Transdermal glyceryl trinitrate as an effective adjunctive treatment with artemether for late-stage experimental cerebral malaria

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 11, 2013, Pages 5462-5471

  Orjuela Sánchez, Pamela ^a   Ong, Peng Kai ^a   Zanini, Graziela M ^a,b   Melchior, Benoît ^a   Martins, Yuri C ^a   Meays, Diana ^a   Frangos, John A ^a   Carvalho, Leonardo J M ^a,c  

^a LA JOLLA BIOENGINEERING INSTITUTE   (United States)

^b Funda??o Oswaldo Cruz   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMETHER; ARTESIANE; GLYCERYL TRINITRATE; NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY DIAMETER; ARTICLE; BLOOD PRESSURE MEASUREMENT; BRAIN ARTERY; BRAIN MALARIA; BRAIN TISSUE; BRAIN VASOSPASM; C57BL 6 MOUSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; FEMALE; HYPOTENSION; INFECTION PREVENTION; MEAN ARTERIAL PRESSURE; MORTALITY; MOUSE; NONHUMAN; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSDERMAL PATCH; VASOCONSTRICTION; WESTERN BLOTTING;

ADMINISTRATION, CUTANEOUS; ANIMALS; ANTIMALARIALS; ARTEMISININS; ARTERIAL PRESSURE; BRAIN; DRUG SYNERGISM; FEMALE; GENE EXPRESSION; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE I; NITROGLYCERIN; PLASMODIUM BERGHEI; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VASOCONSTRICTION; VASODILATOR AGENTS;

EID: 84885911305     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00488-13     Document Type: Article

References (65)

1. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379:413-431.
2. John CC, Kutamba E, Mugarura K, Opoka RO. 2010. Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev. Anti-Infect. Ther. 8:997-1008.
3. Shikani HJ, Freeman BD, Lisanti MP, Weiss LM, Tanowitz HB, Desruisseaux MS. 2012. Cerebral malaria: we have come a long way. Am. J. Pathol. 181:1484-1492.
4. von Seidlein L, Olaosebikan R, Hendriksen IC, Lee SJ, Adedoyin OT, Agbenyega T, Nguah SB, Bojang K, Deen JL, Evans J, Fanello CI, Gomes E, Pedro AJ, Kahabuka C, Karema C, Kivaya E, Maitland K, Mokuolu OA, Mtove G, Mwanga-Amumpaire J, Nadjm B, Nansumba M, Ngum WP, Onyamboko MA, Reyburn H, Sakulthaew T, Silamut K, Tshefu AK, Umulisa N, Gesase S, Day NP, White NJ, Dondorp AM. 2012. Predicting the clinical outcome of severe falciparum malaria in African children: findings from a large randomized trial. Clin. Infect. Dis. 54:1080-1090.
5. Pongponratn E, Turner GD, Day NP, Phu NH, Simpson JA, Stepniewska K, Mai NT, Viriyavejakul P, Looareesuwan S, Hien TT, Ferguson DJ, White NJ. 2003. An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 69:345-359.
6. Ponsford MJ, Medana IM, Prapansilp P, Hien TT, Lee SJ, Dondorp AM, Esiri MM, Day NP, White NJ, Turner GD. 2012. Sequestration and microvascular congestion are associated with coma in human cerebral malaria. J. Infect. Dis. 205:663-671.
7. Clark IA, Awburn MM, Whitten RO, Harper CG, Liomba NG, Molyneux ME, Taylor TE. 2003. Tissue distribution of migration inhibitory factor and inducible nitric oxide synthase in falciparum malaria and sepsis in African children. Malar. J. 2:6.
8. Beare NA, Harding SP, Taylor TE, Lewallen S, Molyneux ME. 2009. Perfusion abnormalities in children with cerebral malaria and malarial retinopathy. J. Infect. Dis. 199:263-271.
9. Lopansri BK, Anstey NM, Weinberg JB, Stoddard GJ, Hobbs MR, Levesque MC, Mwaikambo ED, Granger DL. 2003. Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 361:676-678.
10. Yeo TW, Lampah DA, Tjitra E, Gitawati R, Kenangalem E, Piera K, Granger DL, Lopansri BK, Weinberg JB, Price RN, Duffull SB, Celermajer DS, Anstey NM. 2009. Relationship of cell-free hemoglobin to impaired endothelial nitric oxide bioavailability and perfusion in severe falciparum malaria. J. Infect. Dis. 200:1522-1529.
11. Yeo TW, Lampah DA, Tjitra E, Gitawati R, Darcy CJ, Jones C, Kenangalem E, McNeil YR, Granger DL, Lopansri BK, Weinberg JB, Price RN, Duffull SB, Celermajer DS, Anstey NM. 2010. Increased asymmetric dimethylarginine in severe falciparum malaria: association with impaired nitric oxide bioavailability and fatal outcome. PLoS Pathog. 6:e1000868. doi:10.1371/journal.ppat.1000868.
12. Wenisch C, Wenisch H, Wilairatana P, Looareesuwan S, Vannaphan S, Wagner O, Graninger W, Schonthal E, Rumpold H. 1996. Big endothelin in patients with complicated Plasmodium falciparum malaria. J. Infect. Dis. 173:1281-1284.
13. Lovegrove FE, Tangpukdee N, Opoka RO, Lafferty EI, Rajwans N, Hawkes M, Krudsood S, Looareesuwan S, John CC, Liles WC, Kain KC. 2009. Serum angiopoietin-1 and -2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS One 4:e4912. doi:10.1371/journal.pone.0004912.
14. Polder TW, Jerusalem CR, Eling WM. 1991. Morphological characteristics of intracerebral arterioles in clinical (Plasmodium falciparum) and experimental (Plasmodium berghei) cerebral malaria. J. Neurol. Sci. 101: 35-46.
15. de Souza JB, Hafalla JC, Riley EM, Couper KN. 2010. Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease. Parasitology 137:755-772.
16. White NJ, Turner GD, Medana IM, Dondorp AM, Day NP. 2010. The murine cerebral malaria phenomenon. Trends Parasitol. 26:11-15.
17. Carvalho LJ. 2010. Murine Cerebral Malaria: How Far from Human Cerebral Malaria? Trends Parasitol. 26:271-272.
18. Hunt NH, Grau GE, Engwerda C, Barnum SR, van der Heyde H, Hansen DS, Schofield L, Golenser J. 2010. Murine cerebral malaria: the whole story. Trends Parasitol. 26:272-274.
19. Stevenson MM, Gros P, Olivier M, Fortin A, Serghides L. 2010. Cerebral malaria: human versus mouse studies. Trends Parasitol. 26:274-275.
20. Renia L, Gruner AC, Snounou G. 2010. Cerebral malaria: in praise of epistemes. Trends Parasitol. 26:275-277.
21. Riley EM, Couper KN, Helmby H, Hafalla JC, de Souza JB, Langhorne J, Jarra WB, Zavala F. 2010. Neuropathogenesis of human and murine malaria. Trends Parasitol. 26:277-278.
22. 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.
