Interaction between host genes and Mycobacterium tuberculosis lineage can affect tuberculosis severity: Evidence for coevolution?


Autoři: Michael L. McHenry aff001;  Jacquelaine Bartlett aff001;  Robert P. Igo, Jr aff001;  Eddie M. Wampande aff002;  Penelope Benchek aff001;  Harriet Mayanja-Kizza aff003;  Kyle Fluegge aff001;  Noemi B. Hall aff001;  Sebastien Gagneux aff004;  Sarah A. Tishkoff aff006;  Christian Wejse aff007;  Giorgio Sirugo aff009;  W. Henry Boom aff010;  Moses Joloba aff002;  Scott M. Williams aff001;  Catherine M. Stein aff001
Působiště autorů: Department of Population and Quantitative Health Sciences, Case Western Reserve University School of Medicine, Cleveland, Ohio, United States of America aff001;  Department of Medical Microbiology, College of Health Sciences, Makerere University, Kampala, Uganda aff002;  Department of Medicine and Mulago Hospital, School of Medicine, Makerere University, Kampala, Uganda aff003;  Swiss Tropical and Public Health Institute, Basel, Switzerland aff004;  University of Basel, Basel, Switzerland aff005;  Departments of Genetics and Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America aff006;  Department of Infectious Diseases and Center for Global Health, Aarhus University, Aarhus, Denmark aff007;  Bandim Health Project, INDEPTH Network, Bissau, Guinea Bissau aff008;  Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, Unites States of America aff009;  Tuberculosis Research Unit, Case Western Reserve University School of Medicine, Cleveland, Ohio, United States of America aff010;  Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Cleveland, Ohio, United States of America aff011
Vyšlo v časopise: Interaction between host genes and Mycobacterium tuberculosis lineage can affect tuberculosis severity: Evidence for coevolution?. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008728
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008728

Souhrn

Genetic studies of both the human host and Mycobacterium tuberculosis (MTB) demonstrate independent association with tuberculosis (TB) risk. However, neither explains a large portion of disease risk or severity. Based on studies in other infectious diseases and animal models of TB, we hypothesized that the genomes of the two interact to modulate risk of developing active TB or increasing the severity of disease, when present. We examined this hypothesis in our TB household contact study in Kampala, Uganda, in which there were 3 MTB lineages of which L4-Ugandan (L4.6) is the most recent. TB severity, measured using the Bandim TBscore, was modeled as a function of host SNP genotype, MTB lineage, and their interaction, within two independent cohorts of TB cases, N = 113 and 121. No association was found between lineage and severity, but association between multiple polymorphisms in IL12B and TBscore was replicated in two independent cohorts (most significant rs3212227, combined p = 0.0006), supporting previous associations of IL12B with TB susceptibility. We also observed significant interaction between a single nucleotide polymorphism (SNP) in SLC11A1 and the L4-Ugandan lineage in both cohorts (rs17235409, meta p = 0.0002). Interestingly, the presence of the L4-Uganda lineage in the presence of the ancestral human allele associated with more severe disease. These findings demonstrate that IL12B is associated with severity of TB in addition to susceptibility, and that the association between TB severity and human genetics can be due to an interaction between genes in the two species, consistent with host-pathogen coevolution in TB.

Klíčová slova:

HIV – Host-pathogen interactions – Human genetics – Molecular genetics – Mycobacterium tuberculosis – Tuberculosis – Variant genotypes – Coevolution


Zdroje

1. Organization WH. Global Tuberculosis Report 2018 Factsheet. 2018.

2. Curtis J, Luo Y, Zenner HL, Cuchet-Lourenco D, Wu C, Lo K, et al. Susceptibility to tuberculosis is associated with variants in the ASAP1 gene encoding a regulator of dendritic cell migration. Nature genetics. 2015;47(5):523–7. Epub 2015/03/17. doi: 10.1038/ng.3248 25774636; PubMed Central PMCID: PMC4414475.

3. Hoal EG, Dippenaar A, Kinnear C, van Helden PD, Moller M. The arms race between man and Mycobacterium tuberculosis: Time to regroup. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2017. Epub 2017/08/28. doi: 10.1016/j.meegid.2017.08.021 28843547.

4. Orlova M, Schurr E. Human Genomics of Mycobacterium tuberculosis Infection and Disease. Current genetic medicine reports. 2017;5(3):125–31. Epub 2017/07/25. doi: 10.1007/s40142-017-0124-7 29201558.

