Comprehensive transcriptome and mutational profiling of endemic Burkitt lymphoma reveals EBV type–specific differences

Kaymaz, Yasin; Oduor, Cliff I.; Yu, Hongbo; Otieno, Juliana A.; Ong'echa, John Michael; Moormann, Ann M.; Bailey, Jeffrey A.

doi:10.1158/1541-7786.mcr-16-0305

Cited by 120Viral-associated cancers and disordersLymphoma Diagnosis and TreatmentCNS Lymphoma Diagnosis and Treatment

Comprehensive transcriptome and mutational profiling of endemic Burkitt lymphoma reveals EBV type–specific differences

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Kaymaz, Yasin, Oduor, Cliff I., Yu, Hongbo, Otieno, Juliana A., Ong'echa, John Michael, Moormann, Ann M., Bailey, Jeffrey A.·2017·Molecular Cancer Research

DOI 10.1158/1541-7786.mcr-16-0305PMC PMC5471630

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Abstract

Endemic Burkitt lymphoma (eBL) is the most common pediatric cancer in malaria-endemic equatorial Africa and nearly always contains Epstein–Barr virus (EBV), unlike sporadic Burkitt lymphoma (sBL) that occurs with a lower incidence in developed countries. Given these differences and the variable clinical presentation and outcomes, we sought to further understand pathogenesis by investigating transcriptomes using RNA sequencing (RNAseq) from multiple primary eBL tumors compared with sBL tumors. Within eBL tumors, minimal expression differences were found based on: anatomical presentation site, in-hospital survival rates, and EBV genome type, suggesting that eBL tumors are homogeneous without marked subtypes. The outstanding difference detected using surrogate variable analysis was the significantly decreased expression of key genes in the immunoproteasome complex (PSMB9/β1i, PSMB10/β2i, PSMB8/β5i, and PSME2/PA28β) in eBL tumors carrying type 2 EBV compared with type 1 EBV. Second, in comparison with previously published pediatric sBL specimens, the majority of the expression and pathway differences was related to the PTEN/PI3K/mTOR signaling pathway and was correlated most strongly with EBV status rather than geographic designation. Third, common mutations were observed significantly less frequently in eBL tumors harboring EBV type 1, with mutation frequencies similar between tumors with EBV type 2 and without EBV. In addition to the previously reported genes, a set of new genes mutated in BL, including TFAP4, MSH6, PRRC2C, BCL7A, FOXO1, PLCG2, PRKDC, RAD50, and RPRD2, were identified. Overall, these data establish that EBV, particularly EBV type 1, supports BL oncogenesis, alleviating the need for certain driver mutations in the human genome. Implications: Genomic and mutational analyses of Burkitt lymphoma tumors identify key differences based on viral content and clinical outcomes suggesting new avenues for the development of prognostic molecular biomarkers and therapeutic interventions. Mol Cancer Res; 15(5); 563–76. ©2017 AACR.

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An RNA-seq study of patient tumors of endemic Burkitt lymphoma showed that the vast majority of cases which harbor EBV contain PLCγ2 mutations, along with mutations in other genes including MYC.
“In addition, an RNA-seq study of patient tumors of EBL, a common childhood cancer from equatorial Africa where malaria is endemic, showed that the vast majority of cases which harbor EBV contain PLCγ2 mutations, along with mutations in other genes including MYC (142).”
From The role of PLCγ2 in immunological disorders, cancer, and neurodegeneration (2021) · cites this paper as [142]
The Results (Table 2; page unavailable) report PLCG2 mutations in 0% of EBV type 1 tumors and 25% of EBV type 2 tumors, contrary to the claim that the vast majority of EBV-positive cases had them. The study did use RNA-seq on patient tumors and report MYC mutations, but those points do not support the claimed PLCG2 prevalence. (LLM, conf=0.94)
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Mutations in PLCγ2 are relevant to disease initiation in endemic Burkitt lymphoma.
“Interestingly, while MYC translocation and hyperexpression is a hallmark of EBL, it in itself is not sufficient to induce lymphogenesis (143), which may at least in part explain why mutations in PLCγ2 are relevant to the disease initiation (142).”
