Association of Interferon-γ Receptor-1 Gene Polymorphism with Nontuberculous Mycobacterial Lung Infection among Iranian Patients with Pulmonary Disease

Poopak Farnia Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran;
Department of Biotechnology, Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

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Jalaledin Ghanavi Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran;

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Shima Saif Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran;

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Parissa Farnia Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran;

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Ali Akbar Velayati Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran;

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Nontuberculous mycobacteria (NTM) cause significant pulmonary infections in humans. Researchers have reported an association between interferon-gamma receptor-1 (IFN-γR1 or IFNGR1) deficiency and susceptibility to NTM, but the relevance of polymorphism within these genes is not yet clear. In this study, a single nucleotide polymorphism (SNP), T to C, at position-56 in NTM patients with pulmonary disease was investigated. Molecular identification of Mycobacterium isolates was performed with hsp65 genes using polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP). Then, the host genomic DNA from confirmed NTM patients (N = 80) and control subjects (N = 80) were screened for SNPs of IFNGR1 (T-56C) by PCR-RFLP. The results indicated that NTM patients had higher TC (26/80; 32.5%) or CC (46/80; 57.5%) genotypes in comparison with control groups (TC genotypes [22/80, 27.5%]; CC genotypes [6/80, 7.5%]) (P < 0.05). In this regard, all the patients infected with rapid-growing Mycobacterium (RGM, i.e., Mycobacterium chelonae and Mycobacterium fortuitum) had CC genotypes (100%). In contrary, only 50.7% (35/69) of infected patients with slow-growing Mycobacterium (i.e., Mycobacterium simiae, Mycobacterium kansasii, and Mycobacterium avium-intracellulare) had CC genotypes. Thus, patients with CC mutation in IFNGR1 at position-56 are more likely to develop RGM infection. In overall, there is a significant association between SNP of IFNGR1 at position-56 and susceptibility to NTM infection. Based on these data, we propose SNP of IFNGR1 at position-56 as a suitable “biomarker” for identifying populations at higher risk of infection.

Author Notes

Address correspondence to Jalaledin Ghanavi, Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran. E-mail: ghanavi@theaasm.org

Financial support: This study was funded by a grant from Mycobacteriology Research Centre (MRC.NRITLD/018/2014).

Authors’ addresses: Poopak Farnia, Department of Biotechnology, Advanced Technologies in Medicine, Tehran, Iran, E-mail: farniaff@theaasm.org. Jalaledin Ghanavi, Shima Saif, Parissa Farnia, and Ali Akbar Velayati, Mycobacteriology Research Centre (MRC), National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Tehran, Iran, E-mails: ghanavi@theaasm.org, saif@yahoo.com, farnia@hotmail.com, and velayati@theaasm.org.

  • 1.

    Cassidy PM, Hedberg K, Saulson A, McNelly E, Winthrop KL, 2009. Nontuberculous mycobacterial disease prevalence and risk factors: a changing epidemiology. Clin Infect Dis 49: 124129.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Falkinham JO, 2009. Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 107: 356367.

  • 3.

    Hruska K, Kaevska M, 2012. Mycobacteria in water, soil, plants and air: a review. Vet Med (Praha) 57: 623679.

  • 4.

    Winthrop KL, Chang E, Yamashita S, Iademarco MF, LoBue PA, 2009. Nontuberculous mycobacteria infections and anti-tumor necrosis factor-alpha therapy. Emerg Infect Dis 15: 15561561.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Glassroth J, 2008. Pulmonary disease due to nontuberculous mycobacteria. Chest 133: 243251.

  • 6.

    Johnson MM, Odell JA, 2014. Nontuberculous mycobacterial pulmonary infections. J Thorac Dis 6: 210220.

  • 7.

    Benator DA, Gordin FM, 1996. Nontuberculous mycobacteria in patients with human immunodeficiency virus infection. Semin Respir Infect 11: 285300.

  • 8.

