Latent membrane proteins from EBV differentially target cellular pathways to accelerate MYC-induced lymphomagenesis

Blood Adv. 2022 Jul 26;6(14):4283-4296. doi: 10.1182/bloodadvances.2022007695.

Abstract

MYC translocations in association with Epstein-Barr virus (EBV) infection are often observed in B-cell lymphomas. A subset of Burkitt lymphoma (BL) expresses EBV latent membrane proteins 1 and 2A (LMP1 and LMP2A) in addition to the typical restricted EBV latent gene expression. EBV-associated diffuse large B-cell lymphoma (DLBCL) typically exhibits latency type II or III and expresses LMP1. Here, we investigate the role of LMP1 in MYC-driven lymphomagenesis in our murine model. λ-MYC mice develop tumors having a "starry sky" appearance and have abnormal p53 expression that is also observed in human BL. LMP2A/λ-MYC double-transgenic mice develop tumors significantly faster than mice only expressing MYC. Similar to LMP2A/λ-MYC mice, LMP1/λ-MYC mice also have accelerated MYC-driven lymphomagenesis. As observed in LMP2A/λ-MYC mice, p27kip1 was degraded in LMP1/λ-MYC pretumor and tumor B cells. Coexpression of LMP1 and LMP2A resulted in the enhancement of B cell proliferation. In contrast to LMP2A, the inhibition of Syk or cyclin-dependant kinase (CDK)4/6 activity did not effectively inhibit LMP1-mediated MYC lymphomagenesis. Also, in contrast to LMP2A, LMP1 did not lessen abnormal p53 expression in λ-MYC tumors. To investigate the significance of LMP1 expression in human BL development, we reanalyzed RNA sequencing (RNA-Seq) data of primary human BL from previous studies. Interestingly, p53 mutations were less observed in LMP1-expressing BL, although they were not significantly changed by EBV infection, indicating LMP1 may lessen p53 mutations in human primary BL. This suggests that LMP1 effects in EBV-associated human BL vary from what we observe in our murine model. Finally, our studies suggest a novel pathogenic role of LMP1 in lymphomagenesis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Burkitt Lymphoma* / genetics
  • Burkitt Lymphoma* / virology
  • Disease Models, Animal
  • Epstein-Barr Virus Infections* / complications
  • Epstein-Barr Virus Infections* / metabolism
  • Herpesvirus 4, Human / metabolism
  • Humans
  • Lymphoma, Large B-Cell, Diffuse* / etiology
  • Lymphoma, Large B-Cell, Diffuse* / virology
  • Mice
  • Proto-Oncogene Proteins c-myc* / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Viral Matrix Proteins* / metabolism

Substances

  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Tumor Suppressor Protein p53
  • Viral Matrix Proteins