Development of a Multilocus Sequence Typing (MLST) scheme for Treponema pallidum subsp. pertenue: Application to yaws in Lihir Island, Papua New Guinea

PLoS Neglected Tropical Diseases

Volumn 11, Issue 12, 2017, Pages

  Godornes, Charmie ^a   Giacani, Lorenzo ^a   Barry, Alyssa E ^b,c   Mitja, Oriol ^d,e,f   Lukehart, Sheila A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^e UNIVERSITY OF PAPUA NEW GUINEA   (Papua New Guinea)

^f Department of Medicine   (Papua New Guinea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BONA FIDE OUTER MEMBRANE PROTEIN; GENOMIC DNA; OUTER MEMBRANE PROTEIN; PUTATIVE OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CLINICAL EVALUATION; DISEASE CONTROL; GENE AMPLIFICATION; GENE LOCUS; GENE SEQUENCE; GENOTYPE; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MICROBIAL DIVERSITY; MULTILOCUS SEQUENCE TYPING; NUCLEOTIDE SEQUENCE; PAPUA NEW GUINEA; PHYLOGENY; SEQUENCE ANALYSIS; TP0136 GENE; TP0326 GENE; TP0619 GENE; TREPONEMA PALLIDUM; TREPONEMA PALLIDUM SUBSP. PERTENUE; ULCER; YAWS; CHILD; CLASSIFICATION; DEVELOPING COUNTRY; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; PROCEDURES; SEQUENCE ALIGNMENT; VIROLOGY;

BASE SEQUENCE; CHILD; DEVELOPING COUNTRIES; DNA, BACTERIAL; HUMANS; MULTILOCUS SEQUENCE TYPING; PAPUA NEW GUINEA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TREPONEMA PALLIDUM; YAWS;

EID: 85039999771     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0006113     Document Type: Article

References (52)

