KSHV Latency Locus Cooperates with Myc to Drive Lymphoma in Mice

1. Meyer N, Penn LZ (2008) Reflecting on 25 years with MYC. Nat Rev Cancer 8: 976–990. doi: 10.1038/nrc2231 19029958

2. Jaffe ES, Pittaluga S (2011) Aggressive B-cell lymphomas: a review of new and old entities in the WHO classification. Hematology / the Education Program of the American Society of Hematology American Society of Hematology Education Program 2011: 506–514. doi: 10.1182/asheducation-2011.1.506 22160082

3. Ott G, Rosenwald A, Campo E (2013) Understanding MYC-driven aggressive B-cell lymphomas: pathogenesis and classification. Blood 122: 3884–3891. doi: 10.1182/blood-2013-05-498329 24009228

4. Valera A, Colomo L, Martinez A, de Jong D, Balague O, et al. (2013) ALK-positive large B-cell lymphomas express a terminal B-cell differentiation program and activated STAT3 but lack MYC rearrangements. Mod Pathol 26: 1329–1337. doi: 10.1038/modpathol.2013.73 23599149

5. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, et al. (1985) The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533–538. 3906410

6. Butzler C, Zou XG, Popov AV, Bruggemann M (1997) Rapid induction of B-cell lymphomas in mice carrying a human IgH/c-mycYAC. Oncogene 14: 1383–1388. 9178899

7. Cheung WC, Kim JS, Linden M, Peng L, Van Ness B, et al. (2004) Novel targeted deregulation of c-Myc cooperates with Bcl-XL to cause plasma cell neoplasms in mice. The Journal of Clinical Investigation 113: 1763–1773. 15199411

8. Kovalchuk AL, Qi C-F, Torrey TA, Taddesse-Heath L, Feigenbaum L, et al. (2000) Burkitt Lymphoma in the Mouse. The Journal of Experimental Medicine 192: 1183–1190. 11034608

9. Park SS, Kim JS, Tessarollo L, Owens JD, Peng L, et al. (2005) Insertion of c-Myc into Igh Induces B-Cell and Plasma-Cell Neoplasms in Mice. Cancer Research 65: 1306–1315. 15735016

10. Schmidt EV, Pattengale PK, Weir L, Leder P (1988) Transgenic mice bearing the human c-myc gene activated by an immunoglobulin enhancer: a pre-B-cell lymphoma model. Proceedings of the National Academy of Sciences 85: 6047–6051.

11. Suda Y, Aizawa S, Hirai S, Inoue T, Furuta Y, et al. (1987) DRIVEN BY THE SAME IG ENHANCER AND SV40-T PROMOTER RAS INDUCED LUNG ADENOMATOUS TUMORS, MYC INDUCED PRE-B CELL LYMPHOMAS AND SV40 LARGE T-GENE A VARIETY OF TUMORS IN TRANSGENIC MICE. EMBO Journal 6: 4055–4065. 2832150

12. Yukawa K, Kikutani H, Inomoto T, Uehira M, Bin SH, et al. (1989) Strain dependency of B and T lymphoma development in immunoglobulin heavy chain enhancer (E mu)-myc transgenic mice. The Journal of Experimental Medicine 170: 711–726. 2504875

13. Linden MA, Kirchhof N, Carlson CS, Van Ness BG (2012) Targeted overexpression of an activated N-ras gene results in B-cell and plasma cell lymphoproliferation and cooperates with c-myc to induce fatal B-cell neoplasia. Experimental Hematology 40: 216–227. doi: 10.1016/j.exphem.2011.11.006 22120021

14. Rutsch S, Neppalli VT, Shin D-M, DuBois W, Morse HC, et al. (2010) IL-6 and MYC collaborate in plasma cell tumor formation in mice. Blood 115: 1746–1754. doi: 10.1182/blood-2009-08-237941 20018915

15. Refaeli Y, Young RM, Turner BC, Duda J, Field KA, et al. (2008) The B cell antigen receptor and overexpression of MYC can cooperate in the genesis of B cell lymphomas. PLoS Biol 6: e152. doi: 10.1371/journal.pbio.0060152 18578569

16. Poe JC, Minard-Colin V, Kountikov EI, Haas KM, Tedder TF (2012) A c-Myc and Surface CD19 Signaling Amplification Loop Promotes B Cell Lymphoma Development and Progression in Mice. The Journal of Immunology 189: 2318–2325. doi: 10.4049/jimmunol.1201000 22826319

