Journal of Traditional Chinese Medicine ›› 2022, Vol. 42 ›› Issue (6): 922-931.DOI: 10.19852/j.cnki.jtcm.20220817.002
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Transcriptome profile and its partly verification of human hepatocellular carcinoma cells exposed to Yuzhizi (Fructus Akebiae Quinatae) seed extract
FAN Xiaoyan1, LI Mingzhe1, CHEN Long2, LIANG Chao1, LU Wenli1, PAN Zhiqiang1, JIA Dongwei1, PENG Peike1, FANG Zhaoqin1(
), LIU Xiaomei1()
- 1 Department of Experimental Traditional Chinese Medicine, School of Basic Medical Science, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
2 Experiment Center of Science and Technology, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
-
Received:2021-11-11Accepted:2022-01-22Online:2022-12-15Published:2022-08-17 -
Contact:FANG Zhaoqin,LIU Xiaomei -
About author:LIU Xiaomei, Department of Experimental Traditional Chinese Medicine, School of Basic Medical Science, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China. wfjlxm2005@126.com, Telephone: +86-21-51322118; +86-21-51322117
FANG Zhaoqin, Department of Experimental Traditional Chinese Medicine, School of Basic Medical Science, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China. zq_fang@qq.com;
-
Supported by:grants from Shanghai Municipal Commission of Education: Study on the Synergistic Effect and Action Mechanism of Yuzhizi (Fructus Akebiae Quinatae) Seed Extract on Sorafenib(2019LK065);Shanghai Municipal Commission of Health and Family Planning [No. ](ZY (2018-2020)-CCCX-2001-01)
Cite this article
FAN Xiaoyan, LI Mingzhe, CHEN Long, LIANG Chao, LU Wenli, PAN Zhiqiang, JIA Dongwei, PENG Peike, FANG Zhaoqin, LIU Xiaomei. Transcriptome profile and its partly verification of human hepatocellular carcinoma cells exposed to Yuzhizi (Fructus Akebiae Quinatae) seed extract[J]. Journal of Traditional Chinese Medicine, 2022, 42(6): 922-931.
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Table 1 Primers used in polymerase chain reaction
| Gene | Primer sequence |
|---|---|
| Ribosomal protein S27a (RPS27A) | Sense 5’-GCCCTTCTGATGAATGTGGT-3’ |
| Anti-sense 5’-TGGTGTGACCATCAATTTGG-3’ | |
| Transferrin (TF) | Sense 5’-GCTGCTTTGGGAGACAGAAC-3’ |
| Anti-sense 5’-ACAGCTTAAGATCGGCCTCA-3’ | |
| Ribosomal protein S20 (RPS20) | Sense 5’-AAGGGCTGAGGATTTTTGGT-3’ |
| Anti-sense 5’-GGGTGTTTTTCCGGTATCCT-3’ | |
| Ribosomal protein L9 (RPL9) | Sense 5’-ATGCTCACTTCCCCATCAAC-3’ |
| Anti-sense 5’-ACACCTGGTCTCATCCGAAC-3’ | |
| Protein phosphatase 2 regulatory Subunit b alpha (PPP2R2A) | Sense 5’-AGTCAGTTTGGGGTCAGTGG-3’ |
| Anti-sense 5’-TGCCCAAAGGTATGACACAA-3’ | |
| Transthyretin (TTR) | Sense 5’-ATGGCTTCTCATCGTCTGCT-3’ |
| Anti-sense 5’-TGTCATCAGCAGCCTTTCTG-3’ | |
| Thioredoxin reductase 1 (TXNRD1) | Sense 5’-AGGAAGATTGCTGGCTCAGA-3’ |
| Anti-sense 5’-CTCCTCAGAAAGGCCACAAG-3’ | |
