The Identification of RNA-Binding Proteins Functionally Associated with Tumor Progression in Gastrointestinal Cancer
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Cell Culture
2.2. siRNA and Transfection
2.3. SRB Assays
2.4. MTT Assays
2.5. Western Blotting
2.6. cDNA Analyses
2.7. Data Corrections
2.8. Statistical Assessments
3. Results
3.1. Growth Change by the Knockdown of RBPs in Gastrointestinal Cancer Cells
3.2. The Association between Expressional Changes and Tumor Growth Promotive Functions of RBPs in Gastrointestinal Cancer Cells
3.3. Identification of Tumor Growth-Associated RBPs without Any Significant Expressional Changes in Gastrointestinal Cancer Cells
3.4. Interactome Analysis of RBPs in Cancer Cells
3.5. Identification of Organ-Specific RBPs Exhibiting the Tumor-Promotive Function
3.6. Identification of Tumor Growth Associated RBPs without Genetic Mutations in Gastrointestinal Cancer Cells
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Name | Characteristics | Organs | Morphology | Supplier |
---|---|---|---|---|
HCT116 | Colorectal cancer cells | Colon | Epithelial | American Type Culture Collection (ATCC) |
SW480 | Colorectal cancer cells | Colon | Epithelial | American Type Culture Collection (ATCC) |
HCEC-1CT | Immortalized colorectal epithelial cells | Colon | Epithelial | Evercyte |
SUIT2 | Pancreatic cancer cells | Pancreas | Epithelial | Health Science Research Resources Bank |
PANC-1 | Pancreatic cancer cells | Pancreas | Epithelial | American Type Culture Collection (ATCC) |
HPPEC | Primary pancreatic epithelial cells | Pancreas | Epithelial | Cell Biologics, Inc. |
OE33 | Esophageal cancer cells | Esophagus | Epithelial | European Collection of Authenticated Cell Cultures (ECACC) |
KYSE70 | Esophageal cancer cells | Esophagus | Epithelial | European Collection of Authenticated Cell Cultures (ECACC) |
Het-1A | Immortalized esophageal epithelial cells | Esophagus | Epithelial | American Type Culture Collection (ATCC) |
Gene Symbol | siRNA ID | Growth Inhibition Effect | Array ID | Fold Change | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
HCT 116 | SW 480 | SUIT -2 | PANC -1 | OE 33 | KYSE 70 | HCT 116 | SW 480 | SUIT -2 | PANC −1 | OE 33 | KYSE 70 | |||
DHX8 | s4018 | 94.6% | 10.7% | 64.5% | 39.5% | 88.8% | 20.8% | TC1700012263.hg.1 | 1.28 | 1.10 | −1.02 | −2.79 | −1.43 | −2.39 |
s4017 | 91.5% | 41.8% | 58.4% | 61.3% | 109.1% | 47.3% | ||||||||
s4016 | 80.8% | 10.3% | 60.7% | 53.5% | 75.8% | 36.9% | ||||||||
EIF2S1 | s4557 | 92.0% | 10.5% | 79.1% | 24.9% | 63.0% | 42.5% | TC1400007494.hg.1 | 1.29 | 1.39 | −1.45 | 1.01 | −1.04 | 1.24 |
s4556 | 90.1% | 4.2% | 80.1% | 30.4% | 65.1% | 42.5% | ||||||||
