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Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy

Yıl 2021, Cilt: 12 Sayı: 2, 147 - 154, 30.06.2021
https://doi.org/10.18663/tjcl.907688

Öz

Aim: Mitochondrial DNA (mtDNA) polymorphisms can be considered as a molecular marker in susceptibility to various types of cancer. In this study, we aimed to investigate the potential relationship of mtDNA polymorphisms with disease etiopathogenesis in patients with hematological malignancy.
Material and Methods: This study was carried out with the participation of 80 patients diagnosed with hematological malignancy and 80 healthy individuals in the Department of Medical Genetics, Atatürk University. In all participants, 13 polymorphism regions of 6 coding genes of mtDNA were investigated by Polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) method. SNPs evaluated in the study; NADH dehydrogenase subunit 5-13704 (C/T), Cytochrome b 15315 (C/T), 12S rRNA 740 (G/A) and 680 (T/C), Cytochrome C Oxidase I 7319 (T/C), -7444 (G/A), Cytochrome C Oxidase II 8252 (C/G), 7660 (G/A), 7975 (A/G), 8014 (A/G), 8113 (C/A), 8152 (G/A) and tRNA lysine 8310 (T/C) were identified as.
Results: ND-5 13704 (C>T) polymorphism was statistically significant in patients with hematological malignancies compared to healthy controls (p = 0.001). There was no significant difference between patients and controls in other evaluated polymorphisms.
Conclusion: Although the findings obtained from this study suggest that mtDNA ND-5 13704 (C>T) polymorphism may play a role in the etiopathogenesis of hematological malignancies, large-scale studies are needed to determine the importance of this polymorphic region.

Destekleyen Kurum

Ataturk University Scientific Research Project

Proje Numarası

(2009/305)

