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KILLER IMMUNOGLOBULINE LIKE RECEPTOR GENE ANALYSIS IN CHRONIC LYMPHOCYTIC LEUKEMIA AND ITS RELATION WITH AUTOIMMUNITY

Year 2021, Volume: 84 Issue: 2, 227 - 236, 25.04.2021
https://doi.org/10.26650/IUITFD.2020.0037

Abstract

Objective: Our study was performed on 49 chronic lymphocytic leukemia (CLL) patients followed in the outpatient clinic of the Istanbul University Cerrahpasa Medical Faculty Department of Hematology. We aimed to analyze the relationship between autoimmune phenomena and CLL. Methods: Twenty-five CLL patients with and 24 CLL patients without autoimmune phenomenon were included. Thirty-two of them were male and 17 were female. No statistically significant difference in the median age at diagnosis (60 vs 64) and in the median follow-up time (59 months vs 71 months) was detected. The initial diagnostic parameters were similar. Results: In our autoimmune phenomenon cohort, the most frequent autoimmune disease was autoimmune hemolytic anemia (AIHA) followed by immune thrombocytopenia (ITP) and pure red cell aplasia (PRCA). The direct antiglobulin positivity at the time of diagnosis was increased in the autoimmune phenomenon group (p=0.024). Additionally, the stage of CLL in patients of the autoimmune phenomenon group was more advanced than the other group (p=0.04). Although the number of autoimmune phenomena was not high enough, the CD38 positive cell ratio over 30% in the peripheral blood was more frequent in PRCA group (p=0.008). Conclusion: We could not determine a relationship between autoimmunity in CLL and KIR genotypes. We believe that a new study in a larger cohort with superior technical conditions should be planned to find accurate responses to our study.