s4555 | 87.0% | 31.0% | 92.7% | 44.1% | 66.7% | 48.9% | ||||||||
EIF3G | s225017 | 89.6% | 26.7% | 88.0% | 72.9% | 84.2% | 67.6% | TC1900009608.hg.1 | 1.34 | 1.01 | −1.80 | −2.10 | −1.42 | 1.02 |
s16505 | 88.8% | 39.2% | 84.5% | 46.7% | 77.1% | 70.8% | ||||||||
s16504 | 83.2% | 47.8% | 90.7% | 67.3% | 85.1% | 79.0% | ||||||||
RBM22 | s31272 | 95.3% | 44.3% | 54.7% | 49.5% | 61.3% | 53.3% | TC0500012485.hg.1 | 1.71 | 1.78 | 1.05 | 1.77 | −1.82 | −1.66 |
s31273 | 54.6% | 15.5% | 53.9% | 43.9% | 55.4% | 28.3% | ||||||||
s31274 | 50.8% | 1.0% | 41.0% | 14.7% | 37.8% | 29.6% | ||||||||
RBM8A | s532199 | 121.7% | 116.8% | 112.3% | 75.7% | 106.9% | 49.2% | TC0100018477.hg.1 | 1.48 | 1.22 | 1.55 | 1.81 | −1.08 | −1.11 |
s532200 | 113.3% | 53.9% | 108.5% | 74.2% | 115.4% | 36.7% | ||||||||
s19292 | 112.1% | 73.5% | 97.3% | 62.7% | 112.4% | 64.9% | ||||||||
RPS3 | s12255 | 96.2% | 48.9% | 88.6% | 60.3% | 79.8% | 71.9% | TC1100008462.hg.1 | 1.26 | 1.43 | 1.15 | −1.21 | 1.08 | −1.34 |
s12257 | 91.3% | 37.6% | 83.5% | 80.1% | 78.2% | 85.0% | ||||||||
s12256 | 90.5% | 66.0% | 91.8% | 52.6% | 74.5% | 85.3% | ||||||||
SF3A1 | s20116 | 105.1% | 38.7% | 105.7% | 57.3% | 89.0% | 60.7% | TC2200008434.hg.1 | 1.62 | 1.26 | 1.99 | 1.88 | −1.33 | −1.00 |
s20118 | 96.7% | 11.5% | 79.0% | 59.2% | 63.7% | 54.1% | ||||||||
s20117 | 88.1% | 49.7% | 85.1% | 43.5% | 79.3% | 51.1% | ||||||||
SNRPE | s13238 | 102.4% | 56.8% | 89.4% | 77.9% | 75.8% | 74.4% | TC0100011276.hg.1 | 1.85 | 2.00 | 1.42 | 1.36 | 1.57 | 1.52 |
s13239 | 92.4% | 27.6% | 75.3% | 55.8% | 81.8% | 64.3% | ||||||||
SUPT6H | s13636 | 87.3% | 24.6% | 70.8% | 55.5% | 88.3% | 71.7% | TC1700007381.hg.1 | −1.05 | −1.32 | 1.07 | −1.05 | 1.18 | −2.53 |
s13634 | 84.9% | 64.5% | 64.2% | 48.9% | 76.9% | 54.5% | ||||||||
s13635 | 71.7% | 40.4% | 62.9% | 48.6% | 61.6% | 72.7% | ||||||||
U2AF1 | s14555 | 60.2% | 15.4% | 77.6% | 51.2% | 68.8% | 30.7% | TC2100008286.hg.1 | 1.92 | 2.82 | 1.80 | 1.28 | 1.21 | 3.73 |
s14553 | 57.8% | 38.4% | 92.4% | 30.1% | 85.3% | 20.6% | TC2100007492.hg.1 | 1.85 | 2.68 | 1.73 | 1.67 | 1.34 | 2.85 | |
s14554 | 50.3% | 14.0% | 104.1% | 18.6% | 68.2% | 10.9% | ||||||||
UPF1 | s11926 | 83.0% | 11.9% | 98.0% | 32.4% | 64.6% | 43.3% | TC1900007410.hg.1 | 1.41 | 1.04 | −1.36 | 3.15 | −1.08 | −1.49 |
s11928 | 54.9% | 7.4% | 90.3% | 44.1% | 80.6% | 34.9% | ||||||||
s11927 | 10.6% | −0.2% | −13.6% | 32.3% | 34.2% | 9.8% | ||||||||
YBX1 | s9733 | 99.2% | 14.0% | 78.9% | 28.9% | 100.2% | 10.8% | TC0100008026.hg.1 | 1.25 | 1.42 | 1.12 | 1.03 | −1.29 | 1.11 |
s9731 | 60.8% | 18.9% | 68.5% | 75.6% | 97.5% | 36.2% | TC0100008025.hg.1 | 1.09 | 1.32 | −1.25 | −1.14 | −4.14 | −3.16 | |
s9732 | 41.7% | 15.7% | 41.4% | 19.9% | 37.2% | 14.1% |
