Intestinal Microbiota and Lymphoma
DOI:
https://doi.org/10.6000/1929-5634.2016.05.02.2Keywords:
Lymphoma, intestinal microbiota, cancer, bacteriaAbstract
The intestinal microbiota and gut immune system must constantly communicate to maintain a balance between tolerance and activation: on one hand, our immune system should protect us from pathogenic microbes and on the other hand, most of the millions of microbes in and on our body are innocuous symbionts and some can even be beneficial. Since there is such a close interaction between the immune system and the intestinal microbiota, it is not surprising that some lymphomas such as mucosal-associated lymphoid tissue (MALT) lymphoma have been shown to be caused by the presence of certain bacteria. Animal models played an important role in establishing causation and mechanism of bacteria-induced MALT lymphoma. In this review we discuss different ways that animal models have been applied to establish a link between the gut microbiota and lymphoma and how animal models have helped to elucidate mechanisms of microbiota-induced lymphoma. While there are not a plethora of studies demonstrating a connection between microbiota and lymphoma development, we believe that animal models are a system which can be exploited in the future to enhance our understanding of causation and improve prognosis and treatment of lymphoma.
References
Compare D, Nardone G. Contribution of gut microbiota to colonic and extracolonic cancer development. Dig Dis 2011; 29(6): 554-561. http://dx.doi.org/10.1159/000332967
Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal mucosal inflammation leads to systemic genotoxicity in mice. Cancer Res 2009; 69(11): 4827-4834. http://dx.doi.org/10.1158/0008-5472.CAN-08-4416
Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal inflammation induces genotoxicity to extraintestinal tissues and cell types in mice. Int J Cancer 2011; 129(8): 1815-1825. http://dx.doi.org/10.1002/ijc.26146
Umesaki Y, Setoyama H. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect 2000; 2(11): 1343-1351. http://dx.doi.org/10.1016/S1286-4579(00)01288-0
Tlaskalova-Hogenova H, Stepankova R, Kozakova H, et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol 2011; 8(2): 110-120. http://dx.doi.org/10.1038/cmi.2010.67
Faith JJ, Rey FE, O'Donnell D, et al. Creating and characterizing communities of human gut microbes in gnotobiotic mice. ISME J 2010; 4(9): 1094-1098. http://dx.doi.org/10.1038/ismej.2010.110
Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 2004; 101(44): 15718-15723. http://dx.doi.org/10.1073/pnas.0407076101
Yi P, Li L. The germfree murine animal: an important animal model for research on the relationship between gut microbiota and the host. Vet Microbiol 2012; 157(1-2): 1-7. http://dx.doi.org/10.1016/j.vetmic.2011.10.024
Bultman SJ. Emerging roles of the microbiome in cancer. Carcinogenesis 2014; 35(2): 249-255. http://dx.doi.org/10.1093/carcin/bgt392
Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338(6103): 120-123. http://dx.doi.org/10.1126/science.1224820
Iliev ID, Funari VA, Taylor KD, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 2012; 336(6086): 1314-1317. http://dx.doi.org/10.1126/science.1221789
Chassaing B, Aitken JD, Gewirtz AT, Vijay-Kumar M. Gut microbiota drives metabolic disease in immunologically altered mice. Adv Immunol 2012; 116: 93-112. http://dx.doi.org/10.1016/B978-0-12-394300-2.00003-X
Erdman SE, Poutahidis T, Tomczak M, et al. CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 2003; 162(2): 691-702. http://dx.doi.org/10.1016/S0002-9440(10)63863-1
Haseman JK, Hailey JR, Morris RW. Spontaneous neoplasm incidences in Fischer 344 rats and B6C3F1 mice in two-year carcinogenicity studies: a National Toxicology Program update. Toxicol Pathol 1998; 26(3): 428-441. http://dx.doi.org/10.1177/019262339802600318
Haseman JK, Huff JE, Rao GN, Eustis SL. Sources of variability in rodent carcinogenicity studies. Fundam Appl Toxicol 1989; 12(4): 793-804. http://dx.doi.org/10.1016/0272-0590(89)90011-0
