Comparison of phylogenetically distinct Histoplasma strains reveals evolutionarily divergent virulence strategies

mBio

Volumn 5, Issue 4, 2014, Pages

  Sepúlveda, Victoria E ^a,b   Williams, Corinne L ^a   Goldman, William E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA (1,3) GLUCAN; GAMMA INTERFERON; GLUCAN; INTERLEUKIN 12; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CLADISTICS; CONTROLLED STUDY; FUNGAL STRAIN; FUNGAL VIRULENCE; HISTOPLASMA CAPSULATUM; HISTOPLASMOSIS; INFLAMMATORY INFILTRATE; MALE; MONOCYTE; MOUSE; NONHUMAN; PHYLOGENY; PNEUMONIA; ANIMAL; C57BL MOUSE; CLASSIFICATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EVOLUTION; HISTOPLASMA; LUNG; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

AJELLOMYCES;

ANIMALS; BIOLOGICAL EVOLUTION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HISTOPLASMA; HISTOPLASMOSIS; LUNG; MALE; MICE; MICE, INBRED C57BL; VIRULENCE;

EID: 84908235252     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01376-14     Document Type: Article

References (50)

1. Edwards LB, Acquaviva FA, Livesay VT, Cross FW, Palmer CE. 1969. An atlas of sensitivity to tuberculin, PPD-B, and histoplasmin in the United States. Am. Rev. Respir. Dis. 99:1-132.
2. Edwards LB, Acquaviva FA, Livesay VT. 1973. Further observations on histoplasmin sensitivity in the United States. Am. J. Epidemiol. 98: 315-325.
3. Eissenberg LG, Goldman WE. 1991. Histoplasma variation and adaptive strategies for parasitism: new perspectives on histoplasmosis. Clin. Microbiol. Rev. 4:411-421.
4. Larsh HW, Cozad GC. 1965. Respiratory infection of mice with Histoplasma capsulatum. Mycopathol. Mycol. Appl. 27:305-310. http://dx.doi.org/10.1007/BF02053788.
5. Durkin M, Kohler S, Schnizlein-Bick C, LeMonte A, Connolly P, Goldberg J, Garringer T, Wheat LJ. 2001. Chronic infection and reactivation in a pulmonary challenge model of histoplasmosis. J. Infect. Dis. 183:1822-1824. http://dx.doi.org/10.1086/320720.
6. Maresca B, Kobayashi GS. 1989. Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol. Rev. 53:186-209.
7. Rappleye CA, Goldman WE. 2006. Defining virulence genes in the dimorphic fungi. Annu. Rev. Microbiol. 60:281-303. http://dx.doi.org/10.1146/annurev.micro.59.030804.121055.
8. Medoff G, Sacco M, Maresca B, Schlessinger D, Painter A, Kobayashi GS, Carratu L. 1986. Irreversible block of the mycelial-to-yeast phase transition of Histoplasma capsulatum. Science 231:476-479. http://dx.doi.org/10.1126/science.3001938.
9. Klein BS, Tebbets B. 2007. Dimorphism and virulence in fungi. Curr. Opin. Microbiol. 10:314-319. http://dx.doi.org/10.1016/j.mib.2007.04.002.
10. Nguyen VQ, Sil A. 2008. Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc. Natl. Acad. Sci. U. S. A. 105:4880-4885. http://dx.doi.org/10.1073/pnas.0710448105.
11. Webster RH, Sil A. 2008. Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc. Natl. Acad. Sci. U. S. A. 105:14573-14578. http://dx.doi.org/10.1073/pnas.0806221105.
12. Kasuga T, Taylor JW, White TJ. 1999. Phylogenetic relationships of varieties and geographical groups of the human pathogenic fungus Histoplasma capsulatum Darling. J. Clin. Microbiol. 37:653-663.
13. Kasuga T, White TJ, Koenig G, Mcewen J, Restrepo A, Castañeda E, Da Silva Lacaz C, Heins-Vaccari EM, De Freitas RS, Zancopé-Oliveira RM, Qin Z, Negroni R, Carter DA, Mikami Y, Tamura M, Taylor ML, Miller GF, Poonwan N, Taylor JW. 2003. Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol. Ecol. 12:3383-3401. http://dx.doi.org/10.1046/j.1365-294X.2003.01995.x.
