Inhibiting the mammalian target of rapamycin blocks the development of experimental cerebral malaria

mBio

Volumn 6, Issue 3, 2015, Pages

  Gordon, Emile B ^a,b   Hart, Geoffrey T ^a   Tran, Tuan M ^a   Waisberg, Michael ^a,c   Akkaya, Munir ^a   Skinner, Jeff ^a   Zinöcker, Severin ^a,d   Pena, Mirna ^a   Yazew, Takele ^a   Qi, Chen Feng ^a   Miller, Louis H ^a   Pierce, Susan K ^a  

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

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d ABBVIE INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTESUNATE; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN HEMORRHAGE; BRAIN MALARIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; ERYTHROCYTE AGGREGATION; EXPERIMENTAL CEREBRAL MALARIA; FEMALE; LEUKOCYTE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; GENE EXPRESSION PROFILING; MALARIA, CEREBRAL; PATHOLOGY; SURVIVAL ANALYSIS;

ANIMALIA; MAMMALIA; MUS; PLASMODIUM FALCIPARUM;

ANIMALS; BRAIN; GENE EXPRESSION PROFILING; MALARIA, CEREBRAL; MICE; SIROLIMUS; SURVIVAL ANALYSIS; TOR SERINE-THREONINE KINASES;

EID: 84936984369     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00725-15     Document Type: Article

References (46)