From The role of PLCγ2 in immunological disorders, cancer, and neurodegeneration (2021) · cites this paper as [142]
The Results report PLCG2 mutations in endemic Burkitt lymphoma and identify PLCγ2 as an enzyme in B-cell receptor signaling. The Discussion links signaling pathways to lymphoma development, but does not establish that PLCG2 mutations contribute specifically to disease initiation. Page numbers are not available in our copy. (LLM, conf=0.84)
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The 5th edition of the World Health Organization Classification of Haematolymphoid Tumours: Lymphoid Neoplasms
Alaggio, R., Amador, C., Anagnostopoulos, I., Attygalle, A. D., Araújo, I., Berti, E., Bhagat, G., Borges, A. M., Boyer, D. F., Calaminici, M., et al. (2022) · Leukemia · doi:10.1038/s41375-022-01620-2 · Cited by 4,059 · see citing works
Epstein–Barr virus-associated lymphomas
Shannon-Lowe, C. D., Rickinson, A. B., & Bell, A. I. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0271 · Cited by 427 · see citing works
Genome-wide discovery of somatic coding and noncoding mutations in pediatric endemic and sporadic Burkitt lymphoma
Grande, B. M., Gerhard, D. S., Jiang, A., Griner, N. B., Abramson, J. S., Alexander, T., Allen, H., Ayers, L. W., Bethony, J., Bhatia, K. G., et al. (2019) · Blood · doi:10.1182/blood-2018-09-871418 · Cited by 268 · see citing works
MRE11-RAD50-NBS1 complex alterations and DNA damage response: implications for cancer treatment
Bian, L., Meng, Y., Zhang, M., & Li, D. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1100-5 · Cited by 253 · see citing works
The whole-genome landscape of Burkitt lymphoma subtypes
Panea, R., Love, C., Shingleton, J. R., Reddy, A., Bailey, J. A., Moormann, A. M., Otieno, J. A., Ong’echa, J. M., Oduor, C. I., Schroeder, K., et al. (2019) · Blood · doi:10.1182/blood.2019001880 · Cited by 190 · see citing works
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Genomic and transcriptomic changes complement each other in the pathogenesis of sporadic Burkitt lymphoma
López, C., Kleinheinz, K., Aukema, S., Rohde, M., Bernhart, S. H., Hübschmann, D., Wagener, R., Toprak, U. H., Raimondi, F., Kreuz, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08578-3 · Cited by 151 · see citing works
Burkitt lymphoma
López, C., Burkhardt, B., Chan, J. K. C., Leoncini, L., Mbulaiteye, S. M., Ogwang, M. D., Orem, J., Rochford, R. A., Roschewski, M. J., & Siebert, R. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00404-3 · Cited by 144 · see citing works
The role of PLCγ2 in immunological disorders, cancer, and neurodegeneration
Jackson, J. T., Mulazzani, E., Nutt, S. L., & Masters, S. L. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100905 · Cited by 113 · see citing works
“In addition, an RNA-seq study of patient tumors of EBL, a common childhood cancer from equatorial Africa where malaria is endemic, showed that the vast majority of cases which harbor EBV contain PLCγ2 mutations, along with mutations in other genes including MYC (142).”
Burkitt’s Lymphoma
Roschewski, M. J., Staudt, L. M., & Wilson, W. H. (2022) · New England Journal of Medicine · doi:10.1056/nejmra2025746 · Cited by 108 · see citing works
Understanding human health through metatranscriptomics
Ojala, T., Kankuri, E. M., & Kankainen, M. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.02.002 · Cited by 107 · see citing works
EBV-associated diseases: Current therapeutics and emerging technologies
Chakravorty, S., Afzali, B., & Kazemian, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1059133 · Cited by 108 · see citing works
Genetic subgroups inform on pathobiology in adult and pediatric Burkitt lymphoma
Thomas, N., Dreval, K., Gerhard, D. S., Hilton, L. K., Abramson, J. S., Ambinder, R. F., Barta, S. K., Bartlett, N. L., Bethony, J. M., Bhatia, K. G., et al. (2022) · Blood · doi:10.1182/blood.2022016534 · Cited by 91 · see citing works
EBV and Apoptosis: The Viral Master Regulator of Cell Fate?
