A Multifactorial Role for Malaria in Endemic Burkitt's Lymphoma Pathogenesis

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Endemic Burkitt's lymphoma (eBL) is a common tumor of young children in tropical Africa that is closely linked geographically with P. falciparum malaria. This association was noted more than 50 years ago. Since then we have learned that eBL contains the oncogenic herpes virus Epstein-Barr virus and a defining translocation that activates the c-myc oncogene. However the link to malaria has never been explained. Here we show that malaria has multiple effects that all focus on germinal center (GC) B cells that are known to be the origin of eBL. Together these effects of malaria act synergistically to dramatically increase the risk of developing eBL in individuals infected with the parasite. Clinical interventions that lessen the impact of malaria on GC B cells should dramatically decrease the incidence eBL.

Vyšlo v časopise: A Multifactorial Role for Malaria in Endemic Burkitt's Lymphoma Pathogenesis. PLoS Pathog 10(5): e32767. doi:10.1371/journal.ppat.1004170
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004170

Souhrn

Zdroje

1. GoldsteinJA, BernsteinRL (1990) Burkitt's lymphoma and the role of Epstein-Barr virus. J Trop Pediatr 36: 114–120.

2. KleinU, Dalla-FaveraR (2008) Germinal centres: role in B-cell physiology and malignancy. Nat Rev Immunol 8: 22–33.

3. VictoraGD, Dominguez-SolaD, HolmesAB, DeroubaixS, Dalla-FaveraR, et al. (2012) Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood 120: 2240–2248.

4. KleinG (1983) Specific chromosomal translocations and the genesis of B-cell-derived tumors in mice and men. Cell 32: 311–315.

5. Leder P (1985) Translocations among antibody genes in human cancer. In: Lenoir GM, O'Conor GT, Olweny CLM, editors. Burkitt's Lymphoma: a human cancer model. New York: Oxford University Press. pp. 341–371.

6. ManolovG, ManolovaY (1972) Marker band in one chromosome 14 from Burkitt lymphomas. Nature 237: 33–34.

7. RamiroAR, JankovicM, CallenE, DifilippantonioS, ChenHT, et al. (2006) Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440: 105–109.

8. RamiroAR, JankovicM, EisenreichT, DifilippantonioS, Chen-KiangS, et al. (2004) AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118: 431–438.

9. RobbianiDF, BothmerA, CallenE, Reina-San-MartinB, DorsettY, et al. (2008) AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135: 1028–1038.

10. MuramatsuM, KinoshitaK, FagarasanS, YamadaS, ShinkaiY, et al. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553–563.

11. BurkittD (1962) A children's cancer dependent on climatic factors. Nature 194: 232–234.

12. Morrow RH, Jr. (1985) Epidemiological evidence for the role of falciparum malaria in the pathogenesis of Burkitt's lymphoma. IARC Sci Publ: 177–186.

13. Kieff E, Rickinson AB (2007) Epstein-Barr Virus and Its Replication. In: Knipe DM, Howley PM, editors. Fields Virology. 5th ed. Philadelphia: Lippincott Williams & Wilkins. pp. 2603–2654.

14. Thorley-LawsonDA, GrossA (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350: 1328–1337.

15. BabcockGJ, DeckerLL, VolkM, Thorley-LawsonDA (1998) EBV persistence in memory B cells in vivo. Immunity 9: 395–404.

16. Thorley-LawsonDA (2001) Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75–82.

17. BabcockGJ, HochbergD, Thorley-LawsonAD (2000) The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell. Immunity 13: 497–506.

18. RoughanJE, Thorley-LawsonDA (2009) The intersection of Epstein-Barr virus with the germinal center. J Virol 83: 3968–3976.

19. PaschosK, ParkerGA, WatanatanasupE, WhiteRE, AlldayMJ (2012) BIM promoter directly targeted by EBNA3C in polycomb-mediated repression by EBV. Nucleic Acids Res 40: 7233–7246.

20. VereideDT, SetoE, ChiuYF, HayesM, TagawaT, et al. (2013) Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene 33: 1258–1264.

21. Westhoff SmithD, SugdenB (2013) Potential cellular functions of Epstein-Barr Nuclear Antigen 1 (EBNA1) of Epstein-Barr Virus. Viruses 5: 226–240.

22. Thorley-LawsonDA, AlldayMJ (2008) The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 6: 913–924.

23. HochbergD, MiddeldorpJM, CatalinaM, SullivanJL, LuzuriagaK, et al. (2004) Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc Natl Acad Sci U S A 101: 239–244.

24. MoormannAM, ChelimoK, SumbaPO, TischDJ, RochfordR, et al. (2007) Exposure to holoendemic malaria results in suppression of Epstein-Barr virus-specific T cell immunosurveillance in Kenyan children. J Infect Dis 195: 799–808.

25. MoormannAM, ChelimoK, SumbaOP, LutzkeML, Ploutz-SnyderR, et al. (2005) Exposure to holoendemic malaria results in elevated Epstein-Barr virus loads in children. J Infect Dis 191: 1233–1238.