Rao GN, Haseman JK, Grumbein S, Crawford DD, Eustis SL. Growth, body weight, survival, and tumor trends in F344/N rats during an eleven-year period. Toxicol Pathol 1990; 18(1 Pt 1): 61-70. http://dx.doi.org/10.1177/019262339001800109
Walburg HE, Jr., Cosgrove GE, Upton AC. Influence of microbial environment on development of myeloid leukemia in x-irradiated RFM mice. Int J Cancer 1968; 3(1): 150-154. http://dx.doi.org/10.1002/ijc.2910030118
Reliene R, Schiestl RH. Differences in animal housing facilities and diet may affect study outcomes-a plea for inclusion of such information in publications. DNA Repair (Amst) 2006; 5(6): 651-653. http://dx.doi.org/10.1016/j.dnarep.2006.02.001
Fanning SL, Appel MY, Berger SA, Korngold R, Friedman TM. The immunological impact of genetic drift in the B10.BR congenic inbred mouse strain. J Immunol 2009; 183(7): 4261-4272. http://dx.doi.org/10.4049/jimmunol.0900971
Stevens JC, Banks GT, Festing MF, Fisher EM. Quiet mutations in inbred strains of mice. Trends Mol Med 2007; 13(12): 512-519. http://dx.doi.org/10.1016/j.molmed.2007.10.001
Rao GN, Crockett PW. Effect of diet and housing on growth, body weight, survival and tumor incidences of B6C3F1 mice in chronic studies. Toxicol Pathol 2003; 31(2): 243-250. http://dx.doi.org/10.1080/01926230390183742
Bleich A, Hansen AK. Time to include the gut microbiota in the hygienic standardisation of laboratory rodents. Comp Immunol Microbiol Infect Dis 2012; 35(2): 81-92. http://dx.doi.org/10.1016/j.cimid.2011.12.006
Yamamoto ML, Maier I, Dang AT, et al. Intestinal bacteria modify lymphoma incidence and latency by affecting systemic inflammatory state, oxidative stress, and leukocyte genotoxicity. Cancer Res 2013; 73(14): 4222-4232. http://dx.doi.org/10.1158/0008-5472.CAN-13-0022
Saito Y, Suzuki H, Tsugawa H, et al. Overexpression of miR-142-5p and miR-155 in gastric mucosa-associated lymphoid tissue (MALT) lymphoma resistant to Helicobacter pylori eradication. PLoS One 2012; 7(11): e47396. http://dx.doi.org/10.1371/journal.pone.0047396
Isaacson PG, Du MQ. MALT lymphoma: from morphology to molecules. Nat Rev Cancer 2004; 4(8): 644-653. http://dx.doi.org/10.1038/nrc1409
Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 1991; 338(8776): 1175-1176. http://dx.doi.org/10.1016/0140-6736(91)92035-Z
Bayerdorffer E, Neubauer A, Rudolph B, et al. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of Helicobacter pylori infection. MALT Lymphoma Study Group. Lancet 1995; 345(8965): 1591-1594. http://dx.doi.org/10.1016/S0140-6736(95)90113-2
Enno A, O'Rourke JL, Howlett CR, Jack A, Dixon MF, Lee A. MALToma-like lesions in the murine gastric mucosa after long-term infection with Helicobacter felis. A mouse model of Helicobacter pylori-induced gastric lymphoma. Am J Pathol 1995; 147(1): 217-222.
Hirayama F, Takagi S, Kusuhara H, Iwao E, Yokoyama Y, Ikeda Y. Induction of gastric ulcer and intestinal metaplasia in mongolian gerbils infected with Helicobacter pylori. J Gastroenterol 1996; 31(5): 755-757. http://dx.doi.org/10.1007/BF02347631
Mueller A, O'Rourke J, Grimm J, et al. Distinct gene expression profiles characterize the histopathological stages of disease in Helicobacter-induced mucosa-associated lymphoid tissue lymphoma. Proc Natl Acad Sci U S A 2003; 100(3): 1292-1297. http://dx.doi.org/10.1073/pnas.242741699
O'Rourke JL. Gene expression profiling in Helicobacter-induced MALT lymphoma with reference to antigen drive and protective immunization. J Gastroenterol Hepatol 2008; 23(Suppl 2): S151-156. http://dx.doi.org/10.1111/j.1440-1746.2008.05553.x
Suzuki A, Kobayashi M, Matsuda K, et al. Induction of high endothelial venule-like vessels expressing GlcNAc6ST-1-mediated L-selectin ligand carbohydrate and mucosal addressin cell adhesion molecule 1 (MAdCAM-1) in a mouse model of "Candidatus Helicobacter heilmannii"-induced gastritis and gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Helicobacter 2010; 15(6): 538-548. http://dx.doi.org/10.1111/j.1523-5378.2010.00801.x
O'Rourke JL, Dixon MF, Jack A, Enno A, Lee A. Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of 'Helicobacter heilmannii' infection. J Pathol 2004; 203(4): 896-903. http://dx.doi.org/10.1002/path.1593