14. Reiss E, Miller SE, Kaplan W, Kaufman L. 1977. Antigenic, chemical, and structural properties of cell walls of Histoplasma capsulatum yeastform chemotypes 1 and 2 after serial enzymatic hydrolysis. Infect. Immun. 16:690-700.
15. Domer JE. 1971. Monosaccharide and chitin content of cell walls of Histoplasma capsulatum and Blastomyces dermatitidis. J. Bacteriol. 107: 870-877.
16. Rappleye CA, Eissenberg LG, Goldman WE. 2007. Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the betaglucan receptor. Proc. Natl. Acad. Sci. U. S. A. 104:1366-1370. http://dx.doi.org/10.1073/pnas.0609848104.
17. San-Blas G, Ordaz D, Yegres FJ. 1978. Histoplasma capsulatum: Chemical variability of the yeast cell wall. Sabouraudia 16:279-284. http://dx.doi.org/10.1080/00362177885380381.
18. Eissenberg LG, West JL, Woods JP, Goldman WE. 1991. Infection of P388D1 macrophages and respiratory epithelial cells by Histoplasma capsulatum: selection of avirulent variants and their potential role in persistent histoplasmosis. Infect. Immun. 59:1639-1646.
19. Klimpel KR, Goldman WE. 1987. Isolation and characterization of spontaneous avirulent variants of Histoplasma capsulatum. Infect. Immun. 55: 528-533.
20. Klimpel KR, Goldman WE. 1988. Cell walls from avirulent variants of Histoplasma capsulatum lack alpha-(1,3)-glucan. Infect. Immun. 56: 2997-3000.
21. Rappleye CA, Engle JT, Goldman WE. 2004. RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol. Microbiol. 53:153-165. http://dx.doi.org/10.1111/j.1365-2958.2004.04131.x.
22. Edwards JA, Alore EA, Rappleye CA. 2011. The yeast-phase virulence requirement for_-glucan synthase differs among Histoplasma capsulatum chemotypes. Eukaryot. Cell 10:87-97. http://dx.doi.org/10.1128/EC.00214-10.
23. Tewari RP, Berkhout FJ. 1972. Comparative pathogenicity of albino and brown types of Histoplasma capsulatum for mice. J. Infect. Dis. 125: 504-508. http://dx.doi.org/10.1093/infdis/125.5.504.
24. Mayfield JA, Rine J. 2007. The genetic basis of variation in susceptibility to infection with Histoplasma capsulatum in the mouse. Genes Immun. 8:468-474. http://dx.doi.org/10.1038/sj.gene.6364411.
25. Medoff G, Maresca B, Lambowitz AM, Kobayashi G, Painter A, Sacco M, Carratu L. 1986. Correlation between pathogenicity and temperature sensitivity in different strains of Histoplasma capsulatum. J. Clin. Invest. 78:1638-1647. http://dx.doi.org/10.1172/JCI112757.
26. Furcolow ML. 1961. Airborne histoplasmosis. Bacteriol. Rev. 25:301-309.
27. Gass M, Kobayashi GS. 1969. Histoplasmosis. An illustrative case with unusual vaginal and joint involvement. Arch. Dermatol. 100:724-727. http://dx.doi.org/10.1001/archderm.100.6.724.
28. Spitzer ED, Keath EJ, Travis SJ, Painter AA, Kobayashi GS, Medoff G. 1990. Temperature-sensitive variants of Histoplasma capsulatum isolated from patients with acquired immunodeficiency syndrome. J. Infect. Dis. 162:258-261. http://dx.doi.org/10.1093/infdis/162.1.258.
29. Broad Institute. 2007. Histoplasma capsulatum database. Broad Institute, Cambridge, MA. http://broadinstitute.org/annotation/genome/histoplasma_capsulatum/MultiHome.html.
30. Goodwin TJD, Butler MI, Poulter RTM. 2003. Cryptons: a group of tyrosine-recombinase-encoding DNA transposons from pathogenic fungi. Microbiology (Reading, Engl.) 149:3099-3109.
31. Edwards JA, Rappleye CA. 2011. Histoplasma mechanisms of pathogenesis— one portfolio doesn’t fit all. FEMS Microbiol. Lett. 324:1-9. http://dx.doi.org/10.1111/j.1574-6968.2011.02363.x.