26. RastiN, FalkKI, DonatiD, GyanBA, GokaBQ, et al. (2005) Circulating epstein-barr virus in children living in malaria-endemic areas. Scand J Immunol 61: 461–465.

27. BabcockGJ, DeckerLL, FreemanRB, Thorley-LawsonDA (1999) Epstein-barr virus-infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J Exp Med 190: 567–576.

28. HopwoodP, CrawfordDH (2000) The role of EBV in post-transplant malignancies: a review. J Clin Pathol 53: 248–254.

29. XuZ, PoneEJ, Al-QahtaniA, ParkSR, ZanH, et al. (2007) Regulation of aicda expression and AID activity: relevance to somatic hypermutation and class switch DNA recombination. Crit Rev Immunol 27: 367–397.

30. AreseP, SchwarzerE (1997) Malarial pigment (haemozoin): a very active ‘inert’ substance. Ann Trop Med Parasitol 91: 501–516.

31. CobanC, IshiiKJ, KawaiT, HemmiH, SatoS, et al. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201: 19–25.

32. ParrocheP, LauwFN, GoutagnyN, LatzE, MonksBG, et al. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A 104: 1919–1924.

33. SmitLA, BendeRJ, AtenJ, GuikemaJE, AartsWM, et al. (2003) Expression of activation-induced cytidine deaminase is confined to B-cell non-Hodgkin's lymphomas of germinal-center phenotype. Cancer Res 63: 3894–3898.

34. CutronaG, DonoM, PastorinoS, UliviM, BurgioVL, et al. (1997) The propensity to apoptosis of centrocytes and centroblasts correlates with elevated levels of intracellular myc protein. Eur J Immunol 27: 234–238.

35. Dominguez-SolaD, VictoraGD, YingCY, PhanRT, SaitoM, et al. (2012) The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol 13: 1083–1091.

36. KleinU, TuY, StolovitzkyGA, KellerJL, HaddadJJr, et al. (2003) Transcriptional analysis of the B cell germinal center reaction. Proc Natl Acad Sci U S A 100: 2639–2644.

37. Martinez-ValdezH, GuretC, de BouteillerO, FugierI, BanchereauJ, et al. (1996) Human germinal center B cells express the apoptosis-inducing genes Fas, c-myc, P53, and Bax but not the survival gene bcl-2. J Exp Med 183: 971–977.

38. LiuYJ, ArpinC (1997) Germinal center development. Immunol Rev 156: 111–126.

39. MacLennanIC (1994) Germinal centers. Annu Rev Immunol 12: 117–139.

40. AllenCD, OkadaT, TangHL, CysterJG (2007) Imaging of germinal center selection events during affinity maturation. Science 315: 528–531.

41. VictoraGD, SchwickertTA, FooksmanDR, KamphorstAO, Meyer-HermannM, et al. (2010) Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143: 592–605.

42. EpeldeguiM, HungYP, McQuayA, AmbinderRF, Martinez-MazaO (2007) Infection of human B cells with Epstein-Barr virus results in the expression of somatic hypermutation-inducing molecules and in the accrual of oncogene mutations. Mol Immunol 44: 934–942.

43. HeathE, Begue-PastorN, ChagantiS, Croom-CarterD, Shannon-LoweC, et al. (2012) Epstein-Barr virus infection of naive B cells in vitro frequently selects clones with mutated immunoglobulin genotypes: implications for virus biology. PLoS Pathog 8: e1002697.

44. HeB, Raab-TraubN, CasaliP, CeruttiA (2003) EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J Immunol 171: 5215–5224.

45. SmithJD, ChitnisCE, CraigAG, RobertsDJ, Hudson-TaylorDE, et al. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101–110.

46. DonatiD, ZhangLP, CheneA, ChenQ, FlickK, et al. (2004) Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect Immun 72: 5412–5418.

47. GriffithJW, SunT, McIntoshMT, BucalaR (2009) Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208–5220.

48. JaramilloM, BellemareMJ, MartelC, ShioMT, ContrerasAP, et al. (2009) Synthetic Plasmodium-like hemozoin activates the immune response: a morphology - function study. PLoS One 4: e6957.

49. RoughanJE, TorgborC, Thorley-LawsonDA (2010) Germinal center B cells latently infected with Epstein-Barr virus proliferate extensively but do not increase in number. J Virol 84: 1158–1168.

50. GrossAJ, HochbergD, RandWM, Thorley-LawsonDA (2005) EBV and systemic lupus erythematosus: a new perspective. J Immunol 174: 6599–6607.

51. HoM, WebsterHK, LooareesuwanS, SupanaranondW, PhillipsRE, et al. (1986) Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J Infect Dis 153: 763–771.

52. HadinotoV, ShapiroM, GreenoughTC, SullivanJL, LuzuriagaK, et al. (2008) On the dynamics of acute EBV infection and the pathogenesis of infectious mononucleosis. Blood 111: 1420–1427.

53. TragerW, JensenJB (1976) Human malaria parasites in continuous culture. Science 193: 673–675.

54. HornungV, BauernfeindF, HalleA, SamstadEO, KonoH, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847–856.