Skip to main content

Advertisement

SpringerLink
Log in

CXCR5 polymorphisms in non-Hodgkin lymphoma risk and prognosis

  • Original Article
  • Published:
Cancer Immunology, Immunotherapy Aims and scope Submit manuscript

Abstract

CXCR5 [chemokine (C-X-C motif) receptor 5; also known as Burkitt lymphoma receptor 1 (BCR1)] is expressed on mature B-cells, subsets of CD4+ and CD8+ T-cells, and skin-derived migratory dendritic cells. Together with its ligand, CXCL13, CXCR5 is involved in guiding B-cells into the B-cell zones of secondary lymphoid organs as well as T-cell migration. This study evaluated the role of common germline genetic variation in CXCR5 in the risk and prognosis of non-Hodgkin lymphoma (NHL) using a clinic-based study of 1,521 controls and 2,694 NHL cases including 710 chronic lymphocytic leukemia/small lymphocytic lymphoma, 586 diffuse large B-cell lymphoma (DLBCL), 588 follicular lymphoma (FL), 137 mantle cell lymphoma (MCL), 230 marginal zone lymphoma (MZL), and 158 peripheral T-cell lymphoma (PTCL). Of the ten CXCR5 tag SNPs in our study, five were associated with risk of NHL, with rs1790192 having the strongest association (OR 1.19, 95 % CI 1.08–1.30; p = 0.0003). This SNP was most strongly associated with the risk of FL (OR 1.44, 95 % CI 1.25–1.66; p = 3.1 × 10−7), with a lower degree of association with DLBCL (OR 1.16, 95 % CI 1.01–1.33; p = 0.04) and PTCL (OR 1.29, 95 % CI 1.02–1.64; p = 0.04) but no association with the risk of MCL or MZL. For FL patients that were observed as initial disease management, the number of minor alleles of rs1790192 was associated with better event-free survival (HR 0.64; 95 % CI 0.47–0.87; p = 0.004). These results provide additional evidence for a role of host genetic variation in CXCR5 in lymphomagenesis, particularly for FL.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62(1):10–29. doi:10.3322/caac.20138

    Article  PubMed  Google Scholar 

  2. Morton LM, Wang SS, Cozen W, Linet MS, Chatterjee N, Davis S, Severson RK, Colt JS, Vasef MA, Rothman N, Blair A, Bernstein L, Cross AJ, De Roos AJ, Engels EA, Hein DW, Hill DA, Kelemen LE, Lim U, Lynch CF, Schenk M, Wacholder S, Ward MH, Hoar Zahm S, Chanock SJ, Cerhan JR, Hartge P (2008) Etiologic heterogeneity among non-Hodgkin lymphoma subtypes. Blood 112(13):5150–5160. doi:10.1182/blood-2008-01-133587

    Article  PubMed  CAS  Google Scholar 

  3. Forster R, Mattis AE, Kremmer E, Wolf E, Brem G, Lipp M (1996) A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87(6):1037–1047

    Article  PubMed  CAS  Google Scholar 

  4. Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, Browning JL, Lipp M, Cyster JG (2000) A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406(6793):309–314. doi:10.1038/35018581

    Article  PubMed  CAS  Google Scholar 

  5. Kurtova AV, Tamayo AT, Ford RJ, Burger JA (2009) Mantle cell lymphoma cells express high levels of CXCR4, CXCR5, and VLA-4 (CD49d): importance for interactions with the stromal microenvironment and specific targeting. Blood 113(19):4604–4613. doi:10.1182/blood-2008-10-185827

    Article  PubMed  CAS  Google Scholar 

  6. Krenacs L, Schaerli P, Kis G, Bagdi E (2006) Phenotype of neoplastic cells in angioimmunoblastic T-cell lymphoma is consistent with activated follicular B helper T cells. Blood 108(3):1110–1111. doi:10.1182/blood-2006-01-0394

    Article  PubMed  CAS  Google Scholar 

  7. Deutsch AJ, Aigelsreiter A, Steinbauer E, Fruhwirth M, Kerl H, Beham-Schmid C, Schaider H, Neumeister P (2008) Distinct signatures of B-cell homeostatic and activation-dependent chemokine receptors in the development and progression of extragastric MALT lymphomas. J Pathol 215(4):431–444. doi:10.1002/path.2372

    Article  PubMed  CAS  Google Scholar 

  8. Machado L, Jarrett R, Morgan S, Murray P, Hunter B, Hamilton E, Crocker J, Thomas W, Steven N, Ismail T, Chapman A, Adams DH, Lee SP (2009) Expression and function of T cell homing molecules in Hodgkin’s lymphoma. Cancer Immunol Immunother 58(1):85–94. doi:10.1007/s00262-008-0528-z