Kaynakça

  • 1.Lane N, Martin W. The energetics of genome complexity. Nature. 2010; 467: 929-34.
  • 2.Wallace DC. Mitochondria and cancer. Nature Reviews Cancer. 2012; 12 :685-98.
  • 3.Fernández‐Silva P, Enriquez JA, Montoya J. Replication and transcription of mammalian mitochondrial DNA. Experimental physiology. 2003; 88 :41-56.
  • 4.Singh KK, Kulawiec M. Mitochondrial DNA polymorphism and risk of cancer. Cancer Epidemiology: Springer; 2009: 291-303.
  • 5.Hertweck KL, Dasgupta S. The landscape of mtDNA modifications in cancer: a tale of two cities. Frontiers in oncology. 2017; 7: 262.
  • 6.Hüttemann M, Lee I, Grossman LI, et al. Phosphorylation of mammalian cytochrome c and cytochrome c oxidase in the regulation of cell destiny: respiration, apoptosis, and human disease. Mitochondrial Oxidative Phosphorylation: Springer; 2012: 237-64.
  • 7.Wang H, Xu J, Li D, Zhang S, et al. Identification of sequence polymorphisms in the mitochondrial cytochrome c oxidase genes as risk factors for hepatocellular carcinoma. Journal of clinical laboratory analysis. 2018; 32: 22299.
  • 8.Meng X-L, Meng H, Zhang W, et al. The role of mitochondrial tRNA variants in female breast cancer. Mitochondrial DNA Part A. 2016; 27: 3199-201.
  • 9.Vardiman JW, Thiele J, Arber DA, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009; 114: 937-51.
  • 10.Campo E, Swerdlow SH, Harris NL, et al. The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood, The Journal of the American Society of Hematology. 2011; 117: 5019-32.
  • 11.McCormick EM, Lott MT, Dulik MC, et al. Specifications of the ACMG/AMP standards and guidelines for mitochondrial DNA variant interpretation. Human Mutation. 2020.
  • 12.Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nature genetics. 1999; 23: 147.
  • 13.Lu J, Qian Y, Li Z, et al. Mitochondrial haplotypes may modulate the phenotypic manifestation of the deafness-associated 12S rRNA 1555A> G mutation. Mitochondrion. 2010; 10: 69-81.
  • 14.Beckstead WA, Ebbert MT, Rowe MJ, et al. Evolutionary pressure on mitochondrial cytochrome b is consistent with a role of CytbI7T affecting longevity during caloric restriction. PLoS One. 2009; 4: 5836.
  • 15.Öz Ö. JAK2 V617F Mutation Frequency in Chronic Myeloproliferative Disease Cases. Harran University Faculty of Medicine Journal. 2019; 16: 492-5.
  • 16.Goode EL, Ulrich CM, Potter JD. Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiology and Prevention Biomarkers. 2002; 11: 1513-30.
  • 17.Parr RL, Dakubo GD, Thayer RE, et al. Mitochondrial DNA as a potential tool for early cancer detection. Human genomics. 2006; 2: 252.
  • 18.Clayton DA, Vinograd J. Complex mitochondrial DNA in leukemic and normal human myeloid cells. Proceedings of the National Academy of Sciences. 1969; 62: 1077-84.
  • 19.Gattermann N. From sideroblastic anemia to the role of mitochondrial DNA mutations in myelodysplastic syndromes. Leukemia research. 2000; 24: 141-51.
  • 20.Wulfert M, Küpper AC, Tapprich C, et al. Analysis of mitochondrial DNA in 104 patients with myelodysplastic syndromes. Experimental hematology. 2008; 36: 577-86.
  • 21.Yao Y-G, Ogasawara Y, Kajigaya S, et al. Mitochondrial DNA sequence variation in single cells from leukemia patients. Blood. 2007; 109: 756-62.
  • 22.Zhou J, Gou H, Ye Y, et al. Sequence variations of mitochondrial DNA D‑loop region in patients with acute myeloid leukemia. Oncology letters. 2017; 14: 6269-76.
  • 23.Lee H, Geng C, Cheng M, et al. Single nucleotide polymorphisms in the mitochondrial displacement loop and age-at-onset of familial breast cancer. Mitochondrial DNA Part A. 2016; 27: 3082-5.
  • 24.Li S, Wan P, Peng T, et al. Associations between sequence variations in the mitochondrial DNA D-loop region and outcome of hepatocellular carcinoma. Oncology letters. 2016; 11: 3723-8.
  • 25.Cerezo M, Bandelt H-J, Martín-Guerrero I, et al. High mitochondrial DNA stability in B-cell chronic lymphocytic leukemia. PloS one. 2009; 4: 7902.
  • 26.Carew J, Zhou Y, Albitar M, et al. Mitochondrial DNA mutations in primary leukemia cells after chemotherapy: clinical significance and therapeutic implications. Leukemia. 2003; 17: 1437-47.
  • 27.Grist SA, Lu X, Morley AA. Mitochondrial mutations in acute leukaemia. Leukemia. 2004; 18: 1313-6.