Nakamura M, Murayama SY, Serizawa H, et al. "Candidatus Helicobacter heilmannii" from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect Immun 2007; 75(3): 1214-1222. http://dx.doi.org/10.1128/IAI.01459-06
Suarez F, Lortholary O, Hermine O, Lecuit M. Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood 2006; 107(8): 3034-3044. http://dx.doi.org/10.1182/blood-2005-09-3679
Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg 2004; 139(7): 760-765. http://dx.doi.org/10.1001/archsurg.139.7.760
Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100(1): 57-70. http://dx.doi.org/10.1016/S0092-8674(00)81683-9
Newman JV, Kosaka T, Sheppard BJ, Fox JG, Schauer DB. Bacterial infection promotes colon tumorigenesis in Apc(Min/+) mice. J Infect Dis 2001; 184(2): 227-230. http://dx.doi.org/10.1086/321998
Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009; 15(9): 1016-1022. http://dx.doi.org/10.1038/nm.2015
Diwan BA, Ward JM, Ramljak D, Anderson LM. Promotion by Helicobacter hepaticus-induced hepatitis of hepatic tumors initiated by N-nitrosodimethylamine in male A/JCr mice. Toxicol Pathol 1997; 25(6): 597-605. http://dx.doi.org/10.1177/019262339702500610
Barlow C, Hirotsune S, Paylor R, et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996; 86(1): 159-171. http://dx.doi.org/10.1016/S0092-8674(00)80086-0
Reliene R, Schiestl RH. Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair (Amst) 2006; 5(7): 852-859. http://dx.doi.org/10.1016/j.dnarep.2006.05.003
Fujiwara D, Wei B, Presley LL, et al. Systemic control of plasmacytoid dendritic cells by CD8+ T cells and commensal microbiota. J Immunol 2008; 180(9): 5843-5852. http://dx.doi.org/10.4049/jimmunol.180.9.5843
Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8(6): 411-420. http://dx.doi.org/10.1038/nri2316
MacDonald TT, Gordon JN. Bacterial regulation of intestinal immune responses. Gastroenterol Clin North Am 2005; 34(3): 401-412, vii-viii. http://dx.doi.org/10.1016/j.gtc.2005.05.012
Reddy BS, Mangat S, Weisburger JH, Wynder EL. Effect of high-risk diets for colon carcinogenesis on intestinal mucosal and bacterial beta-glucuronidase activity in F344 rats. Cancer Res 1977; 37(10): 3533-3536.
Takada H, Hirooka T, Hiramatsu Y, Yamamoto M. Effect of beta-glucuronidase inhibitor on azoxymethane-induced colonic carcinogenesis in rats. Cancer Res 1982; 42(1): 331-334.
Knasmuller S, Steinkellner H, Hirschl AM, Rabot S, Nobis EC, Kassie F. Impact of bacteria in dairy products and of the intestinal microflora on the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Mutat Res 2001; 480-481: 129-138. http://dx.doi.org/10.1016/S0027-5107(01)00176-2
Kassie F, Rabot S, Kundi M, Chabicovsky M, Qin HM, Knasmuller S. Intestinal microflora plays a crucial role in the genotoxicity of the cooked food mutagen 2-amino-3-methylimidazo [4,5-f]quinoline. Carcinogenesis 2001; 22(10): 1721-1725. http://dx.doi.org/10.1093/carcin/22.10.1721
Hayatsu H, Hayatsu T. Suppressing effect of Lactobacillus casei administration on the urinary mutagenicity arising from ingestion of fried ground beef in the human. Cancer Lett 1993; 73(2-3): 173-179. http://dx.doi.org/10.1016/0304-3835(93)90261-7
Kullisaar T, Songisepp E, Mikelsaar M, Zilmer K, Vihalemm T, Zilmer M. Antioxidative probiotic fermented goats' milk decreases oxidative stress-mediated atherogenicity in human subjects. Br J Nutr 2003; 90(2): 449-456. http://dx.doi.org/10.1079/BJN2003896
Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest 2004; 113(3): 321-333. http://dx.doi.org/10.1172/JCI20925
Arabski M, Klupinska G, Chojnacki J, et al. DNA damage and repair in Helicobacter pylori-infected gastric mucosa cells. Mutat Res 2005; 570(1): 129-135. http://dx.doi.org/10.1016/j.mrfmmm.2004.10.006
Smoot DT, Elliott TB, Verspaget HW, et al. Influence of Helicobacter pylori on reactive oxygen-induced gastric epithelial cell injury. Carcinogenesis 2000; 21(11): 2091-2095. http://dx.doi.org/10.1093/carcin/21.11.2091
Parsonnet J. Bacterial infection as a cause of cancer. Environ Health Perspect 1995; 103(Suppl 8): 263-268. http://dx.doi.org/10.1289/ehp.95103s8263