References

  • 1. Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Dohner H, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008;111(12):5446-56. [CrossRef]
  • 2. Hamblin TJ, Orchard JA, Ibbotson RE, Davis Z, Thomas PW, Stevenson FK, et al. CD38 expression and immunoglobulin variable region mutations are independent prognostic variables in chronic lymphocytic leukemia, but CD38 expression may vary during the course of the disease. Blood 2002;99(3):1023-9. [CrossRef]
  • 3. Hamblin TJ. Autoimmune complications of chronic lymphocytic leukemia. Semin Oncol 2006;33(2):230-9. [CrossRef]
  • 4. Hodgson K, Ferrer G, Montserrat E, Moreno C. Chronic lymphocytic leukemia and autoimmunity: a systematic review. Haematologica 2011;96(5):752-61. [CrossRef]
  • 5. Ghia P, Guida G, Stella S, Gottardi D, Geuna M, Strola G, et al. The pattern of CD38 expression defines a distinct subset of chronic lymphocytic leukemia (CLL) patients at risk of disease progression. Blood 2003;101(4):1262-9. [CrossRef]
  • 6. Hodgson K, Ferrer G, Pereira A, Moreno C, Montserrat E. Autoimmune cytopenia in chronic lymphocytic leukaemia: diagnosis and treatment. Br J Haematol 2011;154(1):14-22. [CrossRef]
  • 7. Akpinar S. Kronik Lenfositik Lösemide KIR gen polimorfizmi [Yandal Uzmanlık Tezi]. Edirne: Trakya Üniversitesi Tıp Fakültesi; 2013.
  • 8. Campbell KS, Purdy AK. Structure/function of human killer cell immunoglobulin-like receptors: lessons from polymorphisms, evolution, crystal structures and mutations. Immunology 2011;132(3):315-25. [CrossRef]
  • 9. Purdy AK, Campbell KS. Natural killer cells and cancer: regulation by the killer cell Ig-like receptors (KIR). Cancer Biol Ther 2009;8(23):2211-20. [CrossRef]
  • 10. Nourse JP, Lea R, Crooks P, Wright G, Tran H, Catalano J, et al. The KIR2DS2/DL2 genotype is associated with adult persistent/chronic and relapsed immune thrombocytopenia independently of FCGR3a-158 polymorphisms. Blood Coagul Fibrinolysis 2012;23(1):45-50. [CrossRef]
  • 11. Shastry A, Sedimbi SK, Rajalingam R, Rumba I, Kanungo A, Sanjeevi CB. Different KIRs confer susceptibility and protection to adults with latent autoimmune diabetes in Latvian and Asian Indian populations. Ann N Y Acad Sci 2008;1150:133-8. [CrossRef]
  • 12. Salim PH, Jobim M, Jobim LF, Xavier RM. Autoimmune rheumatic diseases and their association with killer immunoglobulin-like receptor genes. Rev Bras Reumatol. 2011;51(4):351-6, 62-4. doi: S0482-50042011000400007
  • 13. Karabon L, Jedynak A, Giebel S, Wolowiec D, Kielbinski M, Woszczyk D, et al. KIR/HLA gene combinations influence susceptibility to B-cell chronic lymphocytic leukemia and the clinical course of disease. Tissue Antigens 2011;78(2):129- 38. [CrossRef]
  • 14. Junevik K, Werlenius O, Hasselblom S, Jacobsson S, Nilsson- Ehle H, Andersson PO. The expression of NK cell inhibitory receptors on cytotoxic T cells in B-cell chronic lymphocytic leukaemia (B-CLL). Ann Hematol 2007;86(2):89-94. [CrossRef]
  • 15. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood 1975;46(2):219-34. [CrossRef]
  • 16. Binet JL, Auquier A, Dighiero G, Chastang C, Piguet H, Goasguen J, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer 1981;48(1):198-206. [CrossRef]
  • 17. Olerup. KIR genotyping [11.07.2015]. Available from: http:// www.olerup-ssp.com/productfiles/interpretation_tables/ KIR%20Genotyping%202013%2078R%20R01.pdf.
  • 18. Bastion Y, Coiffier B, Dumontet C, Espinouse D, Bryon PA. Severe autoimmune hemolytic anemia in two patients treated with fludarabine for chronic lymphocytic leukemia. Ann Oncol 1992;3(2):171-2. [CrossRef]
  • 19. Tosti S, Caruso R, D’Adamo F, Picardi A, Ali Ege M, Girelli G, et al. Severe autoimmune hemolytic anemia in a patient with chronic lymphocytic leukemia responsive to fludarabinebased treatment. Ann Hematol 1992;65(5):238-9. [CrossRef]
  • 20. Myint H, Copplestone JA, Orchard J, Craig V, Curtis D, Prentice AG, et al. Fludarabine-related autoimmune haemolytic anaemia in patients with chronic lymphocytic leukaemia. Br J Haematol 1995;91(2):341-4. [CrossRef]
  • 21. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010;11(1):7-13. [CrossRef]
  • 22. Borthakur G, O’Brien S, Wierda WG, Thomas DA, Cortes JE, Giles FJ, et al. Immune anaemias in patients with chronic lymphocytic leukaemia treated with fludarabine, cyclophosphamide and rituximab--incidence and predictors. Br J Haematol 2007;136(6):800-5. [CrossRef]
  • 23. Dearden C, Wade R, Else M, Richards S, Milligan D, Hamblin T, et al. The prognostic significance of a positive direct antiglobulin test in chronic lymphocytic leukemia: a beneficial effect of the combination of fludarabine and cyclophosphamide on the incidence of hemolytic anemia. Blood 2008;111(4):1820-6. [CrossRef]
