Frequency of EBV LMP-1 Promoter and Coding Variations in Burkitt Lymphoma Samples in Africa and South America and Peripheral Blood in Uganda
Abstract
:1. Introduction
2. Results
2.1. Comparison of EBV LMP-1 Genetic Diversity in 114 Published Genomes Classified by Seven Techniques
2.2. Discovery of Novel Pattern A-Like Variations in Samples Studied by PCR-Sanger Sequencing
2.3. Frequency of Pattern A in 64 BL Tumors from Ghana, Argentina, and Brazil
2.4. Frequency of Pattern A in Peripheral Blood of 113 Children with- and 115 Children without-BL in Uganda
3. Discussion
3.1. LMP-1 Classification Using the Lei et al. Technique Applicable to HTS Data and Has Parsimony of Variants
3.2. Pattern A Variations Frequently Detected in BL Tumors or Peripheral Blood of eBL Cases
3.3. Novel Pattern A-Like Variations Suggest a Much Broader Undiscovered LMP-1 Genetic Diversity
3.4. Pattern A and D Heterozygosity in Tumors Suggests Multiple EBV Infections in Single Pre-Cancer B Cells
3.5. Implications of Detecting a High Frequency of Pattern A in BL Tumors or Peripheral Blood of eBL Cases
4. Materials and Methods
4.1. Subjects and IRB
4.2. DNA Extraction
4.3. PCR Amplification of the Targeted Hypervariable Region of LMP-1
4.4. Sanger Sequencing and Data Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
EBV | Epstein-Barr virus |
LMP-1 | Latent membrane protein-1 |
EBNA-1 | Epstein–Barr nuclear antigens-1 |
BZLF-1 | Trans-activator protein BZLF1 |
HTS | High throughput sequencing |
SNV | Single nucleotide polymorphism |
PCR | Polymerase chain reaction |
BL | Burkitt lymphoma |
eBL | endemic Burkitt lymphoma |
NPC | Nasopharyngeal carcinoma |
PTLD | Post-transplant lymphoproliferative disease |
HL | Hodgkin Lymphoma |
GC | EBV-positive gastric carcinoma |
IM | Infectious mononucleosis |
EMBLEM | Epidemiology of Burkitt’s Lymphoma in East-African Children and Minors |
sLCL | Spontaneous transformed lymphoblastoid cell line |
CTAR-1, 2, 3 | Carboxyl-terminal activator regions 1, -2, -3 |
IL-6, -8, -10 | Interleukin-6, -8, -10 |
SSCP | Single strand conformational polymorphism |
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Characteristic | LMP-2B Exon1 | LMP-1 Promoter | LMP-1 Exon1 | LMP-1 Exon3 | |||||||||||||||||||||||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
nt position | 1. −426 | 2. −412 | 3. −410 | 4. −367 | −372 | −356 | 5. −354 | −329 | −328 | −315 | −286 | −284 | −240 | −238 | −234 | −233 | 6. −227 | −207 | −199 | 7. −184 | 8. −172 | −163 | −136 | −70 | 9. −50 | −44 | −43 | −37 | −34 | 10. −39 | −17 | 11. −12 | −6 | −4 | −3 | +11 | +12 | 12. +18 | +26 | +32 | +41 | 13. E2D | 14.15. H3L | R17L | 16. V43I | 17. S57A | 18.19. I63V | 20. I124V | 21. I152L | 22. H213N | 23. E214Q |