1. Antal GM, Lukehart SA, Meheus AZ, TheEndemic Treponematoses. Microbes Infect. 2002;4: 83–94.
2. Giacani L, Lukehart SA, The Endemic Treponematoses. Clin Microbiol Rev. 2014;27: 89–115. doi: 10.1128/CMR.00070-13 24396138
3. Asiedu K, Fitzpatrick C, Jannin J, Eradication of Yaws: Historical Efforts and Achieving WHO’s 2020 Target. PLoS Negl Trop Dis. 2014;8: e3016. doi: 10.1371/journal.pntd.0003016 25254372
4. Čejková D, Zobaníková M, Chen L, Pospíšilová P, Strouhal M, Qin X, et al. Whole Genome Sequences of Three Treponema pallidum ssp. pertenue Strains: Yaws and Syphilis Treponemes Differ in Less than 0.2% of the Genome Sequence. PLoS Negl Trop Dis. 2012;6: e1471. doi: 10.1371/journal.pntd.0001471 22292095
5. Mikalová L, Strouhal M, Čejková D, Zobaníková M, Pospíšilová P, Norris SJ, et al. Genome Analysis of Treponema pallidum subsp. pallidum and subsp. pertenue Strains: Most of the Genetic Differences Are Localized in Six Regions. PLoS ONE. 2010;5: e15713. doi: 10.1371/journal.pone.0015713 21209953
6. Centurion-Lara A, Molini BJ, Godornes C, Sun E, Hevner K, Van Voorhis WC, et al. Molecular Differentiation of Treponema pallidum subspecies. J Clin Microbiol. 2006;44: 3377–80. doi: 10.1128/JCM.00784-06 16954278
7. Zobaníková M, Strouhal M, Mikalová L, Čejková D, Ambrožová L, Pospíšilová P, et al. Whole Genome Sequence of the Treponema Fribourg-Blanc: Unspecified Simian Isolate Is Highly Similar to the Yaws Subspecies. PLoS Negl Trop Dis. 2013;7: e2172. doi: 10.1371/journal.pntd.0002172 23638193
8. Brinkman MB, McGill MA, Pettersson J, Rogers A, Matějková P, Šmajs D, et al. A Novel Treponema pallidum Antigen, TP0136, Is an Outer Membrane Protein That Binds Human Fibronectin. Infect Immun. 2008;76: 1848–1857. doi: 10.1128/IAI.01424-07 18332212
9. Centurion-Lara A, Castro C, Castillo R, Shaffer JM, Van Voorhis WC, Lukehart SA, The Flanking Region Sequences of the 15-kDa Lipoprotein Gene Differentiate Pathogenic Treponemes. J Infect Dis. 1998;177: 1036–40. 9534979
10. Pillay A, Liu H, Chen CY, Holloway B, Sturm AW, Steiner B, et al. Molecular subtyping of Treponema pallidum subspecies pallidum. Sex Transm Dis. 1998;25: 408–14. 9773432
11. Marra CM, Sahi SK, Tantalo LC, Godornes C, Reid T, Behets F, et al. Enhanced Molecular Typing of Treponema pallidum: Geographical Distribution of Strain Types and Association with Neurosyphilis. J Infect Dis. 2010;202: 1380–1388. doi: 10.1086/656533 20868271
12. Oliver S, Sahi SK, Tantalo LC, Godornes C, Neblett Fanfair R, Markowitz LE, et al. Molecular Typing of Treponema pallidum in Ocular Syphilis. Sex Transm Dis. 2016;43: 524–527. doi: 10.1097/OLQ.0000000000000478 27419819
13. Mikalová L, Pospíšilová P, Woznicová V, Kuklová I, Zákoucká H, Šmajs D, Comparison of CDC and Sequence-based Molecular Typing of Syphilis Treponemes: tpr and arp loci are Variable in Multiple Samples From the Same Patient. BMC Microbiol. 2013;13: 178–178. doi: 10.1186/1471-2180-13-178 23898829
14. Florindo C, Reigado V, Gomes JP, Azevedo J, Santo I, Borrego MJ, Molecular typing of Treponema pallidum clinical strains from Lisbon, Portugal. J Clin Microbiol. 2008;46: 3802–3. doi: 10.1128/JCM.00128-08 18753355
15. Flasarová M, Pospíšilová P, Mikalová L, Vališová Z, Dastychová E, Strnadel R, et al. Sequencing-based Molecular Typing of Treponema pallidum Strains in the Czech Republic: All Identified Genotypes Are Related to the Sequence of the SS14 strain. Acta Derm Venereol. 2012;92: 669–674. doi: 10.2340/00015555-1335 22434073
16. Flasarová M, Smajs D, Matejková P, Woznicová V, Heroldová-Dvoráková M, Votava M, Molecular Detection and Subtyping of Treponema pallidum subsp. pallidum In Clinical specimens]. Epidemiol Mikrobiol Imunol Cas Spolecnosti Epidemiol Mikrobiol Ceské Lékarské Spolecnosti JE Purkyne. 2006;55: 105–111.