  • 24. Hamblin TJ, Oscier DG, Young BJ. Autoimmunity in chronic lymphocytic leukaemia. J Clin Pathol 1986;39(7):713-6. [CrossRef]
  • 25. Zent CS, Ding W, Schwager SM, Reinalda MS, Hoyer JD, Jelinek DF, et al. The prognostic significance of cytopenia in chronic lymphocytic leukaemia/small lymphocytic lymphoma. Br J Haematol 2008;141(5):615-21. [CrossRef]
  • 26. Barcellini W, Capalbo S, Agostinelli RM, Mauro FR, Ambrosetti A, Calori R, et al. Relationship between autoimmune phenomena and disease stage and therapy in B-cell chronic lymphocytic leukemia. Haematologica 2006;91(12):1689-92.
  • 27. Mauro FR, Foa R, Cerretti R, Giannarelli D, Coluzzi S, Mandelli F, et al. Autoimmune hemolytic anemia in chronic lymphocytic leukemia: clinical, therapeutic, and prognostic features. Blood 2000;95(9):2786-92. [CrossRef]
  • 28. Moreno C, Hodgson K, Ferrer G, Elena M, Filella X, Pereira A, et al. Autoimmune cytopenia in chronic lymphocytic leukemia: prevalence, clinical associations, and prognostic significance. Blood 2010;116(23):4771-6. [CrossRef]
  • 29. Visco C, Ruggeri M, Laura Evangelista M, Stasi R, Zanotti R, Giaretta I, et al. Impact of immune thrombocytopenia on the clinical course of chronic lymphocytic leukemia. Blood 2008;111(3):1110-6. [CrossRef]
  • 30. Hall AM, Vickers MA, McLeod E, Barker RN. Rh autoantigen presentation to helper T cells in chronic lymphocytic leukemia by malignant B cells. Blood 2005;105(5):2007-15. [CrossRef]
  • 31. Galletti J, Canones C, Morande P, Borge M, Oppezzo P, Geffner J, et al. Chronic lymphocytic leukemia cells bind and present the erythrocyte protein band 3: possible role as initiators of autoimmune hemolytic anemia. J Immunol. 2008;181(5):3674-83. [CrossRef]
  • 32. von Bergwelt-Baildon M, Maecker B, Schultze J, Gribben JG. CD40 activation: potential for specific immunotherapy in B-CLL. Ann Oncol 2004;15(6):853-7. [CrossRef]
  • 33. Dreger P, Ghia P, Schetelig J, van Gelder M, Kimby E, Michallet M, et al. High-risk chronic lymphocytic leukemia in the era of pathway inhibitors: integrating molecular and cellular therapies. Blood 2018;132(9):892-902. [CrossRef]
  • 34. Bachanova V, Weisdorf DJ, Wang T, Marsh SGE, Cereb N, Haagenson MD, et al. Donor Killer Cell Immunoglobulin- Like Receptor Genotype Does Not Improve Graft-versus- Leukemia Responses in Chronic Lymphocytic Leukemia after Unrelated Donor Transplant: A Center for International Blood and Marrow Transplant Research Analysis. Biol Blood Marrow Transplant 2019;25(5):949-54. doi: 10.1016/j. bbmt.2018.12.763. [CrossRef]
  • 35. Williams F, Meenagh A, Sleator C, Cook D, Fernandez-Vina M, Bowcock AM, et al. Activating killer cell immunoglobulinlike receptor gene KIR2DS1 is associated with psoriatic arthritis. Hum Immunol 2005;66(7):836-41. [CrossRef]
  • 36. Romero V, Zuniga J, Azocar J, Clavijo OP, Terreros D, Kidwai H, et al. Genetic interactions of KIR and G1M immunoglobulin allotypes differ in obese from nonobese individuals with type 2 diabetes. Mol Immunol. 2008;45(14):3857-62. [CrossRef]
  • 37. Pellett F, Siannis F, Vukin I, Lee P, Urowitz MB, Gladman DD. KIRs and autoimmune disease: studies in systemic lupus erythematosus and scleroderma. Tissue Antigens 2007;69 Suppl 1:106-8. [CrossRef]
  • 38. Lowe DP, Cook MA, Bowman SJ, Briggs DC. Association of killer cell immunoglobulin-like receptors with primary Sjogren’s syndrome. Rheumatology (Oxford) 2009;48(4):359- 62. [CrossRef]
  • 39. Jiao YL, Zhang BC, You L, Li JF, Zhang J, Ma CY, et al. Polymorphisms of KIR gene and HLA-C alleles: possible association with susceptibility to HLA-B27-positive patients with ankylosing spondylitis. J Clin Immunol 2010;30(6):840- 4. [CrossRef]
  • 40. Fusco C, Guerini FR, Nocera G, Ventrella G, Caputo D, Valentino MA, et al. KIRs and their HLA ligands in remittingrelapsing multiple sclerosis. J Neuroimmunol 2010;229(1- 2):232-7. [CrossRef]
  • 41. Cosentini E, Gargiulo L, Bruno P, Lastraioli S, Risitano A, Camerlingo R, et al. Killer immunoglobulin-like receptors (KIR) and their HLA-ligands in Italian paroxysmal nocturnal haemoglobinuria (PNH) patients. Tissue Antigens 2012;80(4):322-7. [CrossRef]
  • 42. Taintor AR, Leiferman KM, Hashimoto T, Ishii N, Zone JJ, Hull CM. A novel case of IgA paraneoplastic pemphigus associated with chronic lymphocytic leukemia. J Am Acad Dermatol 2007;56(5 Suppl):S73-6. [CrossRef]
  • 43. Seymour LA, Nourse JP, Crooks P, Wockner L, Bird R, Tran H, et al. The presence of KIR2DS5 confers protection against adult immune thrombocytopenia. Tissue Antigens. 2014;83(3):154-60. [CrossRef]

KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ

Year 2021, Volume: 84 Issue: 2, 227 - 236, 25.04.2021
https://doi.org/10.26650/IUITFD.2020.0037

Abstract

Amaç: İstanbul Üniversitesi Cerrahpaşa Tıp Fakültesi Hematoloji Polikliniği’nde takip edilen 49 Kronik Lenfositik Lösemi (KLL) hastası çalışmaya dahil edilmiştir. Çalışmanın amacı, çeşitli otoimmün hastalıklar ile ilişkisi gösterilmiş olan Killer Immunoglobuline Like Receptor (KIR) gen düzeylerini, otoimmün olay gözlenmiş ve gözlenmemiş KLL hasta grupları arasında karşılaştırmaktır. Gereç ve Yöntem: Bu doğrultuda otoimmün olay gözlenmiş olan 25 ve otoimmün olay gözlenmemiş 24 KLL hastası çalışmaya dahil edilmiştir. Hastaların 32’si erkek, 17’si kadındır. Otoimmün hastalık gözlenen grup ile otoimmün olay gözlenmeyen KLL grubu arasında tanı anındaki yaş (60 vs 64) ve ortanca takip süresi (59 ay vs 71 ay), tanı anındaki parametreleri istatistiki olarak benzerdir. Bulgular: Gözlenen en sık otoimmün olay otoimmün hemolitik anemi (OİHA) iken onu immün trombositopeni (İTP) ve saf eritroid aplazi (PRCA) takip etmiştir. Otoimmün olay gözlenmiş hastaların tanı anında direkt antiglobulin testi pozitiflik oranı, otoimmün olay gözlenmemiş KLL hastalarına göre artmış olduğu gözlenmiştir (p=0,024). Ayrıca otoimmün olay gözlenen hastaların tanı anında KLL hastalık evrelerinin daha ileri olduğu görülmüştür (p=0,04). Otoimmün olaylar kendi aralarında değerlendirildiğinde ise, sayı az olmasına karşın, PRCA’da çevresel kanda CD38 pozitif hücre oranının %30’un üstünde olma sıklığının arttığı gözlenmiştir (p=0,008). Sonuç: Çalışmamızda KIR genlerinin otoimmün olaylarla ilişkisi incelendiğinde, otoimmünite gözlenmeyen gruba göre herhangi bir istatistiki fark tespit edilememiştir. Daha iyi teknik şartlarda yeni çalışmalar yapılmasında fayda vardır.