nt change | G>A | T>G | C>A | G>A | G>A | C>A | A>G | C>T | G>A | C>T | A>G | G>T | G>A | A>G | G>T | G>A | G>A | C>T | C>T | A>T | T>C | C>T | A>T | A>C | T>A | G>T | A>T | C>G | C>G | A>C | A>T | G>A | C>T | C>A | C>G | A>G | C>T | T>G | A>C | G>A | G>C | GAA>GAC | CAC>CTG | CGA>CTA | GTT>ATT | TCC>GCC | ATA>GTG | ATC>GTC | ATC>CTC | CAT>AAT | GAA>CAA |
Pattern A (23 variants) | A | G | A | A | G | C | G | C | G | C | A | G | G | A | G | C | A | C | C | T | C | C | A | A | A | C | A | C | C | C | A | A | C | C | C | A | C | G | A | G | C | C | TG | G | A | G | GG | G | C | A | C |
Pattern B (29 variants) | G | T | C | G | A | A | A | T | A | T | G | T | A | G | T | A | G | T | T | A | T | T | T | C | T | C | T | G | G | A | T | G | T | A | G | G | T | T | C | A | G | A | AC | T | G | T | AA | A | A | C | G |
Pattern C (3 variants) | G | T | C | G | G | C | A | C | G | C | A | G | G | A | G | G | G | C | C | A | T | C | A | A | T | T | A | C | C | A | A | G | C | C | C | A | C | T | A | G | C | C | AC | G | G | T | AA | A | A | C | G |
Pattern D (wild-type) | G | T | C | G | G | C | A | C | G | C | A | G | G | A | G | G | G | C | C | A | T | C | A | A | T | G | A | C | C | A | A | G | C | C | C | A | C | T | A | G | G | A | AC | G | G | T | AA | A | A | C | G |
EBV Genome | Lei et al. [18] Patterns | Source | Origin | EBV Type | Hu et al. [23] Loss of Xho I Site | Miller et al. [24] 30 bp Deletion | 33 bp Repeats (# of RP Unit) | † Edwards et al. [25] C-Terminal Variants | # Sandvej et al. [27] Group |
---|---|---|---|---|---|---|---|---|---|
KP968263**(H058015C) | A | BL biopsy | Ghana | Type 1 | No | Yes | 4 | China 1 | ND |
KP968262**(H018436D) | A | BL biopsy | Ghana | Type 1 | No | Yes | 4 | China 1 | ND |
KP968264**(H002213) | A | BL biopsy | Ghana | Type 1 | No | Yes | 4 | China 1 | ND |
KP968261**(HU11393) | A | BL biopsy | Ghana | Type 1 | No | Yes | 4 | ND | ND |
KR063342**(H03753A) | A | BL biopsy | Ghana | Type 1 | No | No | 4 | China 1 | ND |
KR063345**(FNR) | A | BL biopsy | Brazil | Type 1 | No | Yes | 4 | China 1 | ND |
KR063344**(RPF) | A | BL biopsy | Brazil | Type 1 | No | Yes | 4 | China 1 | ND |
KP968258**(MP) | A | BL biopsy | Brazil | Type 1 | No | Yes | 4 | China 1 | ND |
KP968257**(CCH) | A | BL biopsy | Brazil | Type 1 | No | Yes | 4 | China 1 | ND |
KR063343**(CV-ARG) | A | BL biopsy | Argentina | Type 1 | No | Yes | 4 | China 1 | ND |
KT001102 (VA) | A | BL biopsy | Argentina | N/A | Gap | Gap | 4 | China 1 | ND |
KT001103 (SG) | A | BL biopsy | Argentina | Type 1 | No | Gap | 4 | China 1 | ND |
KP968259**(SCL) | A | BL biopsy | Brazil | Type 1 | No | No | 4 | B95–8 | ND |
LN827554(LCL-AFB1) | A | LCL | Unknown | Type 2 | No | Yes | 5 | China 1 | ND |
LN824206(pLCL-TRL1-post) | A | sLCL. PTLD (post) | USA | Type 1 | No | Yes | 5 | China 1 | ND |
LN824207(pLCL-TRL1-pre) | A | sLCL. PTLD (pre) | USA | Type 1 | No | Yes | 5 | China 1 | ND |
LN827591(sLCL-2.15) | A | sLCL | Kenya | Type 2 | No | Yes | 5 | China 1 | ND |
LN827594(sLCL-IS1.07) | A | sLCL. PTLD | Australia | Type 1 | No | Yes | 5 | China 1 | ND |
