Acanthamoeba culbertsoni elicits soluble factors that exert anti-microglial cell activity

Infection and Immunity

Volumn 78, Issue 9, 2010, Pages 4001-4011

  Harrison, Jenica L ^a   Ferreira, Gabriela A ^a   Raborn, Erinn S ^a   Lafrenaye, Audrey D ^a   Marciano Cabral, Francine ^a   Cabral, Guy A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1GAMMA; MACROPHAGE INFLAMMATORY PROTEIN 2; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; PEPTIDASE; THROMBOCYTE FACTOR 4; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; CHEMOKINE; CYTOKINE; MESSENGER RNA; SERINE PROTEINASE;

ACANTHAMOEBA; ACANTHAMOEBA CULBERTSONI; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL CONTACT; COCULTURE; CONTROLLED STUDY; MACROPHAGE FUNCTION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; ANIMAL; BRAIN; CELL LINE; GENETICS; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PHYSIOLOGY; SECRETION;

ACANTHAMOEBA; ANIMALS; APOPTOSIS; BRAIN; CELL LINE; CHEMOKINES; CYTOKINES; IMMUNE EVASION; MICE; MICROGLIA; RATS; RNA, MESSENGER; SERINE PROTEASES;

EID: 77956629713     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00047-10     Document Type: Article

References (57)