References

  • 1. Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Dohner H, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008;111(12):5446-56. [CrossRef]
  • 2. Hamblin TJ, Orchard JA, Ibbotson RE, Davis Z, Thomas PW, Stevenson FK, et al. CD38 expression and immunoglobulin variable region mutations are independent prognostic variables in chronic lymphocytic leukemia, but CD38 expression may vary during the course of the disease. Blood 2002;99(3):1023-9. [CrossRef]
  • 3. Hamblin TJ. Autoimmune complications of chronic lymphocytic leukemia. Semin Oncol 2006;33(2):230-9. [CrossRef]
  • 4. Hodgson K, Ferrer G, Montserrat E, Moreno C. Chronic lymphocytic leukemia and autoimmunity: a systematic review. Haematologica 2011;96(5):752-61. [CrossRef]
  • 5. Ghia P, Guida G, Stella S, Gottardi D, Geuna M, Strola G, et al. The pattern of CD38 expression defines a distinct subset of chronic lymphocytic leukemia (CLL) patients at risk of disease progression. Blood 2003;101(4):1262-9. [CrossRef]
  • 6. Hodgson K, Ferrer G, Pereira A, Moreno C, Montserrat E. Autoimmune cytopenia in chronic lymphocytic leukaemia: diagnosis and treatment. Br J Haematol 2011;154(1):14-22. [CrossRef]
  • 7. Akpinar S. Kronik Lenfositik Lösemide KIR gen polimorfizmi [Yandal Uzmanlık Tezi]. Edirne: Trakya Üniversitesi Tıp Fakültesi; 2013.
  • 8. Campbell KS, Purdy AK. Structure/function of human killer cell immunoglobulin-like receptors: lessons from polymorphisms, evolution, crystal structures and mutations. Immunology 2011;132(3):315-25. [CrossRef]
  • 9. Purdy AK, Campbell KS. Natural killer cells and cancer: regulation by the killer cell Ig-like receptors (KIR). Cancer Biol Ther 2009;8(23):2211-20. [CrossRef]
  • 10. Nourse JP, Lea R, Crooks P, Wright G, Tran H, Catalano J, et al. The KIR2DS2/DL2 genotype is associated with adult persistent/chronic and relapsed immune thrombocytopenia independently of FCGR3a-158 polymorphisms. Blood Coagul Fibrinolysis 2012;23(1):45-50. [CrossRef]
  • 11. Shastry A, Sedimbi SK, Rajalingam R, Rumba I, Kanungo A, Sanjeevi CB. Different KIRs confer susceptibility and protection to adults with latent autoimmune diabetes in Latvian and Asian Indian populations. Ann N Y Acad Sci 2008;1150:133-8. [CrossRef]
  • 12. Salim PH, Jobim M, Jobim LF, Xavier RM. Autoimmune rheumatic diseases and their association with killer immunoglobulin-like receptor genes. Rev Bras Reumatol. 2011;51(4):351-6, 62-4. doi: S0482-50042011000400007
  • 13. Karabon L, Jedynak A, Giebel S, Wolowiec D, Kielbinski M, Woszczyk D, et al. KIR/HLA gene combinations influence susceptibility to B-cell chronic lymphocytic leukemia and the clinical course of disease. Tissue Antigens 2011;78(2):129- 38. [CrossRef]
  • 14. Junevik K, Werlenius O, Hasselblom S, Jacobsson S, Nilsson- Ehle H, Andersson PO. The expression of NK cell inhibitory receptors on cytotoxic T cells in B-cell chronic lymphocytic leukaemia (B-CLL). Ann Hematol 2007;86(2):89-94. [CrossRef]
  • 15. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood 1975;46(2):219-34. [CrossRef]