LN827559(pLCL-TRL595) | A | sLCL. PTLD | USA | Type 1 | No | Yes | 5 | China 1 | ND |
LN827563(sLCL-1.18) | A | sLCL | Kenya | Type 1 | No | Yes | 5 | China 1 | ND |
KF717093**(Raji) | A | BL | Nigeria | Type 1 | No | No | 4 | B95-8 | ND |
KP968260**(VGO) | B | BL biopsy | Brazil | Type 1 | Yes | No | 5 | ND | ND |
KC207813**(Akata) | B | BL | Japan | Type 1 | Yes | Yes | 4 | China 1 | ND |
LN824208**(Akata) | B | BL | Japan | Type 1 | Yes | Yes | 4 | China 1 | ND |
KC617875(C666-1) | B | NPC | Asia | Type 1 | Yes | Yes | 4 | China 1 | ND |
KJ411974(C666-1) | B | NPC | Asia | Type 1 | Yes | Yes | 1 | China 1 | ND |
KC617875(C666-1) | B | NPC | Asia | Type 1 | Yes | Yes | 4 | China 1 | ND |
AY961628(GD1) | B | NPC | China | Type 1 | Yes | Yes | 4 | China 1 | ND |
HQ020558(GD2) | B | NPC | China | Type 1 | Yes | Yes | 3 | China 1 | ND |
KF373730(M81) | B | NPC | Asia | Type 1 | Yes | Yes | 4 | China 1 | ND |
LN824142(Saliva) | B | Healthy saliva | UK | Type 1 | Yes | Yes | 2 | China 1 | ND |
LN827562(sLCL-1.19) | B | sLCL | Kenya | Type 1 | Yes | No | 4 | ND | ND |
LN827561(YCCEL1) | B | GC cell line | South Korea | Type 1 | Yes | Yes | 5 | China 1 | ND |
LN824209(HKN14) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 5 | China 1 | ND |
LN827547(HKN15) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 4 | China 1 | ND |
LN824224(HKN19) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 4 | China 1 | ND |
LN827549(D3201.2) | B | NPC | China | Type 1 | Yes | Yes | 6 | China 1 | ND |
JQ009376(HKNPC1) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 5 | China 1 | ND |
KF992564(HKNPC2) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 1 | China 1 | ND |
KF992565(HKNPC3) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 4 | China 1 | ND |
KF992566(HKNPC4) | B | NPC | Hong Kong | Type 1 | Gap | Gap | Gap | Gap | ND |
KF992567(HKNPC5) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 1 | China 1 | ND |
KF992568(HKNPC6) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 1 | China 1 | ND |
KF992569(HKNPC7) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 1 | China 1 | ND |
KF992570(HKNPC8) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 2 | China 1 | ND |
KF992571(HKNPC9) | B | NPC | Hong Kong | Type 1 | Yes | Yes | 1 | China 1 | ND |
LN827523(L591) | B | HL cell line | Germany | Type 1 | Yes | No | 4 | NC | ND |
LN827799(sLCL-IM1.16) | B | sLCL. IM. | Australia | Type 1 | Yes | No | 4 | NC | ND |
LN827578(sLCL-IS1.13) | B | sLCL. PTLD | Australia | Type 1 | Yes | No | 4 | NC | ND |
LN827586(sLCL-IS1.15) | B | sLCL. PTLD | Australia | Type 1 | Yes | No | 4 | NC | ND |
LN827800**(Jijoye) | C | BL | Nigeria | Type 2 | No | No | 4 | B95-8 | ND |
LN827548**(P3HR1_c16) | C | BL | Nigeria | Type 2 | No | No | 4 | B95-8 | ND |
LN827557**(BL36) | C | BL | N. Africa | Type 1 | No | No | 4 | B95-8 | ND |