    Article  PubMed  CAS  Google Scholar 

  9. Song H, Tong D, Cha Z, Bai J (2012) C-X-C chemokine receptor type 5 gene polymorphisms are associated with non-Hodgkin lymphoma. Mol Biol Rep. doi:10.1007/s11033-012-1717-6

    Google Scholar 

  10. Mells GF, Floyd JA, Morley KI, Cordell HJ, Franklin CS, Shin SY, Heneghan MA, Neuberger JM, Donaldson PT, Day DB, Ducker SJ, Muriithi AW, Wheater EF, Hammond CJ, Dawwas MF, Jones DE, Peltonen L, Alexander GJ, Sandford RN, Anderson CA (2011) Genome-wide association study identifies 12 new susceptibility loci for primary biliary cirrhosis. Nat Genet 43(4):329–332. doi:10.1038/ng.789

    Article  PubMed  CAS  Google Scholar 

  11. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, Freeman C, Hunt SE, Edkins S, Gray E, Booth DR, Potter SC, Goris A, Band G, Oturai AB, Strange A, Saarela J, Bellenguez C, Fontaine B, Gillman M, Hemmer B, Gwilliam R, Zipp F, Jayakumar A, Martin R, Leslie S, Hawkins S, Giannoulatou E, D’Alfonso S, Blackburn H, Martinelli Boneschi F, Liddle J, Harbo HF, Perez ML, Spurkland A, Waller MJ, Mycko MP, Ricketts M, Comabella M, Hammond N, Kockum I, McCann OT, Ban M, Whittaker P, Kemppinen A, Weston P, Hawkins C, Widaa S, Zajicek J, Dronov S, Robertson N, Bumpstead SJ, Barcellos LF, Ravindrarajah R, Abraham R, Alfredsson L, Ardlie K, Aubin C, Baker A, Baker K, Baranzini SE, Bergamaschi L, Bergamaschi R, Bernstein A, Berthele A, Boggild M, Bradfield JP, Brassat D, Broadley SA, Buck D, Butzkueven H, Capra R, Carroll WM, Cavalla P, Celius EG, Cepok S, Chiavacci R, Clerget-Darpoux F, Clysters K, Comi G, Cossburn M, Cournu-Rebeix I, Cox MB, Cozen W, Cree BA, Cross AH, Cusi D, Daly MJ, Davis E, de Bakker PI, Debouverie M, D’Hooghe M B, Dixon K, Dobosi R, Dubois B, Ellinghaus D, Elovaara I, Esposito F, Fontenille C, Foote S, Franke A, Galimberti D, Ghezzi A, Glessner J, Gomez R, Gout O, Graham C, Grant SF, Guerini FR, Hakonarson H, Hall P, Hamsten A, Hartung HP, Heard RN, Heath S, Hobart J, Hoshi M, Infante-Duarte C, Ingram G, Ingram W, Islam T, Jagodic M, Kabesch M, Kermode AG, Kilpatrick TJ, Kim C, Klopp N, Koivisto K, Larsson M, Lathrop M, Lechner-Scott JS, Leone MA, Leppa V, Liljedahl U, Bomfim IL, Lincoln RR, Link J, Liu J, Lorentzen AR, Lupoli S, Macciardi F, Mack T, Marriott M, Martinelli V, Mason D, McCauley JL, Mentch F, Mero IL, Mihalova T, Montalban X, Mottershead J, Myhr KM, Naldi P, Ollier W, Page A, Palotie A, Pelletier J, Piccio L, Pickersgill T, Piehl F, Pobywajlo S, Quach HL, Ramsay PP, Reunanen M, Reynolds R, Rioux JD, Rodegher M, Roesner S, Rubio JP, Ruckert IM, Salvetti M, Salvi E, Santaniello A, Schaefer CA, Schreiber S, Schulze C, Scott RJ, Sellebjerg F, Selmaj KW, Sexton D, Shen L, Simms-Acuna B, Skidmore S, Sleiman PM, Smestad C, Sorensen PS, Sondergaard HB, Stankovich J, Strange RC, Sulonen AM, Sundqvist E, Syvanen AC, Taddeo F, Taylor B, Blackwell JM, Tienari P, Bramon E, Tourbah A, Brown MA, Tronczynska E, Casas JP, Tubridy N, Corvin A, Vickery J, Jankowski J, Villoslada P, Markus HS, Wang K, Mathew CG, Wason J, Palmer CN, Wichmann HE, Plomin R, Willoughby E, Rautanen A, Winkelmann J, Wittig M, Trembath RC, Yaouanq J, Viswanathan AC, Zhang H, Wood NW, Zuvich R, Deloukas P, Langford C, Duncanson A, Oksenberg JR, Pericak-Vance MA, Haines JL, Olsson T, Hillert J, Ivinson AJ, De Jager PL, Peltonen L, Stewart GJ, Hafler DA, Hauser SL, McVean G, Donnelly P, Compston A (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476(7359):214–219. doi:10.1038/nature10251

