publication . Article . 2016

A Method for Amplicon Deep Sequencing of Drug Resistance Genes in Plasmodium falciparum Clinical Isolates from India

Akshaya Kumar Mohanty; Samuel C. Wassmer; Sonal Kale; Nabamita Bandyopadhyay; Om Singh; Sriti Kayal; Pavitra N. Rao; Sanjib Mohanty; Prashant K. Mallick; Swapna Uplekar; ...
Open Access
  • Published: 23 Mar 2016 Journal: Journal of Clinical Microbiology, volume 54, pages 1,500-1,511 (issn: 0095-1137, eissn: 1098-660X, Copyright policy)
  • Publisher: American Society for Microbiology
  • Country: United Kingdom
Abstract
<jats:p>A major challenge to global malaria control and elimination is early detection and containment of emerging drug resistance. Next-generation sequencing (NGS) methods provide the resolution, scalability, and sensitivity required for high-throughput surveillance of molecular markers of drug resistance. We have developed an amplicon sequencing method on the Ion Torrent PGM platform for targeted resequencing of a panel of six<jats:named-content content-type="genus-species">Plasmodium falciparum</jats:named-content>genes implicated in resistance to first-line antimalarial therapy, including artemisinin combination therapy, chloroquine, and sulfadoxine-pyrimeth...
Subjects
free text keywords: Microbiology (medical), Parasitology, Ion semiconductor sequencing, Genotype, Drug resistance, Biology, Amplicon, Deep sequencing, Genetics, Malaria, medicine.disease, medicine, Plasmodium falciparum, biology.organism_classification, Genotyping Techniques
Funded by
NIH| Genomics Core
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5U19AI089676-04
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
88 references, page 1 of 6

1. WHO/UNICEF. 2015. Achieving the malaria MDG target: reversing the incidence of malaria 2000 -2015. World Health Organization, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/184521/1/9789241 509442_eng.pdf?ua 1.

2. WHO. 2015. India drives down malaria rates, sets sights on elimination. World Health Organization, Geneva, Switzerland. http://www.who.int /features/2015/india-programme-end-malaria/en/.

3. Abdul-Ghani R, Al-Maktari MT, Al-Shibani LA, Allam AF. 2014. A better resolution for integrating methods for monitoring Plasmodium falciparum resistance to antimalarial drugs. Acta Trop 137:44 -57. http://dx .doi.org/10.1016/j.actatropica.2014.04.031.

4. Duraisingh MT, Curtis J, Warhurst DC. 1998. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol 89:1- 8. http://dx.doi.org/10.1006/expr.1998.4274. [OpenAIRE]

5. Durand R, Eslahpazire J, Jafari S, Delabre JF, Marmorat-Khuong A, di Piazza JP, Le Bras J. 2000. Use of molecular beacons to detect an antifolate resistance-associated mutation in Plasmodium falciparum. Antimicrob Agents Chemother 44:3461-3464. http://dx.doi.org/10.1128/AAC .44.12.3461-3464.2000. [OpenAIRE]

6. Wilson PE, Alker AP, Meshnick SR. 2005. Real-time PCR methods for monitoring antimalarial drug resistance. Trends Parasitol 21:278 -283. http://dx.doi.org/10.1016/j.pt.2005.04.007.

7. Alker AP, Mwapasa V, Purfield A, Rogerson SJ, Molyneux ME, Kamwendo DD, Tadesse E, Chaluluka E, Meshnick SR. 2005. Mutations associated with sulfadoxine-pyrimethamine and chlorproguanil resistance in Plasmodium falciparum isolates from Blantyre, Malawi. Antimicrob Agents Chemother 49:3919 -3921. http://dx.doi.org/10.1128/AAC .49.9.3919-3921.2005.

8. Ranford-Cartwright LC, Johnston KL, Abdel-Muhsin AM, Khan BK, Babiker HA. 2002. Critical comparison of molecular genotyping methods for detection of drug-resistant Plasmodium falciparum. Trans R Soc Trop Med Hyg 96:568 -572. http://dx.doi.org/10.1016/S0035 -9203(02)90446-3.

9. Nair S, Brockman A, Paiphun L, Nosten F, Anderson TJC. 2002. Rapid genotyping of loci involved in antifolate drug resistance in Plasmodium falciparum by primer extension. Int J Parasitol 32:852- 858. http://dx.doi .org/10.1016/S0020-7519(02)00033-4. [OpenAIRE]

10. Cruz RE, Shokoples SE, Manage DP, Yanow SK. 2010. High-throughput genotyping of single nucleotide polymorphisms in the Plasmodium falciparum dhfr gene by asymmetric PCR and melt-curve analysis. J Clin Microbiol 48:3081-3087. http://dx.doi.org/10.1128/JCM.00634-10.