  • 16. Binet JL, Auquier A, Dighiero G, Chastang C, Piguet H, Goasguen J, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer 1981;48(1):198-206. [CrossRef]
  • 17. Olerup. KIR genotyping [11.07.2015]. Available from: http:// www.olerup-ssp.com/productfiles/interpretation_tables/ KIR%20Genotyping%202013%2078R%20R01.pdf.
  • 18. Bastion Y, Coiffier B, Dumontet C, Espinouse D, Bryon PA. Severe autoimmune hemolytic anemia in two patients treated with fludarabine for chronic lymphocytic leukemia. Ann Oncol 1992;3(2):171-2. [CrossRef]
  • 19. Tosti S, Caruso R, D’Adamo F, Picardi A, Ali Ege M, Girelli G, et al. Severe autoimmune hemolytic anemia in a patient with chronic lymphocytic leukemia responsive to fludarabinebased treatment. Ann Hematol 1992;65(5):238-9. [CrossRef]
  • 20. Myint H, Copplestone JA, Orchard J, Craig V, Curtis D, Prentice AG, et al. Fludarabine-related autoimmune haemolytic anaemia in patients with chronic lymphocytic leukaemia. Br J Haematol 1995;91(2):341-4. [CrossRef]
  • 21. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010;11(1):7-13. [CrossRef]
  • 22. Borthakur G, O’Brien S, Wierda WG, Thomas DA, Cortes JE, Giles FJ, et al. Immune anaemias in patients with chronic lymphocytic leukaemia treated with fludarabine, cyclophosphamide and rituximab--incidence and predictors. Br J Haematol 2007;136(6):800-5. [CrossRef]
  • 23. Dearden C, Wade R, Else M, Richards S, Milligan D, Hamblin T, et al. The prognostic significance of a positive direct antiglobulin test in chronic lymphocytic leukemia: a beneficial effect of the combination of fludarabine and cyclophosphamide on the incidence of hemolytic anemia. Blood 2008;111(4):1820-6. [CrossRef]
  • 24. Hamblin TJ, Oscier DG, Young BJ. Autoimmunity in chronic lymphocytic leukaemia. J Clin Pathol 1986;39(7):713-6. [CrossRef]
  • 25. Zent CS, Ding W, Schwager SM, Reinalda MS, Hoyer JD, Jelinek DF, et al. The prognostic significance of cytopenia in chronic lymphocytic leukaemia/small lymphocytic lymphoma. Br J Haematol 2008;141(5):615-21. [CrossRef]
  • 26. Barcellini W, Capalbo S, Agostinelli RM, Mauro FR, Ambrosetti A, Calori R, et al. Relationship between autoimmune phenomena and disease stage and therapy in B-cell chronic lymphocytic leukemia. Haematologica 2006;91(12):1689-92.
  • 27. Mauro FR, Foa R, Cerretti R, Giannarelli D, Coluzzi S, Mandelli F, et al. Autoimmune hemolytic anemia in chronic lymphocytic leukemia: clinical, therapeutic, and prognostic features. Blood 2000;95(9):2786-92. [CrossRef]
  • 28. Moreno C, Hodgson K, Ferrer G, Elena M, Filella X, Pereira A, et al. Autoimmune cytopenia in chronic lymphocytic leukemia: prevalence, clinical associations, and prognostic significance. Blood 2010;116(23):4771-6. [CrossRef]
  • 29. Visco C, Ruggeri M, Laura Evangelista M, Stasi R, Zanotti R, Giaretta I, et al. Impact of immune thrombocytopenia on the clinical course of chronic lymphocytic leukemia. Blood 2008;111(3):1110-6. [CrossRef]
  • 30. Hall AM, Vickers MA, McLeod E, Barker RN. Rh autoantigen presentation to helper T cells in chronic lymphocytic leukemia by malignant B cells. Blood 2005;105(5):2007-15. [CrossRef]