Fitzsimmons, L., & Kelly, G. L. (2017) · Viruses · doi:10.3390/v9110339 · Cited by 79 · see citing works
A comparison of the International Consensus and 5th World Health Organization classifications of mature B-cell lymphomas
Falini, B., Martino, G., & Lazzi, S. (2022) · Leukemia · doi:10.1038/s41375-022-01764-1 · Cited by 79 · see citing works
SWI/SNF complexes in hematological malignancies: biological implications and therapeutic opportunities
Andrades, Á., Peinado, P., Álvarez-Pérez, J. C., Sanjuán‐Hidalgo, J., García, D. J., Arenas, A. M., Matia‐González, A. M., & Medina, P. P. (2023) · Molecular Cancer · doi:10.1186/s12943-023-01736-8 · Cited by 71 · see citing works
Deciphering the roles of FOXO1 in human neoplasms
Jiang, S., Li, T. X., Yang, Z. P., Hu, W., & Yang, Y. (2018) · International Journal of Cancer · doi:10.1002/ijc.31338 · Cited by 64 · see citing works
Poorly cytotoxic terminally differentiated CD56negCD16pos NK cells accumulate in Kenyan children with Burkitt lymphomas
Forconi, C. S., Cosgrove, C., Lakshmi, P. S., Nixon, C. E., Foley, J., Ong’echa, J. M., Otieno, J. A., Alter, G., Münz, C., & Moormann, A. M. (2018) · Blood Advances · doi:10.1182/bloodadvances.2017015404 · Cited by 62 · see citing works
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A New Hope for CD56negCD16pos NK Cells as Unconventional Cytotoxic Mediators: An Adaptation to Chronic Diseases
Forconi, C. S., Oduor, C. I., Oluoch, P. O., Ong’echa, J. M., Münz, C., Bailey, J. A., & Moormann, A. M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00162 · Cited by 62 · see citing works
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Epstein–Barr virus nuclear antigen 2 extensively rewires the human chromatin landscape at autoimmune risk lociPreprint
Hong, T., Parameswaran, S., Donmez, O., Miller, D. E., Forney, C., Lape, M., Ribeiro, M. S. J., Liang, J., Edsall, L. E., Magnusen, A., et al. (2021) · Genome Research · doi:10.1101/gr.264705.120 · Cited by 50 · see citing works
Alternative splicing of its 5′-UTR limits CD20 mRNA translation and enables resistance to CD20-directed immunotherapies
Ang, Z., Paruzzo, L., Hayer, K. E., Schmidt, C., Torres-Diz, M., Xu, F., Zankharia, U. S., Zhang, Y., Soldan, S. S., Zheng, S., et al. (2023) · Blood · doi:10.1182/blood.2023020400 · Cited by 54 · see citing works
Epstein-Barr Virus Type 2 Infects T Cells and Induces B Cell Lymphomagenesis in Humanized Mice
Coleman, C. B., Lang, J., Sweet, L. A., Smith, N. A., Freed, B. M., Pan, Z., Haverkos, B. M., Pelanda, R., & Rochford, R. A. (2018) · Journal of Virology · doi:10.1128/jvi.00813-18 · Cited by 54 · see citing works
Epstein–Barr virus status of sporadic Burkitt lymphoma is associated with patient age and mutational features
Richter, J., John, K., Staiger, A. M., Rosenwald, A., Kurz, K. S., Michgehl, U., Ott, G., Franzenburg, S., Kohler, C., Finger, J., et al. (2021) · British Journal of Haematology · doi:10.1111/bjh.17874 · Cited by 48 · see citing works
The variant landscape and function of DDX3X in cancer and neurodevelopmental disorders
Gadek, M., Sherr, E. H., & Floor, S. N. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.06.003 · Cited by 47 · see citing works
Epstein-Barr Virus Genomes Reveal Population Structure and Type 1 Association with Endemic Burkitt Lymphoma
Kaymaz, Y., Oduor, C. I., Aydemir, Ö., Luftig, M. A., Otieno, J. A., Ong’echa, J. M., Bailey, J. A., & Moormann, A. M. (2020) · Journal of Virology · doi:10.1128/jvi.02007-19 · Cited by 37 · see citing works
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A Survey of Reported Disease-Related Mutations in the MRE11-RAD50-NBS1 Complex