    Google Scholar 

  12. Cerhan JR, Fredericksen ZS, Wang AH, Habermann TM, Kay NE, Macon WR, Cunningham JM, Shanafelt TD, Ansell SM, Call TG, Witzig TE, Slager SL, Liebow M (2011) Design and validity of a clinic-based case-control study on the molecular epidemiology of lymphoma. Int J Mol Epidemiol Genet 2(2):95–113

    PubMed  Google Scholar 

  13. Jaffe ES, Harris NL, Stein H, Vardiman JW (2001) World Health Organization classification of tumours: pathology and genetics, tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon

    Google Scholar 

  14. Campo E, Swerdlow SH, Harris NL, Pileri S, Stein H, Jaffe ES (2011) The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood 117(19):5019–5032. doi:10.1182/blood-2011-01-293050

    Article  PubMed  CAS  Google Scholar 

  15. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, Falini B, Banham AH, Rosenwald A, Staudt LM, Connors JM, Armitage JO, Chan WC (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103(1):275–282. doi:10.1182/blood-2003-05-1545

    Article  PubMed  CAS  Google Scholar 

  16. Drake MT, Maurer MJ, Link BK, Habermann TM, Ansell SM, Micallef IN, Kelly JL, Macon WR, Nowakowski GS, Inwards DJ, Johnston PB, Singh RJ, Allmer C, Slager SL, Weiner GJ, Witzig TE, Cerhan JR (2010) Vitamin D insufficiency and prognosis in non-Hodgkin’s lymphoma. J Clin Oncol 28(27):4191–4198. doi:10.1200/JCO.2010.28.6674

    Article  PubMed  Google Scholar 

  17. Link BK, Maurer MJ, Nowakowski GS, Ansell SM, Macon WR, Syrbu SI, Slager SL, Thompson CA, Inwards DJ, Johnston PB, Colgan JP, Witzig TE, Habermann TM, Cerhan JR (2013) Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy Era: a report from the University of Iowa/Mayo Clinic SPORE molecular epidemiology resource. J Clin Oncol (in press)

  18. Lossos IS, Gascoyne RD (2011) Transformation of follicular lymphoma. Best Pract Res Clin Haematol 24(2):147–163. doi:10.1016/j.beha.2011.02.006

    Article  PubMed  CAS  Google Scholar 

  19. Al-Tourah AJ, Gill KK, Chhanabhai M, Hoskins PJ, Klasa RJ, Savage KJ, Sehn LH, Shenkier TN, Gascoyne RD, Connors JM (2008) Population-based analysis of incidence and outcome of transformed non-Hodgkin’s lymphoma. J Clin Oncol 26(32):5165–5169. doi:10.1200/JCO.2008.16.0283

    Article  PubMed  Google Scholar 

  20. The International Non-Hodgkin’s Lymphoma Prognostic Factors Project (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med 329(14):987–994. doi:10.1056/NEJM199309303291402

    Google Scholar 

  21. Solal-Celigny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, Au WY, Bellei M, Brice P, Caballero D, Coiffier B, Conde-Garcia E, Doyen C, Federico M, Fisher RI, Garcia-Conde JF, Guglielmi C, Hagenbeek A, Haioun C, LeBlanc M, Lister AT, Lopez-Guillermo A, McLaughlin P, Milpied N, Morel P, Mounier N, Proctor SJ, Rohatiner A, Smith P, Soubeyran P, Tilly H, Vitolo U, Zinzani PL, Zucca E, Montserrat E (2004) Follicular lymphoma international prognostic index. Blood 104(5):1258–1265. doi:10.1182/blood-2003-12-4434

    Article  PubMed  CAS  Google Scholar 

  22. Hoster E, Dreyling M, Klapper W, Gisselbrecht C, van Hoof A, Kluin-Nelemans HC, Pfreundschuh M, Reiser M, Metzner B, Einsele H, Peter N, Jung W, Wormann B, Ludwig WD, Duhrsen U, Eimermacher H, Wandt H, Hasford J, Hiddemann W, Unterhalt M (2008) A new prognostic index (MIPI) for patients with advanced-stage mantle cell lymphoma. Blood 111(2):558–565. doi:10.1182/blood-2007-06-095331