  • 28.Shin MG, Kajigaya S, Levin BC, et al. Mitochondrial DNA mutations in patients with myelodysplastic syndromes. Blood, The Journal of the American Society of Hematology. 2003; 101: 3118-25.
  • 29.Monnat RJ, Maxwell CL, Loeb LA. Nucleotide sequence preservation of human leukemic mitochondrial DNA. Cancer research. 1985; 45: 1809-14.
  • 30.Linnartz B, Anglmayer R, Zanssen S. Comprehensive scanning of somatic mitochondrial DNA alterations in acute leukemia developing from myelodysplastic syndromes. Cancer research. 2004; 64: 1966-71.
  • 31.He L, Luo L, Proctor S, et al. Somatic mitochondrial DNA mutations in adult-onset leukaemia. Leukemia. 2003; 17: 2487-91.
  • 32.Canter JA, Kallianpur AR, Parl FF, et al. Mitochondrial DNA G10398A polymorphism and invasive breast cancer in African-American women. Cancer research. 2005; 65: 8028-33.
  • 33.Allegra E, Garozzo A, Lombardo N, et al. Mutations and polymorphisms in mitochondrial DNA in head and neck cancer cell lines. Acta otorhinolaryngologica italica. 2006; 26: 185.
  • 34.LaBiche RA, Yoshida M, Gallick GE, et al. Gene expression and tumor cell escape from host effector mechanisms in murine large cell lymphoma. Journal of cellular biochemistry. 1988; 36: 393-403.
  • 35.LaBiche RA, Demars M, Nicolson GL. Transcripts of the mitochondrial gene ND5 are overexpressed in highly metastatic murine large cell lymphoma cells. Vivo. 1992; 6: 317-24.
  • 36.Bargou RC, Daniel PT, Mapara MY, et al. Expression of the bcl‐2 gene family in normal and malignant breast tissue: low bax‐α expression in tumor cells correlates with resistance towards apoptosis. International journal of cancer. 1995; 60: 854-9.
  • 37.Binder C, Marx D, Binder L, Schauer A, Hiddemann W. Expression of Bax in relation to Bcl-2 and other predictive parameters in breast cancer. Annals of oncology. 1996; 7: 129-33.
  • 38.Vanniarajan A, Nayak D, Reddy AG, et al. Clinical and genetic uniqueness in an individual with MELAS. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics. 2006; 141: 440-4.
  • 39.Tanaka M, Ozawa T. Strand asymmetry in human mitochondrial DNA mutations. Genomics. 1994; 22: 327-35.
  • 40.Marcus JH, Posth C, Ringbauer H, et al. Genetic history from the Middle Neolithic to present on the Mediterranean island of Sardinia. Nature communications. 2020; 11: 1-14.
  • 41.Finnilä S, Lehtonen MS, Majamaa K. Phylogenetic network for European mtDNA. The American Journal of Human Genetics. 2001; 68: 1475-84.
  • 42.Mishmar D, Ruiz-Pesini E, Golik P, et al. Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences. 2003; 100: 171-6.
  • 43.van Oven M. Revision of the mtDNA tree and corresponding haplogroup nomenclature. Proceedings of the National Academy of Sciences. 2010; 107: 38-9.
  • 44.Dobrowolski SF, Gray J, Miller T, et al. Identifying sequence variants in the human mitochondrial genome using high‐resolution melt (HRM) profiling. Human mutation. 2009; 30: 891-8.
  • 45.Batini C, Lopes J, Behar DM, et al. Insights into the demographic history of African Pygmies from complete mitochondrial genomes. Molecular biology and evolution. 2011; 28: 1099-110.
  • 46.Hamblet NS, Ragland B, Ali M, et al. Mutations in mitochondrial‐encoded cytochrome c oxidase subunits I, II, and III genes detected in Alzheimer's disease using single‐strand conformation polymorphism. Electrophoresis. 2006; 27: 398-408.
  • 47.Gómez-Durán A, Pacheu-Grau D, López-Gallardo E, et al. Unmasking the causes of multifactorial disorders: OXPHOS differences between mitochondrial haplogroups. Human molecular genetics. 2010; 19: 3343-53.
  • 48.Loo J-H, Trejaut JA, Yen J-C, et al. Genetic affinities between the Yami tribe people of Orchid Island and the Philippine Islanders of the Batanes archipelago. BMC genetics. 2011; 12: 21.
  • 49.Ruvolo M, Zehr S, von Dornum M, et al. Mitochondrial COII sequences and modern human origins. Molecular Biology and Evolution. 1993; 10: 1115-35.
  • 50.Kumar S, Bellis C, Zlojutro M, et al. Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evolutionary Biology. 2011; 11: 293.
  • 51.Zsurka G, Schröder R, Kornblum C, et al. Tissue dependent co-segregation of the novel pathogenic G12276A mitochondrial tRNALeu (CUN) mutation with the A185G D-loop polymorphism. Journal of Medical Genetics. 2004; 41: 124.