Gene Symbol | Growth Inhibition Effect | ||
---|---|---|---|
HCEC-1CT | HPPEC | Het1A | |
DHX8 | 27.0% | 11.3% | −14.9% |
EIF2S1 | 52.9% | 21.8% | 6.4% |
EIF3G | 20.8% | 18.0% | 19.9% |
RBM22 | 11.0% | 29.0% | −2.1% |
RBM8A | 53.4% | 69.3% | −8.5% |
RPS3 | 58.1% | 46.2% | 2.1% |
SF3A1 | 24.9% | −6.7% | −10.6% |
SNRPE | 34.4% | 37.8% | 17.0% |
SUPT6H | 35.5% | 22.8% | 49.0% |
U2AF1 | 8.4% | 0.9% | 39.8% |
UPF1 | 31.9% | 31.9% | 17.0% |
YBX1 | 29.9% | 31.9% | −2.1% |
From | To | Effect | Mechanism |
---|---|---|---|
Bcl-3 | RBM22 | Transcription regulation | Unspecified |
c-Myc | RBM8 (Y14) | Transcription regulation | Unspecified |
N-Myc | RBM8 (Y14) | Transcription regulation | Unspecified |
SOX2 | RBM8 (Y14) | Transcription regulation | Unspecified |
Androgen receptor | RENT1 | Transcription regulation | Unspecified |
KDM2B | RENT1 | Co-regulation of transcription | Unspecified |
Oct-3/4 | RENT1 | Transcription regulation | Unspecified |
TCF8 | RENT1 | Transcription regulation | Unspecified |
Beta-catenin | snRNP-E | Co-regulation of transcription | Unspecified |
c-Myc | snRNP-E | Transcription regulation | Unspecified |
NANOG | snRNP-E | Transcription regulation | Unspecified |
N-Myc | snRNP-E | Transcription regulation | Unspecified |
SOX2 | snRNP-E | Transcription regulation | Activation |
SOX9 | snRNP-E | Transcription regulation | Unspecified |
CDK2 | SUPT6H | Phosphorylation | Unspecified |
c-Myc | SUPT6H | Transcription regulation | Unspecified |
NANOG | SUPT6H | Transcription regulation | Unspecified |
SOX2 | SUPT6H | Transcription regulation | Unspecified |
TCF8 | SUPT6H | Transcription regulation | Unspecified |
c-Myc | U2AF35 | Transcription regulation | Activation |
CTCF | U2AF35 | Transcription regulation | Unspecified |
Esrrb | U2AF35 | Transcription regulation | Unspecified |
N-Myc | U2AF35 | Transcription regulation | Unspecified |
Oct-3/4 | U2AF35 | Transcription regulation | Unspecified |
STAT3 | U2AF35 | Transcription regulation | Unspecified |
c-Myc | YB-1 | Transcription regulation | Activation |
E2F1 | YB-1 | Transcription regulation | Activation |
ERK1/2 | YB-1 | Phosphorylation | Inhibition |
ERK2 (MAPK1) | YB-1 | Phosphorylation | Activation |
HSP60 | YB-1 | Binding | Inhibition |
HSP70 | YB-1 | Binding | Activation |
MYOD | YB-1 | Transcription regulation | Activation |
NANOG | YB-1 | Transcription regulation | Unspecified |
Oct-3/4 | YB-1 | Transcription regulation | Unspecified |
p53 | YB-1 | Binding | Inhibition |
STAT1 | YB-1 | Transcription regulation | Unspecified |
Ubiquitin | YB-1 | Binding | Inhibition |
YB-1 | Androgen receptor | Transcription regulation | Unspecified |
RENT1 | ATF-3 | Binding | Inhibition |
RENT1 | Bcl-3 | Binding | Inhibition |