LN827545**(Daudi) | C | BL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827551**(Makau) | C | BL | Kenya | Type 1 | No | No | 5 | Med | ND |
LN824205(sLCL-1.12) | C | sLCL | Kenya | Type 1 | No | No | 5 | Med | ND |
LN824203**(Mak1) | C | BL | Kenya | Type 1 | No | No | 5 | Med | ND |
LN827544**(Wewak1) | D | BL | PNG | Type 2 | No | No | 4 | ND | ND |
LN827556**(Cheptages) | D | BL | Kenya | Type 2 | No | No | 4 | B95-8 | ND |
LN827526**(BL37) | D | BL | Africa | Type 1 | No | Yes | 6 | Med | ND |
KC207814**(Mutu) | D | BL | Kenya | Type 1 | No | No | 4 | Med | ND |
NC_009334**(AG876) | D | BL | Ghana | Type 2 | No | Yes | 4 | China 1 | ND |
NC_007605 (WT-EBV) | D | B98-8 | USA | type 1 | No | No | 4 | B95-8 | ND |
AJ507799(WT-EBV) | D | B98-8 | USA | Type 1 | No | No | 4 | B95-8 | ND |
V01555(WT-EBV) | D | B95-8 | USA | Type 1 | No | No | 4 | B95-8 | ND |
KC440851(K4123-Mi) | D | healthy donor | USA | Type 1 | No | No | 4 | Med | ND |
KC440852(K4413-Mi) | D | healthy donor | USA | Type 1 | No | No | 4 | B95-8 | A |
NA19114 | D | healthy donor | Yoruba | Type 1 | No | No | 4 | B95-8 | ND |
NA19315 | D | healthy donor | Kenya | Type 1 | No | No | 4 | B95-8 | ND |
NA19384 | D | healthy donor | Kenya | Type 1 | Gap | No | 4 | China 1 | ND |
LN827739(LCL_B958) | D | LCL, B95-8 | USA | Type 1 | No | No | 4 | B95-8 | ND |
LN827597(sLCL-IS1.04) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | B95-8 | ND |
LN827596(sLCL-IM1.02) | D | sLCL. IM. | Australia | Type 1 | No | Yes | 6 | China 1 | ND |
LN827595(sLCL-IS1.03) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | Med | ND |
LN827593(sLCL-IS1.12) | D | sLCL. PTLD | Australia | Type 1 | No | No | 4 | B95-8 | A |
LN827592(sLCL-IS1.10) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | Med | ND |
LN827590(sLCL-IM1.05) | D | sLCL. IM. | Australia | Type 1 | No | Yes | 6 | China 1 | ND |
LN827589(sLCL-IS2.01) | D | sLCL. PTLD | Australia | Type 2 | No | Yes | 4 | China 1 | ND |
LN827588(sLCL-IS1.19) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | B95-8 | A |
LN827587(sLCL-2.21) | D | sLCL | Kenya | Type 2 | No | Yes | 4 | China 1 | ND |
LN827585(sLCL-1.04) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827584(sLCL-IS1.06) | D | sLCL. PTLD | Australia | Type 1 | No | No | 4 | Med | ND |
LN827583(sLCL-IM1.17) | D | sLCL. IM. | Australia | Type 1 | No | No | 4 | B95-8 | ND |
LN827582(sLCL-BL1.03) | D | sLCL | Kenya | Type 1 | No | No | 4 | B95-8 | ND |
LN827581(sLCL-1.05) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827580(sLCL-2.16) | D | sLCL | Kenya | Type 2 | No | No | 5 | B95-8 | ND |
LN827579(sLCL-1.13) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827577(sLCL-1.17) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | A |
LN827576(sLCL-IS1.20) | D | sLCL. PTLD | Australia | Type 1 | No | Yes | 7 | China 1 | ND |
LN827575(sLCL-IS1.14) | D | sLCL. PTLD | Australia | Type 1 | No | No | 4 | B95-8 | A |
