Melanin dependent survival of Apergillus fumigatus conidia in lung epithelial cells

International Journal of Medical Microbiology

Volumn 304, Issue 5-6, 2014, Pages 626-636

  Amin, Shayista ^a,b   Thywissen, Andreas ^a   Heinekamp, Thorsten ^a   Saluz, Hans Peter ^a,b   Brakhage, Axel A ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Alveolar epithelial cells; Apoptosis; Aspergillus fumigatus; Melanin; Persistence

Indexed keywords

DOPA; MELANIN;

ACIDIFICATION; ARTICLE; ASPERGILLUS FUMIGATUS; CELL WALL; CONIDIUM; EPITHELIUM CELL; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; MUTANT; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; SURVIVAL RATE; WILD TYPE; CELL LINE; ENDOCYTOSIS; FUNGUS SPORE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY;

ASPERGILLUS FUMIGATUS; CELL LINE; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; MELANINS; MICROBIAL VIABILITY; SPORES, FUNGAL;

EID: 84903820401     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.04.009     Document Type: Article

References (57)

1. Amitani R., Kawanami R. Interaction of Aspergillus with human respiratory mucosa: a study with organ culture model. Med. Mycol. Off. Publ. Int. Soc. Hum. Anim. Mycol. 2009, 47(Suppl. 1):S127-S131.
2. Behnsen J., Hartmann A., Schmaler J., Gehrke A., Brakhage A.A., Zipfel P.F. The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system. Infect. Immun. 2008, 76:820-827.
3. Beisswenger C., Hess C., Bals R. Aspergillus fumigatus conidia induce interferon-beta signalling in respiratory epithelial cells. Eur. Respir. J. 2012, 39:411-418.
4. Berkova N., Lair-Fulleringer S., Femenia F., Huet D., Wagner M.C., Gorna K., Tournier F., Ibrahim-Granet O., Guillot J., Chermette R., et al. Aspergillus fumigatus conidia inhibit tumour necrosis factor- or staurosporine-induced apoptosis in epithelial cells. Int. Immunol. 2006, 18:139-150.
5. Brakhage A.A. Systemic fungal infections caused by Aspergillus species: epidemiology, infection process and virulence determinants. Curr. Drug Targets 2005, 6:875-886.
6. Brakhage A.A., Bruns S., Thywissen A., Zipfel P.F., Behnsen J. Interaction of phagocytes with filamentous fungi. Curr. Opin. Microbiol. 2010, 13:409-415.
7. Brakhage A.A., Liebmann B. Aspergillus fumigatus conidial pigment and cAMP signal transduction: significance for virulence. Med. Mycol. Off. Publ. Int. Soc. Hum. Anim. Mycol. 2005, 43(Suppl. 1):S75-S82.
8. Brown G.D., Taylor P.R., Reid D.M., Willment J.A., Williams D.L., Martinez-Pomares L., Wong S.Y., Gordon S. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 2002, 196:407-412.
9. Carmody R.J., Cotter T.G. Signalling apoptosis: a radical approach. Redox Rep. 2001, 6:77-90.
10. Chai L.Y., Vonk A.G., Kullberg B.J., Verweij P.E., Verschueren I., van der Meer J.W., Joosten L.A., Latge J.P., Netea M.G. Aspergillus fumigatus cell wall components differentially modulate host TLR2 and TLR4 responses. Microbes Infect. 2011, 13:151-159.
11. Chandra J., Samali A., Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 2000, 29:323-333.
12. Chose O., Sarde C.O., Noel C., Gerbod D., Jimenez J.C., Brenner C., Capron M., Viscogliosi E., Roseto A. Cell death in protists without mitochondria. Ann. N Y Acad. Sci. 2003, 1010:121-125.
13. Clark C.S., Maurelli A.T. Shigella flexneri inhibits staurosporine-induced apoptosis in epithelial cells. Infect. Immun. 2007, 75:2531-2539.
14. D'Enfert C., Diaquin M., Delit A., Wuscher N., Debeaupuis J.P., Huerre M., Latge J.P. Attenuated virulence of uridine-uracil auxotrophs of Aspergillus fumigatus. Infect. Immun. 1996, 64:4401-4405.