5. Stein CM, Sausville L, Wejse C, Sobota RS, Zetola NM, Hill PC, et al. Genomics of human pulmonary tuberculosis: from genes to pathways. Current genetic medicine reports. 2017;5(4):149–66. Epub 2017/10/12. doi: 10.1007/s40142-017-0130-9 29805915.

6. Thye T, Vannberg FO, Wong SH, Owusu-Dabo E, Osei I, Gyapong J, et al. Genome-wide association analyses identifies a susceptibility locus for tuberculosis on chromosome 18q11.2. Nature genetics. 2010;42(9):739–41. Epub 2010/08/10. doi: 10.1038/ng.639 20694014; PubMed Central PMCID: PMC4975513.

7. Thye T, Owusu-Dabo E, Vannberg FO, van CR, Curtis J, Sahiratmadja E, et al. Common variants at 11p13 are associated with susceptibility to tuberculosis. Nat Genet. 2012;44(3):257–9. doi: 10.1038/ng.1080 22306650

8. Sobota RS, Stein CM, Kodaman N, Scheinfeldt LB, Maro I, Wieland-Alter W, et al. A Locus at 5q33.3 Confers Resistance to Tuberculosis in Highly Susceptible Individuals. American journal of human genetics. 2016;98(3):514–24. Epub 2016/03/05. doi: 10.1016/j.ajhg.2016.01.015 26942285; PubMed Central PMCID: PMC4800052.

9. Ganachari M, Guio H, Zhao N, Flores-Villanueva PO. Host gene-encoded severe lung TB: from genes to the potential pathways. Genes and immunity. 2012;13(8):605–20. Epub 2012/09/21. doi: 10.1038/gene.2012.39 22992722; PubMed Central PMCID: PMC3518758.

10. Coscolla M, Gagneux S. Consequences of genomic diversity in Mycobacterium tuberculosis. Seminars in immunology. 2014;26(6):431–44. Epub 2014/10/22. doi: 10.1016/j.smim.2014.09.012 25453224.

11. Di Pietrantonio T, Hernandez C, Girard M, Verville A, Orlova M, Belley A, et al. Strain-specific differences in the genetic control of two closely related mycobacteria. PLoS pathogens. 2010;6(10):e1001169–e. doi: 10.1371/journal.ppat.1001169 21060820.

12. Di Pietrantonio T, Schurr E. Host-pathogen specificity in tuberculosis. Advances in experimental medicine and biology. 2013;783:33–44. Epub 2013/03/08. doi: 10.1007/978-1-4614-6111-1_2 23468102.

13. Tientcheu LD, Koch A, Ndengane M, Andoseh G, Kampmann B, Wilkinson RJ. Immunological consequences of strain variation within the Mycobacterium tuberculosis complex. European journal of immunology. 2017;47(3):432–45. Epub 2017/02/06. doi: 10.1002/eji.201646562 28150302; PubMed Central PMCID: PMC5363233.

14. Stucki D, Brites D, Jeljeli L, Coscolla M, Liu Q, Trauner A, et al. Mycobacterium tuberculosis lineage 4 comprises globally distributed and geographically restricted sublineages. Nature genetics. 2016;48(12):1535–43. Epub 2016/11/01. doi: 10.1038/ng.3704 27798628; PubMed Central PMCID: PMC5238942.

15. Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. The Lancet Infectious diseases. 2007;7(5):328–37. Epub 2007/04/24. doi: 10.1016/S1473-3099(07)70108-1 17448936.

16. Gagneux S. Ecology and evolution of Mycobacterium tuberculosis. Nature reviews Microbiology. 2018;16(4):202–13. Epub 2018/02/20. doi: 10.1038/nrmicro.2018.8 29456241.

17. Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nature genetics. 2013;45(10):1176–82. Epub 2013/09/03. doi: 10.1038/ng.2744 23995134; PubMed Central PMCID: PMC3800747.

18. Gagneux S. Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci. 2012;367(1590):850–9. doi: 10.1098/rstb.2011.0316 22312052.

19. Kodaman N, Sobota RS, Mera R, Schneider BG, Williams SM. Disrupted human-pathogen co-evolution: a model for disease. Frontiers in genetics. 2014;5:290. Epub 2014/09/10. doi: 10.3389/fgene.2014.00290 25202324; PubMed Central PMCID: PMC4142859.