    Keating MR, Daly JS; AST Infectious Diseases Community of Practice, 2013. Nontuberculous mycobacterial infections in solid organ transplantation. Am J Transplant 13: 7782.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Velayati AA, Bakayev V, Bahadori M, Tabatabaei SJ, Alaei A, Farahbood A, Masjedi MR, 2007. Religious and cultural traits in HIV/AIDS epidemics in sub-Saharan Africa. Arch Iran Med 10: 486497.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Cooke GS, Campbell SJ, Sillah J, Gustafson P, Bah B, Sirugo G, Bennett S, McAdam KP, Sow O, Lienhardt C, Hill AV, 2006. Polymorphism within the interferon-gamma/receptor complex is associated with pulmonary tuberculosis. Am J Respir Crit Care Med 174: 339343.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Park HY, Kwon YS, Ki CS, Suh GY, Chung MP, Kim H, Kwon OJ, Koh WJ, 2008. Interleukin-12 receptor beta1 polymorphisms and nontuberculous mycobacterial lung diseases. Lung 186: 241245.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Hwang JH, Kim EJ, Koh WJ, Kim SY, Lee SH, Suh GY, Kwon OJ, Ki CS, Ji Y, Kang M, Kim DH, 2007. Polymorphisms of interferon-gamma and interferon-gamma receptor 1 genes and non-tuberculous mycobacterial lung diseases. Tuberculosis (Edinb) 87: 166171.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Mansouri D, Mahdaviani SA, Khalilzadeh S, Mohajerani SA, Hasanzad M, Sadr S, Nadji SA, Karimi S, Droodinia A, Rezaei N, Linka RM, Bienemann K, Borkhardt A, Masjedi MR, Velayati AA, 2012. IL-2-inducible T-cell kinase deficiency with pulmonary manifestations due to disseminated Epstein-Barr virus infection. Int Arch Allergy Immunol 158: 418422.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Bakayev VV, Mohammadi F, Bahadori M, Sheikholslami M, Javeri A, Masjedi MR, Velayati AA, 2004. Arylamine N-acetyltransferase 2 slow acetylator polymorphisms in unrelated Iranian individuals. Eur J Clin Pharmacol 60: 467471.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Varahram M, Farnia P, Nasiri MJ, Karahrudi MA, Kazempour Dizagie M, Velayati AA, 2014. Association of Mycobacterium tuberculosis lineages with IFN-γ and TNF-α gene polymorphisms among pulmonary tuberculosis patient. Mediterr J Hematol Infect Dis 6: e2014015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Cooper AM, Khader SA, 2008. The role of cytokines in the initiation, expansion, and control of cellular immunity to tuberculosis. Immunol Rev 226: 191204.

  • 17.

    Shtrichman R, Samuel CE, 2001. The role of gamma interferon in antimicrobial immunity. Curr Opin Microbiol 4: 251259.

  • 18.

    Merlin G, van der Leede BJ, McKune K, Knezevic N, Bannwarth W, Romquin N, Viegas-Pequignot E, Kiefer H, Aguet M, Dembic Z, 1997. The gene for the ligand binding chain of the human interferon gamma receptor. Immunogenetics 45: 413421.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Le Coniat M, Alcaide-Loridan C, Fellous M, Berger R, 1989. Human interferon gamma receptor 1 (IFNGR1) gene maps to chromosome region 6q23-6q24. Hum Genet 84: 9294.

  • 20.

    Wang W, Ren W, Zhang X, Liu Y, Li C, 2014. Association between interferon gamma receptor 1-56C/T gene polymorphism and tuberculosis susceptibility: a meta-analysis. Chin Med J (Engl) 127: 37823788.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Jouanguy E, Lamhamedi-Cherradi S, Altare F, Fondanèche MC, Tuerlinckx D, Blanche S, Emile JF, Gaillard JL, Schreiber R, Levin M, Fischer A, Hivroz C, Casanova JL, 1997. Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guérin infection and a sibling with clinical tuberculosis. J Clin Invest 100: 26582664.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Sampaio MC, Coutinho A, 2007. Immunity to microbes: lessons from primary immunodeficiencies. Infect Immun 75: 15451555.

  • 23.

    Jüliger S, Bongartz M, Luty AJ, Kremsner PG, Kun JF, 2003. Functional analysis of a promoter variant of the gene encoding the interferon-gamma receptor chain I. Immunogenetics 54: 675680.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Velayati AA, Farnia P, Khalizadeh S, Farahbod AM, Hasanzadh M, Sheikolslam MF, 2011. Interferon-gamma receptor-1 gene promoter polymorphisms and susceptibility to leprosy in children of a single family. Am J Trop Med Hyg 84: 627629.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C, Gordin F, Holland SM, Horsburgh R, Huitt G, Iademarco MF, Iseman M, Olivier K, Ruoss S, von Reyn CF, Wallace RJ Jr, Winthrop KATS Mycobacterial Diseases Subcommittee; American Thoracic Society; Infectious Disease Society of America, 2007. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 175: 367416.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Miller SA, Dykes DD, Polesky HF, 1989. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16: 1215.