15. Dagenais T.R., Keller N.P. Pathogenesis of Aspergillus fumigatus in invasive Aspergillosis. Clin. Microbiol. Rev. 2009, 22:447-465.
16. DeHart D.J., Agwu D.E., Julian N.C., Washburn R.G. Binding and germination of Aspergillus fumigatus conidia on cultured A549 pneumocytes. J. Infect. Dis. 1997, 175:146-150.
17. Faherty C.S., Maurelli A.T. Staying alive: bacterial inhibition of apoptosis during infection. Trends Microbiol. 2008, 16:173-180.
18. Femenia F., Huet D., Lair-Fulleringer S., Wagner M.C., Sarfati J., Shingarova L., Guillot J., Boireau P., Chermette R., Berkova N. Effects of conidia of various Aspergillus species on apoptosis of human pneumocytes and bronchial epithelial cells. Mycopathologia 2009, 167:249-262.
19. Filler S.G., Sheppard D.C. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2006, 2:e129.
20. Flannagan R.S., Cosio G., Grinstein S. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 2009, 7:355-366.
21. Gong J., Traganos F., Darzynkiewicz Z. A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal. Biochem. 1994, 218:314-319.
22. Grosse C., Heinekamp T., Kniemeyer O., Gehrke A., Brakhage A.A. Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Appl. Environ. Microbiol. 2008, 74:4923-4933.
23. Haas A. The phagosome: compartment with a license to kill. Traffic (Copenhagen, Denmark) 2007, 8:311-330.
24. Heinekamp T., Thywissen A., Macheleidt J., Keller S., Valiante V., Brakhage A.A. Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence. Front. Microbiol. 2012, 3:440.
25. Ibata-Ombetta S., Idziorek T., Trinel P.A., Poulain D., Jouault T. Candida albicans phospholipomannan promotes survival of phagocytosed yeasts through modulation of bad phosphorylation and macrophage apoptosis. J. Biol. Chem. 2003, 278:13086-13093.
26. Jacobson M.D. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 1996, 21:83-86.
27. Jahn B., Boukhallouk F., Lotz J., Langfelder K., Wanner G., Brakhage A.A. Interaction of human phagocytes with pigmentless Aspergillus conidia. Infect. Immun. 2000, 68:3736-3739.
28. Jahn B., Koch A., Schmidt A., Wanner G., Gehringer H., Bhakdi S., Brakhage A.A. Isolation and characterization of a pigmentless-conidium mutant of Aspergillus fumigatus with altered conidial surface and reduced virulence. Infect. Immun. 1997, 65:5110-5117.
29. Jahn B., Langfelder K., Schneider U., Schindel C., Brakhage A.A. PKSP-dependent reduction of phagolysosome fusion and intracellular kill of Aspergillus fumigatus conidia by human monocyte-derived macrophages. Cell. Microbiol. 2002, 4:793-803.
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
31. Langfelder K., Jahn B., Gehringer H., Schmidt A., Wanner G., Brakhage A.A. Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med. Microbiol. Immunol. 1998, 187:79-89.
32. Latge J.P. Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 1999, 12:310-350.
33. Luther K., Torosantucci A., Brakhage A.A., Heesemann J., Ebel F. Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cell. Microbiol. 2007, 9:368-381.
34. Martinou J.C., Green D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell. Biol. 2001, 2:63-67.
35. Mech F., Thywissen A., Guthke R., Brakhage A.A., Figge M.T. Automated image analysis of the host-pathogen interaction between phagocytes and Aspergillus fumigatus. PloS one 2011, 6:e19591.
36. Osherov N. Interaction of the pathogenic mold Aspergillus fumigatus with lung epithelial cells. Front. Microbiol. 2012, 3:346.
37. Paris S., Boisvieux-Ulrich E., Crestani B., Houcine O., Taramelli D., Lombardi L., Latge J.P. Internalization of Aspergillus fumigatus conidia by epithelial and endothelial cells. Infect. Immun. 1997, 65:1510-1514.