1. World Health Organization. 2013. World malaria Report: 2013. World Health Organization, Geneva, Switzerland.
2. Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley M, Marsh V, Newton C, Winstanley P, Warn P, Peshu N, Pasvol G, Snow R. 1995. Indicators of life-threatening malaria in African children. N Engl J Med 332:1399-1404. http://dx.doi.org/10.1056/NEJM199505253322102.
3. Dondorp AM, Fanello CI, Hendriksen IC, Gomes E, Seni A, Chhaganlal KD, Bojang K, Olaosebikan R, Anunobi N, Maitland K, Kivaya E, Agbenyega T, Nguah SB, Evans J, Gesase S, Kahabuka C, Mtove G, Nadjm B, Deen J, Mwanga-Amumpaire J, Nansumba M, Karema C, Umulisa N, Uwimana A, Mokuolu OA, Adedoyin OT, Johnson WB, Tshefu AK, Onyamboko MA, Sakulthaew T, Ngum WP, Silamut K, Stepniewska K, Woodrow CJ, Bethell D, Wills B, Oneko M, Peto TE, von Seidlein L, Day NP, White NJ, AQUAMAT group. 2010. Artesunate versus quinine in the treatment of severe falciparum malaria in African children. (AQUAMAT): an open-label, randomised trial. Lancet 376: 1647-1657. http://dx.doi.org/10.1016/S0140-6736(10)61924-1.
4. 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. http://dx.doi.org/10.1016/j.ajpath.2012.08.010.
5. Dorovini-Zis K, Schmidt K, Huynh H, Fu W, Whitten RO, Milner D, Kamiza S, Molyneux M, Taylor TE. 2011. The neuropathology of fatal cerebral malaria in Malawian children. Am J Pathol 178:2146-2158. http://dx.doi.org/10.1016/j.ajpath.2011.01.016.
6. Milner DA, Jr, Whitten RO, Kamiza S, Carr R, Liomba G, Dzamalala C, Seydel KB, Molyneux ME, Taylor TE. 2014. The systemic pathology of cerebral malaria in African children. Front Cell Infect Microbiol 4:104. http://dx.doi.org/10.3389/fcimb.2014.00104.
7. Grau GE, Craig AG. 2012. Cerebral malaria pathogenesis: revisiting parasite and host contributions. Future Microbiol 7:291-302. http:// dx.doi.org/10.2217/fmb.11.155.
8. MacCormick IJ, Beare NA, Taylor TE, Barrera V, White VA, Hiscott P, Molyneux ME, Dhillon B, Harding SP. 2014. Cerebral malaria in children: using the retina to study the brain. Brain 137:2119-2142. http:// dx.doi.org/10.1093/brain/awu001.
9. Turner GD, Ly YO, Nguyen TH, Tran TH, Nguyen HP, Bethell D, Wyllie S, Louwrier K, Fox SB, Gatter KC, Day NP, Tran TH, White NJ, Berendt AR. 1998. Systemic endothelial activation occurs in both mild and severe malaria. Correlating dermal microvascular endothelial cell phenotype and soluble cell adhesion molecules with disease severity. Am J Pathol 152:1477-1487.
10. Schofield L, Grau GE. 2005. Immunological processes in malaria pathogenesis. Nat Rev Immunol 5:722-735. http://dx.doi.org/10.1038/nri1686.
11. Cunnington AJ, Riley EM, Walther M. 2013. Stuck in a rut? Reconsidering the role of parasite sequestration in severe malaria syndromes. Trends Parasitol 29:585-592. http://dx.doi.org/10.1016/j.pt.2013.10.004.
12. Grau GE, Mackenzie CD, Carr RA, Redard M, Pizzolato G, Allasia C, Cataldo C, Taylor TE, Molyneux ME. 2003. Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 187: 461-466. http://dx.doi.org/10.1086/367960.
13. Rénia L, Howland SW, Claser C, Gruner A, Suwanarusk R, Teo T, Russell B, Ng LF. 2012. Cerebral malaria: mysteries at the blood-brain barrier. Virulence 3:193-201. http://dx.doi.org/10.4161/viru.19013.
14. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, Turner G, Langhorne J, participants of the Hinxton Retreat meeting on Animal Models for Research on Severe Malaria. 2012. The role of animal models for research on severe malaria. PLoS Pathog 8:e1002401. http:// dx.doi.org/10.1371/journal.ppat.1002401.
15. Haque A, Best SE, Unosson K, Amante FH, de Labastida F, Anstey NM, Karupiah G, Smyth MJ, Heath WR, Engwerda CR. 2011. Granzyme B expression byCD8+T cells is required for the development of experimental cerebral malaria. J Immunol 186:6148-6156. http://dx.doi.org/ 10.4049/jimmunol.1003955.
16. Baptista FG, Pamplona A, Pena AC, Mota MM, Pied S, Vigário 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. http://dx.doi.org/10.1128/IAI.00079-10.
17. 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. http://dx.doi.org/10.1016/j.ijpara.2010.08.003.
18. Yañez DM, Manning DD, Cooley AJ, Weidanz WP, van der Heyde HC. 1996. Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157:1620-1624.
19. Belnoue E, Kayibanda M, Vigario AM, Deschemin JC, van Rooijen N, Viguier M, Snounou G, Rénia L. 2002. On the pathogenic role of brainsequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 169:6369-6375. http://dx.doi.org/10.4049/jimmunol.169.11.6369.
20. Howland SW, Poh CM, Gun SY, Claser C, Malleret B, Shastri N, Ginhoux F, Grotenbreg GM, Rénia L. 2013. Brain microvessel crosspresentation is a hallmark of experimental cerebral malaria. EMBO Mol Med 5:916-931. http://dx.doi.org/10.1002/emmm.201202273.
21. Pai S, Qin J, Cavanagh L, Mitchell A, El-Assaad F, Jain R, Combes V, Hunt NH, Grau GE, Weninger W. 2014. Real-time imaging reveals the dynamics of leukocyte behaviour during experimental cerebral malaria pathogenesis. PLoS Pathog 10:e1004236. http://dx.doi.org/10.1371/ journal.ppat.1004236.
22. Schmidt KE, Schumak B, Specht S, Dubben B, Limmer A, Hoerauf A. 2011. Induction of pro-inflammatory mediators in Plasmodium berghei infected BALB/c mice breaks blood-brain-barrier and leads to cerebral malaria in an IL-12 dependent manner. Microbes Infect 13:828-836. http://dx.doi.org/10.1016/j.micinf.2011.04.006.
23. Poh CM, Howland SW, Grotenbreg GM, Rénia L. 2014. Damage to the blood-brain barrier during experimental cerebral malaria results from synergistic effects of CD8+ T cells with different specificities. Infect Immun 82:4854-4864. http://dx.doi.org/10.1128/IAI.02180-14.