    Article  PubMed  CAS  Google Scholar 

  23. Ziebarth JD, Bhattacharya A, Chen A, Cui Y (2012) PolymiRTS Database 2.0: linking polymorphisms in microRNA target sites with human diseases and complex traits. Nucleic Acids Res 40(Database issue):D216–D221. doi:10.1093/nar/gkr1026

  24. Ward LD, Kellis M (2012) HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res 40(Database issue):D930–D934. doi:10.1093/nar/gkr917

  25. Nogai H, Dorken B, Lenz G (2011) Pathogenesis of non-Hodgkin’s lymphoma. J Clin Oncol 29(14):1803–1811. doi:10.1200/JCO.2010.33.3252

    Article  PubMed  CAS  Google Scholar 

  26. Muller G, Hopken UE, Lipp M (2003) The impact of CCR7 and CXCR5 on lymphoid organ development and systemic immunity. Immunol Rev 195:117–135

    Article  PubMed  Google Scholar 

  27. Saez de Guinoa J, Barrio L, Mellado M, Carrasco YR (2011) CXCL13/CXCR5 signaling enhances BCR-triggered B-cell activation by shaping cell dynamics. Blood 118(6):1560–1569. doi:10.1182/blood-2011-01-332106

    Article  PubMed  CAS  Google Scholar 

  28. Widney DP, Gui D, Popoviciu LM, Said JW, Breen EC, Huang X, Kitchen CM, Alcantar JM, Smith JB, Detels R, Martinez-Maza O (2010) Expression and function of the Chemokine, CXCL13, and Its Receptor, CXCR5, in Aids-Associated Non-Hodgkin’s Lymphoma. AIDS Res Treat 2010:164586. doi:10.1155/2010/164586

    PubMed  Google Scholar 

  29. Hussain S, Zhu W, Chang SC, Crabb Breen E, Vendrame E, Magpantay L, Widney D, Conn D, Sehl ME, Jacobson L, Bream J, Wolinsky S, Rinaldo C Jr, Ambinder R, Detels R, Zhang ZF, Martinez-Maza O (2012) Serum levels of the chemokine CXCL13, genetic variation in CXCL13 and its receptor CXCR5, and HIV-associated non-Hodgkin B cell lymphoma risk. Cancer Epidemiol Biomarkers Prev. doi:10.1158/1055-9965.EPI-12-1122

    PubMed  Google Scholar 

  30. De Roos AJ, Mirick DK, Edlefsen KL, LaCroix AZ, Kopecky KJ, Madeleine MM, Magpantay L, Martinez-Maza O (2012) Markers of B-cell activation in relation to risk of non-Hodgkin lymphoma. Cancer Res 72(18):4733–4743. doi:10.1158/0008-5472.CAN-12-1639

    Article  PubMed  Google Scholar 

  31. Burkle A, Niedermeier M, Schmitt-Graff A, Wierda WG, Keating MJ, Burger JA (2007) Overexpression of the CXCR5 chemokine receptor, and its ligand, CXCL13 in B-cell chronic lymphocytic leukemia. Blood 110(9):3316–3325. doi:10.1182/blood-2007-05-089409

    Article  PubMed  Google Scholar 

  32. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270(5240):1326–1331

    Article  PubMed  CAS  Google Scholar 

  33. Vineis P, Crosignani P, Vigano C, Fontana A, Masala G, Stagnaro E, Miligi L, Costantini AS, Nanni O, Ramazzotti V, Rodella S, Tumino R, Vindigni C (2001) Lymphomas and multiple sclerosis in a multicenter case-control study. Epidemiology 12(1):134–135

    Article  PubMed  CAS  Google Scholar 

  34. Zhang Y, Holford TR, Leaderer B, Zahm SH, Boyle P, Morton LM, Zhang B, Zou K, Flynn S, Tallini G, Owens PH, Zheng T (2004) Prior medical conditions and medication use and risk of non-Hodgkin lymphoma in Connecticut United States women. Cancer Causes Control: CCC 15(4):419–428. doi:10.1023/B:CACO.0000027506.55846.5d