38. Pihet M., Vandeputte P., Tronchin G., Renier G., Saulnier P., Georgeault S., Mallet R., Chabasse D., Symoens F., Bouchara J.P. Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol. 2009, 9:177.
39. Rodrigues V., Cordeiro-da-Silva A., Laforge M., Ouaissi A., Silvestre R., Estaquier J. Modulation of mammalian apoptotic pathways by intracellular protozoan parasites. Cell. Microbiol. 2012, 14:325-333.
40. Rudel T., Kepp O., Kozjak-Pavlovic V. Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat. Rev. Microbiol. 2010, 8:693-705.
41. Ruhland A., Leal N., Kima P.E. Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis. Cell. Microbiol. 2007, 9:84-96.
42. Seagle B.L., Gasyna E.M., Mieler W.F., Norris J.R. Photoprotection of human retinal pigment epithelium cells against blue light-induced apoptosis by melanin free radicals from Sepia officinalis. Proc. Natl. Acad. Sci. U S A 2006, 103:16644-16648.
43. Slesiona S., Gressler M., Mihlan M., Zaehle C., Schaller M., Barz D., Hube B., Jacobsen I.D., Brock M. Persistence versus escape: Aspergillus terreus and Aspergillus fumigatus employ different strategies during interactions with macrophages. PloS one 2012, 7:e31223.
44. Sturtevant J.E., Latge J.P. Interactions between conidia of Aspergillus fumigatus and human complement component C3. Infect. Immun. 1992, 60:1913-1918.
45. Susin S.A., Daugas E., Ravagnan L., Samejima K., Zamzami N., Loeffler M., Costantini P., Ferri K.F., Irinopoulou T., Prevost M.C., et al. Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 2000, 192:571-580.
46. Suzuki T., Nakanishi K., Tsutsui H., Iwai H., Akira S., Inohara N., Chamaillard M., Nunez G., Sasakawa C. A novel caspase-1/toll-like receptor 4-independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J. Biol. Chem. 2005, 280:14042-14050.
47. Szewczyk E., Krappmann S. Conserved regulators of mating are essential for Aspergillus fumigatus cleistothecium formation. Eukaryot. Cell 2010, 9:774-783.
48. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell. Biol. 2008, 9:231-241.
49. Thywissen A., Heinekamp T., Dahse H.M., Schmaler-Ripcke J., Nietzsche S., Zipfel P.F., Brakhage A.A. Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front. Microbiol. 2011, 2:96.
50. Tsai H.F., Chang Y.C., Washburn R.G., Wheeler M.H., Kwon-Chung K.J. The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J. Bacteriol. 1998, 180:3031-3038.
51. Tsai H.F., Washburn R.G., Chang Y.C., Kwon-Chung K.J. Aspergillus fumigatus arp1 modulates conidial pigmentation and complement deposition. Mol. Microbiol. 1997, 26:175-183.
52. Volling K., Brakhage A.A., Saluz H.P. Apoptosis inhibition of alveolar macrophages upon interaction with conidia of Aspergillus fumigatus. FEMS Microbiol. Lett. 2007, 275:250-254.
53. Volling K., Thywissen A., Brakhage A.A., Saluz H.P. Phagocytosis of melanized Aspergillus conidia by macrophages exerts cytoprotective effects by sustained PI3K/Akt signalling. Cell. Microbiol. 2011, 13:1130-1148.
54. Wasylnka J.A., Moore M.M. Uptake of Aspergillus fumigatus conidia by phagocytic and nonphagocytic cells in vitro: quantitation using strains expressing green fluorescent protein. Infect. Immun. 2002, 70:3156-3163.
55. Wasylnka J.A., Moore M.M. Aspergillus fumigatus conidia survive and germinate in acidic organelles of A549 epithelial cells. J. Cell Sci. 2003, 116:1579-1587.
56. Weidner G., d'Enfert C., Koch A., Mol P.C., Brakhage A.A. Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5'-monophosphate decarboxylase. Curr. Genet. 1998, 33:378-385.
57. Youngchim S., Morris-Jones R., Hay R.J., Hamilton A.J. Production of melanin by Aspergillus fumigatus. J. Med. Microbiol. 2004, 53:175-181.