NOS2 variants reveal a dual genetic control of nitric oxide levels, susceptibility to Plasmodium infection, and cerebral malaria

Infection and Immunity

Volumn 82, Issue 3, 2014, Pages 1287-1295

  de Jesus Trovoada, Maria ^a,b   Martins, Madalena ^a,c   Mansour, Riadh Ben ^a   Do Rosário Sambo, Maria ^a,d   Fernandes, Ana B ^e   Gonçalves, Lígia Antunes ^a   Borja, Artur ^f   Moya, Roni ^a   Almeida, Paulo ^a   Costa, João ^a   Marques, Isabel ^a   Paula Macedo, M ^e   Coutinho, António ^a   Narum, David L ^g   Penha Gonçalves, Carlos ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b Centro National de Endemias   (Sao Tome and Principe)

^c INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^d Universidade Agostinho Neto   (Angola)

^e NOVA MEDICAL SCHOOL   (Portugal)

^f Hospital Dr Manuel Quaresma Dias da Graça   (Sao Tome and Principe)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELES; BIOLOGICAL MARKERS; HUMANS; MALARIA; MALARIA, CEREBRAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PLASMODIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC;

EID: 84894261379     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01070-13     Document Type: Article

References (41)

1. Driss A, Hibbert JM, Wilson NO, Iqbal SA, Adamkiewicz TV, Stiles JK.2011. Genetic polymorphisms linked to susceptibility to malaria. Malar. J. 10:271. http://dx.doi.org/10.1186/1475-2875-10-271.
2. Lopez C, Saravia C, Gomez A, Hoebeke J, Patarroyo MA. 2010. Mechanisms of genetically based resistance to malaria. Gene 467:1-12. http://dx .doi.org/10.1016/j.gene.2010.07.008.
3. Miller LH, Ackerman HC, Su XZ, Wellems TE. 2013. Malaria biology and disease pathogenesis: insights for new treatments. Nat. Med. 19:156-167. http://dx.doi.org/10.1038/nm.3073.
4. Brunet LR. 2001. Nitric oxide in parasitic infections. Int. Immunopharmacol. 1:1457-1467. http://dx.doi.org/10.1016/S1567-5769(01)00090-X.
5. Gudo ES, Prista A, Jani IV. 2013. Impact of asymptomatic Plasmodium falciparum parasitemia on the immunohematological indices among school children and adolescents in a rural area highly endemic for Malaria in southern Mozambique. BMC Infect. Dis. 13:244. http://dx.doi.org/10 .1186/1471-2334-13-244.
6. Dhangadamajhi G, Mohapatra BN, Kar SK, Ranjit MR. 2009. The CCTTT pentanucleotide microsatellite in iNOS promoter influences the clinical outcome in Plasmodium falciparum infection. Parasitol. Res. 104: 1315-1320. http://dx.doi.org/10.1007/s00436-009-1329-9.
7. Parikh S, Dorsey G, Rosenthal PJ. 2004. Host polymorphisms and the incidence of malaria in Ugandan children. Am. J. Trop. Med. Hyg. 71: 750-753.
8. Cramer JP, Mockenhaupt FP, Ehrhardt S, Burkhardt J, Otchwemah RN, Dietz E, Gellert S, Bienzle U. 2004. iNOS promoter variants and severe malaria in Ghanaian children. Trop. Med. Int. Health 9:1074-1080. http://dx.doi.org/10.1111/j.1365-3156.2004.01312.x.
9. Ohashi J, Naka I, Patarapotikul J, Hananantachai H, Looareesuwan S, Tokunaga K. 2002. Significant association of longer forms of CCTTT Microsatellite repeat in the inducible nitric oxide synthase promoter with severe malaria in Thailand. J. Infect. Dis. 186:578-581. http://dx.doi.org /10.1086/341779.
10. Burgner D, Usen S, Rockett K, Jallow M, Ackerman H, Cervino A, Pinder M, Kwiatkowski DP. 2003. Nucleotide and haplotypic diversity of the NOS2A promoter region and its relationship to cerebral malaria. Hum. Genet. 112:379-386. http://dx.doi.org/10.1007/s00439-002-0882-4.
11. Hobbs MR, Udhayakumar V, Levesque MC, Booth J, Roberts JM, Tkachuk AN, Pole A, Coon H, Kariuki S, Nahlen BL, Mwaikambo ED, Lal AL, Granger DL, Anstey NM, Weinberg JB. 2002. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children. Lancet 360: 1468-1475. http://dx.doi.org/10.1016/S0140-6736(02)11474-7.