Rahman, S., Canny, M. D., Buschmann, T. A., & Latham, M. P. (2020) · Cells · doi:10.3390/cells9071678 · Cited by 35 · see citing works
Noncatalytic Bruton's tyrosine kinase activates PLCγ2 variants mediating ibrutinib resistance in human chronic lymphocytic leukemia cells
Wist, M., Meier, L., Gutman, O., Haas, J., Endres, S., Zhou, Y., Rösler, R., Wiese, S., Stilgenbauer, S., Hobeika, E., et al. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011946 · Cited by 34 · see citing works
Burkitt Lymphomas Evolve to Escape Dependencies on Epstein-Barr Virus
Hutcheson, R., Chakravorty, A. “., & Sugden, B. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.606412 · Cited by 33 · see citing works
Functional Implications of Epstein-Barr Virus Lytic Genes in Carcinogenesis
Yap, L. F., Wong, A. K. C., Paterson, I. C., & Young, L. S. (2022) · Cancers · doi:10.3390/cancers14235780 · Cited by 33 · see citing works
Sporadic and endemic Burkitt lymphoma have frequent FOXO1 mutations but distinct hotspots in the AKT recognition motif
Zhou, P., Blain, A. E., Newman, A. M., Zaka, M., Chagaluka, G., Adlar, F. R., Offor, U. T., Broadbent, C., Chaytor, L., Whitehead, A., et al. (2019) · Blood Advances · doi:10.1182/bloodadvances.2018029546 · Cited by 32 · see citing works
Integrative microRNA and mRNA deep-sequencing expression profiling in endemic Burkitt lymphoma
Oduor, C. I., Kaymaz, Y., Chelimo, K., Otieno, J. A., Ong’echa, J. M., Moormann, A. M., & Bailey, J. A. (2017) · BMC Cancer · doi:10.1186/s12885-017-3711-9 · Cited by 29 · see citing works
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Human and Epstein-Barr Virus miRNA Profiling as Predictive Biomarkers for Endemic Burkitt Lymphoma
Oduor, C. I., Movassagh, M. J., Kaymaz, Y., Chelimo, K., Otieno, J. A., Ong’echa, J. M., Moormann, A. M., & Bailey, J. A. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00501 · Cited by 28 · see citing works
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Reframing Burkitt lymphoma: virology not epidemiology defines clinical variants
Rochford, R. A. (2021) · Annals of Lymphoma · doi:10.21037/aol-21-18 · Cited by 27 · see citing works
Increased expression of PSME2 is associated with clear cell renal cell carcinoma invasion by regulating BNIP3‑mediated autophagy
Wang, X., Wu, F., Deng, Y., Chai, J., Zhang, Y., He, G., & Li, X. (2021) · International Journal of Oncology · doi:10.3892/ijo.2021.5286 · Cited by 27 · see citing works
Malaria and Cancer: a critical review on the established associations and new perspectives
Ellis, T., Eze, E., & Raimi‐Abraham, B. T. (2021) · Infectious Agents and Cancer · doi:10.1186/s13027-021-00370-7 · Cited by 25 · see citing works
Genetic errors of immunity distinguish pediatric nonmalignant lymphoproliferative disorders
Forbes, L. R., Eckstein, O. S., Gulati, N., Peckham‐Gregory, E. C., Ozuah, N. W., Lubega, J., El‐Mallawany, N. K., Agrusa, J. E., Poli, M. C., Vogel, T. P., et al. (2021) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2021.07.015 · Cited by 25 · see citing works
Phospholipase Cγ2 regulates endocannabinoid and eicosanoid networks in innate immune cells
Jing, H., Reed, A., Ulanovskaya, O. A., Grigoleit, J.-S., Herbst, D. M., Henry, C. L., Li, H., Barbas, S., Germain, J., Masuda, K., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2112971118 · Cited by 24 · see citing works
Worldwide Prevalence of Epstein–Barr Virus in Patients with Burkitt Lymphoma: A Systematic Review and Meta-Analysis
Al‐Khreisat, M. J., Ismail, N. H., Tabnjh, A. K., Hussain, F. A., Yusoff, A. A. M., Johan, M. F., & Islam, M. A. (2023) · Diagnostics · doi:10.3390/diagnostics13122068 · Cited by 23 · see citing works
