67
Table 6. Total anthocyanins content in extracts of pigmented rice grains and black rice leaf. 70
Table 7. Total proanthocyanidins content in extracts of pigmented rice grains and black rice leaf. 71
Table 8. EC50 values of DPPH radical scavenging activity of pigmented rice grains and black rice leaf extracts. 74
Table 9. EC50 values of ABTS radical scavenging activity of pigmented rice grains and black rice leaf extracts. 75
Table 10. IC50 values of reducing power of black rice leaf and pigmented rice extracts. 76
Table 11. Extraction yield, TPC, TFC, and TAC contents of different fractions derived from BRLEE. 80
Table 12. EC50 values of antioxidant activities of different fractions derived from the crude ethanolic extract of black rice leaf. 83
Table 13. The percentage of live, early, late apoptotic, and necrotic HepG2 cells measured by flow cytometry after treatment with ethyl acetate fraction and 5-FU for 24 h and 48 h. 98
Table 14. Phenolic compounds identified in EtOAc fraction by UV-LC-MS/MS. 106
Table 15. Extraction yield, TPC, and TFC of ethyl acetate subfractions derived from black rice leaf. 109
Table 16. IC50 values of antioxidant activities of ethyl acetate subfractions derived from black rice leaf. 111
Table 17. Antiproliferative activity of ethyl acetate subfractions derived from black rice leaf against several human cancer cell lines. 114
Table 18. The percentage of live, early, late apoptotic, and necrotic HepG2 cells measured by flow cytometry after treatment with subfraction 5 and 5-FU for 24 h and 48 h. 121
Table 19. Phenolic compounds identified in Sub5 by UV-LC-MS/MS. 130
LIST OF FIGURES
Figure 1. Chemical structures of benzoic acid and cinnamic acid derivatives. 19
Figure 2. Subgroups of flavonoids: flavones, flavonols, flavanones, flavanonols, flavanols or catechins, anthocyanins and chalcones. 22
Figure 3. Structure and immunogenicity of lipopolysaccharide from Gram-negative bacteria. 25
Figure 4. The cell cycle: different phases and checkpoints. 31
Figure 5. The morphology of apoptosis. 33
Figure 6. Schematic diagram of the intrinsic and extrinsic apoptosis signaling pathways. 37
Figure 7. A schematic diagram of the PI3K/AKT signaling pathway. 39
Figure 8. Diagram of whole protocols. 40
Figure 9. Effect of black rice leaf BRLEE and its solvent fractions on the viability of (A) and the production of nitric oxide (NO) (B) by RAW 264.7 cells stimulated with LPS. ## p < 0.01, compared with non-stimulated LPS; * p < 0.05 and ** p < 0.01 compared with 100 ng/mL, LPS-stimulated. 85
Figure 10. Effects of BRLEE and EtOAc fractions on PGE2 (A), IL-6 (B), IL-1β (C), and TNF-α (D) production in LPS-induced RAW 264.7 cells. * p < 0.05 and ** p < 0.01 compared with 100 ng/mL, LPS-stimulated. 87
Figure 11. Effects of BRLEE (A) and EtOAc (B) fractions on iNOS and COX-2 protein secretion in LPS-induced RAW 264.7 cells. ## p < 0.01, compared with non-stimulated LPS; * p < 0.05 and ** p < 0.01 compared with 100 ng/mL, LPS-stimulated. 89
Figure 12. Cytotoxicity of BRLEE and various solvent fractions on normal liver cell (FL83B). Cell growth was determined after treatment with 0–1000 µg/mL of BRLEE and solvent fractions for 48 h using the MTT assay. 91
Figure 13. Antiproliferative effects of BRLEE and various solvent fractions on HepG2 cells. Cell growth was determined after treatment with 0–1000 µg/mL of BRLEE and solvent fractions for 24 h (A) and 48 h (B) using the MTT assay. * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. 92
Figure 14. Cell morphology of HepG2 cells was observed by inverted microscopy after treatment with 0–1000 µg/mL of EtOAc fraction for 24 h and 48 h. 93
Figure 15. The effect of EtoAc fraction on Sub-G1 phase accumulation and cell-cycle arrest in HepG2 cells. The cells were treated with EtOAc (0–1000 µg/mL) for 24 h (A) and 48 h (B) and stained with PI, followed by flow cytometry. Data represent the percentages of cell proportion in each cell-cycle phase (Sub-G1, G0/G1, S, and G2/M). ** p < 0.01 significant difference between the control and the concentration of each sample. 95
Figure 16. The effect of EtOAc fraction on HepG2 cell apoptosis. The cells were treated with 0–1000 µg/mL of EtOAc for 24 h (A) and 48 h (B) and labeled with Annexin V-FITC and PI, followed by the measurement of cell apoptosis by flow cytometry. Data represent the percentages of total apoptotic cell population of HepG2 cells (C). ** p < 0.01, significant difference between the control and the concentration of each sample. ## p < 0.01, significant difference between 24 h and 48 h of each concentration. 97