Hematolojik maligniteli hastalarda mitokondriyal DNA polimorfizmlerinin araştırılması

Yıl 2021, Cilt: 12 Sayı: 2, 147 - 154, 30.06.2021
https://doi.org/10.18663/tjcl.907688

Öz

Amaç: Mitokondriyal DNA (mtDNA) polimorfizmleri, çeşitli kanser türlerine duyarlılıkta moleküler bir belirteç olarak düşünülebilir. Bu çalışmada, hematolojik malignite tanılı hastalarda mtDNA polimorfizmlerinin hastalık etyopatogenezi ile muhtemel ilişkisini araştırmayı amaçladık.
Gereç ve Yöntemler: Bu çalışma Atatürk Üniversitesi Tıbbi Genetik Anabilim Dalı'nda hematolojik malignite tanısı almış 80 hasta ve 80 sağlıklı bireyin katılımıyla gerçekleştirildi. Tüm katılımcılarda, mtDNA'nın 6 kodlama genindeki 13 polimorfizm bölgesi, PCR-RFLP yöntemi ile araştırıldı. Çalışmada değerlendirilen SNP'ler; NADH dehidrojenaz alt birimi 5-13704 (C / T), Sitokrom b 15315 (C / T), 12S rRNA 740 (G / A) ve 680 (T / C), Sitokrom C Oksidaz I 7319 (T / C), -7444 (G / A), Sitokrom C Oksidaz II 8252 (C / G), 7660 (G / A), 7975 (A / G), 8014 (A / G), 8113 (C / A), 8152 (G / A ) ve tRNA lizin 8310 (T / C) olarak tanımlandı.
Bulgular: ND-5 13704 (C> T) polimorfizmi, hematolojik maligniteli hastalarda sağlıklı kontrollere göre istatistiksel olarak anlamlı bulundu (p=0,001). Değerlendirilen diğer polimorfizmlerde hastalar ve kontroller arasında anlamlı bir fark yoktu.
Sonuç: Bu çalışmadan elde edilen bulgular, mtDNA ND-5 13704 (C>T) polimorfizminin, hematolojik malignitelerin etiyopatogenezinde rol oynayabileceğini düşündürtse de, bu polimorfik bölgenin önemini belirlemek için büyük ölçekli çalışmalara ihtiyaç vardır

Proje Numarası

(2009/305)