Frequent co-reactivation of Epstein–Barr virus in patients with cytomegalovirus viremia under immunosuppressive therapy and/or chemotherapy
Hatayama, Y., Hashimoto, Y., & Motokura, T. (2020) · Journal of International Medical Research · doi:10.1177/0300060520972880 · Cited by 21 · see citing works
Decoding the molecular heterogeneity of pediatric monomorphic post–solid organ transplant lymphoproliferative disorders
Salmerón‐Villalobos, J., de Anta, N. C., Guerra‐García, P., Ramis-Zaldivar, J. E., López‐Guerra, M., Mato, S., Colomer, D., Diaz-Crespo, F. J., Menárguez, J., Garrido‐Pontnou, M., et al. (2023) · Blood · doi:10.1182/blood.2022019543 · Cited by 21 · see citing works
Frequent mutations of FBXO11 highlight BCL6 as a therapeutic target in Burkitt lymphoma
Pighi, C., Cheong, T.-C., Compagno, M., Patrucco, E., Arigoni, M., Olivero, M., Wang, Q., López, C., Bernhart, S. H., Grande, B. M., et al. (2021) · Blood Advances · doi:10.1182/bloodadvances.2021005682 · Cited by 19 · see citing works
The distribution of cancer cases in Somalia
Baş, Y., Hassan, H. A., Adıgüzel, C., Bulur, O., Ibrahim, İ. A., & Soydan, S. (2017) · Seminars in Oncology · doi:10.1053/j.seminoncol.2017.10.007 · Cited by 19 · see citing works
Burkitt lymphoma
Fang, H., Wang, W., & Medeiros, L. J. (2024) · Human Pathology · doi:10.1016/j.humpath.2024.105703 · Cited by 18 · see citing works
The Functional Interaction Between Epstein–Barr Virus and MYC in the Pathogenesis of Burkitt Lymphoma
Solares, S., León, J., & García-Gutiérrez, L. (2024) · Cancers · doi:10.3390/cancers16244212 · Cited by 18 · see citing works
Epstein–Barr Virus Latent Membrane Protein 2A (LMP2A) Enhances ATP Production in B Cell Tumors through mTOR and HIF-1α
Incrocci, R., Toro, R. M. D., Devitt, G., Salimian, M., Braich, K., & Swanson-Mungerson, M. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073944 · Cited by 16 · see citing works
Functional characterization of phospholipase C-γ2 mutant protein causing both somatic ibrutinib resistance and a germline monogenic autoinflammatory disorder
Walliser, C., Wist, M., Hermkes, E., Zhou, Y., Schade, A., Haas, J., Deinzer, J., Désiré, L., Li, S. S. C., Stilgenbauer, S., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.26173 · Cited by 17 · see citing works
The role of EBV in haematolymphoid proliferations: emerging concepts relevant to diagnosis and treatment
Ababneh, E. I., Saad, A. M., & Crane, G. M. (2021) · Histopathology · doi:10.1111/his.14379 · Cited by 17 · see citing works
Chromatin-Remodeled State in Lymphoma
Liu, Y., Gonzalez, Y., & Amengual, J. E. (2019) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-019-00541-9 · Cited by 16 · see citing works
FOXO1 Gene Downregulation and Promoter Methylation Exhibits Significant Correlation With Clinical Parameters in Indian Breast Cancer Patients
Khan, M. A., Massey, S., Ahmad, I. S., Sadaf, S., Akhter, N., Habib, M., Mustafa, S., Deo, S. V. S., & Husain, S. A. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.842943 · Cited by 16 · see citing works
SOX11 expression is restricted to EBV-negative Burkitt lymphoma and is associated with molecular genetic features
Sureda-Gómez, M., Iaccarino, I., Bolòs, A. D., Meyer, M., Balsas, P., Richter, J., Rodríguez, M.-L., López, C., Carreras-Caballé, M., Glaser, S., et al. (2024) · Blood · doi:10.1182/blood.2023023242 · Cited by 16 · see citing works
The X-Linked Helicase DDX3X Is Required for Lymphoid Differentiation and MYC-Driven Lymphomagenesis
