Endemic Burkitt lymphoma - an aggressive childhood cancer linked to Plasmodium falciparum exposure, but not to exposure to other malaria parasites.


Journal

APMIS : acta pathologica, microbiologica, et immunologica Scandinavica
ISSN: 1600-0463
Titre abrégé: APMIS
Pays: Denmark
ID NLM: 8803400

Informations de publication

Date de publication:
Feb 2020
Historique:
received: 29 10 2019
accepted: 02 12 2019
pubmed: 7 3 2020
medline: 10 5 2020
entrez: 6 3 2020
Statut: ppublish

Résumé

Burkitt lymphoma (BL) is an aggressive non-Hodgkin lymphoma. The prevalence of BL is ten-fold higher in areas with stable transmission of Plasmodium falciparum malaria, where it is the most common childhood cancer, and is referred to as endemic BL (eBL). In addition to its association with exposure to P. falciparum infection, eBL is strongly associated with Epstein-Barr virus (EBV) infection (>90%). This is in contrast to BL as it occurs outside P. falciparum-endemic areas (sporadic BL), where only a minority of the tumours are EBV-positive. Although the striking geographical overlap in the distribution of eBL and P. falciparum was noted shortly after the first detailed description of eBL in 1958, the molecular details of the interaction between malaria and eBL remain unresolved. It is furthermore unexplained why exposure to P. falciparum appears to be essentially a prerequisite to the development of eBL, whereas other types of malaria parasites that infect humans have no impact. In this brief review, we summarize how malaria exposure may precipitate the malignant transformation of a B-cell clone that leads to eBL, and propose an explanation for why P. falciparum uniquely has this capacity.

Identifiants

pubmed: 32133709
doi: 10.1111/apm.13018
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

129-135

Informations de copyright

© 2020 APMIS. Published by John Wiley & Sons Ltd.