17. Tuveson D, Carter R, Soltoff S, Fearon D (1993) CD19 of B cells as a surrogate kinase insert region to bind phosphatidylinositol 3-kinase. Science 260: 986–989. 7684160

18. Sander S, Calado Dinis P, Srinivasan L, Köchert K, Zhang B, et al. (2012) Synergy between PI3K Signaling and MYC in Burkitt Lymphomagenesis. Cancer cell 22: 167–179. doi: 10.1016/j.ccr.2012.06.012 22897848

19. Carbone A, Vaccher E, Gloghini A, Pantanowitz L, Abayomi A, et al. (2014) Diagnosis and management of lymphomas and other cancers in HIV-infected patients. Nat Rev Clin Oncol 11: 223–238. doi: 10.1038/nrclinonc.2014.31 24614140

20. Du MQ, Diss TC, Liu HX, Ye HT, Hamoudi RA, et al. (2002) KSHV- and EBV-associated germinotropic lymphoproliferative disorder. Blood 100: 3415–3418. 12384445

21. Dupin N, Diss TL, Kellam P, Tulliez M, Du MQ, et al. (2000) HHV-8 is associated with a plasmablastic variant of Castleman disease that is linked to HHV-8-positive plasmablastic lymphoma. Blood 95: 1406–1412. 10666218

22. Ganem D (2010) KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. Journal of Clinical Investigation 120: 939–949. doi: 10.1172/JCI40567 20364091

23. Fakhari FD, Dittmer DP (2002) Charting latency transcripts in Kaposi's sarcoma-associated herpesvirus by whole-genome real-time quantitative PCR. J Virol 76: 6213–6223. 12021355

24. Marshall V, Parks T, Bagni R, Wang CD, Samols MA, et al. (2007) Conservation of Virally Encoded MicroRNAs in Kaposi Sarcoma-Associated Herpesvirus in Primary Effusion Lymphoma Cell Lines and in Patients with Kaposi Sarcoma or Multicentric Castleman Disease. Journal of Infectious Diseases 195: 645–659. 17262705

25. Dittmer DP (2003) Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays. Cancer Res 63: 2010–2015. 12727810

26. Fakhari FD, Jeong JH, Kanan Y, Dittmer DP (2006) The latency-associated nuclear antigen of Kaposi sarcoma-associated herpesvirus induces B cell hyperplasia and lymphoma. J Clin Invest 116: 735–742. 16498502

27. Jeong JH, Hines-Boykin R, Ash JD, Dittmer DP (2002) Tissue specificity of the Kaposi's sarcoma-associated herpesvirus latent nuclear antigen (LANA/orf73) promoter in transgenic mice. J Virol 76: 11024–11032. 12368345

28. Sin S-H, Fakhari FD, Dittmer DP (2010) The viral latency-associated nuclear antigen augments the B-cell response to antigen in vivo. J Virol 84: 10653–10660. doi: 10.1128/JVI.00848-10 20686032

29. Sin S-H, Dittmer DP (2013) Viral latency locus augments B-cell response in vivo to induce chronic marginal zone enlargement, plasma cell hyperplasia, and lymphoma. Blood 121: 2952–2963. doi: 10.1182/blood-2012-03-415620 23365457

30. Bubman D, Guasparri I, Cesarman E (2007) Deregulation of c-Myc in primary effusion lymphoma by Kaposi's sarcoma herpesvirus latency-associated nuclear antigen. Oncogene.

31. Liu J, Martin HJ, Liao G, Hayward SD (2007) The Kaposi's sarcoma-associated herpesvirus LANA protein stabilizes and activates c-Myc. J Virol 81: 10451–10459. 17634226

32. Lubyova B, Kellum MJ, Frisancho JA, Pitha PM (2007) Stimulation of c-Myc Transcriptional Activity by vIRF-3 of Kaposi Sarcoma-associated Herpesvirus. Journal of Biological Chemistry 282: 31944–31953. 17728244

33. Nador R, Cesarman E, Chadburn A, Dawson D, Ansari M, et al. (1996) Primary effusion lymphoma: a distinct clinicopathologic entity associated with the Kaposi's sarcoma-associated herpes virus. Blood 88: 645–656. 8695812