Kaynakça

  • 1.Lane N, Martin W. The energetics of genome complexity. Nature. 2010; 467: 929-34.
  • 2.Wallace DC. Mitochondria and cancer. Nature Reviews Cancer. 2012; 12 :685-98.
  • 3.Fernández‐Silva P, Enriquez JA, Montoya J. Replication and transcription of mammalian mitochondrial DNA. Experimental physiology. 2003; 88 :41-56.
  • 4.Singh KK, Kulawiec M. Mitochondrial DNA polymorphism and risk of cancer. Cancer Epidemiology: Springer; 2009: 291-303.
  • 5.Hertweck KL, Dasgupta S. The landscape of mtDNA modifications in cancer: a tale of two cities. Frontiers in oncology. 2017; 7: 262.
  • 6.Hüttemann M, Lee I, Grossman LI, et al. Phosphorylation of mammalian cytochrome c and cytochrome c oxidase in the regulation of cell destiny: respiration, apoptosis, and human disease. Mitochondrial Oxidative Phosphorylation: Springer; 2012: 237-64.
  • 7.Wang H, Xu J, Li D, Zhang S, et al. Identification of sequence polymorphisms in the mitochondrial cytochrome c oxidase genes as risk factors for hepatocellular carcinoma. Journal of clinical laboratory analysis. 2018; 32: 22299.
  • 8.Meng X-L, Meng H, Zhang W, et al. The role of mitochondrial tRNA variants in female breast cancer. Mitochondrial DNA Part A. 2016; 27: 3199-201.
  • 9.Vardiman JW, Thiele J, Arber DA, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009; 114: 937-51.
  • 10.Campo E, Swerdlow SH, Harris NL, et al. The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood, The Journal of the American Society of Hematology. 2011; 117: 5019-32.
  • 11.McCormick EM, Lott MT, Dulik MC, et al. Specifications of the ACMG/AMP standards and guidelines for mitochondrial DNA variant interpretation. Human Mutation. 2020.
  • 12.Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nature genetics. 1999; 23: 147.
  • 13.Lu J, Qian Y, Li Z, et al. Mitochondrial haplotypes may modulate the phenotypic manifestation of the deafness-associated 12S rRNA 1555A> G mutation. Mitochondrion. 2010; 10: 69-81.
  • 14.Beckstead WA, Ebbert MT, Rowe MJ, et al. Evolutionary pressure on mitochondrial cytochrome b is consistent with a role of CytbI7T affecting longevity during caloric restriction. PLoS One. 2009; 4: 5836.
  • 15.Öz Ö. JAK2 V617F Mutation Frequency in Chronic Myeloproliferative Disease Cases. Harran University Faculty of Medicine Journal. 2019; 16: 492-5.
  • 16.Goode EL, Ulrich CM, Potter JD. Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiology and Prevention Biomarkers. 2002; 11: 1513-30.
  • 17.Parr RL, Dakubo GD, Thayer RE, et al. Mitochondrial DNA as a potential tool for early cancer detection. Human genomics. 2006; 2: 252.
  • 18.Clayton DA, Vinograd J. Complex mitochondrial DNA in leukemic and normal human myeloid cells. Proceedings of the National Academy of Sciences. 1969; 62: 1077-84.
  • 19.Gattermann N. From sideroblastic anemia to the role of mitochondrial DNA mutations in myelodysplastic syndromes. Leukemia research. 2000; 24: 141-51.
  • 20.Wulfert M, Küpper AC, Tapprich C, et al. Analysis of mitochondrial DNA in 104 patients with myelodysplastic syndromes. Experimental hematology. 2008; 36: 577-86.
  • 21.Yao Y-G, Ogasawara Y, Kajigaya S, et al. Mitochondrial DNA sequence variation in single cells from leukemia patients. Blood. 2007; 109: 756-62.
  • 22.Zhou J, Gou H, Ye Y, et al. Sequence variations of mitochondrial DNA D‑loop region in patients with acute myeloid leukemia. Oncology letters. 2017; 14: 6269-76.
  • 23.Lee H, Geng C, Cheng M, et al. Single nucleotide polymorphisms in the mitochondrial displacement loop and age-at-onset of familial breast cancer. Mitochondrial DNA Part A. 2016; 27: 3082-5.
  • 24.Li S, Wan P, Peng T, et al. Associations between sequence variations in the mitochondrial DNA D-loop region and outcome of hepatocellular carcinoma. Oncology letters. 2016; 11: 3723-8.
  • 25.Cerezo M, Bandelt H-J, Martín-Guerrero I, et al. High mitochondrial DNA stability in B-cell chronic lymphocytic leukemia. PloS one. 2009; 4: 7902.
  • 26.Carew J, Zhou Y, Albitar M, et al. Mitochondrial DNA mutations in primary leukemia cells after chemotherapy: clinical significance and therapeutic implications. Leukemia. 2003; 17: 1437-47.
  • 27.Grist SA, Lu X, Morley AA. Mitochondrial mutations in acute leukaemia. Leukemia. 2004; 18: 1313-6.
