SYNE1 Exonic Variant rs9479297 Contributes to Concurrent Hepatocellular and Transitional Cell Carcinoma Double Primary Cancer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients and Samples
2.2. Targeted Exome Sequencing (TES)
2.3. SYNE1-rs9479297 Genotyping
2.4. SYNE1-rs9479297 Genotyping
2.5. Cell Culture
2.6. Lentivirus-Mediated Knockdown of SYNE1
2.7. Cell Proliferation Assay
2.8. Cell Migration Assay
2.9. RNA Isolation and Quantitative RT-PCR
2.10. Statistical Analysis
3. Results
3.1. Identifying a Panel of Potentially Pathogenic Exonic Variants in Patients with HCC/TCC DPC
3.2. SYNE1-rs9479297 as a Potentially Pathogenic Allele for Occurrence of HCC/TCC DPC in Taiwan
3.3. SYNE1-rs9479297-TT Genotype Associated with Occurrence of HCC/TCC DPC in Taiwan
3.4. SYNE1 Expression is Downregulated in HCC and TCC and Associated with Clinical Outcomes in HCC Patients
3.5. SYNE1-rs9479297 Genotypes Predict Postoperative Prognosis in Patients with HCC
3.6. SYNE1 Silencing Promotes Cell Proliferation and Migration in HCC and TCC 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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Cohort | Cohort-1 | Cohort-1 | Cohort-2 | Cohort-3 | Cohort-3 | Cohort-3 |
---|---|---|---|---|---|---|
Case number | n = 15 | n = 101 | n = 216 | n = 44 | n = 265 | n = 153 |
Disease | DPC | DPC | Healthy | TCC | HCC | Non-HCC Non-TCC |
Experiment or assay | TES | Rs9479297 genotype comparison | Rs9479297 genotype comparison | Rs9479297 genotype comparison | 265 for Rs9479297 genotype comparison; 156 paired noncancerous and cancerous tissues for RT-qPCR; 20 paired noncancerous and cancerous tissues for IHC | Rs9479297 genotype comparison |
Baseline characteristics | ||||||
Gender, male, n (%) | 11 (73.3%) | 65 (64.4%) | 108 (50.0%) | 34 (77.3%) | 211 (79.6%) | 91 (59.5%) |
Age of sampling ± SD | 59.3 ± 11.9 | 65.7 ± 9.3 | 70.6 ± 9.5 | 59.0 ± 8.9 | 54.8 ± 14.3 | 71.9 ± 6.0 |
HCC Ages (years) ± SD | 59.3 ± 11.9 | 65.7 ± 9.3 | NA | NA | 54.8 ± 14.3 | NA |
TCC Ages (years) ± SD | 59.5 ± 14.0 | 65.2 ± 9.6 | NA | 59.0 ± 8.9 | NA | NA |
Sequential order score ± SD a | 2.1 ± 0.8 | 1.9 ± 0.8 | NA | NA | NA | NA |
Body weight ± SD | 65.0 ± 15.5 | 62.5 ± 11.7 | NA | NA | NA | NA |
Body height ± SD | 164.7 ± 9.1 | 161.2 ± 7.5 | NA | NA | NA | NA |
Heavy smoker, n (%) | 7 (46.7%) | 41 (40.6%) | NA | NA | NA | NA |
BCLC stage for HCC, n (%) Stage 0 Stage A Stage B Stage C Stage D | 4 (26.7%) 7 (46.7%) 4 (26.7%) 0 (0%) 0 (0%) | 15 (14.9%) 23 (22.8%) 20 (19.8%) 42 (41.5%) 1 (1.0%) | NA NA NA NA NA | NA NA NA NA NA | 0 (0.0%) 8 (3.0%) 88 (33.2%) 144 (54.3%) 25 (9.4%) | NA NA NA NA NA |