Lacroix, M., Beauchemin, H., Fraszczak, J., Ross, J., Shooshtarizadeh, P., Chen, R., & Möröy, T. (2022) · Cancer Research · doi:10.1158/0008-5472.can-21-2454 · Cited by 16 · see citing works
Association of PD-1/PD-L1 expression and Epstein-–Barr virus infection in patients with invasive breast cancer
Zhang, W., Zhu, G.-L., Xu, W., Zhang, W., Wang, H.-Z., Wang, Y., & Li, Y. (2022) · Diagnostic Pathology · doi:10.1186/s13000-022-01234-3 · Cited by 16 · see citing works
Kaposi Sarcoma-Associated Herpesvirus Infection and Endemic Burkitt Lymphoma
Oluoch, P. O., Oduor, C. I., Forconi, C. S., Ong’echa, J. M., Münz, C., Dittmer, D. P., Bailey, J. A., & Moormann, A. M. (2020) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaa060 · Cited by 15 · see citing works
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Viral and host factors drive a type 1 Epstein–Barr virus spontaneous lytic phenotype
Willard, K. A., Barry, A. P., Oduor, C. I., Ong’echa, J. M., Bailey, J. A., Moormann, A. M., & Luftig, M. A. (2023) · mBio · doi:10.1128/mbio.02204-23 · Cited by 14 · see citing works
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Latent membrane proteins from EBV differentially target cellular pathways to accelerate MYC-induced lymphomagenesis
Ikeda, M., Hayes, C. K., Schaller, S. J., & Longnecker, R. (2022) · Blood Advances · doi:10.1182/bloodadvances.2022007695 · Cited by 13 · see citing works
The RNA helicase DDX3 and its role in c-MYC driven germinal center-derived B-cell lymphoma
Lacroix, M., Beauchemin, H., Khandanpour, C., & Möröy, T. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1148936 · Cited by 14 · see citing works
A Diagnostic Approach in Large B-Cell Lymphomas According to the Fifth World Health Organization and International Consensus Classifications and a Practical Algorithm in Routine Practice
Zanelli, M., Sanguedolce, F., Zizzo, M., Ricci, S., Bisagni, A., Palicelli, A., Fragliasso, V., Donati, B., Broggi, G., Boutas, I., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252313213 · Cited by 13 · see citing works
Burkitt lymphoma-related TCF3 mutations alter TCF3 alternative splicing by disrupting hnRNPH1 binding
Yamazaki, T., Liu, L., Conlon, E. G., & Manley, J. L. (2020) · RNA Biology · doi:10.1080/15476286.2020.1772559 · Cited by 13 · see citing works
Construction of a DNA damage repair gene signature for predicting prognosis and immune response in breast cancer
Chang, Y., Huang, Z., Quan, H., Li, H., Yang, S., Song, Y., Wang, J., Yuan, J., & Wu, C. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2022.1085632 · Cited by 12 · see citing works
Endemic Burkitt lymphoma avatar mouse models for exploring inter-patient tumor variation and testing targeted therapies
Lakshmi, P. S., Oduor, C. I., Forconi, C. S., M’Bana, V., Bly, C. S., Gerstein, R. M., Otieno, J. A., Ong’echa, J. M., Münz, C., Luftig, M. A., et al. (2023) · Life Science Alliance · doi:10.26508/lsa.202101355 · Cited by 12 · see citing works
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METTL3 regulates M6A methylation-modified EBV-pri-miR-BART3-3p to promote NK/T cell lymphoma growth
Wu, S., Wang, H., Yang, Q., Liu, Z., Du, J., Wang, L., Chen, S., Lu, Q., & Yang, D. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.217058 · Cited by 11 · see citing works
Subtyping Burkitt Lymphoma by DNA Methylation
Glaser, S., Wagener, R., Kretzmer, H., López, C., Baptista, M. J., Bens, S., Bernhart, S. H., Bhatia, K. G., Borkhardt, A., Elgaafary, S., et al. (2025) · Genes Chromosomes and Cancer · doi:10.1002/gcc.70042 · Cited by 11 · see citing works
Identification of clinical molecular targets for childhood Burkitt lymphoma