  • 28.Shin MG, Kajigaya S, Levin BC, et al. Mitochondrial DNA mutations in patients with myelodysplastic syndromes. Blood, The Journal of the American Society of Hematology. 2003; 101: 3118-25.
  • 29.Monnat RJ, Maxwell CL, Loeb LA. Nucleotide sequence preservation of human leukemic mitochondrial DNA. Cancer research. 1985; 45: 1809-14.
  • 30.Linnartz B, Anglmayer R, Zanssen S. Comprehensive scanning of somatic mitochondrial DNA alterations in acute leukemia developing from myelodysplastic syndromes. Cancer research. 2004; 64: 1966-71.
  • 31.He L, Luo L, Proctor S, et al. Somatic mitochondrial DNA mutations in adult-onset leukaemia. Leukemia. 2003; 17: 2487-91.
  • 32.Canter JA, Kallianpur AR, Parl FF, et al. Mitochondrial DNA G10398A polymorphism and invasive breast cancer in African-American women. Cancer research. 2005; 65: 8028-33.
  • 33.Allegra E, Garozzo A, Lombardo N, et al. Mutations and polymorphisms in mitochondrial DNA in head and neck cancer cell lines. Acta otorhinolaryngologica italica. 2006; 26: 185.
  • 34.LaBiche RA, Yoshida M, Gallick GE, et al. Gene expression and tumor cell escape from host effector mechanisms in murine large cell lymphoma. Journal of cellular biochemistry. 1988; 36: 393-403.
  • 35.LaBiche RA, Demars M, Nicolson GL. Transcripts of the mitochondrial gene ND5 are overexpressed in highly metastatic murine large cell lymphoma cells. Vivo. 1992; 6: 317-24.
  • 36.Bargou RC, Daniel PT, Mapara MY, et al. Expression of the bcl‐2 gene family in normal and malignant breast tissue: low bax‐α expression in tumor cells correlates with resistance towards apoptosis. International journal of cancer. 1995; 60: 854-9.
  • 37.Binder C, Marx D, Binder L, Schauer A, Hiddemann W. Expression of Bax in relation to Bcl-2 and other predictive parameters in breast cancer. Annals of oncology. 1996; 7: 129-33.
  • 38.Vanniarajan A, Nayak D, Reddy AG, et al. Clinical and genetic uniqueness in an individual with MELAS. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics. 2006; 141: 440-4.
  • 39.Tanaka M, Ozawa T. Strand asymmetry in human mitochondrial DNA mutations. Genomics. 1994; 22: 327-35.
  • 40.Marcus JH, Posth C, Ringbauer H, et al. Genetic history from the Middle Neolithic to present on the Mediterranean island of Sardinia. Nature communications. 2020; 11: 1-14.
  • 41.Finnilä S, Lehtonen MS, Majamaa K. Phylogenetic network for European mtDNA. The American Journal of Human Genetics. 2001; 68: 1475-84.
  • 42.Mishmar D, Ruiz-Pesini E, Golik P, et al. Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences. 2003; 100: 171-6.
  • 43.van Oven M. Revision of the mtDNA tree and corresponding haplogroup nomenclature. Proceedings of the National Academy of Sciences. 2010; 107: 38-9.
  • 44.Dobrowolski SF, Gray J, Miller T, et al. Identifying sequence variants in the human mitochondrial genome using high‐resolution melt (HRM) profiling. Human mutation. 2009; 30: 891-8.
  • 45.Batini C, Lopes J, Behar DM, et al. Insights into the demographic history of African Pygmies from complete mitochondrial genomes. Molecular biology and evolution. 2011; 28: 1099-110.
  • 46.Hamblet NS, Ragland B, Ali M, et al. Mutations in mitochondrial‐encoded cytochrome c oxidase subunits I, II, and III genes detected in Alzheimer's disease using single‐strand conformation polymorphism. Electrophoresis. 2006; 27: 398-408.
  • 47.Gómez-Durán A, Pacheu-Grau D, López-Gallardo E, et al. Unmasking the causes of multifactorial disorders: OXPHOS differences between mitochondrial haplogroups. Human molecular genetics. 2010; 19: 3343-53.
  • 48.Loo J-H, Trejaut JA, Yen J-C, et al. Genetic affinities between the Yami tribe people of Orchid Island and the Philippine Islanders of the Batanes archipelago. BMC genetics. 2011; 12: 21.
  • 49.Ruvolo M, Zehr S, von Dornum M, et al. Mitochondrial COII sequences and modern human origins. Molecular Biology and Evolution. 1993; 10: 1115-35.
  • 50.Kumar S, Bellis C, Zlojutro M, et al. Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evolutionary Biology. 2011; 11: 293.
  • 51.Zsurka G, Schröder R, Kornblum C, et al. Tissue dependent co-segregation of the novel pathogenic G12276A mitochondrial tRNALeu (CUN) mutation with the A185G D-loop polymorphism. Journal of Medical Genetics. 2004; 41: 124.
Toplam 51 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Özgün Makale
Yazarlar