Références

Hämmerl L, Colombet M, Rochford R, Ogwang DM, Parkin DM. The burden of Burkitt lymphoma in Africa. Infect Agent Cancer 2019;14:17.
Dozzo M, Carobolante F, Donisi PM, Scattolin A, Maino E, Sancetta R, et al. Burkitt lymphoma in adolescents and young adults: management challenges. Adolesc Health Med Ther 2017;8:11-29.
Moormann AM, Skiles JL, Otieno JA, Buckle GC, Vik TA. Optimal management of endemic Burkitt lymphoma: a holistic approach mindful of limited resources. Blood Lymphat Cancer 2014;4:91-9.
Howard SC, Metzger ML, Wilimas JA, Quintana Y, Pui CH, Robison LL, et al. Childhood cancer epidemiology in low-income countries. Cancer 2008;112:461-72.
Njuguna F, Mostert S, Slot A, Langat S, Skiles J, Sitaresmi MN, et al. Abandonment of childhood cancer treatment in Western Kenya. Arch Dis Child 2014;99:609-14.
Pui CH, Schrappe M, Masera G, Nachman J, Gadner H, Eden OB, et al. Ponte di Legno Working Group: statement on the right of children with leukemia to have full access to essential treatment and report on the Sixth International Childhood Acute Lymphoblastic Leukemia Workshop. Leukemia 2004;18:1043-53.
Burkitt D. A sarcoma involving the jaws in African children. Br J Surg 1958;46:218-23.
O'Conor GT, Davies JN. Malignant tumors in African children. With special reference to malignant lymphoma. J Pediatr 1960;56:526-35.
Burkitt D. A children's cancer dependent on climatic factors. Nature 1962;194:232-4.
Burkitt DP. Observations on the geography of malignant lymphoma. East Afr Med J 1961;38:511-4.
Epstein MA, Achong BG, Barr YM. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1964;1:702-3.
de-Thé G, Geser A, Day NE, Tukei PM, Williams EH, Beri DP, et al. Epidemiological evidence for causal relationship between Epstein-Barr virus and Burkitt's lymphoma from Ugandan prospective study. Nature 1978;274:756-61.
zur Hausen H, Schulte-Holthausen H, Klein G, Henle W, Henle G, Clifford P,, et al. EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature 1970;228:1056-8.
Thorley-Lawson DA, Allday MJ. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 2008;6:913-24.
Dalldorf G, Linsell CA, Barnhart FE, Martyn R. An epidemiological approach to the lymphomas of African children and Burkitt's sarcoma of the jaws. Perspect Biol Med 1964;7:435-49.
Edington GM, MacLean CM, Okubadejo OA.One-hundred one necropsies on tumours of the reticulo-endothelial system in Ibadan, Nigeria, with special reference to childhood lymphosarcoma, The lymphoreticular tumours in Africa, Karger, Basel, 1964, pp. 236-52.
Burkitt DP. Etiology of Burkitt's lymphoma - an alternative hypothesis to a vectored virus. J Natl Cancer Inst 1969;42:19-28.
ten Seldam RE, Cooke R, Atkinson L. Childhood lymphoma in the territories of Papua and New Guinea. Cancer 1966;19:437-46.
Rowe NH, Johnson CM. A search for the Burkitt lymphoma in tropical Central America. Br J Cancer 1964;18:228-32.
Pramanik R, Paral CC, Ghosh A. Pattern of solid malignant tumours in children - a ten-year study. J Indian Med Assoc 1997;95:107-8.
Geser A, Brubaker G, Draper CC. Effect of a malaria suppression program on the incidence of African Burkitt's lymphoma. Am J Epidemiol 1989;129:740-52.
Moormann AM, Snider CJ, Chelimo K. The company malaria keeps: how co-infection with Epstein-Barr virus leads to endemic Burkitt lymphoma. Curr Opin Infect Dis 2011;24:435-41.
Moormann AM, Bailey JA. Malaria - how this parasitic infection aids and abets EBV-associated Burkitt lymphomagenesis. Curr Opin Virol 2016;20:78-84.
O'Reilly RJ, Small TN, Papadopoulos E, Lucas K, Lacerda J, Koulova L. Biology and adoptive cell therapy of Epstein-Barr virus-associated lymphoproliferative disorders in recipients of marrow allografts. Immunol Rev 1997;157:195-216.
Forconi CS, Cosgrove CP, Saikumar-Lakshmi P, Nixon CE, Foley J, Ong'echa JM, et al. Poorly cytotoxic terminally differentiated CD56negCD16pos NK cells accumulate in Kenyan children with Burkitt lymphomas. Blood Adv 2018;2:1101-14.
Whittle HC, Brown J, Marsh K, Greenwood BM, Seidelin P, Tighe H, et al. T-cell control of Epstein-Barr virus-infected B cells is lost during P. falciparum malaria. Nature 1984;312:449-50.
Gunapala DE, Facer CA, Davidson R, Weir WRC. In vitro analysis of Epstein-Barr virus: host balance in patients with acute Plasmodium falciparum malaria. Parasitol Res 1990;76:531-5.
Moormann AM, Chelimo K, Sumba PO, Tisch DJ, Rochford R, Kazura JW. Exposure to holoendemic malaria results in suppression of Epstein-Barr virus-specific T cell immunosurveillance in Kenyan children. J Infect Dis 2007;195:799-808.
Falanga YT, Frascoli M, Kaymaz Y, Forconi C, Ong'echa JM, Bailey JA, et al. High pathogen burden in childhood promotes the development of unconventional innate-like CD8+ T cells. JCI Insight 2017;2.
Njie R, Bell AI, Jia H, Croom-Carter D, Chaganti S, Hislop AD, et al. The effects of acute malaria on Epstein-Barr virus (EBV) load and EBV-specific T cell immunity in Gambian children. J Infect Dis 2009;199:31-8.