    Article  PubMed  Google Scholar 

  35. Ekstrom Smedby K, Vajdic CM, Falster M, Engels EA, Martinez-Maza O, Turner J, Hjalgrim H, Vineis P, Seniori Costantini A, Bracci PM, Holly EA, Willett E, Spinelli JJ, La Vecchia C, Zheng T, Becker N, De Sanjose S, Chiu BC, Dal Maso L, Cocco P, Maynadie M, Foretova L, Staines A, Brennan P, Davis S, Severson R, Cerhan JR, Breen EC, Birmann B, Grulich AE, Cozen W (2008) Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood 111(8):4029–4038. doi:10.1182/blood-2007-10-119974

    Article  PubMed  Google Scholar 

  36. Koshiol J, Lam TK, Gridley G, Check D, Brown LM, Landgren O (2011) Racial differences in chronic immune stimulatory conditions and risk of non-Hodgkin’s lymphoma in veterans from the United States. J Clin Oncol 29(4):378–385. doi:10.1200/JCO.2010.30.1515

    Article  PubMed  Google Scholar 

  37. Krumbholz M, Derfuss T, Hohlfeld R, Meinl E (2012) B cells and antibodies in multiple sclerosis pathogenesis and therapy. Nat Rev Neurol 8(11):613–623. doi:10.1038/nrneurol.2012.203

    Article  PubMed  CAS  Google Scholar 

  38. Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331(6024):1565–1570. doi:10.1126/science.1203486

    Article  PubMed  CAS  Google Scholar 

  39. Sauna ZE, Kimchi-Sarfaty C (2011) Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet 12(10):683–691. doi:10.1038/nrg3051

    Article  PubMed  CAS  Google Scholar 

  40. Katoh M (2003) Identification and characterization of human BCL9L gene and mouse Bcl9 l gene in silico. Int J Mol Med 12(4):643–649

    PubMed  CAS  Google Scholar 

  41. Willis TG, Zalcberg IR, Coignet LJ, Wlodarska I, Stul M, Jadayel DM, Bastard C, Treleaven JG, Catovsky D, Silva ML, Dyer MJ (1998) Molecular cloning of translocation t(1;14)(q21;q32) defines a novel gene (BCL9) at chromosome 1q21. Blood 91(6):1873–1881

    PubMed  CAS  Google Scholar 

  42. Brembeck FH, Wiese M, Zatula N, Grigoryan T, Dai Y, Fritzmann J, Birchmeier W (2011) BCL9-2 promotes early stages of intestinal tumor progression. Gastroenterology 141(4):1359–1370, 1370:e1351–e1353. doi:10.1053/j.gastro.2011.06.039

    Google Scholar 

Download references

Acknowledgments

This study was supported by National Institutes of Health (NIH) Grants R01 CA92153, R01 CA129539, and P50 CA97274; Dr. Charbonneau was supported by R25 CA92049.

Conflict of interest

The authors have no known conflict of interests.

Author information

Authors and Affiliations

  1. Department of Health Sciences Research, College of Medicine, Mayo Clinic, 200 First Street SW, Rochester, MN, USA

    Bridget Charbonneau, Alice H. Wang, Matthew J. Maurer, Yan W. Asmann, Susan L. Slager & James R. Cerhan

  2. Division of Hematology, Department of Internal Medicine, College of Medicine, Mayo Clinic, 200 First Street SW, Rochester, MN, USA

    Clive S. Zent, Stephen M. Ansell, Thomas E. Witzig, Thomas M. Habermann & Anne J. Novak

  3. Division of Hematology, Oncology, Blood and Marrow Transplantation, Department of Internal Medicine, College of Medicine, University of Iowa, Iowa City, IA, USA

    Brian K. Link & George J. Weiner

  4. Department of Pathology, Faculty of Medicine, Ege University, Bornova, İzmir, Turkey

    Nazan Ozsan

  5. Department of Laboratory Medicine and Pathology, College of Medicine, Mayo Clinic, 200 First Street SW, Rochester, MN, USA

    Andrew L. Feldman, Julie M. Cunningham & Ahmet Dogan

Authors
  1. Bridget Charbonneau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice H. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew J. Maurer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yan W. Asmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Clive S. Zent
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brian K. Link
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stephen M. Ansell
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. George J. Weiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nazan Ozsan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Andrew L. Feldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Thomas E. Witzig
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Julie M. Cunningham
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ahmet Dogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Thomas M. Habermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Susan L. Slager
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Anne J. Novak
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. James R. Cerhan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James R. Cerhan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 129 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Charbonneau, B., Wang, A.H., Maurer, M.J. et al. CXCR5 polymorphisms in non-Hodgkin lymphoma risk and prognosis. Cancer Immunol Immunother 62, 1475–1484 (2013). https://doi.org/10.1007/s00262-013-1452-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00262-013-1452-4

Keywords

Search

Navigation