11. Daniels R, Ndiaye D, Wall M, McKinney J, Séne PD, Sabeti PC, Volkman SK, Mboup S, Wirth DF. 2012. Rapid, field-deployable method for genotyping and discovery of drug-resistance single nucleotide polymorphisms in Plasmodium falciparum. Antimicrob Agents Chemother 56:2976 -2986. http://dx.doi.org/10.1128/AAC.05737-11.

12. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC. 2008. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 7:223. http://dx.doi.org/10.1186/1475-2875 -7-223. [OpenAIRE]

13. Campino S, Auburn S, Kivinen K, Zongo I, Ouedraogo J-B, Mangano V, Djimde A, Doumbo OK, Kiara SM, Nzila A, Borrmann S, Marsh K, Michon P, Mueller I, Siba P, Jiang H, Su X-Z, Amaratunga C, Socheat D, Fairhurst RM, Imwong M, Anderson T, Nosten F, White NJ, Gwilliam R, Deloukas P, MacInnis B, Newbold CI, Rockett K, Clark TG, Kwiatkowski DP. 2011. Population genetic analysis of Plasmodium falciparum parasites using a customized Illumina GoldenGate genotyping assay. PLoS One 6:e20251. http://dx.doi.org/10.1371/journal.pone .0020251. [OpenAIRE]

14. Kamau E, Alemayehu S, Feghali KC, Tolbert LS, Ogutu B, Ockenhouse CF. 2012. Development of a TaqMan allelic discrimination assay for detection of single nucleotides polymorphisms associated with anti-malarial drug resistance. Malaria J 11:23. http://dx.doi.org/10.1186/1475-2875-11 -23. [OpenAIRE]

15. Ali IM, Evehe M-SB, Netongo PM, Atogho-Tiedeu B, Akindeh-Nji M, Ngora H, Domkam IK, Diakite M, Baldip K, Ranford-Cartwright L, Mimche PN, Lamb T, Mbacham WF. 2014. Host candidate gene polymorphisms and associated clearance of P. falciparum amodiaquine and fansidar resistance mutants in children less than 5 years in Cameroon. Pathog Glob Health 108:323-333. http://dx.doi.org/10.1179 /2047773214Y.0000000159.

88 references, page 1 of 6
Abstract
<jats:p>A major challenge to global malaria control and elimination is early detection and containment of emerging drug resistance. Next-generation sequencing (NGS) methods provide the resolution, scalability, and sensitivity required for high-throughput surveillance of molecular markers of drug resistance. We have developed an amplicon sequencing method on the Ion Torrent PGM platform for targeted resequencing of a panel of six<jats:named-content content-type="genus-species">Plasmodium falciparum</jats:named-content>genes implicated in resistance to first-line antimalarial therapy, including artemisinin combination therapy, chloroquine, and sulfadoxine-pyrimeth...
Subjects
free text keywords: Microbiology (medical), Parasitology, Ion semiconductor sequencing, Genotype, Drug resistance, Biology, Amplicon, Deep sequencing, Genetics, Malaria, medicine.disease, medicine, Plasmodium falciparum, biology.organism_classification, Genotyping Techniques
Funded by
NIH| Genomics Core
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5U19AI089676-04
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
88 references, page 1 of 6

1. WHO/UNICEF. 2015. Achieving the malaria MDG target: reversing the incidence of malaria 2000 -2015. World Health Organization, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/184521/1/9789241 509442_eng.pdf?ua 1.

2. WHO. 2015. India drives down malaria rates, sets sights on elimination. World Health Organization, Geneva, Switzerland. http://www.who.int /features/2015/india-programme-end-malaria/en/.

3. Abdul-Ghani R, Al-Maktari MT, Al-Shibani LA, Allam AF. 2014. A better resolution for integrating methods for monitoring Plasmodium falciparum resistance to antimalarial drugs. Acta Trop 137:44 -57. http://dx .doi.org/10.1016/j.actatropica.2014.04.031.

