Battling brain-eating amoeba: Enigmas surrounding immunity to Naegleria fowleri

1. Kemble SK, Lynfield R, DeVries AS, Drehner DM, Pomputius WF, Beach MJ, et al. Fatal Naegleria fowleri infection acquired in Minnesota: possible expanded range of a deadly thermophilic organism. Clin Infect Dis. 2012 Mar;54(6):805–809. doi: 10.1093/cid/cir961 22238170

2. Visvesvara GS, Moura H, Schuster FL. Pathogenic and opportunistic free-living amoebae: Acanthamoebaspp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol. 2007 Jun;50(1):1–26. doi: 10.1111/j.1574-695X.2007.00232.x 17428307

3. Culbertson CG, Ensminger PW, Overton WM. Amebic cellulocutaneous invasion by Naegleria aerobia with generalized visceral lesions after subcutaneous inoculation: an experimental study in guinea pigs. Am J Clin Pathol. 1972 Mar;57(3):375–86. doi: 10.1093/ajcp/57.3.375 5018608

4. Rojas-Hernández S, Jarillo-Luna A, Rodríguez-Monroy M, Moreno-Fierros L, Campos-Rodríguez R. Immunohistochemical characterization of the initial stages of Naegleria fowleri meningoencephalitis in mice. Parasitol Res. 2004 Sep;94(1):31–36. doi: 10.1007/s00436-004-1177-6 15338289

5. Jarolim KL, McCosh JK, Howard MJ, John DT. A light microscopy study of the migration of Naegleria fowleri from the nasal submucosa to the central nervous system during the early stage of primary amebic meningoencephalitis in mice. J Parasitol. 2000 Feb 1;86(1):50–55. doi: 10.1645/0022-3395(2000)086[0050:ALMSOT]2.0.CO;2 10701563

6. Baig AM. Primary Amoebic Meningoencephalitis: Neurochemotaxis and Neurotropic Preferences of Naegleria fowleri. ACS Chem Neurosci. 2016 Apr 13;7(8):1026–1029. doi: 10.1021/acschemneuro.6b00197 27447543

7. DUBRAY BL, WILHELM WE, JENNINGS BR. Serology of Naegleria fowleri and Naegleria lovaniensis in a Hospital Survey1. J Eukaryot Microbiol. 1987 Aug 1;34(3):322–327.

8. Marciano-Cabral F, Cline ML, Bradley SG. Specificity of antibodies from human sera for Naegleria species. J Clin Microbiol. 1987 Apr;25(4):692–627. 2437151

9. Rivera V, Hernández D, Rojas S, Oliver G, Serrano J, Shibayama M, et al. IgA and IgM anti-Naegleria fowleri antibodies in human serum and saliva. Can J Microbiol. 2001 May;47(5):464–466. 11400739

10. Lares-Jiménez LF, Borquez-Román MA, Alfaro-Sifuentes R, Meza-Montenegro MM, Casillas-Hernández R, Lares-Villa F. Detection of serum antibodies in children and adolescents against Balamuthia mandrillaris, Naegleria fowleri and Acanthamoeba T4. Exp Parasitol. 2018 May 31;189:28–33. doi: 10.1016/j.exppara.2018.04.011 29673623

11. Marciano-Cabral F, Cabral GA. The immune response to Naegleria fowleri amebae and pathogenesis of infection. FEMS Immunol Med Microbiol. 2007 Nov;51(2):243–259. doi: 10.1111/j.1574-695X.2007.00332.x 17894804

12. Ferrante A, Carter RF, Lopez AF, Rowan-Kelly B, Hill NL, Vadas MA. Depression of immunity to Naegleria fowleri in mice by selective depletion of neutrophils with a monoclonal antibody. Infect Immun. 1988 Sep;56(9):2286–2291. 3410537

13. Cervantes-Sandoval I, Serrano-Luna J de J, García-Latorre E, Tsutsumi V, Shibayama M. Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitol Int. 2008 Sep;57(3):307–313. doi: 10.1016/j.parint.2008.01.006 18374627

14. Ferrante A, Thong YH. Unique Phagocytic Process in Neutrophil-Mediated Killing of Naeglaria-Fowleri. Immunol Lett. 1980;2(1):37–41.

15. Rowan-Kelly B, Ferrante A, Thong YH. Activation of complement by Naegleria. Trans R Soc Trop Med Hyg. 1980;74(3):333–336. doi: 10.1016/0035-9203(80)90092-9 7434428

16. Whiteman LY, Marciano-Cabral F. Resistance of highly pathogenic Naegleria fowleri amoebae to complement-mediated lysis. Infect Immun. 1989 Dec;57(12):3869–3875. 2807551

17. John DT, Cole TB, Marciano-Cabral FM. Sucker-like structures on the pathogenic amoeba Naegleria fowleri. Appl Environ Microbiol. 1984 Jan;47(1):12–14. 6696410

18. Jassam YN, Izzy S, Whalen M, Mcgavern DB, Khoury El J. Neuroimmunology of Traumatic Brain Injury: Time for a Paradigm Shift. Neuron. 2017 Sep 13;95(6):1246–1265. doi: 10.1016/j.neuron.2017.07.010 28910616