AJCC7 stage for TCC, n (%) Stage 0 Stage I Stage II Stage III Stage IV | 0 (0%) 10 (66.7%) 2 (13.3%) 3 (20.0%) 0 (0%) | 23 (22.8%) 49 (48.5%) 15 (14.9%) 12 (11.9%) 2 (2.0%) | NA NA NA NA NA | 5 (11.4%) 12 (27.3%) 6 (13.6%) 10 (22.7%) 11 (25.0%) | NA NA NA NA NA | NA NA NA NA NA |
HBsAg positive, n (%) | 8 (53.3%) | 30 (29.7%) | NA | NA | 210 (79.2%) | 124 (81.0%) |
Anti-HCV positive, n (%) | 5 (33.3%) | 47 (46.5%) | NA | NA | 66 (24.9%) | 54 (35.3%) |
Biochemistry and hemogram | ||||||
Total bilirubin (mg/dL) ± SD | 0.7 ± 0.3 | 1.0 ± 0.9 | NA | NA | 1.3 ± 1.7 | NA |
AST(U/L) ± SD | 44.3 ± 25.5 | 143.2 ± 55.3 | NA | NA | 76.5 ± 103.3 | NA |
ALT(U/L) ± SD | 37.2 ± 19.0 | 108.3 ± 51.2 | NA | NA | 75.6 ± 97.5 | NA |
Albumin (g/dL) ± SD | 4.0 ± 0.6 | 3.7 ± 0.6 | NA | NA | 3.9 ± 0.6 | NA |
Platelet count (×103/mL) ± SD | 153.0 ± 42.4 | 163 ± 72.0 | NA | NA | NA | NA |
AFP (ng/mL), median (range) | 5.7 (2.4–87.2) | 8.1 (2.1–20844.1) | NA | NA | 33.0 (1.0–443209.0) | NA |
Symbol | SNP ID | Chr | Position | Ref | Var | NM_ID | cDNA Change | Codon Change | EXON | Protein Change | CADD Score |
---|---|---|---|---|---|---|---|---|---|---|---|
DCC | rs9951523 | 18 | 49867224 | T | C | NM_005215 | c.67T > C | Ttc/Ctc | 1/29 | p.F23L | 22.3 |
EML4 | rs6736913 | 2 | 42510018 | A | G | NM_019063 | c.847A > G | Aaa/Gaa | 8/23 | p.K283E | 22.5 |
ERCC5 | rs9514066 | 13 | 103527849 | G | C | NM_000123 | c.3157G > C | Gga/Cga | 15/15 | p.G1053R | 21.5 |
FN1 | rs386524617 | 2 | 216235089 | C | T | NM_002026 | c.6415G > A | Gtc/Atc | 41/46 | p.V2139I | 20.3 |
ITGB2 | rs235330 | 21 | 46314907 | T | A | NM_000211 | c.1062A > T | caA/caT | 10/17 | p.Q354H | 21.5 |
PKHD1 | rs2435322 | 6 | 51875250 | A | C | NM_138694 | c.5608T > G | Ttg/Gtg | 35/67 | p.L1870V | 20.3 |
ITGA9 | rs267561 | 3 | 37574951 | G | A | NM_002207 | c.1520G > A | gGa/gAa | 14/28 | p.G507E | 24.4 |
FN1 | rs1250259 | 2 | 216300482 | T | A | NM_002026 | c.44A > T | cAg/cTg | 1/46 | p.Q15L | 22 |
DPYD | rs1801265 | 1 | 98348885 | G | A | NM_000110 | c.85C > T | Cgt/Tgt | 2/23 | p.R29C | 23.2 |
PLCG1 | rs753381 | 20 | 39797465 | T | C | NM_002660 | c.2438T > C | aTc/aCc | 22/33 | p.I813T | 22.9 |
SYNE1 | rs214976 | 6 | 152772264 | A | G | NM_033071 | c.3125T > C | gTa/gCa | 26/146 | p.V1042A | 20.1 |
FLT3 | rs1933437 | 13 | 28624294 | G | A | NM_004119 | c.680C > T | aCg/aTg | 6/24 | p.T227M | 21.4 |
SYNE1 | rs2306916 | 6 | 152647681 | A | T | NM_033071 | c.14830T > A | Ttg/Atg | 78/146 | p.L4944M | 21 |
PBX1 | rs2275558 | 1 | 164529120 | G | A | NM_001204961 | c.61G > A | Ggc/Agc | 1/9 | p.G21S | 20.9 |