17. Grillová L, Pĕtrošová H, Mikalová L, Strnadel R, Dastychová E, Kuklová I, et al. Molecular Typing of Treponema pallidum in the Czech Republic During 2011 to 2013: Increased Prevalence of Identified Genotypes and of Isolates with Macrolide Resistance. Munson E, editor. J Clin Microbiol. 2014;52: 3693–3700. doi: 10.1128/JCM.01292-14 25100820
18. Katz KA, Pillay A, Ahrens K, Kohn RP, Hermanstyne K, Bernstein KT, et al. Molecular Epidemiology of Syphilis—San Francisco, 2004–2007: Sex Transm Dis. 2010; 1.
19. Cameron CE, Lukehart SA, Castro C, Molini B, Godornes C, Van Voorhis WC, Opsonic Potential, Protective Capacity, and Sequence Conservation of the Treponema pallidum subspecies pallidum Tp92. J Infect Dis. 2000;181: 1401–13. doi: 10.1086/315399 10762571
20. Desrosiers DC, Anand A, Luthra A, Dunham-Ems SM, LeDoyt M, Cummings MA, et al. TP0326, a Treponema pallidum Beta-Barrel Assembly Machinery A (BamA) Orthologue and Rare Outer Membrane Protein. Mol Microbiol. 2011;80: 1496–515. doi: 10.1111/j.1365-2958.2011.07662.x 21488980
21. Ke W, Molini BJ, Lukehart SA, Giacani L, Treponema pallidum subsp. pallidum TP0136 Protein Is Heterogeneous Among Isolates and Binds Cellular and Plasma Fibronectin via its NH(2)-Terminal End. PLoS Negl Trop Dis. 2015;9: e0003662. doi: 10.1371/journal.pntd.0003662 25793702
22. Lukehart SA, Marra CM, Isolation and laboratory maintenance of Treponema pallidum. Curr Protoc Microbiol. 2007;Chapter 12: Unit 12A 1.
23. Gastinel P, Vaisman A, Hamelin A, Dunoyer F, Study of a recently isolated strain of Treponema pertenue]. Ann Dermatol Syphiligr Paris. 1963;90: 155–61. 13946771
24. Liska SL, Perine PL, Hunter EF, Crawford JA, Feeley JC, Isolation and Transportation of Treponema pertenue in Golden Hamsters. Curr Microbiol. 1982;7: 41–3.
25. Turner TB, Hollander DH, Biology of the Treponematoses. Geneva: World Health Organization; 1957.
26. Engelkens HJ, Oranje AP, Stolz E, Early Yaws, Imported in The Netherlands. Genitourin Med. 1989;65: 316–8. 2583714
27. Fribourg-Blanc A, Mollaret HH, Niel G, Serologic and microscopic confirmation of treponemosis in Guinea baboons]. Bull Soc Pathol Exot Fil. 1966;59: 54–9.
28. Mitjà O, Houinei W, Moses P, Kapa A, Paru R, Hays R, et al. Mass Treatment with Single-Dose Azithromycin for Yaws. N Engl J Med. 2015;372: 703–710. doi: 10.1056/NEJMoa1408586 25693010
29. Mitjà O, Lukehart SA, Pokowas G, Moses P, Kapa A, Godornes C, et al. Haemophilus ducreyi as a Cause of Skin Ulcers in Children from a Yaws-Endemic Area of Papua New Guinea: A Prospective Cohort Study. Lancet Glob Health. 2014;2: e235–e241. doi: 10.1016/S2214-109X(14)70019-1 25103064
30. Centurion-Lara A, Giacani L, Godornes C, Molini BJ, Brinck Reid T, Lukehart SA, Fine Analysis of Genetic Diversity of the tpr Gene Family among Treponemal Species, Subspecies and Strains. PLoS Negl Trop Dis. 2013;7: e2222. doi: 10.1371/journal.pntd.0002222 23696912
31. Hall, T.A. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Ser. 41:95–98. Nucl Acids Symp. 1999;Ser. 41: 95–98.
32. Kumar S, Stecher G, Tamura K, MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33: 1870–1874. doi: 10.1093/molbev/msw054 27004904
33. Knauf S, Raphael J, Mitjà O, Lejora IAV, Chuma IS, Batamuzi EK, et al. Isolation of Treponema DNA from Necrophagous Flies in a Natural Ecosystem. EBioMedicine. 2016;11: 85–90. doi: 10.1016/j.ebiom.2016.07.033 27488881
34. Mikalová L, Grillová L, Osbak K, Strouhal M, Kenyon C, Crucitti T, et al. Molecular Typing of Syphilis-causing Strains Among Human Immunodeficiency Virus-positive Patients in Antwerp, Belgium. Sex Transm Dis. 2017;44: 376–379. doi: 10.1097/OLQ.0000000000000600 28499290
35. Li Z, Wang C, Xiao H, Zhao W, Li Z, Zheng R, et al. Enhanced Molecular Typing of Treponema pallidum Identified a New Tp0548 Gene type in Shandong, China. APMIS. 2017;125: 937–939. doi: 10.1111/apm.12724 28766763
36. Grange PA, Allix-Beguec C, Chanal J, Benhaddou N, Gerhardt P, Morini J-P, et al. Molecular Subtyping of Treponema pallidum in Paris, France. Sex Transm Dis. 2013;40.