23. Anstey NM, Weinberg JB, Hassanali MY, Mwaikambo ED, Manyenga D, Misukonis MA, Arnelle DR, Hollis D, McDonald MI, Granger DL. 1996. Nitric oxide in Tanzanian children with malaria: inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J. Exp. Med. 184:557-567.
24. Cabrales P, Zanini GM, Meays D, Frangos JA, Carvalho LJ. 2011. Nitric oxide protection against murine cerebral malaria is associated with improved cerebral microcirculatory physiology. J. Infect. Dis. 203:1454-1463.
25. Zanini GM, Cabrales P, Barkho W, Frangos JA, Carvalho LJ. 2011. Exogenous nitric oxide decreases brain vascular inflammation, leakage, and venular resistance during Plasmodium berghei ANKA infection in mice. J. Neuroinflammation 8:66.
26. Serghides L, Kim H, Lu Z, Kain DC, Miller C, Francis RC, Liles WC, Zapol WM, Kain KC. 2011. Inhaled nitric oxide reduces endothelial activation and parasite accumulation in the brain, and enhances survival in experimental cerebral malaria. PLoS One 6:e27714. doi:10.1371/journal.pone.0027714.
27. Cabrales P, Zanini GM, Meays D, Frangos JA, Carvalho LJ. 2010. Murine cerebral malaria is associated with a vasospasm-like microcirculatory dysfunction, and survival upon rescue treatment is markedly increased by nimodipine. Am. J. Pathol. 176:1306-1315.
28. Boden WE, Finn AV, Patel D, Peacock WF, Thadani U, Zimmerman FH. 2012. Nitrates as an integral part of optimal medical therapy and cardiac rehabilitation for stable angina: review of current concepts and therapeutics. Clin. Cardiol. 35:263-271.
29. Chen Z, Zhang J, Stamler JS. 2002. Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc. Natl. Acad. Sci. U. S. A. 99:8306-8311.
30. de Berrazueta JR, Sampedro I, Garcia-Unzueta MT, Llorca J, Bustamante M, Amado JA. 2003. Effect of transdermal nitroglycerin on inflammatory mediators in patients with peripheral atherosclerotic vascular disease. Am. Heart J. 146:E14.
31. James MA, Walker PR, Papouchado M, Wilkinson PR. 1985. Efficacy of transdermal glyceryl trinitrate in the treatment of chronic stable angina pectoris. Br. Heart J. 53:631-635.
32. Clemmer L, Martins YC, Zanini GM, Frangos JA, Carvalho LJ. 2011. Artemether and artesunate show the highest efficacies in rescuing mice with late-stage cerebral malaria and rapidly decrease leukocyte accumulation in the brain. Antimicrob. Agents Chemother. 55:1383-1390.
33. Zanini GM, Martins YC, Cabrales P, Frangos JA, Carvalho LJ. 2012. S-nitrosoglutathione prevents experimental cerebral malaria. J. Neuroimmune Pharmacol. 7:477-487.
34. Feng M, DiPetrillo K. 2009. Non-invasive blood pressure measurement in mice. Methods Mol. Biol. 573:45-55.
35. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hubener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L. 2009. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4:1128-1144.
36. Cabrales P, Carvalho LJ. 2010. Intravital microscopy of the mouse brain microcirculation using a closed cranial window. J. Vis. Exp. 45:2184.
37. Ong PK, Melchior B, Martins YC, Hofer A, Orjuela-Sanchez P, Cabrales P, Zanini GM, Frangos JA, Carvalho LJ. 2013. Nitric oxide synthase dysfunction contributes to impaired cerebroarteriolar reactivity in experimental cerebral malaria. PLoS Pathog. 9:e1003444. doi:10.1371/journal.ppat.1003444.
38. Silamut K, Phu NH, Whitty C, Turner GD, Louwrier K, Mai NT, Simpson JA, Hien TT, White NJ. 1999. A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am. J. Pathol. 155:395-410.
39. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B, et al. 1994. An immunohistochemical study of the pathology of fatal malaria: evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am. J. Pathol. 145:1057-1069.
40. van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE. 2006. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation, and hemostasis leading to microcirculatory dysfunction. Trends Parasitol. 22:503-508.
41. Lucchi NW, Jain V, Wilson NO, Singh N, Udhayakumar V, Stiles JK. 2011. Potential serological biomarkers of cerebral malaria. Dis. Markers 31:327-335.
42. Moxon CA, Wassmer SC, Milner DA, Jr, Chisala NV, Taylor TE, Seydel KB, Molyneux ME, Faragher B, Esmon CT, Downey C, Toh CH, Craig AG, Heyderman RS. 2013. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood 122:842-851.
43. Amante FH, Stanley AC, Randall LM, Zhou Y, Haque A, McSweeney K, Waters AP, Janse CJ, Good MF, Hill GR, Engwerda CR. 2007. A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria. Am. J. Pathol. 171:548-559.
44. McQuillan JA, Mitchell AJ, Ho YF, Combes V, Ball HJ, Golenser J, Grau GE, Hunt NH. 2011. Coincident parasite and CD8 T cell sequestration is required for development of experimental cerebral malaria. Int. J. Parasitol. 41:155-163.