CYP2D6 | rs1065852 | 22 | 42526694 | G | A | NM_001025161 | c.100C > T | Cca/Tca | 1/8 | p.P34S | 23.7 |
FLT4 | rs448012 | 5 | 180046344 | G | C | NM_002020 | c.2670C > G | caC/caG | 19/30 | p.H890Q | 22.9 |
SYNE1 | rs9479297 | 6 | 152658142 | T | C | NM_033071 | c.12149A > G | aAg/aGg | 75/146 | p.K4050R | 20.4 |
PTCH1 | rs357564 | 9 | 98209594 | G | A | NM_000264 | c.3944C > T | cCc/cTc | 23/24 | p.P1315L | 24.9 |
ERBB2 | rs1058808 | 17 | 37884037 | C | G | NM_004448 | c.3508C > G | Ccc/Gcc | 27/27 | p.P1170A | 23.5 |
EPHA3 | rs35124509 | 3 | 89521693 | T | C | NM_005233 | c.2770T > C | Tgg/Cgg | 16/17 | p.W924R | 22.3 |
ERCC5 | rs17655 | 13 | 103528002 | G | C | NM_000123 | c.3310G > C | Gat/Cat | 15/15 | p.D1104H | 22.9 |
CSF1R | rs10079250 | 5 | 149450132 | T | C | NM_005211 | c.1085A > G | cAc/cGc | 8/22 | p.H362R | 20.4 |
LRP1B | rs12990449 | 2 | 142567910 | T | C | NM_018557 | c.143A > G | cAg/cGg | 2/91 | p.Q48R | 20.4 |
DST | rs11756977 | 6 | 56420538 | C | T | NM_001144770 | c.6872G > A | cGt/cAt | 41/84 | p.R2291H | 22.9 |
NIN | rs2295847 | 14 | 51202311 | G | C | NM_182946 | c.5800C > G | Caa/Gaa | 28/30 | p.Q1934E | 22.5 |
PARP1 | rs1136410 | 1 | 226555302 | A | G | NM_001618 | c.2285T > C | gTg/gCg | 17/23 | p.V762A | 28.1 |
PIK3R1 | rs386584794 | 5 | 67588148 | G | A | NM_181523 | c.978G > A | atG/atA | 8/16 | p.M326I | 20.7 |
SETD2 | rs76208147 | 3 | 47162886 | C | T | NM_014159 | c.3240G > A | atG/atA | 3/21 | p.M1080I | 20.7 |
CRTC1 | rs3746266 | 19 | 18876309 | A | G | NM_015321 | c.982A > G | Acc/Gcc | 9/14 | p.T328A | 22.5 |
SYNE1 | rs76160752 | 6 | 152629631 | C | T | NM_033071 | c.17126G > A | cGg/cAg | 90/146 | p.R5709Q | 22.4 |
CASC5 | rs11858113 | 15 | 40914177 | T | C | NM_170589 | c.1793T > C | aTg/aCg | 11/27 | p.M598T | 20.8 |
CDH11 | rs35195 | 16 | 65025718 | G | A | NM_001797 | c.764C > T | aCg/aTg | 6/13 | p.T255M | 25.1 |
CDH11 | rs1130821 | 16 | 65022234 | C | T | NM_001797 | c.825G > A | atG/atA | 7/13 | p.M275I | 24.9 |
DST | rs80260070 | 6 | 56351972 | G | C | NM_001144770 | c.13108C > G | Ctg/Gtg | 68/84 | p.L4370V | 23 |
EPHA3 | rs17801309 | 3 | 89521664 | G | A | NM_005233 | c.2741G > A | cGc/cAc | 16/17 | p.R914H | 22.3 |
EPHA7 | rs2278106 | 6 | 94120219 | G | A | NM_004440 | c.832C > T | Ccc/Tcc | 3/17 | p.P278S | 23.4 |
ERBB2 | rs1136201 | 17 | 37879588 | A | G | NM_004448 | c.1963A > G | Atc/Gtc | 17/27 | p.I655V | 22.3 |
FANCA | rs11646374 | 16 | 89857935 | G | A | NM_000135 | c.1235C > T | gCg/gTg | 14/43 | p.A412V | 21.4 |