Klinder A, Forster A, Caderni G, Femia AP, Pool-Zobel BL. Fecal water genotoxicity is predictive of tumor-preventive activities by inulin-like oligofructoses, probiotics (Lactobacillus rhamnosus and Bifidobacterium lactis), and their synbiotic combination. Nutr Cancer 2004; 49(2): 144-155. http://dx.doi.org/10.1207/s15327914nc4902_5
Vieira JM, Seabra SH, Vallim DC, et al. Bacteroides fragilis induce necrosis on mice peritoneal macrophages: In vitro and in vivo assays. Biochem Biophys Res Commun 2009; 387(4): 627-632. http://dx.doi.org/10.1016/j.bbrc.2009.05.124
Kumar A, Wu H, Collier-Hyams LS, et al. Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J 2007; 26(21): 4457-4466. http://dx.doi.org/10.1038/sj.emboj.7601867
Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci U S A 1993; 90(17): 7915-7922. http://dx.doi.org/10.1073/pnas.90.17.7915
Cerutti P, Ghosh R, Oya Y, Amstad P. The role of the cellular antioxidant defense in oxidant carcinogenesis. Environ Health Perspect 1994; 102 Suppl 10: 123-129. http://dx.doi.org/10.1289/ehp.94102s10123
Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420(6917): 860-867. http://dx.doi.org/10.1038/nature01322
Banks PM. Gastrointestinal lymphoproliferative disorders. Histopathology 2007; 50(1): 42-54. http://dx.doi.org/10.1111/j.1365-2559.2006.02571.x
Bende RJ, Aarts WM, Riedl RG, de Jong D, Pals ST, van Noesel CJ. Among B cell non-Hodgkin's lymphomas, MALT lymphomas express a unique antibody repertoire with frequent rheumatoid factor reactivity. J Exp Med 2005; 201(8): 1229-1241. http://dx.doi.org/10.1084/jem.20050068
Shanahan F. Nutrient tasting and signaling mechanisms in the gut V. Mechanisms of immunologic sensation of intestinal contents. Am J Physiol Gastrointest Liver Physiol 2000; 278(2): G191-196.
Arimochi H, Kinouchi T, Kataoka K, Kuwahara T, Ohnishi Y. Effect of intestinal bacteria on formation of azoxymethane-induced aberrant crypt foci in the rat colon. Biochem Biophys Res Commun 1997; 238(3): 753-757. http://dx.doi.org/10.1006/bbrc.1997.7384
Hirayama K, Rafter J. The role of probiotic bacteria in cancer prevention. Microbes Infect 2000; 2(6): 681-686. http://dx.doi.org/10.1016/S1286-4579(00)00357-9
Cebra JJ. Influences of microbiota on intestinal immune system development. Am J Clin Nutr 1999; 69(5): 1046S-1051S.
Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22: 283-307. http://dx.doi.org/10.1146/annurev.nutr.22.011602.092259
Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science 2001; 292(5519): 1115-1118. http://dx.doi.org/10.1126/science.1058709
Wei B, Su TT, Dalwadi H, et al. Resident enteric microbiota and CD8+ T cells shape the abundance of marginal zone B cells. Eur J Immunol 2008; 38(12): 3411-3425. http://dx.doi.org/10.1002/eji.200838432
Wei B, Wingender G, Fujiwara D, et al. Commensal microbiota and CD8+ T cells shape the formation of invariant NKT cells. J Immunol. 2010; 184(3): 1218-1226. http://dx.doi.org/10.4049/jimmunol.0902620
Huang T, Wei B, Velazquez P, Borneman J, Braun J. Commensal microbiota alter the abundance and TCR responsiveness of splenic naive CD4+ T lymphocytes. Clin Immunol 2005; 117(3): 221-230. http://dx.doi.org/10.1016/j.clim.2005.09.012
Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31(4): 677-689. http://dx.doi.org/10.1016/j.immuni.2009.08.020
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122(1): 107-118. http://dx.doi.org/10.1016/j.cell.2005.05.007
Sonnenburg JL, Chen CT, Gordon JI. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 2006; 4(12): e413. http://dx.doi.org/10.1371/journal.pbio.0040413
Vannucci L, Stepankova R, Kozakova H, Fiserova A, Rossmann P, Tlaskalova-Hogenova H. Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int J Oncol 2008; 32(3): 609-617. http://dx.doi.org/10.3892/ijo.32.3.609
Ishikawa H, Akedo I, Otani T, et al. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer 2005; 116(5): 762-767. http://dx.doi.org/10.1002/ijc.21115
Kim JE, Kim JY, Lee KW, Lee HJ. Cancer chemopreventive effects of lactic acid bacteria. J Microbiol Biotechnol 2007; 17(8): 1227-1235.