1. Alfieri, S. C., C. E. B. Correia, S. A. Motegi, and E. M. F. Pral. 2000. Proteinase activities in total extracts and in medium conditioned by Acanthamoeba polyphaga trophozoites. J. Parasitol. 86:220-227.
2. Alsam, S., J. Sissons, S. Jayasekera, and N. A. Khan. 2005. Extracellular proteases of Acanthamoeba castellanii (encephalitis isolate belonging to T1 genotype) contribute to increased permeability in an in vitro model of the human blood-brain barrier. J. Infect. 51:150-156.
3. Balcaitis, S., Y. H. Xie, J. R. Weinstein, H. Andersen, U. K. Hanisch, B. R. Ransom, and T. Möller. 2003. Expression of proteinase-activated receptors in mouse microglial cells. Neuroreport 14:2373-2377.
4. Benedetto, N., and C. Auriault. 2002. Complex network of cytokines activating murine microglial cell activity against Acanthamoeba castellanii. Eur. Cytokine Netw. 13:351-357.
5. Benedetto, N., F. Rossano, F. Gorga, A. Folgore, M. Rao, and C. R. Carratelli. 2003. Defense mechanisms of IFN-gamma and LPS-primed murine microglia against Acanthamoeba castellanii infection. Int. Immunopharmacol. 3:825-834.
6. Blasi, E., R. Barluzzi, V. Bocchini, R. Mazzolla, and F. Bistoni. 1990. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 27:229-237.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Cabral, G. A., and F. Marciano-Cabral. 2004. Cannabinoid-mediated exacerbation of brain infection by opportunistic amebae. J. Neuroimmunol. 147:127-130.
9. Cao, Z. Y., D. M. Jefferson, and N. Panjwani. 1998. Role of carbohydrate-mediated adherence in cytopathogenic mechanisms of Acanthamoeba. J. Biol. Chem. 273:15838-15845.
10. Cho, J. H., B. K. Na, T. S. Kim, and C. Y. Song. 2000. Purification and characterization of an extracellular serine proteinase from Acanthamoeba castellanii. IUBMB Life 50:209-214.
11. Colotta, F., F. L. Sciacca, M. Sironi, W. Luini, M. J. Rabiet, and A. Mantovani. 1994. Expression of monocyte chemotactic protein-1 by monocytes and endothelial cells exposed to thrombin. Am. J. Pathol. 144:975-985.
12. Cursons, R. T. M., T. J. Brown, and E. A. Keys. 1978. Virulence of pathogenic free-living amebae. J. Parasitol. 64:744-745.
13. Flynn, A. N., and A. G. Buret. 2004. Proteinase-activated receptor 1 (PAR-1) and cell apoptosis. Apoptosis 9:729-737.
14. Hadás, E., and T. Mazur. 1993. Proteolytic enzymes of pathogenic and non-pathogenic strains of Acanthamoeba spp. Trop. Med. Parasitol. 44:197-200.
15. Hadás, E., and T. Mazur. 1993. Biochemical markers of pathogenicity and virulence of Acanthamoeba sp. strains. Parasitol. Res. 79:696-698.
16. He, Y., J. Y. Niederkorn, J. P. McCulley, G. L. Stewart, D. R. Meyer, R. Silvany, and J. Dougherty. 1990. In vivo and in vitro collagenolytic activity of Acanthamoeba castellanii. Invest. Ophthalmol. Vis. Sci. 31:2235-2240.
17. Hidalgo-Grass, C., I. Mishalian, M. Dan-Goor, I. Belotserkovsky, Y. Eran, V. Nizet, A. Peled, and E. Hanski. 2006. A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues. EMBO J. 25:4628-4637.
18. Hong, Y. C., H. H. Kong, M. S. Ock, I. S. Kim, and D. I. Chung. 2000. Isolation and characterization of a cDNA encoding a subtilisin-like serine proteinase (ahSUB) from Acanthamoeba healyi. Mol. Biochem. Parasitol. 111:441-446.
19. Hong, Y. C., M. Y. Hwang, H. C. Yun, H. S. Yu, H. H. Kong, T. S. Yong, and D. I. Chung. 2002. Isolation and characterization of a cDNA encoding a mammalian cathepsin L-like cysteine proteinase from Acanthamoeba healyi. Korean J. Parasitol. 40:17-24.
20. Johansson, U., C. Lawson, M. Dabare, D. Syndercombe-Court, A. C. Newland, G. L. Howells, and M. G. Macey. 2005. Human peripheral blood monocytes express protease receptor-2 and respond to receptor activation by production of IL-6, IL-8, and IL-1 beta. J. Leukoc. Biol. 78:967-975.
21. Khan, N. A., E. L. Jarroll, N. Panjwani, Z. Y. Cao, and T. A. Paget. 2000. Proteases as markers for differentiation of pathogenic and nonpathogenic species of Acanthamoeba. J. Clin. Microbiol. 38:2858-2861.
22. Khan, N. A. 2006. Acanthamoeba: biology and increasing importance in human health. FEMS Microbiol. Rev. 30:564-595.
23. Khan, N. A. 2007. Acanthamoeba invasion of the central nervous system. Int. J. Parasitol. 37:131-138.
24. Khan, N. A. 2008. Acanthamoeba and the blood-brain barrier: the breakthrough. J. Med. Microbiol. 57:1051-1057.
25. Kim, W. T., H. H. Kong, Y. R. Ha, Y. C. Hong, H. J. Jeong, H. S. Yu, and D. I. Chung. 2006. Comparison of specific activity and cytopathic effects of a purified 33 kDa serine proteinase from Acanthamoeba strains with different degree of virulence. Korean J. Parasitol. 44:321-330.
26. Kong, H. H., T. H. Kim, and D. I. Chung. 2000. Purification and characterization of a secretory serine proteinase of Acanthamoeba healyi isolated from GAE. J. Parasitol. 86:12-17.
27. Li, T., H. Wang, and S. He. 2006. Induction of interleukin-6 release from monocytes by serine proteinases and its potential mechanisms. Scandinavian J. Immunol. 64:10-16.
28. MacLean, R. C., N. Hafez, S. Tripathi, C. G. Childress, N. R. Ghatak, and F. Marciano-Cabral. 2007. Identification of Acanthamoeba sp. in paraffin-embedded CNS tissue from an HIV+ individual by PCR. Diagn. Microbiol. Infect. Dis. 57:289-294.
29. Marciano-Cabral, F., and D. M. Toney. 1998. The interaction of Acanthamoeba spp. with activated macrophages and with macrophage cell lines. J. Eukaryot. Microbiol. 45:452-458.