Neslihan Duzkale

Çiğdem Yüce Kahraman

İlhami Kiki Bu kişi benim

Rahşan Yıldırım

Gülden Sincan

Abdulgani Tatar

Proje Numarası (2009/305)
Yayımlanma Tarihi 30 Haziran 2021
Yayımlandığı Sayı Yıl 2021 Cilt: 12 Sayı: 2

Kaynak Göster

APA Duzkale, N., Yüce Kahraman, Ç., Kiki, İ., Yıldırım, R., vd. (2021). Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy. Turkish Journal of Clinics and Laboratory, 12(2), 147-154. https://doi.org/10.18663/tjcl.907688
AMA Duzkale N, Yüce Kahraman Ç, Kiki İ, Yıldırım R, Sincan G, Tatar A. Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy. TJCL. Haziran 2021;12(2):147-154. doi:10.18663/tjcl.907688
Chicago Duzkale, Neslihan, Çiğdem Yüce Kahraman, İlhami Kiki, Rahşan Yıldırım, Gülden Sincan, ve Abdulgani Tatar. “Investigation of Mitochondrial DNA Polymorphisms in Patients With Hematological Malignancy”. Turkish Journal of Clinics and Laboratory 12, sy. 2 (Haziran 2021): 147-54. https://doi.org/10.18663/tjcl.907688.
EndNote Duzkale N, Yüce Kahraman Ç, Kiki İ, Yıldırım R, Sincan G, Tatar A (01 Haziran 2021) Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy. Turkish Journal of Clinics and Laboratory 12 2 147–154.
IEEE N. Duzkale, Ç. Yüce Kahraman, İ. Kiki, R. Yıldırım, G. Sincan, ve A. Tatar, “Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy”, TJCL, c. 12, sy. 2, ss. 147–154, 2021, doi: 10.18663/tjcl.907688.
ISNAD Duzkale, Neslihan vd. “Investigation of Mitochondrial DNA Polymorphisms in Patients With Hematological Malignancy”. Turkish Journal of Clinics and Laboratory 12/2 (Haziran 2021), 147-154. https://doi.org/10.18663/tjcl.907688.
JAMA Duzkale N, Yüce Kahraman Ç, Kiki İ, Yıldırım R, Sincan G, Tatar A. Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy. TJCL. 2021;12:147–154.
MLA Duzkale, Neslihan vd. “Investigation of Mitochondrial DNA Polymorphisms in Patients With Hematological Malignancy”. Turkish Journal of Clinics and Laboratory, c. 12, sy. 2, 2021, ss. 147-54, doi:10.18663/tjcl.907688.
Vancouver Duzkale N, Yüce Kahraman Ç, Kiki İ, Yıldırım R, Sincan G, Tatar A. Investigation of mitochondrial DNA polymorphisms in patients with hematological malignancy. TJCL. 2021;12(2):147-54.


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