20. Wampande EM, Mupere E, Debanne SM, Asiimwe BB, Nsereko M, Mayanja H, et al. Long-term dominance of Mycobacterium tuberculosis Uganda family in peri-urban Kampala-Uganda is not associated with cavitary disease. BMC infectious diseases. 2013;13:484. Epub 2013/10/19. doi: 10.1186/1471-2334-13-484 24134504; PubMed Central PMCID: PMC3853102.

21. Schmid Hempel P. Evolutionary parasitologythe integrated study of infections, immunology, ecology, and genetics2011.

22. Frank SA. Models of parasite virulence. The Quarterly review of biology. 1996;71(1):37–78. doi: 10.1086/419267 8919665

23. Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85 (Pt 2):411–26. Epub 1982/10/01. doi: 10.1017/s0031182000055360 6755367.

24. Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(8):2869–73. Epub 2006/02/16. doi: 10.1073/pnas.0511240103 16477032; PubMed Central PMCID: PMC1413851.

25. Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature genetics. 2002;32(4):569–77. doi: 10.1038/ng1202-569 12457190

26. Abel L, Fellay J, Haas DW, Schurr E, Srikrishna G, Urbanowski M, et al. Genetics of human susceptibility to active and latent tuberculosis: present knowledge and future perspectives. The Lancet Infectious diseases. 2018;18(3):e64–e75. Epub 2017/11/08. doi: 10.1016/S1473-3099(17)30623-0 29111156.

27. Kodaman N, Pazos A, Schneider BG, Piazuelo MB, Mera R, Sobota RS, et al. Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(4):1455–60. Epub 2014/01/30. doi: 10.1073/pnas.1318093111 24474772; PubMed Central PMCID: PMC3910595.

28. Sorrell I, White A, Pedersen AB, Hails RS, Boots M. The evolution of covert, silent infection as a parasite strategy. Proceedings of the Royal Society B: Biological Sciences. 2009;276(1665):2217–26. doi: 10.1098/rspb.2008.1915 19324776

29. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. The immune response in tuberculosis. Annual review of immunology. 2013;31:475–527. Epub 2013/03/23. doi: 10.1146/annurev-immunol-032712-095939 23516984.

30. Nahid P, Jarlsberg LG, Kato-Maeda M, Segal MR, Osmond DH, Gagneux S, et al. Interplay of strain and race/ethnicity in the innate immune response to M. tuberculosis. PLoS One. 2018;13(5):e0195392. Epub 2018/05/23. doi: 10.1371/journal.pone.0195392 29787561; PubMed Central PMCID: PMC5963792.

31. Salie M, van der Merwe L, Moller M, Daya M, van der Spuy GD, van Helden PD, et al. Associations between human leukocyte antigen class I variants and the Mycobacterium tuberculosis subtypes causing disease. The Journal of infectious diseases. 2014;209(2):216–23. Epub 2013/08/16. doi: 10.1093/infdis/jit443 23945374; PubMed Central PMCID: PMC3873786.

32. Thuong NT, Tram TT, Dinh TD, Thai PV, Heemskerk D, Bang ND, et al. MARCO variants are associated with phagocytosis, pulmonary tuberculosis susceptibility and Beijing lineage. Genes and immunity. 2016;17(7):419–25. Epub 2016/11/18. doi: 10.1038/gene.2016.43 27853145; PubMed Central PMCID: PMC5133378.

33. Whalen CC, Zalwango S, Chiunda A, Malone L, Eisenach K, Joloba M, et al. Secondary attack rate of tuberculosis in urban households in Kampala, Uganda. PloS one. 2011;6(2):e16137–e. doi: 10.1371/journal.pone.0016137 21339819.

34. van Crevel R, Parwati I, Sahiratmadja E, Marzuki S, Ottenhoff TH, Netea MG, et al. Infection with Mycobacterium tuberculosis Beijing genotype strains is associated with polymorphisms in SLC11A1/NRAMP1 in Indonesian patients with tuberculosis. The Journal of infectious diseases. 2009;200(11):1671–4. Epub 2009/10/30. doi: 10.1086/648477 19863441.

35. Caws M, Thwaites G, Dunstan S, Hawn TR, Lan NT, Thuong NT, et al. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS pathogens. 2008;4(3):e1000034. Epub 2008/03/29. doi: 10.1371/journal.ppat.1000034 18369480; PubMed Central PMCID: PMC2268004.

36. Wejse C, Gustafson P, Nielsen J, Gomes VF, Aaby P, Andersen PL, et al. TBscore: Signs and symptoms from tuberculosis patients in a low-resource setting have predictive value and may be used to assess clinical course. Scandinavian journal of infectious diseases. 2008;40(2):111–20. Epub 2007/09/14. doi: 10.1080/00365540701558698 17852907.