| Ribosomal protein L3 (RPL3) | Sense 5’-CCGCACTGAGATCAACAAGA-3’ |
| Anti-sense 5’-CAGCCTTTCAGCATGACAAA-3’ | |
| Ribophorin I (RPN1) | Sense 5’-GCACATTCAGGACATTGTGG-3’ |
| Anti-sense 5’-CCACTGTTGAGGGTGGAGAT-3’ | |
| Ribosomal protein L24 (RPL24) | Sense 5’-CAAATTCCAGAGGGCCATTA-3’ |
| Anti-sense 5’-GCAGCCCTGATAGCTTGTTC-3’ | |
| Alpha fetoprotein (AFP) | Sense 5’-GTAGCGCTGCAAACAATGAA-3’ |
| Anti-sense 5’-CCCTCTTCAGCAAAGCAGAC-3’ | |
| Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) | Sense 5’-CGACCACTTTGTCAAGCTCA-3’ |
| Anti-sense 5’-AGGGGTCTACATGGCAACTG-3’ |
Table 1 Primers used in polymerase chain reaction
| Gene | Primer sequence |
|---|---|
| Ribosomal protein S27a (RPS27A) | Sense 5’-GCCCTTCTGATGAATGTGGT-3’ |
| Anti-sense 5’-TGGTGTGACCATCAATTTGG-3’ | |
| Transferrin (TF) | Sense 5’-GCTGCTTTGGGAGACAGAAC-3’ |
| Anti-sense 5’-ACAGCTTAAGATCGGCCTCA-3’ | |
| Ribosomal protein S20 (RPS20) | Sense 5’-AAGGGCTGAGGATTTTTGGT-3’ |
| Anti-sense 5’-GGGTGTTTTTCCGGTATCCT-3’ | |
| Ribosomal protein L9 (RPL9) | Sense 5’-ATGCTCACTTCCCCATCAAC-3’ |
| Anti-sense 5’-ACACCTGGTCTCATCCGAAC-3’ | |
| Protein phosphatase 2 regulatory Subunit b alpha (PPP2R2A) | Sense 5’-AGTCAGTTTGGGGTCAGTGG-3’ |
| Anti-sense 5’-TGCCCAAAGGTATGACACAA-3’ | |
| Transthyretin (TTR) | Sense 5’-ATGGCTTCTCATCGTCTGCT-3’ |
| Anti-sense 5’-TGTCATCAGCAGCCTTTCTG-3’ | |
| Thioredoxin reductase 1 (TXNRD1) | Sense 5’-AGGAAGATTGCTGGCTCAGA-3’ |
| Anti-sense 5’-CTCCTCAGAAAGGCCACAAG-3’ | |
| Ribosomal protein L3 (RPL3) | Sense 5’-CCGCACTGAGATCAACAAGA-3’ |
| Anti-sense 5’-CAGCCTTTCAGCATGACAAA-3’ | |
| Ribophorin I (RPN1) | Sense 5’-GCACATTCAGGACATTGTGG-3’ |
| Anti-sense 5’-CCACTGTTGAGGGTGGAGAT-3’ | |
| Ribosomal protein L24 (RPL24) | Sense 5’-CAAATTCCAGAGGGCCATTA-3’ |
| Anti-sense 5’-GCAGCCCTGATAGCTTGTTC-3’ | |
| Alpha fetoprotein (AFP) | Sense 5’-GTAGCGCTGCAAACAATGAA-3’ |
| Anti-sense 5’-CCCTCTTCAGCAAAGCAGAC-3’ | |
| Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) | Sense 5’-CGACCACTTTGTCAAGCTCA-3’ |
| Anti-sense 5’-AGGGGTCTACATGGCAACTG-3’ |
Figure 1 Chromatography of α-hederin standard and FAQSE sample by UPLC-ESI-MS/MS A: α-hederin standard solution, the injection concentration of which was 25, 50, 100, 200 and 400 ng/mL; B: FAQSE sample solution, the injection concentration of which was 5.0 mg/mL; FAQSE: Yuzhizi (Fructus Akebiae Quinatae) seed extract; UPLC-ESI-MS/MS: ultra-performance liquid chromatography-electrospray ionization tandem mass spectrometry.
Figure 1 Chromatography of α-hederin standard and FAQSE sample by UPLC-ESI-MS/MS A: α-hederin standard solution, the injection concentration of which was 25, 50, 100, 200 and 400 ng/mL; B: FAQSE sample solution, the injection concentration of which was 5.0 mg/mL; FAQSE: Yuzhizi (Fructus Akebiae Quinatae) seed extract; UPLC-ESI-MS/MS: ultra-performance liquid chromatography-electrospray ionization tandem mass spectrometry.