30. Marciano-Cabral, F., and G. Cabral. 2003. Acanthamoeba spp. as agents of disease in humans. Clin. Microbiol. Rev. 16:273-307.
31. Marciano-Cabral, F., C. Ludwick, R. A. Puffenbarger, and G. A. Cabral. 2004. Differential stimulation of microglial pro-inflammatory cytokines by Acanthamoeba culbertsoni versus Acanthamoeba castellanii. J. Eukaryot. Microbiol. 51:472-479.
32. Martínez, A. J., C. Sotelo-Avila, J. Garcia-Tamayo, J. T. Morón, E. Willaert, and W. P. Stamm. 1977. Meningoencephalitis due to Acanthamoeba SP. Pathogenesis and clinico-pathological study. Acta Neuropathol. 37:183-191.
33. Martínez, A. J., and G. S. Visvesvara. 1997. Free-living, amphizoic and opportunistic amebas. Brain Pathol. 7:583-598.
34. Martínez, A. J. 1982. Acanthamoebiasis and immunosuppression. Case report. J. Neuropathol. Exp. Neurol. 41:548-557.
35. Mejri, N., and B. Gottstein. 2009. Echinococcus multilocularis metacestode metabolites contain a cysteine protease that digests eotaxin, a CC pro-inflammatory chemokine. Parasitol. Res. 105:1253-1260.
36. Misra, S. K., A. K. Sharma, H. Mehdi, and N. K. Garg. 1983. Phospholipase-A and lipid contents in pathogenic and non-pathogenic Acanthamoeba spp. in relation to their virulence. Protistologica 19:513-521.
37. Mitra, M. M., H. Alizadeh, R. D. Gerard, and J. Y. Niederkorn. 1995. Characterization of a plasminogen activator produced by Acanthamoeba castellanii. Mol. Biochem. Parasitol. 73:157-164.
38. Mitro, K., A. Bhagavathiammai, O. M. Zhou, G. Bobbett, J. H. McKerrow, R. Chokshi, B. Chokshi, and E. R. James. 1994. Partial characterization of the proteolytic secretions of Acanthamoeba polyphaga. Exp. Parasitol. 78:377-385.
39. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application for proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63.
40. Murakawa, G. J., T. McCalmont, J. Altman, G. H. Telang, M. D. Hoffman, G. R. Kantor, and T. G. Berger. 1995. Disseminated acanthamebiasis in patients with AIDS. A report of five cases and a review of the literature. Arch. Dermatol. 131:1291-1296.
41. Na, B. K., J. C. Kim, and C. Y. Song. 2001. Characterization and pathogenetic role of proteinase from Acanthamoeba castellanii. Microb. Pathog. 30:39-48.
42. Na, B. K., J. H. Cho, C. Y. Song, and T. S. Kim. 2002. Degradation of immunoglobulins, protease inhibitors and interleukin-1 by a secretory proteinase of Acanthamoeba castellanii. Korean J. Parasitol. 40:93-99.
43. Naldini, A., D. H. Carney, A. Pucci, A. Pasquali, and F. Carraro. 2000. Thrombin regulates the expression of proangiogenic cytokines via proteolytic activation of protease-activated receptor-1. Gen. Pharmacol. 35:255-259.
44. Naldini, A., A. Pucci, D. H. Carney, G. Fanetti, and F. Carraro. 2002. Thrombin enhancement of interleukin-1 expression in mononuclear cells: involvement of proteinase-activated receptor-1. Cytokine 20:191-199.
45. Pettit, D. A., J. Williamson, G. A. Cabral, and F. Marciano-Cabral. 1996. In vitro destruction of nerve cell cultures by Acanthamoeba spp.: a transmission and scanning electron microscopy study. J. Parasitol. 82:769-777.
46. Qvarnstrom, Y., A. J. da Silva, F. L. Schuster, B. B. Gelman, and G. S. Visvesvara. 2009. Molecular confirmation of Sappinia pedata as a causative agent of amoebic encephalitis. J. Infect. Dis. 199:1139-1142.
47. Rodriguez-Zaragoza, S. 1994. Ecology of free-living amoebae. Crit. Rev. Microbiol. 20:225-241.
48. Ryu, O. H., S. J. Choi, E. Firatli, S. W. Choi, P. S. Hart, R. F. Shen, G. Wang, W. W. Wu, and T. C. Hart. 2005. Proteolysis of macrophage inflammatory protein-1 alpha isoforms LD78β and LD78α by neutrophil-derived serine proteases. J. Biol. Chem. 280:17415-17421.
49. Schuster, F. L. 2002. Cultivation of pathogenic and opportunistic free-living amebas. Clin. Microbiol. Rev. 15:342-354.
50. Serrano-Luna, J. D. J., I. Cervantes-Sandoval, J. Calderón, F. Navarro-García, V. Tsutsumi, and M. Shibayama. 2006. Protease activities of Acanthamoeba polyphaga and Acanthamoeba castellanii. Can. J. Microbiol. 52:16-23.
51. Shin, H. J., M. S. Cho, S. Y. Jung, H. I. Kim, S. Park, J. H. Seo, J. C. Yoo, and K. I. Im. 2001. Cytopathic changes in rat microglial cells induced by pathogenic Acanthamoeba culbertsoni: morphology and cytokine release. Clin. Diagn. Lab. Immunol. 8:837-840.
52. Sissons, J., S. Alsam, G. Goldsworthy, M. Lightfoot, E. L. Jarroll, and N. A. Khan. 2006. Identification and properties of proteases from an Acanthamoeba isolate capable of producing granulomatous encephalitis. BMC Microbiol. 6:42.
53. Slater, C. A., J. Z. Sickel, G. S. Visvesvara, R. C. Pabico, and A. A. Gaspari. 1994. Successful treatment of disseminated Acanthamoeba infection in an immunocompromised patient. N. Engl. J. Med. 331:85-87.
54. Steinhoff, M., J. Buddenkotte, V. Shpacovitch, A. Rattenholl, C. Moormann, N. Vergnolle, T. A. Luger, and M. D. Hollenberg. 2005. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26:1-43.
55. Visvesvara, G. S., F. L. Schuster, and A. J. Martinez. 1993. Balamuthia mandrillaris, n. g., n. sp., agent of amebic meningoencephalitis in humans and other animals. J. Eukaryot. Microbiol. 40:504-514.
56. Visvesvara, G. S., H. Moura, and F. L. Schuster. 2007. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol. Med. Microbiol. 50:1-26.
57. Zheng, L., and M. Martins-Green. 2007. Molecular mechanisms of thrombin-induced interleukin-8 (IL-8/CXCL8) expression in THP-1-derived and primary human macrophages. J. Leukoc. Biol. 82:619-629.