YB-1 | CDK1 (p34) | Transcription regulation | Unspecified |
SUPT6H | CDK2 | Co-regulation of transcription | Unspecified |
YB-1 | CDK2 | Transcription regulation | Activation |
RBM22 | c-Fos | Co-regulation of transcription | Unspecified |
YB-1 | c-IAP1 | Transcription regulation | Activation |
eIF3 | c-Jun | Binding | Activation |
RENT1 | c-Myb | Binding | Inhibition |
SUPT6H | c-Myc | Co-regulation of transcription | Unspecified |
YB-1 | c-Myc | Binding | Activation |
YB-1 | CTCF | Binding | Activation |
RPS3 | E2F1 | Binding | Activation |
YB-1 | E2F2 | Transcription regulation | Activation |
YB-1 | ERK2 (MAPK1) | Binding | Activation |
YB-1 | ESR | Binding | Inhibition |
SUPT6H | ESR1 (nuclear) | Binding | Activation |
YB-1 | ESR1 (nuclear) | Binding | Inhibition |
RENT1 | Esrrb | Binding | Inhibition |
YB-1 | EZH2 | Transcription regulation | Unspecified |
RENT1 | GCR | Binding | Activation |
YB-1 | GRP78 | Binding | Inhibition |
YB-1 | HDAC11 | Transcription regulation | Unspecified |
snRNP-E | HSPA4 | Co-regulation of transcription | Unspecified |
YB-1 | KDM2B | Transcription regulation | Unspecified |
RENT1 | Keratin 8 | Binding | Inhibition |
YB-1 | KLF4 | Transcription regulation | Activation |
YB-1 | KLF5 | Transcription regulation | Unspecified |
YB-1 | MMP-2 | Transcription regulation | Activation |
YB-1 | MNK1 | Transcription regulation | Activation |
RENT1 | MYOD | Ubiquitination | Inhibition |
SUPT6H | NANOG | Co-regulation of transcription | Activation |
YB-1 | NANOG | Binding | Activation |
RPS3 | NF-kB1 (p50) | Binding | Activation |
YB-1 | N-Myc | Binding | Activation |
YB-1 | Nucleophosmin | Transcription regulation | Unspecified |
SUPT6H | Oct-3/4 | Co-regulation of transcription | Activation |
YB-1 | p300 | Binding | Inhibition |
RPS3 | p53 | Binding | Activation |
YB-1 | p53 | Transcription regulation | Inhibition |
YB-1 | p63 | Transcription regulation | Unspecified |
YB-1 | PDGF-B | Transcription regulation | Unspecified |
SUPT6H | PR (nuclear) | Co-regulation of transcription | Activation |
YB-1 | PTP-1B | Transcription regulation | Activation |
RPS3 | RelA (p65 NF-kB subunit) | Binding | Activation |
RPS3 | Sirtuin1 | Binding | Activation |
YB-1 | SNAIL1 | Binding | Activation |
snRNP-E | snRNP-F | Binding | Activation |
SUPT6H | SOX2 | Co-regulation of transcription | Activation |
YB-1 | SOX2 | Transcription regulation | Inhibition |
RBM8 (Y14) | STAT3 | Binding | Activation |
YB-1 | Tat (HIV-1) | Binding | Activation |
YB-1 | TCF8 | Transcription regulation | Activation |
YB-1 | TGF-beta 1 | Binding | Inhibition |
YB-1 | TGF-beta 2 | Transcription regulation | Unspecified |
Cell Lines | Gene List | |||||
---|---|---|---|---|---|---|