37. Rasmussen TA, Sogaard OS, Camara C, Andersen PL, Wejse C. Serum procalcitonin in pulmonary tuberculosis. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2011;15(2):251–6, i. Epub 2011/01/12. 21219690.

38. Rudolf F. The Bandim TBscore—reliability, further development, and evaluation of potential uses. Global health action. 2014;7:24303. Epub 2014/05/27. doi: 10.3402/gha.v7.24303 24857613; PubMed Central PMCID: PMC4032506.

39. Rudolf F, Joaquim LC, Vieira C, Bjerregaard-Andersen M, Andersen A, Erlandsen M, et al. The Bandim tuberculosis score: reliability and comparison with the Karnofsky performance score. Scandinavian journal of infectious diseases. 2013;45(4):256–64. Epub 2012/11/02. doi: 10.3109/00365548.2012.731077 23113626.

40. Theron G, Zijenah L, Chanda D, Clowes P, Rachow A, Lesosky M, et al. Feasibility, accuracy, and clinical effect of point-of-care Xpert MTB/RIF testing for tuberculosis in primary-care settings in Africa: a multicentre, randomised, controlled trial. Lancet (London, England). 2014;383(9915):424–35. Epub 2013/11/02. doi: 10.1016/s0140-6736(13)62073-5 24176144.

41. Mahan CS, Zalwango S, Thiel BA, Malone LL, Chervenak KA, Baseke J, et al. Innate and adaptive immune responses during acute M. tuberculosis infection in adult household contacts in Kampala, Uganda. The American journal of tropical medicine and hygiene. 2012;86(4):690–7. Epub 2012/04/12. doi: 10.4269/ajtmh.2012.11-0553 22492155; PubMed Central PMCID: PMC3403758.

42. Tao L, Zalwango S, Chervenak K, Thiel B, Malone LL, Qiu F, et al. Genetic and shared environmental influences on interferon-gamma production in response to Mycobacterium tuberculosis antigens in a Ugandan population. The American journal of tropical medicine and hygiene. 2013;89(1):169–73. Epub 2013/05/01. doi: 10.4269/ajtmh.12-0670 23629934; PubMed Central PMCID: PMC3748477.

43. Hall NB, Igo RP Jr., Malone LL, Truitt B, Schnell A, Tao L, et al. Polymorphisms in TICAM2 and IL1B are associated with TB. Genes Immun. 2015;16(2):127–33. doi: 10.1038/gene.2014.77 25521228; PubMed Central PMCID: PMC4352113.

44. Morris GA, Edwards DR, Hill PC, Wejse C, Bisseye C, Olesen R, et al. Interleukin 12B (IL12B) genetic variation and pulmonary tuberculosis: a study of cohorts from The Gambia, Guinea-Bissau, United States and Argentina. PLoS One. 2011;6(2):e16656. Epub 2011/02/23. doi: 10.1371/journal.pone.0016656 21339808; PubMed Central PMCID: PMC3037276.

45. Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science (New York, NY). 1998;280(5368):1432–5. Epub 1998/06/20. doi: 10.1126/science.280.5368.1432 9603732.

46. Jouanguy E, Doffinger R, Dupuis S, Pallier A, Altare F, Casanova JL. IL-12 and IFN-gamma in host defense against mycobacteria and salmonella in mice and men. Current opinion in immunology. 1999;11(3):346–51. Epub 1999/06/22. doi: 10.1016/s0952-7915(99)80055-7 10375558.

47. Agranoff D, Monahan IM, Mangan JA, Butcher PD, Krishna S. Mycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. The Journal of experimental medicine. 1999;190(5):717–24. Epub 1999/09/08. doi: 10.1084/jem.190.5.717 10477555; PubMed Central PMCID: PMC2195619.

48. Blackwell JM, Goswami T, Evans CA, Sibthorpe D, Papo N, White JK, et al. SLC11A1 (formerly NRAMP1) and disease resistance. Cellular microbiology. 2001;3(12):773–84. Epub 2001/12/12. doi: 10.1046/j.1462-5822.2001.00150.x 11736990; PubMed Central PMCID: PMC3025745.