  • 31. Galletti J, Canones C, Morande P, Borge M, Oppezzo P, Geffner J, et al. Chronic lymphocytic leukemia cells bind and present the erythrocyte protein band 3: possible role as initiators of autoimmune hemolytic anemia. J Immunol. 2008;181(5):3674-83. [CrossRef]
  • 32. von Bergwelt-Baildon M, Maecker B, Schultze J, Gribben JG. CD40 activation: potential for specific immunotherapy in B-CLL. Ann Oncol 2004;15(6):853-7. [CrossRef]
  • 33. Dreger P, Ghia P, Schetelig J, van Gelder M, Kimby E, Michallet M, et al. High-risk chronic lymphocytic leukemia in the era of pathway inhibitors: integrating molecular and cellular therapies. Blood 2018;132(9):892-902. [CrossRef]
  • 34. Bachanova V, Weisdorf DJ, Wang T, Marsh SGE, Cereb N, Haagenson MD, et al. Donor Killer Cell Immunoglobulin- Like Receptor Genotype Does Not Improve Graft-versus- Leukemia Responses in Chronic Lymphocytic Leukemia after Unrelated Donor Transplant: A Center for International Blood and Marrow Transplant Research Analysis. Biol Blood Marrow Transplant 2019;25(5):949-54. doi: 10.1016/j. bbmt.2018.12.763. [CrossRef]
  • 35. Williams F, Meenagh A, Sleator C, Cook D, Fernandez-Vina M, Bowcock AM, et al. Activating killer cell immunoglobulinlike receptor gene KIR2DS1 is associated with psoriatic arthritis. Hum Immunol 2005;66(7):836-41. [CrossRef]
  • 36. Romero V, Zuniga J, Azocar J, Clavijo OP, Terreros D, Kidwai H, et al. Genetic interactions of KIR and G1M immunoglobulin allotypes differ in obese from nonobese individuals with type 2 diabetes. Mol Immunol. 2008;45(14):3857-62. [CrossRef]
  • 37. Pellett F, Siannis F, Vukin I, Lee P, Urowitz MB, Gladman DD. KIRs and autoimmune disease: studies in systemic lupus erythematosus and scleroderma. Tissue Antigens 2007;69 Suppl 1:106-8. [CrossRef]
  • 38. Lowe DP, Cook MA, Bowman SJ, Briggs DC. Association of killer cell immunoglobulin-like receptors with primary Sjogren’s syndrome. Rheumatology (Oxford) 2009;48(4):359- 62. [CrossRef]
  • 39. Jiao YL, Zhang BC, You L, Li JF, Zhang J, Ma CY, et al. Polymorphisms of KIR gene and HLA-C alleles: possible association with susceptibility to HLA-B27-positive patients with ankylosing spondylitis. J Clin Immunol 2010;30(6):840- 4. [CrossRef]
  • 40. Fusco C, Guerini FR, Nocera G, Ventrella G, Caputo D, Valentino MA, et al. KIRs and their HLA ligands in remittingrelapsing multiple sclerosis. J Neuroimmunol 2010;229(1- 2):232-7. [CrossRef]
  • 41. Cosentini E, Gargiulo L, Bruno P, Lastraioli S, Risitano A, Camerlingo R, et al. Killer immunoglobulin-like receptors (KIR) and their HLA-ligands in Italian paroxysmal nocturnal haemoglobinuria (PNH) patients. Tissue Antigens 2012;80(4):322-7. [CrossRef]
  • 42. Taintor AR, Leiferman KM, Hashimoto T, Ishii N, Zone JJ, Hull CM. A novel case of IgA paraneoplastic pemphigus associated with chronic lymphocytic leukemia. J Am Acad Dermatol 2007;56(5 Suppl):S73-6. [CrossRef]
  • 43. Seymour LA, Nourse JP, Crooks P, Wockner L, Bird R, Tran H, et al. The presence of KIR2DS5 confers protection against adult immune thrombocytopenia. Tissue Antigens. 2014;83(3):154-60. [CrossRef]
There are 43 citations in total.