  • 27.

    Telenti A, Marchesi F, Balz M, Bally F, Böttger EC, Bodmer T, 1993. Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. J Clin Microbiol 31: 175178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Velayati AA, Farnia P, Mozafari M, Malekshahian D, Seif S, Rahideh S, Mirsaeidi M, 2014. Molecular epidemiology of nontuberculous mycobacteria isolates from clinical and environmental sources of a metropolitan city. PLoS One 9: e114428.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Thye T, Burchard GD, Nilius M, Müller-Myhsok B, Horstmann RD, 2003. Genome wide linkage analysis identifies polymorphism in the human interferon-gamma receptor affecting Helicobacter pylori infection. Am J Hum Genet 72: 448453.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kardum LB, Etokebe GE, Knezevic J, 2005. Interferon-γ receptor-1 gene promoter polymorphisms (G 611A; T-56C) and susceptibility to tuberculosis. Scand J Immunol 63: 142150.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA, Williamson R, Levin M, 1996. A mutation in the interferon-γ receptor gene and susceptibility to mycobacterial infection. N Engl J Med 335: 19411948.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    , D’Souza S, Levin M, Newport MJ, Kalabalikis P, Brown IN, Lenicker HM, Agius PV, Davies EG, Thrasher A, Klein N, Blackwell JM, 1995. Familial disseminated atypical mycobacterial infection in childhood: a human mycobacterial susceptibility gene? Lancet 345: 7983.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Bellamy R, 2003. Susceptibility to mycobacterial infections: the importance of host genetics. Genes Immun 23: 411.

  • 34.

    Guide SV, Holland SM, 2002. Host susceptibility factors in mycobacterial infection. Genetics and body morphotype. Infect Dis Clin North Am 16: 163186.

  • 35.

    Dorman SE, Holland SM, 1998. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J Clin Invest 101: 23642369.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Altare F, Jouanguy E, Lamhamedi-Cherradi S, Fondanéche MC, Fizame C, Ribiérre F, Merlin G, Dembic Z, Schreiber R, Lisowska-Grospierre B, Fischer A, Seboun E, Casanova JL, 1998. A causative relationship between mutant IFNgR1 alleles and impaired cellular response to IFNγ in a compound heterozygous child. Am J Hum Genet 62: 723726.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Dupuis S, Döffinger R, Picard C, Fieschi C, Altare F, Jouanguy E, Abel L, Casanova JL, 2000. Human interferon-γ-mediated immunity is a genetically controlled continuous trait that determines the outcome of mycobacterial invasion. Immunol Rev 178: 129137.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Lake MA, Ambrose LR, Lipman M C I, Lowe DM, 2016. “Why me, why now?” Using clinical immunology and epidemiology to explain who gets nontuberculous mycobacterial infection. BMC Med 14: 54.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Mirsaeidi M, Farshidpour M, Allen MB, Ebrahimi G, Falkinham JO, 2014. Highlight on advances in nontuberculous mycobacterial disease in North America. Biomed Res Int 2014: 919474.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Biranvand E, Abedian Kenary S, Ghaheri A, Rezaei MS, Hasannia H, Nasrolahi M, Parsaee MR, Ahanjan M, Biranvand B, Ahmadi Basiri E, Jivad F, 2011. Interferon-gamma gene polymorphism in patients with tuberculosis. Med Lab J 5: 1823.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Baghaei P, Tabarsi P, Farnia P, Marjani M, Sheikholeslami FM, Chitsaz M, Gorji Bayani P, Shamaei M, Mansouri D, Masjedi MR, Velayati AA, 2012. Pulmonary disease caused by Mycobacterium simiae in Iran’s national referral center for tuberculosis. J Infect Dev Ctries 6: 2328.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Velayati AA, Farnia P, Mozafari M, Mirsaeidi M, 2015. Nontuberculous mycobacteria isolation from clinical and environmental samples in Iran: twenty years of surveillance. BioMed Res Int 2015: 254285.

    • PubMed
    • Search Google Scholar
    • Export Citation
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