12. Planche T, Macallan DC, Sobande T, Borrmann S, Kun JF, Krishna S, Kremsner PG. 2010. Nitric oxide generation in children with malaria and the NOS2G-954C promoter polymorphism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299:R1248-R1253. http://dx.doi.org/10.1152/ajpregu .00390.2010.
13. Levesque MC, Hobbs MR, O'Loughlin CW, Chancellor JA, Chen Y, Tkachuk AN, Booth J, Patch KB, Allgood S, Pole AR, Fernandez CA, Mwaikambo ED, Mutabingwa TK, Fried M, Sorensen B, Duffy PE, Granger DL, Anstey NM, Weinberg JB. 2010. Malaria severity and human nitric oxide synthase type 2 (NOS2) promoter haplotypes. Hum. Genet. 127:163-182. http://dx.doi.org/10.1007/s00439-009-0753-3.
14. Boutlis CS, Hobbs MR, Marsh RL, Misukonis MA, Tkachuk AN, Lagog M, Booth J, Granger DL, Bockarie MJ, Mgone CS, Levesque MC, Weinberg JB, Anstey NM. 2003. Inducible nitric oxide synthase (NOS2) promoter CCTTT repeat polymorphism: relationship to in vivo nitric oxide production/NOS activity in an asymptomatic malaria-endemic population. Am. J. Trop. Med. Hyg. 69:569-573.
15. Mombo LE, Ntoumi F, Bisseye C, Ossari S, Lu CY, Nagel RL, Krishnamoorthy R. 2003. Human genetic polymorphisms and asymptomatic Plasmodium falciparum malaria in Gabonese schoolchildren. Am. J. Trop. Med. Hyg. 68:186-190.
16. Le Port A, Cot M, Etard JF, Gaye O, Migot-Nabias F, Garcia A. 2008. Relation between Plasmodium falciparum asymptomatic infection and malaria attacks in a cohort of Senegalese children. Malar. J. 7:193. http: //dx.doi.org/10.1186/1475-2875-7-193.
17. Males S, Gaye O, Garcia A. 2008. Long-term asymptomatic carriage of Plasmodium falciparum protects from malaria attacks: a prospective study among Senegalese children. Clin. Infect. Dis. 46:516-522. http://dx.doi .org/10.1086/526529.
18. Hoyer S, Nguon S, Kim S, Habib N, Khim N, Sum S, Christophel EM, Bjorge S, Thomson A, Kheng S, Chea N, Yok S, Top S, Ros S, Sophal U, Thompson MM, Mellor S, Ariey F, Witkowski B, Yeang C, Yeung S, Duong S, Newman RD, Menard D. 2012. Focused screening and treatment (FSAT): a PCR-based strategy to detect malaria parasite carriers and contain drug resistant P. falciparum, Pailin, Cambodia. PLoS One 7:e45797. http://dx.doi.org/10.1371/journal.pone.0045797.
19. Tran TM, Li S, Doumbo S, Doumtabe D, Huang CY, Dia S, Bathily A, Sangala J, Kone Y, Traore A, Niangaly M, Dara C, Kayentao K, Ongoiba A, Doumbo OK, Traore B, Crompton PD. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin. Infect. Dis. 57:40-47. http://dx.doi.org/10.1093/cid/cit174.
20. Babiker HA, Gadalla AA, Ranford-Cartwright LC. 2013. The role of asymptomatic Plasmodium falciparum parasitaemia in the evolution of antimalarial drug resistance in areas of seasonal transmission. Drug Resist. Update 16:1-9. http://dx.doi.org/10.1016/j.drup.2013.02.001.
21. Bottius E, Guanzirolli A, Trape JF, Rogier C, Konate L, Druilhe P. 1996. Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction. Trans. R. Soc. Trop. Med. Hyg. 90:15-19. http://dx.doi.org/10.1016/S00 35-9203(96)90463-0.
22. Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. 2002. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am. J. Trop. Med. Hyg. 66:641-648.
23. Nkoghe D, Akue JP, Gonzalez JP, Leroy EM. 2011. Prevalence of Plasmodium falciparum infection in asymptomatic rural Gabonese populations. Malar. J. 10:33. http://dx.doi.org/10.1186/1475-2875-10-33.
24. Vinetz JM, Gilman RH. 2002. Asymptomatic Plasmodium parasitemia and the ecology of malaria transmission. Am. J. Trop. Med. Hyg. 66:639-640.
25. Billo MA, Johnson ES, Doumbia SO, Poudiougou B, Sagara I, Diawara SI, Diakite M, Diallo M, Doumbo OK, Tounkara A, Rice J, James MA, Krogstad DJ. 2012. Sickle cell trait protects against Plasmodium falciparum infection. Am. J. Epidemiol. 176(Suppl 7):S175-S185. http://dx.doi .org/10.1093/aje/kws323.