Moormann AM, Chelimo K, Sumba OP, Lutzke ML, Ploutz-Snyder R, Newton D, et al. Exposure to holoendemic malaria results in elevated Epstein-Barr virus loads in children. J Infect Dis 2005;191:1233-8.
Rasti N, Falk KI, Donati D, Gyan BA, Goka BQ, Troye-Blomberg M, et al. Circulating Epstein-Barr virus in children living in malaria-endemic areas. Scand J Immunol 2005;61:461-5.
Robbiani DF, Deroubaix S, Feldhahn N, Oliveira TY, Callen E, Wang Q, et al. Plasmodium infection promotes genomic instability and AID-dependent B cell lymphoma. Cell 2015;162:727-37.
Kalchschmidt JS, Bashford-Rogers R, Paschos K, Gillman AC, Styles CT, Kellam P, et al. Epstein-Barr virus nuclear protein EBNA3C directly induces expression of AID and somatic mutations in B cells. J Exp Med 2016;213:921-8.
Cohen S, McGregor IA, Carrington S. Gammaglobulin and acquired immunity to human malaria. Nature 1961;192:733-7.
Rowe DS, McGregor IA, Smith SJ, Hall P, Williams K. Plasma immunoglobulin concentrations in a West African (Gambian) community and in a group of healthy British adults. Clin Exp Immunol 1968;3:63-79.
Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000;102:553-63.
Wilmore JR, Asito AS, Wei C, Piriou E, Sumba PO, Sanz I, et al. AID expression in peripheral blood of children living in a malaria holoendemic region is associated with changes in B cell subsets and Epstein-Barr virus. Int J Cancer 2015;136:1371-80.
Torgbor C, Awuah P, Deitsch K, Kalantari P, Duca KA, Thorley-Lawson DA. A multifactorial role for P. falciparum malaria in endemic Burkitt's lymphoma pathogenesis. PLoS Pathog 2014;10:e1004170.
Mechtcheriakova D, Svoboda M, Meshcheryakova A, Jensen-Jarolim E. Activation-induced cytidine deaminase (AID) linking immunity, chronic inflammation, and cancer. Cancer Immunol Immunother 2012;61:1591-8.
Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer 2013;13:759-71.
Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, Muramatsu M, et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 2004;118:431-8.
Hommel M, David PH, Oligino LD. Surface alterations of erythrocytes in Plasmodium falciparum malaria. Antigenic variation, antigenic diversity, and the role of the spleen. J Exp Med 1983;157:1137-48.
Jensen AR, Adams Y, Hviid L. Cerebral Plasmodium falciparum malaria: The role of PfEMP1 in its pathogenesis and immunity, and PfEMP1-based vaccines to prevent it. Immunol Rev 2019.
Hviid L, Jensen AT. PfEMP1 - A parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Adv Parasitol 2015;88:51-84.
Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JE, Avril M, et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 2013;498:502-5.
Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K. Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 1989;341:57-9.
Chen Q, Heddini A, Barragan A, Fernandez V, Pearce SF, Wahlgren M. The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. J Exp Med 2000;192:1-10.
Lennartz F, Adams Y, Bengtsson A, Olsen RW, Turner L, Ndam NT, et al. Structure-guided identification of a family of dual receptor-binding PfEMP1 that is associated with cerebral malaria. Cell Host Microbe 2017;21:403-14.
Frech C, Chen N. Genome comparison of human and non-human malaria parasites reveals species subset-specific genes potentially linked to human disease. PLoS Comput Biol 2011;7:e1002320.
Donati D, Zhang LP, Chene A, Cheng Q, Flick K, Nystrom M, et al. Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect Immun 2004;72:5412-8.
Chene A, Donati D, Guerreiro-Cacais AO, Levitsky V, Chen Q, Falk KI, et al. A molecular link between malaria and Epstein-Barr virus reactivation. PLoS Pathog 2007;3:e80.
Simone O, Bejarano MT, Pierce SK, Antonaci S, Wahlgren M, Troye-Blomberg M, et al. TLRs innate immunereceptors and Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) CIDR1a-driven human polyclonal B-cell activation. Acta Trop 2011;119:144-50.
Donati D, Mok B, Chene A, Xu H, Thangarajh M, Glas R, et al. Increased B cell survival and preferential activation of the memory compartment by a malaria polyclonal B cell activator. J Immunol 2006;177:3035-44.
Osunkoya BO, McFarlane H, Luzzatto L, Udeozo IO, Mottram FC, Williams AI, et al. Immunoglobin synthesis by fresh biopsy cells and established cell lines from Burkitt's lymphoma. Immunology 1968;14:851-60.
Nkrumah FK, Sulzer AJ, Maddison SE. Serum immunoglobulin levels and malaria antibodies in Burkitt's lymphoma. Trans R Soc Trop Med Hyg 1979;73:91-5.
Aka P, Vila MC, Jariwala A, Nkrumah F, Emmanuel B, Yagi M, et al. Endemic Burkitt lymphoma is associated with strength and diversity of Plasmodium falciparum malaria stage-specific antigen antibody response. Blood 2013;122:629-35.
Asito AS, Piriou E, Odada PS, Fiore N, Middeldorp JM, Long C, et al. Elevated anti-Zta IgG levels and EBV viral load are associated with site of tumor presentation in endemic Burkitt's lymphoma patients: a case control study. Infect Agent Cancer 2010;5:13.