Table 2 Effect of FAQSE on the viability of HepG2 and Huh7 cells (%, $\bar{x} \pm s$)
| Group | n | HepG2 | Huh7 | |||||
|---|---|---|---|---|---|---|---|---|
| 24 h | 48 h | 24 h | 48 h | |||||
| Control | 3 | 100.0±4.6 | 100.0±2.0 | 100.0±1.6 | 100.0±1.3 | |||
| FAQSE | 0.3125 mg/mL | 3 | 97.8±3.4 | 93.0±1.9 | 97.1±1.2 | 86.2±4.6 | ||
| 0.625 mg/mL | 3 | 82.0±4.1a | 61.4±6.0a | 70.1±3.1a | 50.4±1.4a | |||
| 0.9375 mg/mL | 3 | 70.5±2.3a | 51.6±1.9a | 61.1±4.9a | 40.2±1.2a | |||
| 1.25 mg/mL | 3 | 57.6±3.6a | 40.3±0.7a | 48.6±2.1a | 30.8±1.0a | |||
Table 2 Effect of FAQSE on the viability of HepG2 and Huh7 cells (%, $\bar{x} \pm s$)
| Group | n | HepG2 | Huh7 | |||||
|---|---|---|---|---|---|---|---|---|
| 24 h | 48 h | 24 h | 48 h | |||||
| Control | 3 | 100.0±4.6 | 100.0±2.0 | 100.0±1.6 | 100.0±1.3 | |||
| FAQSE | 0.3125 mg/mL | 3 | 97.8±3.4 | 93.0±1.9 | 97.1±1.2 | 86.2±4.6 | ||
| 0.625 mg/mL | 3 | 82.0±4.1a | 61.4±6.0a | 70.1±3.1a | 50.4±1.4a | |||
| 0.9375 mg/mL | 3 | 70.5±2.3a | 51.6±1.9a | 61.1±4.9a | 40.2±1.2a | |||
| 1.25 mg/mL | 3 | 57.6±3.6a | 40.3±0.7a | 48.6±2.1a | 30.8±1.0a | |||
Table 3 Top 5 KEGG pathways of co-upregulated DEGs
| Pathway ID | Name | Count | P value | Gene |
|---|---|---|---|---|
| hsa04144 | Endocytosis | 10 | 0.002997 | GIT1, RAB7A, RAB31, RAB5B, ARRB2, ARF3, EPS15L1, STAM, HSPA1A, CAPZB |
| hsa00480 | Glutathione metabolism | 3 | 0.133177 | GSTM4, G6PD, MGST1 |
| hsa04141 | Protein processing in endoplasmic reticulum | 5 | 0.160565 | UBQLN4, HSPA1A, DNAJB1, CAPN2, PPP1R15A |
| hsa04721 | Synaptic vesicle cycle | 3 | 0.1859 | STX3, STXBP1, ATP6V0D1 |
| hsa04142 | Lysosome | 4 | 0.192439 | CD68, IDS, ATP6V0D1, GGA3 |
Table 3 Top 5 KEGG pathways of co-upregulated DEGs
| Pathway ID | Name | Count | P value | Gene |
|---|---|---|---|---|
| hsa04144 | Endocytosis | 10 | 0.002997 | GIT1, RAB7A, RAB31, RAB5B, ARRB2, ARF3, EPS15L1, STAM, HSPA1A, CAPZB |
| hsa00480 | Glutathione metabolism | 3 | 0.133177 | GSTM4, G6PD, MGST1 |
| hsa04141 | Protein processing in endoplasmic reticulum | 5 | 0.160565 | UBQLN4, HSPA1A, DNAJB1, CAPN2, PPP1R15A |
| hsa04721 | Synaptic vesicle cycle | 3 | 0.1859 | STX3, STXBP1, ATP6V0D1 |
| hsa04142 | Lysosome | 4 | 0.192439 | CD68, IDS, ATP6V0D1, GGA3 |
Table 4 Top 5 KEGG pathways of co-downregulated DEGs
| Pathway ID | Name | Count | P value | Gene |
|---|---|---|---|---|
| hsa03010 | Ribosome | 11 | 1.16×10-8 | RPSA, RPL17, RPS27, RPS17, RPL9, RPL3, RPL24, RPS20, RPS21, RPS27A, RPS8 |
| hsa01230 | Biosynthesis of amino acids | 4 | 0.011393 | PYCR1, ALDH18A1, ASS1, ALDOC |
| hsa00330 | Arginine and proline metabolism | 3 | 0.042035 | PYCR1, ALDH18A1, AGMAT |