49. Singh N, Gedda MR, Tiwari N, Singh SP, Bajpai S, Singh RK. Solute carrier protein family 11 member 1 (Slc11a1) activation efficiently inhibits Leishmania donovani survival in host macrophages. Journal of parasitic diseases: official organ of the Indian Society for Parasitology. 2017;41(3):671–7. Epub 2017/08/30. doi: 10.1007/s12639-016-0864-4 28848257; PubMed Central PMCID: PMC5555910.

50. Carver PL. The Battle for Iron between Humans and Microbes. Current medicinal chemistry. 2018;25(1):85–96. Epub 2017/07/22. doi: 10.2174/0929867324666170720110049 28730969.

51. Parrow NL, Fleming RE, Minnick MF. Sequestration and scavenging of iron in infection. Infection and immunity. 2013;81(10):3503–14. Epub 2013/07/10. doi: 10.1128/IAI.00602-13 23836822; PubMed Central PMCID: PMC3811770.

52. Sheldon JR, Laakso HA, Heinrichs DE. Iron Acquisition Strategies of Bacterial Pathogens. Microbiology spectrum. 2016;4(2). Epub 2016/05/27. doi: 10.1128/microbiolspec.VMBF-0010-2015 27227297.

53. Stein CM, Baker AR. Tuberculosis as a complex trait: impact of genetic epidemiological study design. Mammalian genome: official journal of the International Mammalian Genome Society. 2011;22(1–2):91–9. Epub 2010/11/23. doi: 10.1007/s00335-010-9301-7 21104256.

54. Wu L, Deng H, Zheng Y, Mansjo M, Zheng X, Hu Y, et al. An association study of NRAMP1, VDR, MBL and their interaction with the susceptibility to tuberculosis in a Chinese population. International journal of infectious diseases: IJID: official publication of the International Society for Infectious Diseases. 2015;38:129–35. Epub 2015/08/12. doi: 10.1016/j.ijid.2015.08.003 26261060.

55. Delgado JC, Baena A, Thim S, Goldfeld AE. Ethnic-specific genetic associations with pulmonary tuberculosis. The Journal of infectious diseases. 2002;186(10):1463–8. Epub 2002/10/31. doi: 10.1086/344891 12404162.

56. Liu W, Cao WC, Zhang CY, Tian L, Wu XM, Habbema JD, et al. VDR and NRAMP1 gene polymorphisms in susceptibility to pulmonary tuberculosis among the Chinese Han population: a case-control study. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2004;8(4):428–34. Epub 2004/05/15. 15141734.

57. Singh A, Gaughan JP, Kashyap VK. SLC11A1 and VDR gene variants and susceptibility to tuberculosis and disease progression in East India. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2011;15(11):1468–74, i. Epub 2011/10/20. doi: 10.5588/ijtld.11.0089 22008758.

58. Nugraha J, Anggraini R. NRAMP1 polymorphism and susceptibility to lung tuberculosis in Surabaya, Indonesia. The Southeast Asian journal of tropical medicine and public health. 2011;42(2):338–41. Epub 2011/06/30. 21710855.

59. Hoal EG, Lewis LA, Jamieson SE, Tanzer F, Rossouw M, Victor T, et al. SLC11A1 (NRAMP1) but not SLC11A2 (NRAMP2) polymorphisms are associated with susceptibility to tuberculosis in a high-incidence community in South Africa. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2004;8(12):1464–71. Epub 2005/01/08. 15636493.

60. Dubaniewicz A, Jamieson SE, Dubaniewicz-Wybieralska M, Fakiola M, Nancy Miller E, Blackwell JM. Association between SLC11A1 (formerly NRAMP1) and the risk of sarcoidosis in Poland. European journal of human genetics: EJHG. 2005;13(7):829–34. Epub 2005/02/11. doi: 10.1038/sj.ejhg.5201370 15702130.

61. Taype CA, Castro JC, Accinelli RA, Herrera-Velit P, Shaw MA, Espinoza JR. Association between SLC11A1 polymorphisms and susceptibility to different clinical forms of tuberculosis in the Peruvian population. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2006;6(5):361–7. Epub 2006/02/08. doi: 10.1016/j.meegid.2006.01.002 16461017.

62. Ben-Selma W, Harizi H, Letaief M, Boukadida J. Age- and gender-specific effects on NRAMP1 gene polymorphisms and risk of the development of active tuberculosis in Tunisian populations. International journal of infectious diseases: IJID: official publication of the International Society for Infectious Diseases. 2012;16(7):e543–50. Epub 2012/05/23. doi: 10.1016/j.ijid.2011.11.016 22609013.