24. Powell JD, Pollizzi KN, Heikamp EB, Horton MR. 2012. Regulation of immune responses by mTOR. Annu Rev Immunol 30:39-68. http:// dx.doi.org/10.1146/annurev-immunol-020711-075024.
25. Pollizzi KN, Powell JD. 2014. Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat Rev Immunol 14:435-446. http://dx.doi.org/10.1038/nri3701.
26. Bharatham N, Chang MW, Yoon HS. 2011. Targeting FK506 binding proteins to fight malarial and bacterial infections: current advances and future perspectives. Curr Med Chem 18:1874-1889. http://dx.doi.org/ 10.2174/092986711795496818.
27. Hanson KK, Ressurreição AS, Buchholz K, Prudêncio M, Herman-Ornelas JD, Rebelo M, Beatty WL, Wirth DF, Hänscheid T, Moreira R, Marti M, Mota MM. 2013. Torins are potent antimalarials that block replenishment of Plasmodium liver stage parasitophorous vacuole membrane proteins. Proc Natl Acad Sci U S A 110:E2838-E2847. http:// dx.doi.org/10.1073/pnas.1306097110.
28. Yen LF, Wei VC, Kuo EY, Lai TW. 2013. Distinct patterns of cerebral extravasation by Evans blue and sodium fluorescein in rats. PLoS One 8:e68595. http://dx.doi.org/10.1371/journal.pone.0068595.
29. Nag S. 2003. Blood-brain barrier permeability using tracers and immunohistochemistry. Methods Mol Med 89:133-144. http://dx.doi.org/ 10.1385/1-59259-419-0:133.
30. Nacer A, Movila A, Baer K, Mikolajczak SA, Kappe SH, Frevert U. 2012. Neuroimmunological blood brain barrier opening in experimental cerebral malaria. PLoS Pathog 8:e1002982. http://dx.doi.org/10.1371/ journal.ppat.1002982.
31. Otto TD, Böhme U, Jackson AP, Hunt M, Franke-Fayard B, Hoeijmakers WA, Religa AA, Robertson L, Sanders M, Ogun SA, Cunningham D, Erhart A, Billker O, Khan SM, Stunnenberg HG, Langhorne J, Holder AA, Waters AP, Newbold CI, Pain A, Berriman M, Janse CJ. 2014. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol 12:86. http://dx.doi.org/10.1186/s12915-014-0086-0.
32. Richmon JD, Fukuda K, Maida N, Sato M, Bergeron M, Sharp FR, Panter SS, Noble LJ. 1998. Induction of heme oxygenase-1 after hyperosmotic opening of the blood-brain barrier. Brain Res 780:108-118. http://dx.doi.org/10.1016/S0006-8993(97)01314-0.
33. Niikura M, Inoue S, Kobayashi F. 2011. Role of interleukin-10 in malaria: focusing on coinfection with lethal and nonlethal murine malaria parasites. J Biomed Biotechnol 2011:383962. http://dx.doi.org/10.1155/2011/ 383962.
34. Liu L, Das S, Losert W, Parent CA. 2010. mTORC2 regulates neutrophil chemotaxis in a cAMP-and RhoA-dependent fashion. Dev Cell 19: 845-857. http://dx.doi.org/10.1016/j.devcel.2010.11.004.
35. Lackner P, Hametner C, Beer R, Burger C, Broessner G, Helbok R, Speth C, Schmutzhard E. 2008. Complement factors C1q, C3 and C5 in brain and serum of mice with cerebral malaria. Malar J 7:207. http:// dx.doi.org/10.1186/1475-2875-7-207.
36. Oakley MS, Anantharaman V, Venancio TM, Zheng H, Mahajan B, Majam V, McCutchan TF, Myers TG, Aravind L, Kumar S. 2011. Molecular correlates of experimental cerebral malaria detectable in whole blood. Infect Immun 79:1244-1253. http://dx.doi.org/10.1128/IAI.00964-10.
37. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, Chora A, Rodrigues CD, Gregoire IP, Cunha-Rodrigues M, Portugal S, Soares MP, MotaMM. 2007. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 13:703-710. http://dx.doi.org/10.1038/nm1586.
38. Mejia P, Treviño-Villarreal JH, Hine C, Harputlugil E, Lang S, Calay E, Rogers R, Wirth D, Duraisingh MT, Mitchell JR. 2015. Dietary restriction protects against experimental cerebral malaria via leptin modulation and T-cell mTORC1 suppression. Nat Commun 6:6050. http:// dx.doi.org/10.1038/ncomms7050.
39. Langhorne J, Ndungu FM, Sponaas AM, Marsh K. 2008. Immunity to malaria: more questions than answers. Nat Immunol 9:725-732. http:// dx.doi.org/10.1038/ni.f.205.
40. Hendriksen IC, Mwanga-Amumpaire J, von Seidlein L, Mtove G, White LJ, Olaosebikan R, Lee SJ, Tshefu AK, Woodrow C, Amos B, Karema C, Saiwaew S, Maitland K, Gomes E, Pan-Ngum W, Gesase S, Silamut K, Reyburn H, Joseph S, Chotivanich K, Fanello CI, Day NP, White NJ, Dondorp AM. 2012. Diagnosing severe falciparum malaria in parasitaemic African children: a prospective evaluation of plasma PfHRP2 measurement. PLoS Med 9:e1001297. http://dx.doi.org/10.1371/ journal.pmed.1001297.
41. Cunnington AJ, Bretscher MT, Nogaro SI, Riley EM, Walther M. 2013. Comparison of parasite sequestration in uncomplicated and severe childhood Plasmodium falciparum malaria. J Infect 67:220-230. http:// dx.doi.org/10.1016/j.jinf.2013.04.013.
42. Waisberg M, Vickers BK, Yager SB, Lin CK, Pierce SK. 2012. Testing in mice the hypothesis that melanin is protective in malaria infections. PLoS One 7:e29493. http://dx.doi.org/10.1371/journal.pone.0029493.
43. Kim JV, Kang SS, Dustin ML, McGavern DB. 2009. Myelomonocytic cell recruitment causes fatalCNSvascular injury during acute viral meningitis. Nature 457:191-195. http://dx.doi.org/10.1038/nature07591.
44. Malleret B, Claser C, Ong AS, Suwanarusk R, Sriprawat K, Howland SW, Russell B, Nosten F, Rénia L. 2011. A rapid and robust tri-color flow cytometry assay for monitoring malaria parasite development. Sci Rep 1:118. http://dx.doi.org/10.1038/srep00118.
45. Qi CF, Hori M, Coleman AE, Torrey TA, Taddesse-Heath L, Ye BH, Chattopadhyay SK, Hartley JW, Morse HC, III. 2000. Genomic organisation and expression of BCL6 in murine B-cell lymphomas. Leuk Res 24:719-732. http://dx.doi.org/10.1016/S0145-2126(00)00028-X.
46. Howland SW, Claser C, Poh CM, Gun SY, Rénia L. 2015. Pathogenic CD8 T cells in experimental cerebral malaria. Semin Immunopathol, in press. http://dx.doi.org/10.1007/s00281-015-0476-6.