Derkach A, Otim I, Pfeiffer RM, Onabajo OO, Legason ID, Nabalende H, et al. Associations between IgG reactivity to Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) antigens and Burkitt lymphoma in Ghana and Uganda case-control studies. EBioMedicine 2019;39:358-68.
Hviid L. Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop 2005;95:270-5.
Burkitt D, Wright D. Geographical and tribal distribution of the African lymphoma in Uganda. Br Med J 1966;1:569-73.
Cham CK, Turner L, Lusingu J, Vestergaard L, Mmbando B, Kurtis JD, et al. Sequential, ordered acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 domains. J Immunol 2009;183:3356-63.
Cham GK, Turner L, Kurtis JD, Mutabingwa T, Fried M, Jensen AT, et al. Hierarchical, domain type-specific acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 in Tanzanian children. Infect Immun 2010;78:4653-9.
Jensen ATR, Magistrado PA, Sharp S, Joergensen L, Lavstsen T, Chiucchiuini A, et al. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by Group A var genes. J Exp Med 2004;199:1179-90.
Bull PC, Kortok M, Kai O, Ndungu F, Ross A, Lowe BS, et al. Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. J Infect Dis 2000;182:252-9.
Bull PC, Marsh K. The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Trends Microbiol 2002;10:55-8.
Nielsen MA, Staalsoe T, Kurtzhals JAL, Goka BQ, Dodoo D, Alifrangis M, et al. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and non-severe malaria and is modified by acquired immunity. J Immunol 2002;168:3444-50.
Lavstsen T, Magistrado P, Hermsen CC, Salanti A, Jensen ATR, Sauerwein R, et al. Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar J 2005;4:21.
Bull PC, Pain A, Ndungu FM, Kinyanjui SM, Roberts DJ, Newbold CI, et al. Plasmodium falciparum antigenic variation: relationships between in vivo selection, acquired antibody response, and disease severity. J Infect Dis 2005;192:1119-26.
Staalsoe T, Hamad AA, Hviid L, Elhassan IM, Arnot DE, Theander TG. In vivo switching between variant surface antigens in human Plasmodium falciparum infection. J Infect Dis 2002;186:719-22.
Matzinger P. The danger model: a renewed sense of self. Science 2002;296:301-5.
Theunissen C, Janssens P, Demulder A, Nouboussie D, Van-Esbroeck M, Van-Gompel A, et al. Falciparum malaria in patient 9 years after leaving malaria-endemic area. Emerg Infect Dis 2009;15:115-6.
Vantomme B, Van Acker J, Rogge S, Ommeslag D, Donck J, Callens S. Plasmodium falciparum malaria occurring four years after leaving an endemic area. Acta Clin Belg 2016;71:111-3.
Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, et al. "Asymptomatic" malaria: a chronic and debilitating infection that should be treated. PLoS Medicine 2016;13:e1001942.
Karimi P, Birmann BM, Anderson LA, McShane CM, Gadalla SM, Sampson JN, et al. Risk factors for Burkitt lymphoma: a nested case-control study in the UK Clinical Practice Research Datalink. Br J Haematol 2018;181:505-14.
Piel FB, Hay SI, Gupta S, Weatherall DJ, Williams TN. Global burden of sickle cell anaemia in children under five, 2010-2050: modelling based on demographics, excess mortality, and interventions. PLoS Medicine 2013;10:e1001484.
Allison AC. Protection afforded by sickle cell trait against subtertian malarial infection. Br Med J 1954;1:290-3.
Williams AO. Haemoglobin genotypes, ABO blood groups, and Burkitt's tumour. J Med Genet 1966;3:177-9.
Pike MC, Morrow RH, Kisuule A, Mafigiri J. Burkitt's lymphoma and sickle cell trait. Br J Prev Soc Med 1970;24:39-41.
Nkrumah FK, Perkins IV. Sickle cell trait, hemoglobin C trait, and Burkitt's lymphoma. Am J Trop Med Hyg 1976;25:633-6.
Mulama DH, Bailey JA, Foley J, Chelimo K, Ouma C, Jura WG, et al. Sickle cell trait is not associated with endemic Burkitt lymphoma: an ethnicity and malaria endemicity-matched case-control study suggests factors controlling EBV may serve as a predictive biomarker for this pediatric cancer. Int J Cancer 2014;134:645-53.
Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, et al. An immune basis for malaria protection by the sickle cell trait. PLoS Medicine 2005;2:e128.
Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, et al. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis 2005;192:178-86.
Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg 1989;83:293-303.

Auteurs

Maria Del Pilar Quintana (MDP)

Centre for Medical Parasitology at Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Cecilia Smith-Togobo (C)

Centre for Medical Parasitology at Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
Department of Biochemistry, Cell and Molecular Biology, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana.

Ann Moormann (A)

Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA, USA.

Lars Hviid (L)

Centre for Medical Parasitology at Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
Department of Infectious Diseases, Rigshospitalet, Copenhagen, Denmark.

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