26. Lawaly YR, Sakuntabhai A, Marrama L, Konate L, Phimpraphi W, Sokhna C, Tall A, Sarr FD, Peerapittayamongkol C, Louicharoen C, Schneider BS, Levescot A, Talman A, Casademont I, Menard D, Trape JF, Rogier C, Kaewkunwal J, Sura T, Nuchprayoon I, Ariey F, Baril L, Singhasivanon P, Mercereau-Puijalon O, Paul R. 2010. Heritability of the human infectious reservoir of malaria parasites. PLoS One 5:e11358. http://dx.doi.org/10.1371/journal.pone.0011358.
27. Sambo MR, Trovoada MJ, Benchimol C, Quinhentos V, Goncalves L, Velosa R, Marques MI, Sepulveda N, Clark TG, Mustafa S, Wagner O, Coutinho A, Penha-Goncalves C. 2010. Transforming growth factor beta 2 and heme oxygenase 1 genes are risk factors for the cerebral malaria syndrome in Angolan children. PLoS One 5:e11141. http://dx.doi.org/10 .1371/journal.pone.0011141.
28. Greenwood BM, Armstrong JR. 1991. Comparison of two simple methods for determining malaria parasite density. Trans. R. Soc. Trop. Med. Hyg. 85:186-188. http://dx.doi.org/10.1016/0035-9203(91)90015-Q.
29. Snounou G. 1996. Detection and identification of the four malaria parasite species infecting humans by PCR amplification. Methods Mol. Biol. 50:263-291.
30. Plassmeyer ML, Reiter K, Shimp RL, Jr, Kotova S, Smith PD, Hurt DE, House B, Zou X, Zhang Y, Hickman M, Uchime O, Herrera R, Nguyen V, Glen J, Lebowitz J, Jin AJ, Miller LH, MacDonald NJ, Wu Y, Narum DL. 2009. Structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate. J. Biol. Chem. 284:26951-26963. http://dx.doi.org/10.1074/jbc.M109.013706.
31. Afonso RA, Fernandes AB, Santos C, Ligeiro D, Ribeiro RT, Lima IS, Patarrao RS, Videira PA, Caldeira J, Macedo MP. 2012. Postprandial insulin resistance in Zucker diabetic fatty rats is associated with parasympathetic-nitric oxide axis deficiencies. J. Neuroendocrinol. 24:1346-1355. http://dx.doi.org/10.1111/j.1365-2826.2012.02341.x.
32. Gonzalez JR, Armengol L, Sole X, Guino E, Mercader JM, Estivill X, Moreno V. 2007. SNPassoc: an R package to perform whole genome association studies. Bioinformatics 23:644-645. http://dx.doi.org/10 .1093/bioinformatics/btm025.
33. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. http: //dx.doi.org/10.1093/bioinformatics/bth457.
34. Druilhe P, Pradier O, Marc JP, Miltgen F, Mazier D, Parent G. 1986. Levels of antibodies to Plasmodium falciparum sporozoite surface antigens reflect malaria transmission rates and are persistent in the absence of reinfection. Infect. Immun. 53:393-397.
35. Kun JF, Mordmuller B, Lell B, Lehman LG, Luckner D, Kremsner PG.1998. Polymorphism in promoter region of inducible nitric oxide synthase gene and protection against malaria. Lancet 351:265-266. http://dx .doi.org/10.1016/S0140-6736(05)78273-8.
36. Kun JF, Mordmuller B, Perkins DJ, May J, Mercereau-Puijalon O, Alpers M, Weinberg JB, Kremsner PG. 2001. Nitric oxide synthase 2(Lambarene) (G-954C), increased nitric oxide production, and protection against malaria. J. Infect. Dis. 184:330-336. http://dx.doi.org/10.1086/322037.
37. Sobolewski P, Gramaglia I, Frangos J, Intaglietta M, van der Heyde HC.2005. Nitric oxide bioavailability in malaria. Trends Parasitol. 21:415-422. http://dx.doi.org/10.1016/j.pt.2005.07.002.
38. Anstey NM, Granger DL, Hassanali MY, Mwaikambo ED, Duffy PE, Weinberg JB. 1999. Nitric oxide, malaria, and anemia: inverse relationship between nitric oxide production and hemoglobin concentration in asymptomatic, malaria-exposed children. Am. J. Trop. Med. Hyg. 61:249-252.
39. Stevenson MM, Riley EM. 2004. Innate immunity to malaria. Nat. Rev. Immunol. 4:169-180. http://dx.doi.org/10.1038/nri1311.
40. Clark IA, Cowden WB. 2003. The pathophysiology of falciparum malaria. Pharmacol. Ther. 99:221-260. http://dx.doi.org/10.1016/S0163-7258(03)00060-3.
41. Gramaglia I, Sobolewski P, Meays D, Contreras R, Nolan JP, Frangos JA, Intaglietta M, van der Heyde HC. 2006. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat. Med. 12:1417-1422. http://dx.doi.org/10.1038/nm1499.