63. Awomoyi AA, Marchant A, Howson JM, McAdam KP, Blackwell JM, Newport MJ. Interleukin-10, polymorphism in SLC11A1 (formerly NRAMP1), and susceptibility to tuberculosis. The Journal of infectious diseases. 2002;186(12):1808–14. Epub 2002/11/26. doi: 10.1086/345920 12447767.

64. Leung KH, Yip SP, Wong WS, Yiu LS, Chan KK, Lai WM, et al. Sex- and age-dependent association of SLC11A1 polymorphisms with tuberculosis in Chinese: a case control study. BMC infectious diseases. 2007;7:19. Epub 2007/03/21. doi: 10.1186/1471-2334-7-19 17371589; PubMed Central PMCID: PMC1847518.

65. Qu Y, Tang Y, Cao D, Wu F, Liu J, Lu G, et al. Genetic polymorphisms in alveolar macrophage response-related genes, and risk of silicosis and pulmonary tuberculosis in Chinese iron miners. International journal of hygiene and environmental health. 2007;210(6):679–89. Epub 2007/01/16. doi: 10.1016/j.ijheh.2006.11.010 17223386.

66. Stein CM, Zalwango S, Malone LL, Thiel B, Mupere E, Nsereko M, et al. Resistance and susceptibility to Mycobacterium tuberculosis infection and disease in tuberculosis households in Kampala, Uganda. Am J Epidemiol. 2018;187:1477–89. doi: 10.1093/aje/kwx380 29304247

67. Stein CM, Zalwango S, Malone LL, Won S, Mayanja-Kizza H, Mugerwa RD, et al. Genome scan of M. tuberculosis infection and disease in Ugandans. PloS one. 2008;3(12):e4094. doi: 10.1371/journal.pone.0004094 19116662

68. Fluegge K, Malone LL, Nsereko M, Okware B, Wejse C, Kisingo H, et al. Impact of geographic distance on appraisal delay for active TB treatment seeking in Uganda: a network analysis of the Kawempe Community Health Cohort Study. BMC public health. 2018;18(1):798. Epub 2018/06/27. doi: 10.1186/s12889-018-5648-6 29940918; PubMed Central PMCID: PMC6019214.

69. Baker AR, Qiu F, Randhawa AK, Horne DJ, Adams MD, Shey M, et al. Genetic variation in TLR genes in Ugandan and South African populations and comparison with HapMap data. PloS one. 2012;7(10):e47597. Epub 2012/11/01. doi: 10.1371/journal.pone.0047597 23112821; PubMed Central PMCID: PMC3480404.

70. Wiens KE, Ernst JD. The Mechanism for Type I Interferon Induction by Mycobacterium tuberculosis is Bacterial Strain-Dependent. PLoS pathogens. 2016;12(8):e1005809. Epub 2016/08/09. doi: 10.1371/journal.ppat.1005809 27500737; PubMed Central PMCID: PMC4976988.

71. Igo RP Jr., Hall NB, Malone LL, Hall JB, Truitt B, Qiu F, et al. Fine-mapping analysis of a chromosome 2 region linked to resistance to Mycobacterium tuberculosis infection in Uganda reveals potential regulatory variants. Genes and immunity. 2018. Epub 2018/08/14. doi: 10.1038/s41435-018-0040-1 30100616.

72. Das S, Forer L, Schonherr S, Sidore C, Locke AE, Kwong A, et al. Next-generation genotype imputation service and methods. Nature genetics. 2016;48(10):1284–7. Epub 2016/08/30. doi: 10.1038/ng.3656 27571263; PubMed Central PMCID: PMC5157836.

73. McCarthy S, Das S, Kretzschmar W, Delaneau O, Wood AR, Teumer A, et al. A reference panel of 64,976 haplotypes for genotype imputation. Nature genetics. 2016;48(10):1279–83. Epub 2016/08/23. doi: 10.1038/ng.3643 27548312; PubMed Central PMCID: PMC5388176.

74. Kato-Maeda M, Gagneux S, Flores LL, Kim EY, Small PM, Desmond EP, et al. Strain classification of Mycobacterium tuberculosis: congruence between large sequence polymorphisms and spoligotypes. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2011;15(1):131–3. 21276309.

75. Wampande EM, Naniima P, Mupere E, Kateete DP, Malone LL, Stein CM, et al. Genetic variability and consequence of Mycobacterium tuberculosis lineage 3 in Kampala-Uganda. PLOS ONE. 2019;14(9):e0221644. doi: 10.1371/journal.pone.0221644 31498808

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 4

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×