LN827574(sLCL-1.09) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | A |
LN827573(sLCL-1.10) | D | sLCL | Kenya | Type 1 | No | No | 3 | Med | ND |
LN827572(sLCL-IS1.18) | D | sLCL. PTLD | Australia | Type 1 | No | No | 4 | B95-8 | ND |
LN827571(sLCL-BL1.20) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827570(sLCL-IS1.01) | D | sLCL. PTLD | Australia | Type 1 | No | Yes | 4 | China 1 | ND |
LN827569(sLCL-IS1.11) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | Med | ND |
LN827568(sLCL-1.24) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827567(sLCL-IM1.09) | D | sLCL. IM. | Australia | Type 1 | No | No | 4 | B95-8 | ND |
LN827566(sLCL-1.06) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827565(sLCL-1.07) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827564(HL04) | D | HL | UK | Type 1 | No | Yes | 3 | China 1 | ND |
LN827560(sLCL-2.14) | D | sLCL | Kenya | Type 2 | No | Yes | 4 | China 1 | ND |
LN827558(sLCL-1.02) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827555(X50-7) | D | LCL | USA | Type 1 | No | No | 4 | B95-8 | ND |
LN827553(sLCL-IS1.08) | D | sLCL. PTLD | Australia | Type 1 | No | No | 5 | Med | ND |
LN827552(sLCL-1.08) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827550(sLCL-1.11) | D | sLCL | Kenya | Type 1 | No | No | 4 | Med | ND |
LN827546(HL02) | D | HL | UK | Type 1 | No | Yes | 3 | China 1 | ND |
LN827527(M-ABA) | D | LCL, NPC virus | N. Africa | Type 1 | No | No | 4 | B95-8 | A |
LN827524(HL11) | D | HL | UK | Type 1 | No | No | 5 | Med | ND |
LN827522(HL09) | D | HL | UK | Type 1 | No | Yes | 6 | China 1 | ND |
LN824226(HL01) | D | HL | UK | Type 1 | No | Yes | 3 | China 1 | ND |
LN824225(HL08) | D | HL | UK | Type 1 | No | Yes | 5 | China 1 | ND |
LN824204(HL05) | D | HL | UK | Type 1 | No | Yes | 5 | China 1 | ND |
Gene Region | LMP-2B Exon1 | LMP-1 Promoter | LMP-1 Exon1 | LMP-1 Exon3 | |||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Primer pair | Lei-F3/Lei-R3 | Lei-F1/Lei-R1 | Lei-F2/Lei-R2 | ||||||||||||||||||||||
Amplicon size | 396 bp | 435 bp | 428 bp | ||||||||||||||||||||||
FT and a.a. affected | AML1 | LBF2 | LBF4 | CREB | E2D | H3L | S24A (new) | V43I | S57A | I63V | I124V | I152L | H213N | E214Q | |||||||||||
Variation | 1. G-426A | 2. T-412G | 3. C-410A | 4. G-376A | 5. A-354G | 6. G-227A | 7. A-184T | 8. T-172C | 9. T-50A | 10. A-39C | 11. G-12A | 12. T+18G | 13. GAA>GAC | 14. CAC>CTG | 15. CAC>CTG | TCC>GCC | 16. GTT>ATT | 17. TCC>GCC | 18. ATA>GTG | 19. ATA>GTG | 20. ATC>GTC | 21. ATC>CTC | 22. CAT>AAT | 23. GAA>CAA | |
Pattern | Example | ||||||||||||||||||||||||
A | BLS000073 | A | G | A | A | G | A | T | C | A | C | A | G | C | T | G | T | A | G | G | G | G | C | A | C |
Mid-Length A | BLS000207 | G | T | C | G | A | G | A | T | T | A | A | G | C | T | G | T | A | G | G | G | G | C | A | C |