Kingma SD, Li N, Sun F, Valladares RB, Neu J, Lorca GL. Lactobacillus johnsonii N6.2 stimulates the innate immune response through Toll-like receptor 9 in Caco-2 cells and increases intestinal crypt Paneth cell number in biobreeding diabetes-prone rats. J Nutr 2011; 141(6): 1023-1028. http://dx.doi.org/10.3945/jn.110.135517
Valladares R, Sankar D, Li N, et al. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS One 5(5): e10507. http://dx.doi.org/10.1371/journal.pone.0010507
Matsuzaki T. Immunomodulation by treatment with Lactobacillus casei strain Shirota. Int J Food Microbiol 1998; 41(2): 133-140. http://dx.doi.org/10.1016/S0168-1605(98)00046-4
Kato I, Endo K, Yokokura T. Effects of oral administration of Lactobacillus casei on antitumor responses induced by tumor resection in mice. Int J Immunopharmacol 1994; 16(1): 29-36. http://dx.doi.org/10.1016/0192-0561(94)90116-3
Kato I, Yokokura T, Mutai M. Macrophage activation by Lactobacillus casei in mice. Microbiol Immunol 1983; 27(7): 611-618. http://dx.doi.org/10.1111/j.1348-0421.1983.tb00622.x
Rafter J. Probiotics and colon cancer. Best Pract Res Clin Gastroenterol 2003; 17(5): 849-859. http://dx.doi.org/10.1016/S1521-6918(03)00056-8
Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341(6145): 569-573. http://dx.doi.org/10.1126/science.1241165
Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504(7480): 451-455. http://dx.doi.org/10.1038/nature12726
Ames BN, Gold LS. Too many rodent carcinogens: mitogenesis increases mutagenesis. Science 1990; 249(4972): 970-971. http://dx.doi.org/10.1126/science.2136249
Cohen SM, Ellwein LB. Cell proliferation in carcinogenesis. Science 1990; 249(4972): 1007-1011. http://dx.doi.org/10.1126/science.2204108
Shaffer AL, Rosenwald A, Staudt LM. Lymphoid malignancies: the dark side of B-cell differentiation. Nat Rev Immunol 2002; 2(12): 920-932. http://dx.doi.org/10.1038/nri953
Pasqualucci L, Neumeister P, Goossens T, et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 2001; 412(6844): 341-346. http://dx.doi.org/10.1038/35085588
Oliver AM, Martin F, Kearney JF. IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol 1999; 162(12): 7198-7207.
Kullisaar T, Zilmer M, Mikelsaar M, et al. Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 2002; 72(3): 215-224. http://dx.doi.org/10.1016/S0168-1605(01)00674-2
Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer 2007; 121(11): 2381-2386. http://dx.doi.org/10.1002/ijc.23192
Epeldegui M, Widney DP, Martinez-Maza O. Pathogenesis of AIDS lymphoma: role of oncogenic viruses and B cell activation-associated molecular lesions. Curr Opin Oncol 2006; 18(5): 444-448. http://dx.doi.org/10.1097/01.cco.0000239882.23839.e5
Illes A, Varoczy L, Papp G, et al. Aspects of B-cell non-Hodgkin's lymphoma development: a transition from immune-reactivity to malignancy. Scand J Immunol 2009; 69(5): 387-400. http://dx.doi.org/10.1111/j.1365-3083.2009.02237.x
Al-Saleem T, Al-Mondhiry H. Immunoproliferative small intestinal disease (IPSID): a model for mature B-cell neoplasms. Blood 2005; 105(6): 2274-2280. http://dx.doi.org/10.1182/blood-2004-07-2755
Lecuit M, Abachin E, Martin A, et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 2004; 350(3): 239-248. http://dx.doi.org/10.1056/NEJMoa031887
Ferreri AJ, Guidoboni M, Ponzoni M, et al. Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. J Natl Cancer Inst 2004; 96(8): 586-594. http://dx.doi.org/10.1093/jnci/djh102
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