HNF1A | rs1169288 | 12 | 121416650 | A | C | NM_000545 | c.79A > C | Atc/Ctc | 1/10 | p.I27L | 23.4 |
IGF2R | rs8191754 | 6 | 160448324 | C | G | NM_000876 | c.754C > G | Ctg/Gtg | 6/48 | p.L252V | 23.4 |
IKBKB | rs2272736 | 8 | 42177163 | G | A | NM_001556 | c.1577G > A | cGg/cAg | 15/22 | p.R526Q | 24.4 |
MTRR | rs2287780 | 5 | 7889304 | C | T | NM_002454 | c.1324C > T | Cgc/Tgc | 9/15 | p.R442C | 23.1 |
ROS1 | rs1998206 | 6 | 117725448 | T | G | NM_002944 | c.433A > C | Act/Cct | 5/43 | p.T145P | 23.7 |
TRIP11 | rs80200454 | 14 | 92460227 | C | T | NM_004239 | c.5086G > A | Gaa/Aaa | 15/21 | p.E1696K | 23.5 |
Symbol | SNP ID | Genotype | Three-Group Comparison | Two-Group Comparison | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
HCC + TCC | Normal Population | p | HCC + TCC | Normal Population | p | ||||||||||
Ref | Var | Var Homo | Hetero | Ref Homo | Var Homo | Hetero | Ref Homo | Var Homo | Non-Var Homo | Var Homo | Non-Var Homo | ||||
SYNE1 | rs9479297 | T | C | 5 | 8 | 2 | 4 | 62 | 150 | 0.002 | 5 | 10 | 4 | 212 | 0.009 |
SYNE1 | rs76160752 | A | G | 1 | 0 | 14 | 0 | 15 | 201 | <0.001 | 1 | 14 | 0 | 216 | 0.077 |
EPHA | rs17801309 | G | C | 1 | 3 | 11 | 0 | 28 | 188 | <0.001 | 1 | 14 | 0 | 216 | 0.077 |
TRIP11 | rs80200454 | C | T | 1 | 0 | 14 | 0 | 19 | 197 | <0.001 | 1 | 14 | 0 | 216 | 0.077 |
ITGA9 | rs267561 | T | A | 14 | 1 | 0 | 151 | 54 | 11 | 0.148 | 14 | 1 | 151 | 65 | 0.100 |
SETD2 | rs76208147 | A | C | 2 | 3 | 10 | 5 | 52 | 159 | 0.055 | 2 | 13 | 5 | 211 | 0.103 |
PBX1 | rs2275558 | G | A | 8 | 5 | 2 | 82 | 101 | 33 | 0.488 | 8 | 7 | 82 | 134 | 0.238 |
CRTC1 | rs3746266 | T | A | 2 | 6 | 7 | 8 | 64 | 144 | 0.113 | 2 | 13 | 8 | 208 | 0.264 |
SYNE1 | rs214976 | G | A | 11 | 4 | 0 | 127 | 75 | 14 | 0.42 | 11 | 4 | 127 | 89 | 0.267 |
EPHA3 | rs35124509 | T | C | 2 | 6 | 7 | 8 | 72 | 136 | 0.15 | 2 | 13 | 8 | 208 | 0.264 |
CYP2D6 | rs1065852 | A | G | 7 | 3 | 5 | 71 | 99 | 46 | 0.147 | 7 | 8 | 71 | 145 | 0.275 |
FLT3 | rs1933437 | G | A | 10 | 4 | 1 | 116 | 84 | 16 | 0.609 | 10 | 5 | 116 | 100 | 0.330 |
FLT4 | rs448012 | A | T | 6 | 2 | 7 | 59 | 93 | 64 | 0.077 | 6 | 9 | 59 | 157 | 0.447 |
ERCC5 | rs17655 | G | A | 2 | 6 | 7 | 55 | 94 | 67 | 0.377 | 2 | 13 | 55 | 161 | 0.457 |
SYNE1 | rs2306916 | G | A | 9 | 5 | 1 | 148 | 63 | 5 | 0.534 | 9 | 6 | 148 | 68 | 0.467 |
NIN | rs2295847 | G | C | 2 | 7 | 6 | 53 | 117 | 46 | 0.216 | 2 | 13 | 53 | 163 | 0.502 |
CDH11 | rs1130821 | T | C | 1 | 8 | 6 | 35 | 108 | 73 | 0.604 | 1 | 14 | 35 | 181 | 0.537 |
MTRR | rs2287780 | G | A | 1 | 4 | 10 | 3 | 65 | 148 | 0.314 | 1 | 14 | 3 | 213 | 0.623 |