Zhang, J., Meng, L., Jiang, W., Zhang, H., Zhou, A., & Zeng, N. (2020) · Translational Oncology · doi:10.1016/j.tranon.2020.100855 · Cited by 10 · see citing works
Cancer Omics in Africa: Present and Prospects
Jaddaoui, I. E., Allali, I., Sehli, S., Ouldim, K., Hamdi, S., Idrissi, N. A., Nejjari, C., Amzazi, S., Bakri, Y., & Ghazal, H. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.606428 · Cited by 12 · see citing works
Genomic landscape of virus-associated cancers
Nam, Y., Gómez, K., Nam, Y., Khamnei, C. C., Khamnei, C., Zheng, V., Lhakhang, T. W., Casula, M., Palmieri, G., Cossu, A., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60836-9 · Cited by 17 · see citing works
Genes associated with diagnosis and prognosis of Burkitt lymphoma
Doughan, A., & Salifu, S. P. (2022) · IET Systems Biology · doi:10.1049/syb2.12054 · Cited by 10 · see citing works
Single-cell transcriptomics of pediatric Burkitt lymphoma reveals intra-tumor heterogeneity and markers of therapy resistance
Corinaldesi, C., Holmes, A. B., Martire, G., Tosato, A., Rizzato, D., Lovisa, F., Gallingani, I., Shen, Q. “., Ferrone, L., Harris, M. H., et al. (2024) · Leukemia · doi:10.1038/s41375-024-02431-3 · Cited by 10 · see citing works
MYC directly transactivates CR2/CD21, the receptor of the Epstein–Barr virus, enhancing the viral infection of Burkitt lymphoma cells
Molina, E., García-Gutiérrez, L., Junco, V., Pérez‐Olivares, M., de Yébenes, V. G., Blanco, R. E., Quevedo, L., Acosta, J. C., Marín, A. V., Ulgiati, D., et al. (2023) · Oncogene · doi:10.1038/s41388-023-02846-9 · Cited by 10 · see citing works
Rare EBV-associated B cell neoplasms of the gastrointestinal tract
Volaric, A. K., Singh, K., & Gru, A. A. (2021) · Seminars in Diagnostic Pathology · doi:10.1053/j.semdp.2021.04.004 · Cited by 10 · see citing works
Sensitive detection of EBV microRNAs across cancer spectrum reveals association with decreased survival in adult acute myelocytic leukemia
Movassagh, M. J., Oduor, C. I., Forconi, C. S., Moormann, A. M., & Bailey, J. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-56472-1 · Cited by 9 · see citing works
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Cytogenomics of B-cell non-Hodgkin lymphomas: The “old” meets the “new”
Grau, M., López, C., Martín-Subero, J. I., & Beà, S. (2023) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2023.101513 · Cited by 8 · see citing works
Interplay between IL-10, IFN-γ, IL-17A and PD-1 Expressing EBNA1-Specific CD4+ and CD8+ T Cell Responses in the Etiologic Pathway to Endemic Burkitt Lymphoma
Forconi, C., Mulama, D. H., Lakshmi, P. S., Foley, J., Otieno, J. A., Kurtis, J., Berg, L., Ong'echa, J., Münz, C., & Moormann, A. (2021) · Cancers · doi:10.3390/cancers13215375 · Cited by 7 · see citing works
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Inhibitor of DNA binding/differentiation proteins as IDs for pancreatic cancer: Role in pancreatic cancer initiation, development and prognosis
Murugesan, P., Begum, H., & Tangutur, A. D. (2022) · Gene · doi:10.1016/j.gene.2022.147092 · Cited by 8 · see citing works
Deletion of the transcriptional regulator TFAP4 accelerates c-MYC-driven lymphomagenesis
Potts, M. A., Mizutani, S., Garnham, A. L., Suen, C. S. N. L. W., Kueh, A. J., Tai, L., Pál, M., Strasser, A., & Herold, M. J. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01145-w · Cited by 6 · see citing works
LMP2A—The Other EBV Oncogene
Riel, M., & Johannsen, E. (2025) · Current topics in microbiology and immunology · doi:10.1007/82_2025_330 · Cited by 8 · see citing works
PLCG2 across human disease: genetic variants, signaling mechanisms, and clinical implications