4. Duraisingh MT, Curtis J, Warhurst DC. 1998. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol 89:1- 8. http://dx.doi.org/10.1006/expr.1998.4274. [OpenAIRE]

5. Durand R, Eslahpazire J, Jafari S, Delabre JF, Marmorat-Khuong A, di Piazza JP, Le Bras J. 2000. Use of molecular beacons to detect an antifolate resistance-associated mutation in Plasmodium falciparum. Antimicrob Agents Chemother 44:3461-3464. http://dx.doi.org/10.1128/AAC .44.12.3461-3464.2000. [OpenAIRE]

6. Wilson PE, Alker AP, Meshnick SR. 2005. Real-time PCR methods for monitoring antimalarial drug resistance. Trends Parasitol 21:278 -283. http://dx.doi.org/10.1016/j.pt.2005.04.007.

7. Alker AP, Mwapasa V, Purfield A, Rogerson SJ, Molyneux ME, Kamwendo DD, Tadesse E, Chaluluka E, Meshnick SR. 2005. Mutations associated with sulfadoxine-pyrimethamine and chlorproguanil resistance in Plasmodium falciparum isolates from Blantyre, Malawi. Antimicrob Agents Chemother 49:3919 -3921. http://dx.doi.org/10.1128/AAC .49.9.3919-3921.2005.

8. Ranford-Cartwright LC, Johnston KL, Abdel-Muhsin AM, Khan BK, Babiker HA. 2002. Critical comparison of molecular genotyping methods for detection of drug-resistant Plasmodium falciparum. Trans R Soc Trop Med Hyg 96:568 -572. http://dx.doi.org/10.1016/S0035 -9203(02)90446-3.

9. Nair S, Brockman A, Paiphun L, Nosten F, Anderson TJC. 2002. Rapid genotyping of loci involved in antifolate drug resistance in Plasmodium falciparum by primer extension. Int J Parasitol 32:852- 858. http://dx.doi .org/10.1016/S0020-7519(02)00033-4. [OpenAIRE]

10. Cruz RE, Shokoples SE, Manage DP, Yanow SK. 2010. High-throughput genotyping of single nucleotide polymorphisms in the Plasmodium falciparum dhfr gene by asymmetric PCR and melt-curve analysis. J Clin Microbiol 48:3081-3087. http://dx.doi.org/10.1128/JCM.00634-10.

11. Daniels R, Ndiaye D, Wall M, McKinney J, Séne PD, Sabeti PC, Volkman SK, Mboup S, Wirth DF. 2012. Rapid, field-deployable method for genotyping and discovery of drug-resistance single nucleotide polymorphisms in Plasmodium falciparum. Antimicrob Agents Chemother 56:2976 -2986. http://dx.doi.org/10.1128/AAC.05737-11.

12. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC. 2008. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 7:223. http://dx.doi.org/10.1186/1475-2875 -7-223. [OpenAIRE]

13. Campino S, Auburn S, Kivinen K, Zongo I, Ouedraogo J-B, Mangano V, Djimde A, Doumbo OK, Kiara SM, Nzila A, Borrmann S, Marsh K, Michon P, Mueller I, Siba P, Jiang H, Su X-Z, Amaratunga C, Socheat D, Fairhurst RM, Imwong M, Anderson T, Nosten F, White NJ, Gwilliam R, Deloukas P, MacInnis B, Newbold CI, Rockett K, Clark TG, Kwiatkowski DP. 2011. Population genetic analysis of Plasmodium falciparum parasites using a customized Illumina GoldenGate genotyping assay. PLoS One 6:e20251. http://dx.doi.org/10.1371/journal.pone .0020251. [OpenAIRE]

14. Kamau E, Alemayehu S, Feghali KC, Tolbert LS, Ogutu B, Ockenhouse CF. 2012. Development of a TaqMan allelic discrimination assay for detection of single nucleotides polymorphisms associated with anti-malarial drug resistance. Malaria J 11:23. http://dx.doi.org/10.1186/1475-2875-11 -23. [OpenAIRE]

15. Ali IM, Evehe M-SB, Netongo PM, Atogho-Tiedeu B, Akindeh-Nji M, Ngora H, Domkam IK, Diakite M, Baldip K, Ranford-Cartwright L, Mimche PN, Lamb T, Mbacham WF. 2014. Host candidate gene polymorphisms and associated clearance of P. falciparum amodiaquine and fansidar resistance mutants in children less than 5 years in Cameroon. Pathog Glob Health 108:323-333. http://dx.doi.org/10.1179 /2047773214Y.0000000159.

88 references, page 1 of 6
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