Details

Primary Language Turkish
Subjects Health Care Administration
Journal Section RESEARCH
Authors

Murat Özbalak This is me 0000-0002-3040-4052

Işıl Erdoğan Özünal This is me 0000-0002-5289-7134

Selin Berk This is me 0000-0001-7495-0218

Tuğrul Elverdi This is me 0000-0001-9496-5353

Ayşe Salihoğlu This is me 0000-0002-8758-7945

Ahmet Emre Eşkazan This is me 0000-0001-9568-0894

Ezgi Pınar Özbalak This is me 0000-0003-1722-8602

Cem Ar This is me 0000-0002-0332-9253

Şeniz Öngören This is me 0000-0002-2809-5510

Zafer Başlar This is me 0000-0002-1807-7351

Yıldız Aydın This is me 0000-0002-1615-5256

Seda Ekizoğlu This is me 0000-0003-4785-8189

Asuman Çelebi This is me 0000-0003-0960-6351

Ayşe Nur Buyru This is me

Teoman Soysal This is me 0000-0002-7417-2118

Publication Date April 25, 2021
Submission Date July 14, 2020
Published in Issue Year 2021 Volume: 84 Issue: 2

Cite

APA Özbalak, M., Erdoğan Özünal, I., Berk, S., Elverdi, T., et al. (2021). KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ. Journal of Istanbul Faculty of Medicine, 84(2), 227-236. https://doi.org/10.26650/IUITFD.2020.0037
AMA Özbalak M, Erdoğan Özünal I, Berk S, Elverdi T, Salihoğlu A, Eşkazan AE, Özbalak EP, Ar C, Öngören Ş, Başlar Z, Aydın Y, Ekizoğlu S, Çelebi A, Buyru AN, Soysal T. KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ. İst Tıp Fak Derg. April 2021;84(2):227-236. doi:10.26650/IUITFD.2020.0037
Chicago Özbalak, Murat, Işıl Erdoğan Özünal, Selin Berk, Tuğrul Elverdi, Ayşe Salihoğlu, Ahmet Emre Eşkazan, Ezgi Pınar Özbalak, Cem Ar, Şeniz Öngören, Zafer Başlar, Yıldız Aydın, Seda Ekizoğlu, Asuman Çelebi, Ayşe Nur Buyru, and Teoman Soysal. “KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ”. Journal of Istanbul Faculty of Medicine 84, no. 2 (April 2021): 227-36. https://doi.org/10.26650/IUITFD.2020.0037.
EndNote Özbalak M, Erdoğan Özünal I, Berk S, Elverdi T, Salihoğlu A, Eşkazan AE, Özbalak EP, Ar C, Öngören Ş, Başlar Z, Aydın Y, Ekizoğlu S, Çelebi A, Buyru AN, Soysal T (April 1, 2021) KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ. Journal of Istanbul Faculty of Medicine 84 2 227–236.
IEEE M. Özbalak, “KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ”, İst Tıp Fak Derg, vol. 84, no. 2, pp. 227–236, 2021, doi: 10.26650/IUITFD.2020.0037.
ISNAD Özbalak, Murat et al. “KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ”. Journal of Istanbul Faculty of Medicine 84/2 (April 2021), 227-236. https://doi.org/10.26650/IUITFD.2020.0037.
JAMA Özbalak M, Erdoğan Özünal I, Berk S, Elverdi T, Salihoğlu A, Eşkazan AE, Özbalak EP, Ar C, Öngören Ş, Başlar Z, Aydın Y, Ekizoğlu S, Çelebi A, Buyru AN, Soysal T. KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ. İst Tıp Fak Derg. 2021;84:227–236.
MLA Özbalak, Murat et al. “KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ”. Journal of Istanbul Faculty of Medicine, vol. 84, no. 2, 2021, pp. 227-36, doi:10.26650/IUITFD.2020.0037.
Vancouver Özbalak M, Erdoğan Özünal I, Berk S, Elverdi T, Salihoğlu A, Eşkazan AE, Özbalak EP, Ar C, Öngören Ş, Başlar Z, Aydın Y, Ekizoğlu S, Çelebi A, Buyru AN, Soysal T. KRONİK LENFOSİTİK LÖSEMİ TANILI HASTALARDA KİLLER İMMÜNOGLOBULİN LİKE RESEPTÖR GEN DÜZEYLERİ VE OTOİMMÜN OLAYLAR İLE İLİŞKİSİ. İst Tıp Fak Derg. 2021;84(2):227-36.

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