FN1 | rs1250259 | C | G | 14 | 1 | 0 | 184 | 30 | 2 | 0.673 | 14 | 1 | 184 | 32 | 0.624 |
DPYD | rs1801265 | T | C | 13 | 2 | 0 | 184 | 31 | 1 | 0.959 | 13 | 2 | 184 | 32 | 0.624 |
LRP1B | rs12990449 | G | C | 2 | 5 | 8 | 48 | 93 | 75 | 0.337 | 2 | 13 | 48 | 168 | 0.628 |
CASC5 | rs11858113 | T | C | 1 | 5 | 9 | 12 | 61 | 143 | 0.887 | 1 | 14 | 12 | 204 | 0.690 |
ERBB2 | rs1136201 | T | C | 1 | 3 | 11 | 4 | 48 | 164 | 0.462 | 1 | 14 | 4 | 212 | 0.748 |
IKBKB | rs2272736 | C | T | 1 | 5 | 9 | 4 | 40 | 172 | 0.152 | 1 | 14 | 4 | 212 | 0.748 |
IGF2R | rs8191754 | G | C | 1 | 4 | 10 | 10 | 70 | 136 | 0.862 | 1 | 14 | 10 | 206 | 0.788 |
FANCA | rs11646374 | A | G | 1 | 6 | 8 | 10 | 75 | 131 | 0.836 | 1 | 14 | 10 | 206 | 0.788 |
PLCG1 | rs753381 | G | A | 11 | 4 | 0 | 144 | 65 | 7 | 0.728 | 11 | 4 | 144 | 72 | 0.805 |
CSF1R | rs10079250 | C | T | 2 | 5 | 8 | 42 | 107 | 67 | 0.203 | 2 | 13 | 42 | 174 | 0.808 |
PARP1 | rs1136410 | A | G | 2 | 8 | 5 | 42 | 98 | 76 | 0.786 | 2 | 13 | 42 | 174 | 0.808 |
CDH11 | rs35195 | C | T | 1 | 3 | 11 | 5 | 76 | 135 | 0.328 | 1 | 14 | 5 | 211 | 0.853 |
ERBB2 | rs1058808 | T | C | 3 | 5 | 7 | 32 | 104 | 80 | 0.536 | 3 | 12 | 32 | 184 | 0.866 |
HNF1A | rs1169288 | G | A | 1 | 7 | 7 | 25 | 109 | 82 | 0.735 | 1 | 14 | 25 | 191 | 0.874 |
DST | rs11756977 | C | T | 2 | 7 | 6 | 34 | 84 | 98 | 0.836 | 2 | 13 | 34 | 182 | 0.905 |
DST | rs80260070 | G | C | 1 | 4 | 10 | 6 | 62 | 148 | 0.695 | 1 | 14 | 6 | 210 | 0.944 |
EPHA7 | rs2278106 | G | A | 1 | 4 | 10 | 7 | 58 | 151 | 0.78 | 1 | 14 | 7 | 209 | 0.977 |
ROS1 | rs1998206 | G | A | 1 | 3 | 11 | 7 | 65 | 144 | 0.59 | 1 | 14 | 7 | 209 | 0.977 |
PTCH1 | rs357564 | A | G | 4 | 8 | 3 | 66 | 104 | 46 | 0.924 | 4 | 11 | 66 | 150 | 0.979 |
DCC | rs9951523 | G | A | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
EML4 | rs6736913 | A | C | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
ERCC5 | rs9514066 | C | G | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
FN1 | rs386524617 | G | A | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
ITGB2 | rs235330 | C | T | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
PKHD1 | rs2435322 | T | G | 15 | 0 | 0 | 216 | 0 | 0 | NA | 15 | 0 | 216 | 0 | NA |
PIK3R1 | rs386584794 | C | T | 2 | 2 | 11 | NA | NA | NA | NA | 2 | 13 | NA | NA | NA |
Population in Taiwan | SYNE1-rs9479297 Genotypes | p | SYNE1-rs9479297 Genotypes | p | |||
---|---|---|---|---|---|---|---|
CC | CT | TT | TT | Non-TT | |||
HCC + TCC patients (n = 101) | 72 | 17 | 12 | 12 | 89 | ||
TCC patients (n = 44) | 34 | 10 | 0 | 0.051 | 0 | 44 | 0.039 |
HCC patients (n = 265) | 187 | 67 | 11 | 0.010 | 11 | 254 | 0.006 |