34. Ohno S, Babonits M, Wiener F, Spira J, Klein G, et al. (1979) Nonrandom chromosome changes involving the Ig gene-carrying chromosomes 12 and 6 in pristane-induced mouse plasmacytomas. Cell 18: 1001–1007. 519762

35. Pone EJ, Zhang J, Mai T, White CA, Li G, et al. (2012) BCR-signalling synergizes with TLR-signalling for induction of AID and immunoglobulin class-switching through the non-canonical NF-κB pathway. Nat Commun 3: 767. doi: 10.1038/ncomms1769 22473011

36. Kulow BF, Cualing H, Steele P, VanHorn J, Breneman JC (2002) Progression of cutaneous B-cell pseudolymphoma to cutaneous B-cell lymphoma. Journal of cutaneous medicine and surgery 6: 519–528. 12404039

37. Martorell M, Gaona Morales JJ, Garcia JA, Gutierrez Herrera JM, Gozalbo Grau F, et al. (2008) Transformation of vulvar pseudolymphoma (lymphoma-like lesion) into a marginal zone B-cell lymphoma of labium majus. Journal of Obstetrics & Gynaecology Research 34: 699–705.

38. Shelley WB, Wood M, Wilson JF, Goodman R (1981) Premalignant lymphoid hyperplasia: Preceding and coexisting with malignant lymphoma in the skin. Archives of Dermatology 117: 500–503. 6894840

39. Bubman D, Guasparri I, Cesarman E (2007) Deregulation of c-Myc in primary effusion lymphoma by Kaposi's sarcoma herpesvirus latency-associated nuclear antigen. Oncogene 26: 4979–4986. 17310999

40. Roy D, Sin S-H, Damania B, Dittmer DP (2011) Tumor suppressor genes FHIT and WWOX are deleted in primary effusion lymphoma (PEL) cell lines. Blood: doi: 10.1182/blood-2010-1112-323659

41. Luan SL, Boulanger E, Ye H, Chanudet E, Johnson N, et al. (2010) Primary effusion lymphoma: genomic profiling revealed amplification of SELPLG and CORO1C encoding for proteins important for cell migration. J Pathol 222: 166–179. doi: 10.1002/path.2752 20690162

42. Bhatt AP, Bhende PM, Sin S-H, Roy D, Dittmer DP, et al. (2010) Dual inhibition of PI3K and mTOR inhibits autocrine and paracrine proliferative loops in PI3K/Akt/mTOR-addicted lymphomas. Blood 115: 4455–4463. doi: 10.1182/blood-2009-10-251082 20299510

43. Yang D, Chen W, Xiong J, Sherrod CJ, Henry DH, et al. (2014) Interleukin 1 receptor-associated kinase 1 (IRAK1) mutation is a common, essential driver for Kaposi sarcoma herpesvirus lymphoma. Proceedings of the National Academy of Sciences.

44. Strasser A, Harris AW, Bath ML, Cory S (1990) Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 348: 331–333. 2250704

45. Dittmer DP (2014) Not like a wrecking ball: EBV fine-tunes MYC lymphomagenesis. Blood 123: 460–461. doi: 10.1182/blood-2013-11-537076 24458272

46. Khuda SE, Loo WM, Janz S, Van Ness B, Erickson LD (2008) Deregulation of c-Myc confers distinct survival requirements for memory B cells, plasma cells, and their progenitors. The Journal of Immunology 181: 7537–7549. 19017943

47. Li X, Chen S, Feng J, Deng H, Sun R (2010) Myc Is Required for the Maintenance of Kaposi's Sarcoma-Associated Herpesvirus Latency. Journal of Virology 84: 8945–8948. doi: 10.1128/JVI.00244-10 20573831

48. Rodrigues L, Popov N, Kaye KM, Simas JP (2013) Stabilization of Myc through Heterotypic Poly-Ubiquitination by mLANA Is Critical for γ-Herpesvirus Lymphoproliferation. PLoS Pathog 9: e1003554. doi: 10.1371/journal.ppat.1003554 23950719

49. Baresova P, Pitha PM, Lubyova B (2012) Kaposi Sarcoma-associated Herpesvirus vIRF-3 Protein Binds to F-box of Skp2 Protein and Acts as a Regulator of c-Myc Protein Function and Stability. Journal of Biological Chemistry 287: 16199–16208. doi: 10.1074/jbc.M111.335216 22453922

50. Ahmad A, Groshong JS, Matta H, Schamus S, Punj V, et al. (2010) Kaposi's sarcoma associated herpesvirus-encoded viral FLICE inhibitory protein (vFLIP) K13 cooperates with Myc to promote lymphoma in mice. Cancer Biology & Therapy 10: 1033–1040.