HCT116 | CPEB4 | MKI67IP | RPS3 | SNRPB | YBX1 | |
DHX8 | NOL8 | RRP7A | SNRPB2 | ZC3H12C | ||
EIF2S1 | PABPN1 | SAMD4A | SNRPC | |||
EIF3G | PNO1 | SF3A1 | SNRPE | |||
HNRNPA1L2 | RAVER1 | SF3B14 | SRRM2 | |||
HNRNPAB | RBM22 | SF3B4 | SRSF5 | |||
HNRNPCL1 | RBM8A | SFRS13A | SUPT6H | |||
LSM2 | RNF113A | SFRS3 | TIA1 | |||
LSM5 | RNPS1 | SFRS7 | TLR2 | |||
LSM8 | ROD1 | SLBP | U2AF1 | |||
SW480 | RBM8A | |||||
SF3B14 | ||||||
SNRPB | ||||||
SUIT-2 | CHERP | LARP6 | RBM11 | RPS3 | SNRPE | UPF3B |
CPSF4 | LIN28B | RBM18 | SF3A1 | SNRPG | YBX1 | |
CPSF4L | LSM6 | RBM22 | SF3B14 | SRRM2 | YTHDC1 | |
DAZL | LSM8 | RBM43 | SFRS13A | SUPT6H | ZC3H12D | |
DHX8 | MKI67IP | RBM45 | SFRS3 | TDRD10 | ZC3H15 | |
EIF2S1 | NCL | RBM4B | SFRS6 | TIA1 | ZC3H18 | |
EIF3B | NONO | RBM7 | SNRPC | TUT1 | ZC3HAV1 | |
EIF3G | PABPN1L | RBM8A | SNRPD1 | U2AF1 | ZC3HAV1L | |
HNRNPAB | POLR2G | RBMY1A1 | SNRPD2 | U2SURP | ZFP36L1 | |
HNRNPK | PUF60 | RC3H1 | SNRPD3 | UPF1 | ||
PANC-1 | RBM8A | SF3B14 | SNRPD3 | |||
RPS3 | SNRPD1 | SNRPE | ||||
SF3A1 | SNRPD2 | SNRPG | ||||
OE33 | CARHSP1 | LARP1 | PABPC1L2A | RBM8A | SRBD1 | ZC3H18 |
CHERP | LARP6 | PABPC1L2B | RPS3 | SUPT6H | ZC3H4 | |
CSDC2 | LEMD3 | PABPC5 | RRP7A | U2AF1 | ZC3H7B | |
DAZL | LIN28B | PARP10 | SF1 | U2SURP | ZC3HAV1L | |
DHX8 | LSM2 | PCBP2 | SF3A1 | UPF1 | ZFP36L1 | |
EIF2S1 | LSM3 | PRPF3 | SFSWAP | UPF3B | ZFP36L2 | |
HNRNPA1L2 | MOV10L1 | RBM14 | SNRPD2 | YTHDC1 | ZGPAT | |
HNRNPC | NONO | RBM22 | SNRPD3 | ZC3H11A | ZNF74 | |
HNRNPCL1 | NUPL2 | RBM25 | SNRPE | ZC3H12B | ZRANB2 | |
HNRNPR | PABPC1 | RBM39 | SNRPG | ZC3H12D | ZRSR2 | |
KYSE-70 | EIF3G | PUF60 | SNRPD2 | |||
LARP1 | RPS3 | SNRPE | ||||
NONO | SF3B4 | SRRM1 |
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Konishi, H.; Kashima, S.; Goto, T.; Ando, K.; Sakatani, A.; Tanaka, H.; Ueno, N.; Moriichi, K.; Okumura, T.; Fujiya, M. The Identification of RNA-Binding Proteins Functionally Associated with Tumor Progression in Gastrointestinal Cancer. Cancers 2021, 13, 3165. https://doi.org/10.3390/cancers13133165
Konishi H, Kashima S, Goto T, Ando K, Sakatani A, Tanaka H, Ueno N, Moriichi K, Okumura T, Fujiya M. The Identification of RNA-Binding Proteins Functionally Associated with Tumor Progression in Gastrointestinal Cancer. Cancers. 2021; 13(13):3165. https://doi.org/10.3390/cancers13133165
Chicago/Turabian StyleKonishi, Hiroaki, Shin Kashima, Takuma Goto, Katsuyoshi Ando, Aki Sakatani, Hiroki Tanaka, Nobuhiro Ueno, Kentaro Moriichi, Toshikatsu Okumura, and Mikihiro Fujiya. 2021. "The Identification of RNA-Binding Proteins Functionally Associated with Tumor Progression in Gastrointestinal Cancer" Cancers 13, no. 13: 3165. https://doi.org/10.3390/cancers13133165