| hsa05322 | Systemic lupus erythematosus | 4 | 0.056687 | HIST1H2BM, C5, HIST1H3B, HIST1H4C |
| hsa04610 | Complement and coagulation cascades | 3 | 0.074505 | FGG, FGA, C5 |
Table 4 Top 5 KEGG pathways of co-downregulated DEGs
| Pathway ID | Name | Count | P value | Gene |
|---|---|---|---|---|
| hsa03010 | Ribosome | 11 | 1.16×10-8 | RPSA, RPL17, RPS27, RPS17, RPL9, RPL3, RPL24, RPS20, RPS21, RPS27A, RPS8 |
| hsa01230 | Biosynthesis of amino acids | 4 | 0.011393 | PYCR1, ALDH18A1, ASS1, ALDOC |
| hsa00330 | Arginine and proline metabolism | 3 | 0.042035 | PYCR1, ALDH18A1, AGMAT |
| hsa05322 | Systemic lupus erythematosus | 4 | 0.056687 | HIST1H2BM, C5, HIST1H3B, HIST1H4C |
| hsa04610 | Complement and coagulation cascades | 3 | 0.074505 | FGG, FGA, C5 |
Figure 2 PPI network of some important co-DEGs Genes with pink and blue background were upregulated and downregulated genes, respectively. PPI: protein-protein interaction; DEGs: differentially expressed genes.
Figure 2 PPI network of some important co-DEGs Genes with pink and blue background were upregulated and downregulated genes, respectively. PPI: protein-protein interaction; DEGs: differentially expressed genes.
Table 5 mRNA expression of some important co-DEGs in HepG2 and Huh7 cells (relative expression compared to control group, $\bar{x} \pm s$)
| Gene | HepG2 | Huh7 | ||||
|---|---|---|---|---|---|---|
| Control group (n = 3) | FAQSE group (n = 3) | Control group (n = 3) | FAQSE group (n = 3) | |||
| RPS27A | 1.00±0.12 | 0.64±0.03a | 1.00±0.12 | 0.81±0.18 | ||
| TF | 1.00±0.17 | 0.21±0.02a | 1.00±0.10 | 0.38±0.18a | ||
| RPS20 | 1.00±0.36 | 0.73±0.10 | 1.00±0.00 | 0.96±0.16 | ||
| RPL9 | 1.00±0.25 | 0.75±0.14 | 1.00±0.13 | 0.93±0.10 | ||
| PPP2R2A | 1.00±0.18 | 0.97±0.06 | 1.00±0.26 | 0.76±0.17 | ||
| TTR | 1.00±0.28 | 0.45±0.04 | 1.00±0.69 | 0.27±0.03 | ||
| TXNRD1 | 1.00±0.14 | 1.56±0.24a | 1.00±0.15 | 2.04±0.53a | ||
| RPL3 | 1.00±0.33 | 0.58±0.11a | 1.00±0.00 | 1.05±0.30 | ||
| RPN1 | 1.00±0.15 | 0.69±0.12 | 1.00±0.07 | 1.29±0.26 | ||
| RPL24 | 1.00±0.42 | 0.68±0.05 | 1.00±0.07 | 1.46±0.46 | ||
| AFP | 1.00±0.26 | 0.32±0.03a | 1.00±0.07 | 0.22±0.04a | ||
Table 5 mRNA expression of some important co-DEGs in HepG2 and Huh7 cells (relative expression compared to control group, $\bar{x} \pm s$)
| Gene | HepG2 | Huh7 | ||||
|---|---|---|---|---|---|---|
| Control group (n = 3) | FAQSE group (n = 3) | Control group (n = 3) | FAQSE group (n = 3) | |||
| RPS27A | 1.00±0.12 | 0.64±0.03a | 1.00±0.12 | 0.81±0.18 | ||
| TF | 1.00±0.17 | 0.21±0.02a | 1.00±0.10 | 0.38±0.18a | ||
| RPS20 | 1.00±0.36 | 0.73±0.10 | 1.00±0.00 | 0.96±0.16 | ||
| RPL9 | 1.00±0.25 | 0.75±0.14 | 1.00±0.13 | 0.93±0.10 | ||