37. Tian H, Li Z, Li Z, Hou J, Zheng R, Li F, et al. Molecular Typing of Treponema pallidum: Identification of a New Sequence of tp0548 Gene in Shandong, China. Sex Transm Dis. 2014;41.
38. Read P, Tagg KA, Jeoffreys N, Guy RJ, Gilbert GL, Donovan B, Treponema pallidum Strain-Types and Association with Macrolide Resistance in Sydney, Australia: New tp0548 Types Identified. J Clin Microbiol. 2016; 54:2172–2174. doi: 10.1128/JCM.00959-16 27194693
39. Šmajs D, Zobaníková M, Strouhal M, Čejková D, Dugan-Rocha S, Pospíšilová P, et al. Complete Genome Sequence of Treponema paraluiscuniculi, Strain Cuniculi A: The Loss of Infectivity to Humans Is Associated with Genome Decay. PLoS ONE. 2011;6: e20415. doi: 10.1371/journal.pone.0020415 21655244
40. Castro R, Prieto E, A M.J., NManata MJ, Botas J, Pereira FM, Molecular subtyping of Treponema pallidum subsp.pallidum in Lisbon, Portugal. J Clin Microbiol. 2009;47: 2510–2512. doi: 10.1128/JCM.00287-08 19494073
41. Salado-Rasmussen K, Cowan S, Gerstoft J, Kiellberg Larsen H, Hoffmann S, Bygum Knudsen T, et al. Molecular Typing of Treponema pallidum in Denmark: A Nationwide Study of Syphilis. Acta Derm Venereol. 2014; 96:202–206
42. Noordhoek GT, Hermans PW, Paul AN, Schouls LM, van der Sluis JJ, van Embden JD, Treponema pallidum subspecies pallidum (Nichols) and Treponema pallidum subspecies pertenue (CDC 2575) differ in at least one nucleotide: comparison of two homologous antigens. Microb Pathog. 1989;6: 29–42. 2471912
43. Strouhal M, Mikalová L, Havlíčková P, Tenti P, Čejková D, Rychlík I, et al. Complete Genome Sequences of Two Strains of Treponema pallidum subsp. pertenue from Ghana, Africa: Identical Genome Sequences in Samples Isolated More Than 7 Years Apart. PLoS Negl Trop Dis. 2017;11: e0005894. doi: 10.1371/journal.pntd.0005894 28886021
44. Mikalová L, Strouhal M, Grillová L, Šmajs D, The Molecular Typing Data of Recently Identified Subtype 11q/j of Treponema pallidum subsp. pallidum Suggest Imported Case of Yaws. Sex Transm Dis. 2014;41.
45. Mikalová L, Strouhal M, Oppelt J, Grange PA, Janier M, Benhaddou N, et al. Human Treponema pallidum 11q/j Isolate Belongs to subsp. endemicum But Contains Two Loci with a Sequence in TP0548 and TP0488 similar to subsp. pertenue and subsp. pallidum, Respectively. PLoS Negl Trop Dis. 2017;11: e0005434. doi: 10.1371/journal.pntd.0005434 28263990
46. Knauf S, Batamuzi EK, Mlengeya T, Kilewo M, Lejora IA, Nordhoff M, et al. Treponema Infection associated with Genital Ulceration in Wild Baboons. Vet Pathol. 2012;49: 292–303. doi: 10.1177/0300985811402839 21411621
47. Harper KN, Fyumagwa RD, Hoare R, Wambura PN, Coppenhaver DH, Sapolsky RM, et al. Treponema pallidum Infection in the Wild Baboons of East Africa: Distribution and Genetic Characterization of the Strains Responsible. PLOS ONE. 2012;7: e50882. doi: 10.1371/journal.pone.0050882 23284649
48. Pětrošová H, Zobaníková M, Čejková D, Mikalová L, Pospíšilová P, Strouhal M, et al. Whole Genome Sequence of Treponema pallidum ssp. pallidum, Strain Mexico A, Suggests Recombination between Yaws and Syphilis Strains. PLoS Negl Trop Dis. 2012;6.
49. Graves S, Downes J, Experimental infection of man with rabbit-virulent Treponema paraluis- cuniculi. Br J Vener Dis. 1981;57: 7–10. 7470837
50. Zhang R-L, Wang Q-Q, Zhang J-P, Yang L-J, Molecular Subtyping of Treponema pallidum and Associated Factors of Serofast Status in Early Syphilis Patients: Identified Novel Genotype and Cytokine Marker. PloS One. 2017;12: e0175477. doi: 10.1371/journal.pone.0175477 28410389
51. Edington GM, Cardiovascular Disease as a Cause of Death in the Gold Coast African. Trans R Soc Trop Med Hyg. 1954;48: 419–425. 13216946
52. Roman GC, Roman LN, Occurrence of Congenital, Cardiovascular, Visceral, Neurologic, and Neuro-Ophthalmologic Complications in Late Yaws: A Theme For Future Research. Rev Infect Dis. 1986;8: 760–70. 3538316