45. Baptista FG, Pamplona A, Pena AC, Mota MM, Pied S, Vigario AM. 2010. Accumulation of Plasmodium berghei-infected red blood cells in the brain is crucial for the development of cerebral malaria in mice. Infect. Immun. 78:4033-4039.
46. Claser C, Malleret B, Gun SY, Wong AY, Chang ZW, Teo P, See PC, Howland SW, Ginhoux F, Renia L. 2011. CD8 T cells and IFN-gamma mediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS One 6:e18720. doi:10.1371/journal.pone. 0018720.
47. Zhen J, Lu H, Wang XQ, Vaziri ND, Zhou XJ. 2008. Upregulation of endothelial and inducible nitric oxide synthase expression by reactive oxygen species. Am. J. Hypertens. 21:28-34.
48. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. 2000. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol. Scand. 168:81-88.
49. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. 1999. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature 399:601-605.
50. Bienvenu AL, Ferrandiz J, Kaiser K, Latour C, Picot S. 2008. Artesunate-erythropoietin combination for murine cerebral malaria treatment. Acta Trop. 106:104-108.
51. Pena AC, Penacho N, Mancio-Silva L, Neres R, Seixas JD, Fernandes AC, Romao CC, Mota MM, Bernardes GJ, Pamplona A. 2012. A novel carbon monoxide-releasing molecule fully protects mice from severe malaria. Antimicrob. Agents Chemother. 56:1281-1290.
52. Achtman AH, Pilat S, Law CW, Lynn DJ, Janot L, Mayer ML, Ma S, Kindrachuk J, Finlay BB, Brinkman FS, Smyth GK, Hancock RE, Schofield L. 2012. Effective adjunctive therapy by an innate defense regulatory peptide in a preclinical model of severe malaria. Sci. Transl. Med. 4:135ra164.
53. Reis PA, Comim CM, Hermani F, Silva B, Barichello T, Portella AC, Gomes FC, Sab IM, Frutuoso VS, Oliveira MF, Bozza PT, Bozza FA, Dal-Pizzol F, Zimmerman GA, Quevedo J, Castro-Faria-Neto HC. 2010. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog. 6:e1000963. doi:10.1371/journal. ppat.1000963.
54. Grau GE, Pointaire P, Piguet PF, Vesin C, Rosen H, Stamenkovic I, Takei F, Vassalli P. 1991. Late administration of monoclonal antibody to leukocyte function-antigen 1 abrogates incipient murine cerebral malaria. Eur. J. Immunol. 21:2265-2267.
55. Piguet PF, Kan CD, Vesin C. 2002. Role of the tumor necrosis factor receptor 2 (TNFR2) in cerebral malaria in mice. Lab. Invest. 82:1155-1166.
56. Wei EP, Moskowitz MA, Boccalini P, Kontos HA. 1992. Calcitonin gene-related peptide mediates nitroglycerin and sodium nitroprussideinduced vasodilation in feline cerebral arterioles. Circ. Res. 70:1313-1319.
57. Read SJ, Manning P, McNeil CJ, Hunter AJ, Parsons AA. 1999. Effects of sumatriptan on nitric oxide and superoxide balance during glyceryl trinitrate infusion in the rat. Implications for antimigraine mechanisms. Brain Res. 847:1-8.
58. Read SJ, Smith MI, Hunter AJ, Parsons AA. 1997. Enhanced nitric oxide release during cortical spreading depression following infusion of glyceryl trinitrate in the anaesthetized cat. Cephalalgia 17:159-165.
59. Bagdy G, Riba P, Kecskemeti V, Chase D, Juhasz G. 2010. Headachetype adverse effects of NO donors: vasodilation and beyond. Br. J. Pharmacol. 160:20-35.
60. Tfelt-Hansen PC, Tfelt-Hansen J. 2009. Nitroglycerin headache and nitroglycerin-induced primary headaches from 1846 and onwards: a historical overview and an update. Headache 49:445-456.
61. Uxa A, Thomas GR, Gori T, Parker JD. 2010. Standard versus low-dose transdermal nitroglycerin: differential effects on the development of tolerance and abnormalities of endothelial function. J. Cardiovasc. Pharmacol. 56:354-359.
62. Elkayam U, Bitar F, Akhter MW, Khan S, Patrus S, Derakhshani M. 2004. Intravenous nitroglycerin in the treatment of decompensated heart failure: potential benefits and limitations. J. Cardiovasc. Pharmacol. Ther. 9:227-241.
63. Agvald P, Hammar L, Gustafsson LE. 2005. Nitroglycerin-patch induced tolerance is associated with reduced ability of nitroglycerin to increase exhaled nitric oxide. Vascul. Pharmacol. 43:449-457.
64. Klemsdal TO, Gjesdal K, Bredesen JE. 1992. Heating and cooling of the nitroglycerin patch application area modify the plasma level of nitroglycerin. Eur. J. Clin. Pharmacol. 43:625-628.
65. Bonini MG, Stadler K, Silva SO, Corbett J, Dore M, Petranka J, Fernandes DC, Tanaka LY, Duma D, Laurindo FR, Mason RP. 2008. Constitutive nitric oxide synthase activation is a significant route for nitroglycerin-mediated vasodilation. Proc. Natl. Acad. Sci. U. S. A. 105: 8569-8574.