| PPP2R2A | 1.00±0.18 | 0.97±0.06 | 1.00±0.26 | 0.76±0.17 | ||
| TTR | 1.00±0.28 | 0.45±0.04 | 1.00±0.69 | 0.27±0.03 | ||
| TXNRD1 | 1.00±0.14 | 1.56±0.24a | 1.00±0.15 | 2.04±0.53a | ||
| RPL3 | 1.00±0.33 | 0.58±0.11a | 1.00±0.00 | 1.05±0.30 | ||
| RPN1 | 1.00±0.15 | 0.69±0.12 | 1.00±0.07 | 1.29±0.26 | ||
| RPL24 | 1.00±0.42 | 0.68±0.05 | 1.00±0.07 | 1.46±0.46 | ||
| AFP | 1.00±0.26 | 0.32±0.03a | 1.00±0.07 | 0.22±0.04a | ||
Figure 3 Protein expression of some important co-DEGs in HepG2 and Huh7 cells Control group: treated only with normal medium; FAQSE group: treated with FAQSE 0.625 mg/mL for 48 h; DEGs: differentially expressed genes; FAQSE: Yuzhizi (Fructus Akebiae Quinatae) seed extract; TXNRD1: thioredoxin reductase 1; TF: transferrin; TTR: transthyretin; AFP: alpha fetoprotein; GAPDH: glyceraldehyde-3-phosphate dehydrogenase.
Figure 3 Protein expression of some important co-DEGs in HepG2 and Huh7 cells Control group: treated only with normal medium; FAQSE group: treated with FAQSE 0.625 mg/mL for 48 h; DEGs: differentially expressed genes; FAQSE: Yuzhizi (Fructus Akebiae Quinatae) seed extract; TXNRD1: thioredoxin reductase 1; TF: transferrin; TTR: transthyretin; AFP: alpha fetoprotein; GAPDH: glyceraldehyde-3-phosphate dehydrogenase.
Table 6 Relative protein expression of some important co-DEGs in HepG2 and Huh7 cells (protein/GAPDH, $\bar{x} \pm s$)
| Protein | HepG2 | Huh7 | |||
|---|---|---|---|---|---|
| Control group (n = 3) | FAQSE group (n = 3) | Control group (n = 3) | FAQSE group (n = 3) | ||
| TXNRD1 | 1.10±0.75 | 1.37±0.52 | 0.91±0.32 | 1.14±0.16 | |
| TTR | 1.08±0.08 | 0.68±0.21a | 0.65±0.16 | 0.76±0.17 | |
| TF | 1.17±0.87 | 0.70±0.15 | 1.11±0.42 | 0.59±0.32 | |
| AFP | 1.12±0.37 | 0.93±0.16 | 1.21±0.48 | 0.53±0.26 | |
Table 6 Relative protein expression of some important co-DEGs in HepG2 and Huh7 cells (protein/GAPDH, $\bar{x} \pm s$)
| Protein | HepG2 | Huh7 | |||
|---|---|---|---|---|---|
| Control group (n = 3) | FAQSE group (n = 3) | Control group (n = 3) | FAQSE group (n = 3) | ||
| TXNRD1 | 1.10±0.75 | 1.37±0.52 | 0.91±0.32 | 1.14±0.16 | |
| TTR | 1.08±0.08 | 0.68±0.21a | 0.65±0.16 | 0.76±0.17 | |
| TF | 1.17±0.87 | 0.70±0.15 | 1.11±0.42 | 0.59±0.32 | |
| AFP | 1.12±0.37 | 0.93±0.16 | 1.21±0.48 | 0.53±0.26 | |
Table 7 FAQSE reduced the AFP release of HepG2 and Huh7 cells
| Group | n | HepG2 | Huh7 |
|---|---|---|---|
| Control | 3 | 284±7 | 95±3 |
| FAQSE | 3 | 242±17a | 64±5a |
Table 7 FAQSE reduced the AFP release of HepG2 and Huh7 cells
| Group | n | HepG2 | Huh7 |
|---|---|---|---|
| Control | 3 | 284±7 | 95±3 |
| FAQSE | 3 | 242±17a | 64±5a |
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