Non-TCC and non-HCC patients (n = 153) | 113 | 38 | 2 | 0.001 | 2 | 146 | <0.001 |
Normal population (n = 216) | 150 | 62 | 4 | <0.001 | 4 | 212 | <0.001 |
Characteristics | rs9479297-TT | rs9479297-Non-TT | p |
---|---|---|---|
Gender, male, n (%) | 8 (58.3%) | 57 (70.4%) | 0.5005 |
HCC diagnosed Ages (years) ± SD | 61.9 ± 8.5 | 67.5 ± 8.1 | 0.0358 |
TCC diagnosed Ages (years) ± SD | 60.3 ± 7.1 | 67.2 ± 8.1 | 0.0067 |
Sequential order score ± SD a | 1.8 ± 0.8 | 1.9 ± 0.8 | 0.5352 |
Body weight ± SD | 61.1 ± 11.4 | 63.3 ± 11.3 | 0.7355 |
Body height ± SD | 161.1 ± 7.7 | 161.2 ± 7.1 | 0.9756 |
Heavy smoker, n (%) | 4 (33.3%) | 37 (41.6%) | 0.8161 |
BCLC stage for HCC, n (%) Stage 0 Stage A Stage B Stage C Stage D | 0 (0.0%) 5 (41.7%) 3 (25.0%) 4 (33.3%) 0 (0.0%) | %15 (16.9%) 18 (20.2%) 17 (19.1%) 38 (42.7%) 1 (1.1%) | 0.2675 0.1950 0.9239 0.7598 0.7121 |
AJCC7 stage for TCC, n (%) Stage 0 Stage I Stage II Stage III Stage IV | 3 (25.0%) 6 (50.0%) 2 (16.7%) 1 (8.3%) 0 (0.0%) | 20 (22.5%) 43 (48.3%) 13 (14.6%) 11 (12.4%) 2 (2.2%) | 0.8446 0.9127 0.8506 0.6857 0.5999 |
HBsAg positive, n (%) | 2 (16.7%) | 28 (31.4%) | 0.4738 |
Anti-HCV positive, n (%) | 7 (58.3%) | 40 (44.9%) | 0.5723 |
Biochemistry and hemogram | |||
Total bilirubin (mg/dL) ± SD | 1.3 ± 1.8 | 0.9 ± 1.3 | 0.5570 |
AST(U/L) ± SD | 142.3 ± 44.5 | 144.5 ± 55.7 | 0.9591 |
ALT(U/L) ± SD | 141.4 ± 63.6 | 89.5 ± 41.6 | 0.3968 |
Albumin (g/dL) ± SD | 3.6 ± 0.4 | 3.8 ± 0.7 | 0.2487 |
Platelet count (×103/mL) ± SD | 179.2 ± 84.3 | 157.2 ± 70.0 | 0.2459 |
AFP (ng/mL), median (range) | 7.9 (2.7–488.1) | 10.7 (2.1–20844.1) | 0.6931 |
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Chu, Y.-D.; Kee, K.-M.; Lin, W.-R.; Lai, M.-W.; Lu, S.-N.; Chung, W.-H.; Pang, S.-T.; Yeh, C.-T. SYNE1 Exonic Variant rs9479297 Contributes to Concurrent Hepatocellular and Transitional Cell Carcinoma Double Primary Cancer. Biomedicines 2021, 9, 1819. https://doi.org/10.3390/biomedicines9121819
Chu Y-D, Kee K-M, Lin W-R, Lai M-W, Lu S-N, Chung W-H, Pang S-T, Yeh C-T. SYNE1 Exonic Variant rs9479297 Contributes to Concurrent Hepatocellular and Transitional Cell Carcinoma Double Primary Cancer. Biomedicines. 2021; 9(12):1819. https://doi.org/10.3390/biomedicines9121819
Chicago/Turabian StyleChu, Yu-De, Kwong-Ming Kee, Wey-Ran Lin, Ming-Wei Lai, Sheng-Nan Lu, Wen-Hung Chung, See-Tong Pang, and Chau-Ting Yeh. 2021. "SYNE1 Exonic Variant rs9479297 Contributes to Concurrent Hepatocellular and Transitional Cell Carcinoma Double Primary Cancer" Biomedicines 9, no. 12: 1819. https://doi.org/10.3390/biomedicines9121819