19. Ferrante A, Mocatta TJ. Human neutrophils require activation by mononuclear leucocyte conditioned medium to kill the pathogenic free-living amoeba, Naegleria fowleri. Clin Exp Immunol. 1984 Jun;56(3):559–566. 6378454

20. Michelson MK, Henderson WR, Chi EY, Fritsche TR, Klebanoff SJ. Ultrastructural studies on the effect of tumor necrosis factor on the interaction of neutrophils and Naegleria fowleri. Am J Trop Med Hyg. 1990 Mar;42(3):225–233. doi: 10.4269/ajtmh.1990.42.225 2316792

21. Ferrante A, Hill NL, Abell TJ, Pruul H. Role of myeloperoxidase in the killing of Naegleria fowleri by lymphokine-altered human neutrophils. Infect Immun. 1987 May;55(5):1047–1050. 3032797

22. Ferrante A. Augmentation of the neutrophil response to Naegleria fowleri by tumor necrosis factor alpha. Infect Immun. 1989 Oct;57(10):3110–3115. 2777375

23. Contis-Montes de Oca A, Carrasco-Yepez M, Campos-Rodriguez R, Pacheco-Yépez J, Bonilla-Lemus P, Pérez-López J, et al. Neutrophils extracellular traps damage Naegleria fowleri trophozoites opsonized with human IgG. Parasite Immunology. 2016 Aug;38(8):481–495. doi: 10.1111/pim.12337 27189133

24. Ferrante A, Lederer E. Curative properties of muramyl dipeptide in experimental Naegleria meningoencephalitis. Trans R Soc Trop Med Hyg. 1986 Jan;80(2):323–326. doi: 10.1016/0035-9203(86)90048-9 3538525

25. Adrover JM, Aroca-Crevillén A, Crainiciuc G, Ostos F, Rojas-Vega Y, Rubio-Ponce A, et al. Programmed “disarming” of the neutrophil proteome reduces the magnitude of inflammation. Nat Immunol. 2020 Feb 1;21(2):135–144. doi: 10.1038/s41590-019-0571-2 31932813

26. Shibayama M, Serrano-Luna J de J, Rojas-Hernández S, Campos-Rodríguez R, Tsutsumi V. Interaction of secretory immunoglobulin A antibodies with Naegleria fowleri trophozoites and collagen type I. Can J Microbiol. 2003 Mar;49(3):164–170. doi: 10.1139/w03-023 12795402

27. Ferrante A, Thong YH. Antibody induced capping and endocytosis of surface antigens in Naegleria fowleri. Int. J. Parasitol.1979 Dec 1;9(6):599–601. doi: 10.1016/0020-7519(79)90018-3 541172

28. Reilly MF, White KL, Bradley SG. Host resistance of mice to Naegleria fowleri infections. Infect Immun. 1983 Nov;42(2):645–652. 6642646

29. Thong YH, Ferrante A, Shepherd C, Rowan-Kelly B. Resistance of mice to Naegleria meningoencephalitis transferred by immune serum. Trans R Soc Trop Med Hyg.1978 Jan 1;72(6):650–652. doi: 10.1016/0035-9203(78)90025-1 734724

30. Lallinger GJ, Reiner SL, Cooke DW, Toffaletti DL, Perfect JR, Granger DL, et al. Efficacy of immune therapy in early experimental Naegleria fowleri meningitis. Infect Immun. 1987 May;55(5):1289–1293. 3570464

31. Tew JG, Burmeister J, Greene EJ, Pflaumer SK, Goldstein J. A radioimmunoassay for human antibody specific for microbial antigens. J Immunol Methods. 1977;14(3–4):231–241. doi: 10.1016/0022-1759(77)90133-8 320268

32. Reilly MF, Marciano-Cabral F, Bradley DW, Bradley SG. Agglutination of Naegleria fowleri and Naegleria gruberi by antibodies in human serum. J Clin Microbiol. 1983 Apr;17(4):576–581. 6853686

33. Cerutti A, Cols M, Puga I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol. 2013 Jan 25;13(2):118–132. doi: 10.1038/nri3383 23348416

34. Cursons RT, Brown TJ, Keys EA, Moriarty KM, Till D. Immunity to pathogenic free-living amoebae: role of cell-mediated immunity. Infect Immun. 1980 Aug;29(2):408–410. 7011975

35. Carrasco-Yepez M, Rojas-Hernandez S, Rodriguez-Monroy Ma, Terrazas Li, Moreno-Fierros L. Protection against Naegleria fowleri infection in mice immunized with Cry1Ac plus amoebic lysates is dependent on the STAT6 Th2 response. Parasite Immunol. 2010 Sep;32(9–10):664–670. doi: 10.1111/j.1365-3024.2010.01222.x 20691018

36. Lee J, Yoo J-K, Sohn H-J, Kang H-K, Kim D, Shin H-J, et al. Protective immunity against Naegleria fowleri infection on mice immunized with the rNfa1 protein using mucosal adjuvants. Parasitol Res. 2015 Apr;114(4):1377–1385. doi: 10.1007/s00436-015-4316-3 25604672

37. Apley J, Clarke SKR, Roome A. P. C. H., Sandry SA, Saygi G, Silk B, et al. Primary Amoebic Meningoencephalitis in Britain. BMJ. 1970 Mar 7;1(5696):596–569. doi: 10.1136/bmj.1.5696.596 5440234