Figure 17. Effect of ethyl acetate fraction (EtOAc) on the expression of Bcl-2 family proteins in HepG2 cells. The cells were treated with 0–1000 µg/mL of EtOAc for 24 h (A) and 48 h (B). * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. β-actin was used in Western blot analysis as a loading control. 100
Figure 18. Effect of ethyl acetate fraction (EtOAc) on the expression of apoptotic proteins (PARP, cleaved PARP, and caspase family) in HepG2 cells. The cells were treated with 0–1000 µg/mL of EtOAc for 24 h (A) and 48 h (B). * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. β-actin was used in Western blot analysis as a loading control. 101
Figure 19. Total ion chromatogram of the EtOAc fraction–Catechin 20 µg/mL produced by UV-LC-MS/MS with UV detection at 280 nm and electrospray ionization negative full scan mode (A). Full scan mass spectra and product ion mass spectra of [M-H]- ions of peak 1–14 (B–O). The peaks are marked with the names of the substances mentioned in Table 14. 104
Figure 20. Sephadex LH-20 column chromatogram of ethyl acetate subfraction from black rice leaf ethanolic extract. 109
Figure 21. Cytotoxicity of ethyl acetate subfractions derived from black rice leaf on normal liver cell (FL83B). Cell growth was determined after treatment with 0–400 µg/mL of different subfractions for 72 h using the MTT assay. 113
Figure 22. Cell morphology of HepG2 cells was observed by inverted microscopy after treatment with subfraction 5 (0–400 µg/mL) for 24 h and 48 h. 116
Figure 23. The effect of Sub5 on Sub-G1 phase accumulation and cell-cycle arrest in HepG2 cells. The cells were treated with subfraction 5 (0–400 µg/mL) for 24 h (A) and 48 h (B) and stained with PI, followed by flow cytometry. Data represent the percentages of cell proportion in each cell-cycle phase (Sub-G1, G0/G1, S, and G2/M). * p < 0.05 and ** p < 0.01 significant difference between the control and the concentration of each sample. 118
Figure 24. The effect of Sub5 on HepG2 cell apoptosis. The cells were treated with 0–400 µg/mL of Sub5 for 24 h (A) and 48 h (B) and labeled with Annexin V-FITC and PI, followed by the measurement of cell apoptosis by flow cytometry. Data represent the percentages of total apoptotic cell population of HepG2 cells (C). ** p < 0.01, significant difference between the control and the concentration of each sample. ## p < 0.01, significant difference between 24 h and 48 h of each concentration. 120
Figure 25. Effect of subfraction 5 (Sub5) on the expression of Bcl-2 family proteins in HepG2 cells. The cells were treated with 0–400 µg/mL of Sub5 or fluorouracil (5-FU) (25 µg/mL) for 24 h. * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. β-actin was used in Western blot analysis as a loading control. 123
Figure 26. Effect of subfraction 5 (Sub5) on the expression of apoptotic proteins (PARP, cleaved PARP, caspase family, and p53) in HepG2 cells. The cells were treated with 0–400 µg/mL of Sub5 for 24 h or fluorouracil (5-FU) (25 µg/mL). * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. β-actin was used in Western blot analysis as a loading control. 124
Figure 27. Effect of subfraction 5 (Sub5) on the expression of apoptotic proteins (Fas, FADD, and caspase 8) in HepG2 cells. The cells were treated with 0–400 µg/mL of Sub5 or fluorouracil (5-FU) (25 µg/mL) for 24 h. * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. GADPH was used in Western blot analysis as a loading control. 125
Figure 28. Effect of subfraction 5 (Sub5) on the expression of proteins from PI3K/Akt and Erk signaling pathway in HepG2 cells. The cells were treated with 0–400 µg/mL of Sub5 for 24 h. * p < 0.05 and ** p < 0.01, significant difference between the control and the concentration of each sample. GADPH was used in Western blot analysis as a loading control. 127
Figure 29. Total ion chromatogram of the Sub5–Catechin 20 µg/mL produced by UV-LC-MS/MS with UV detection at 280 nm and electrospray ionization negative full scan mode (A). Full scan mass spectra and product ion mass spectra of [M-H]- ions of peak 1 (B), peak 2 (C), peak 3 (D), peak 4 (E), peak 5 (F), and peak 6 (G). The peaks are marked with the names of the substances mentioned in Table 19. 129
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校外公開2027/01/23