Jiang, P., Wang, M., Zhang, C., Li, X., Wang, Z. Q., Guo, Y., Zhang, J., Yan, W., & Xi, X. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-025-07632-7 · Cited by 6 · see citing works
Genomic landscape of Epstein–Barr virus-positive extranodal marginal zone lymphomas of mucosa-associated lymphoid tissue
Rea, B. A., Liu, Y., Maguire, A., Soma, L. A., Bacon, C. M., Bayerl, M. G., Smith, M. H., Barrett, M. T., Swerdlow, S. H., & Gibson, S. E. (2021) · Modern Pathology · doi:10.1038/s41379-021-01002-6 · Cited by 6 · see citing works
Burkitt Lymphoma—A Guide to Biological Features, Diagnosis and Differential Diagnosis
Anagnostopoulos, I., Zamò, A., Horn, H., Staiger, A. M., & Ott, G. (2026) · Cancers · doi:10.3390/cancers18040579 · Cited by 5 · see citing works
Aggressive non-Hodgkin lymphoma in the pediatric and young adult population; diagnostic and molecular pearls of wisdom
Singh, A. P., & Obiorah, I. E. (2023) · Seminars in Diagnostic Pathology · doi:10.1053/j.semdp.2023.06.002 · Cited by 5 · see citing works
RNA-seq research landscape in Africa: systematic review reveals disparities and opportunities
Doughan, A., Adingo, W., & Salifu, S. P. (2023) · European journal of medical research · doi:10.1186/s40001-023-01206-3 · Cited by 5 · see citing works
Transcriptional regulation of gene modules in Epstein-Barr virus
Lieberman, P. M. (2025) · Transcription · doi:10.1080/21541264.2025.2562704 · Cited by 5 · see citing works
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Genomic and Transcriptomic Investigation of Endemic Burkitt Lymphoma and Epstein Barr Virus
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Authors: Kaymaz, Y., Oduor, C. I., Yu, H., Otieno, J. A., Ong'echa, J. M., Moormann, A. M., & Bailey, J. A.
Affiliations: University of Massachusetts Chan Medical School (US)
Maseno University (KE)
Ministry of Health (KE)
2Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya.
Corresponding author: Bailey, Jeffrey A.
ORCID: Kaymaz, Yasin
Oduor, Cliff I.
Yu, Hongbo
Otieno, Juliana A.
Moormann, Ann M.
Bailey, Jeffrey A.
Venue: Molecular Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2017-05-01
Volume: 15
Issue: 5
Pages: 563-576
ISSN: 1541-7786 (ISSN-L)
1557-3125
DOI: 10.1158/1541-7786.mcr-16-0305
PMC: PMC5471630
OpenAlex: W2580872164
Cited by: 120
References: 65
Citations by year: 2026: 10 · 2025: 11 · 2024: 17 · 2023: 23 · 2022: 16 · 2021: 14 · 2020: 11 · 2019: 9 · 2018: 4 · 2017: 5
FWCI: 3.50
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Molecular Cancer Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
Funders: National Institutes of Health (UL1TR001453, UL1TR000161)
National Cancer Institute (R01CA134051, R01CA189806)
National Institute of Allergy and Infectious Diseases (R01AI099473)
National Center for Advancing Translational Sciences
Topics: Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
Health Sciences › Medicine › Neurology › CNS Lymphoma Diagnosis and Treatment
Keywords: endemic Burkitt lymphoma, sporadic Burkitt lymphoma, Epstein-Barr virus, transcriptome, mutational profiling, immunoproteasome, PSMB9, TFAP4, MSH6, prognostic factors, pediatric lymphoma
MeSH terms: Adolescent, Burkitt Lymphoma, Child, Child, Preschool, Herpesvirus 4, Human, Female, Humans, Kenya, Male, Mutation, Genome, Viral, Sequence Analysis, RNA, Endemic Diseases, Epstein-Barr Virus Infections, Gene Expression Profiling, Gene Regulatory Networks, Mutation Rate

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Comprehensive transcriptome and mutational profiling of endemic Burkitt lymphoma reveals EBV type–specific differences

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