4nt sub-pattern A | BLS000292 | G | T | C | G | A | G | A | T | T | C | G | T | C | T | G | G | G | T | A | A | A | A | C | G |
3nt sub-pattern A | BLS000020 | G | T | C | G | A | G | A | T | T | A | G | T | C | T | G | G | G | T | A | A | A | A | C | G |
Partial A sub-pattern | BLS001943 | A | G | A | A | G | A | T | C | A | C | A | G | C | T | G | T | G | T | A | A | A | A | C | C |
Geographical Region | PCR Positive * | PCR Negative * | Pattern A | Mid Length-A | Pattern D | Pattern B | Pattern C | Pattern A/D |
---|---|---|---|---|---|---|---|---|
Argentina | 15 | 3 | 8 (66.7%) | 2 (16.7%) | 2 (16.7%) | 0 (0%) | 0 (0%) | 0 (0%) |
Brazil | 11 | 1 | 8 (80.0%) | 0 (0%) | 1 (10.0%) | 1 (10.0%) | 0 (0%) | 0 (0%) |
Ghana | 45 | 3 | 23 (54.8%) | 5 (11.9%) | 11 (26.2%) | 0 (0%) | 1 (2.4%) | 2 (4.8%) |
Total (N) | 71 | 7 | 39 (60.9%) | 7 (10.9%) | 14 (21.9%) | 1 (1.6%) | 1 (1.6%) | 2 (3.1%) |
Sample Batch | Group | Number of PBMCs | PCR Positive * | PCR Negative | Pattern A | Mid-Length A sub-Pattern | Partial A sub-Pattern | 4nt sub-Pattern A | 3nt sub-Pattern A | Pattern D | N.D. # |
---|---|---|---|---|---|---|---|---|---|---|---|
Batch 1 | BL cases | 13 | 13 (100%) | 0 (0%) | 2 (15.4%) | 0 (0%) | 0 (0%) | 1 (7.7%) | 1 (7.7%) | 9 (69.2%) | 0 (0%) |
Controls | 15 | 15 (100%) | 0 (0%) | 0 (0%) | 4 (26.7%) | 0 (0%) | 4 (26.7%) | 0 (0%) | 7 (46.7%) | 0 (0%) | |
Batch 2 | BL cases | 100 | 86 (86%) | 14 (14%) | 10 (10.0%) | 7 (7.0%) | 3 (3.5%) | 8 (9.3%) | 3 (3.5%) | 55 (55.0%) | 0 (0%) |
Controls | 100 | 29 (86%) | 71 (71%) | 3 (3.0%) | 4(4.0%) | 0 (0%) | 0 (0%) | 0 (0%) | 19 (19.0%) | 3 (3.0%) | |
Batch 1 and 2 | BL cases | 113 | 99 (87.6%) | 14 (12.4%) | 12 (10.6%) | 7 (6.2%) | 3 (2.6%) | 9 (8.0%) | 4 (3.5%) | 64 (56.4%) | 0 (0%) |
Controls | 115 | 41 (35.6%) | 71 (64.4%) | 3 (2.6%) | 8 (7.0%) | 0 (0%) | 4 (3.5%) | 0 (0%) | 26 (22.6%) | 3 (2.6%) |
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Share and Cite
Liao, H.-M.; Liu, H.; Lei, H.; Li, B.; Chin, P.-J.; Tsai, S.; Bhatia, K.; Gutierrez, M.; Epelman, S.; Biggar, R.J.; et al. Frequency of EBV LMP-1 Promoter and Coding Variations in Burkitt Lymphoma Samples in Africa and South America and Peripheral Blood in Uganda. Cancers 2018, 10, 177. https://doi.org/10.3390/cancers10060177
Liao H-M, Liu H, Lei H, Li B, Chin P-J, Tsai S, Bhatia K, Gutierrez M, Epelman S, Biggar RJ, et al. Frequency of EBV LMP-1 Promoter and Coding Variations in Burkitt Lymphoma Samples in Africa and South America and Peripheral Blood in Uganda. Cancers. 2018; 10(6):177. https://doi.org/10.3390/cancers10060177
Chicago/Turabian StyleLiao, Hsiao-Mei, Hebing Liu, Heiyan Lei, Bingjie Li, Pei-Ju Chin, Shien Tsai, Kishor Bhatia, Marina Gutierrez, Sidnei Epelman, Robert J. Biggar, and et al. 2018. "Frequency of EBV LMP-1 Promoter and Coding Variations in Burkitt Lymphoma Samples in Africa and South America and Peripheral Blood in Uganda" Cancers 10, no. 6: 177. https://doi.org/10.3390/cancers10060177