51. Graham C, Matta H, Yang Y, Yi H, Suo Y, et al. (2013) Kaposi's Sarcoma-Associated Herpesvirus Oncoprotein K13 Protects against B Cell Receptor-Induced Growth Arrest and Apoptosis through NF-κB Activation. Journal of Virology 87: 2242–2252. doi: 10.1128/JVI.01393-12 23236068

52. Bellare P, Dufresne A, Ganem D (2015) Inefficient codon usage impairs mRNA accumulation: the case of the v-FLIP gene of Kaposi's sarcoma-associated herpesvirus. Journal of Virology.

53. Choi J-K, Lee B-S, Shim SN, Li M, Jung JU (2000) Identification of the Novel K15 Gene at the Rightmost End of the Kaposi's Sarcoma-Associated Herpesvirus Genome. Journal of Virology 74: 436–446. 10590133

54. Lee H, Guo J, Li M, Choi J-K, DeMaria M, et al. (1998) Identification of an Immunoreceptor Tyrosine-Based Activation Motif of K1 Transforming Protein of Kaposi’s Sarcoma-Associated Herpesvirus. Molecular and Cellular Biology 18: 5219–5228. 9710606

55. Damania B, Li MT, Choi JK, Alexander L, Jung JU, et al. (1999) Identification of the R1 oncogene and its protein product from the rhadinovirus of rhesus monkeys. Journal of Virology 73: 5123–5131. 10233975

56. Glenn M, Rainbow L, Auradé F, Davison A, Schulz TF (1999) Identification of a Spliced Gene from Kaposi’s Sarcoma-Associated Herpesvirus Encoding a Protein with Similarities to Latent Membrane Proteins 1 and 2A of Epstein-Barr Virus. Journal of Virology 73: 6953–6963. 10400794

57. Lagunoff M, Majeti R, Weiss A, Ganem D (1999) Deregulated signal transduction by the K1 gene product of Kaposi’s sarcoma-associated herpesvirus. Proceedings of the National Academy of Sciences 96: 5704–5709.

58. Steinbrück L, Gustems M, Medele S, Schulz TF, Lutter D, et al. (2015) K1 and K15 of Kaposi sarcoma-associated herpes virus are partial functional homologues of latent membrane protein 2A of Epstein-Barr virus. Journal of Virology.

59. Niedobitek G, Agathanggelou A, Rowe M, Jones E, Jones D, et al. (1995) Heterogeneous expression of Epstein-Barr virus latent proteins in endemic Burkitt's lymphoma. Blood 86: 659–665. 7605996

60. Xia T, O'Hara A, Araujo I, Barreto J, Carvalho E, et al. (2008) EBV MicroRNAs in Primary Lymphomas and Targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Research 68: 1436–1442. doi: 10.1158/0008-5472.CAN-07-5126 18316607

61. Kennedy G, Komano J, Sugden B (2003) Epstein-Barr virus provides a survival factor to Burkitt's lymphomas. Proceedings of the National Academy of Sciences 100: 14269–14274.

62. Kang M-S, Lu H, Yasui T, Sharpe A, Warren H, et al. (2005) Epstein-Barr virus nuclear antigen 1 does not induce lymphoma in transgenic FVB mice. Proceedings of the National Academy of Sciences of the United States of America 102: 820–825. 15640350

63. Kang M-S, Soni V, Bronson R, Kieff E (2008) Epstein-Barr Virus Nuclear Antigen 1 Does Not Cause Lymphoma in C57BL/6J Mice. Journal of Virology 82: 4180–4183. doi: 10.1128/JVI.02596-07 18256159

64. Wilson JB, Bell JL, Levine AJ (1996) Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice. Embo Journal 15: 3117–3126. 8670812

65. Drotar ME, Silva S, Barone E, Campbell D, Tsimbouri P, et al. (2003) Epstein-Barr virus nuclear antigen-1 and Myc cooperate in lymphomagenesis. International Journal of Cancer 106: 388–395.

66. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9: 671–675.

67. Allred DC, Harvey JM, Berardo M, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Modern Pathology 11: 155–168. 9504686