32. Edwards JA, Zemska O, Rappleye CA. 2011. Discovery of a role for Hsp82 in Histoplasma virulence through a quantitative screen for macrophage lethality. Infect. Immun. 79:3348-3357. http://dx.doi.org/10.1128/IAI.05124-11.
33. Isaac DT, Coady A, Van Prooyen N, Sil A. 2013. The 3-hydroxymethylglutaryl coenzyme A lyase HCL1 is required for macrophage colonization by human fungal pathogen Histoplasma capsulatum. Infect. Immun. 81:411-420. http://dx.doi.org/10.1128/IAI.00833-12.
34. Zhou P, Miller G, Seder RA. 1998. Factors involved in regulating primary and secondary immunity to infection with Histoplasma capsulatum: TNFalpha plays a critical role in maintaining secondary immunity in the absence of IFN-gamma. J. Immunol. 160:1359-1368.
35. Zhou P, Sieve MC, Bennett J, Kwon-Chung KJ, Tewari RP, Gazzinelli RT, Sher A, Seder RA. 1995. IL-12 prevents mortality in mice infected with Histoplasma capsulatum through induction of IFN-gamma. J. Immunol. 155:785-795.
36. Deepe GS, McGuinness M. 2006. Interleukin-1 and host control of pulmonary histoplasmosis. J. Infect. Dis. 194:855-864. http://dx.doi.org/10.1086/506946.
37. Deepe GS. 2005. Modulation of infection with Histoplasma capsulatum by inhibition of tumor necrosis factor-alpha activity. Clin. Infect. Dis. 41: S204-S207. http://dx.doi.org/10.1086/429999.
38. Allendoerfer R, Deepe GS. 1997. Intrapulmonary response to Histoplasma capsulatum in gamma interferon knockout mice. Infect. Immun. 65:2564-2569.
39. Deepe GS. 2007. Tumor necrosis factor-alpha and host resistance to the pathogenic fungus, Histoplasma capsulatum. J. Investig. Dermatol. Symp. Proc. 12:34-37. http://dx.doi.org/10.1038/sj.jidsymp.5650026.
40. Keath EJ, Painter AA, Kobayashi GS, Medoff G. 1989. Variable expression of a yeast-phase-specific gene in Histoplasma capsulatum strains differing in thermotolerance and virulence. Infect. Immun. 57:1384-1390.
41. San-Blas G, San-Blas F, Serrano LE. 1977. Host-parasite relationships in the yeastlike form of Paracoccidioides brasiliensis strain IVIC Pb9. Infect. Immun. 15:343-346.
42. Hogan LH, Klein BS. 1994. Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect. Immun. 62:3543-3546.
43. Reese AJ, Doering TL. 2003. Cell wall alpha-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol. Microbiol. 50: 1401-1409. http://dx.doi.org/10.1046/j.1365-2958.2003.03780.x.
44. Larsh HW. 1960. Natural and experimental epidemiology of histoplasmosis. Ann. N. Y. Acad. Sci. 89:78-90. http://dx.doi.org/10.1111/j.1749-6632.1960.tb20132.x.
45. Cerami A, Beutler B. 1988. The role of cachectin/TNF in endotoxic shock and cachexia. Immunol. Today 9:28-31. http://dx.doi.org/10.1016/0167-5699(88)91353-9.
46. Campbell CC. 1965. The epidemiology of histoplasmosis. Ann. Intern. Med. 62:1333-1336. http://dx.doi.org/10.7326/0003-4819-62-6-1333.
47. Worsham PL, Goldman WE. 1988. Selection and characterization of ura5 mutants of Histoplasma capsulatum. Mol. Gen. Genet. 214:348-352.
48. Eissenberg LG, Schlesinger PH, Goldman WE. 1988. Phagosomelysosome fusion in P388D1 macrophages infected with Histoplasma capsulatum. J. Leukoc. Biol. 43:483-491.
49. Sullivan JT, Young EF, McCann JR, Braunstein M. 2012. The mycobacterium tuberculosis, SecA2 system subverts phagosome maturation to promote growth in macrophages. Infect. Immun. 80:996-1006.
50. Sebghati TS, Engle JT, Goldman WE. 2000. Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290:1368-1372. http://dx.doi.org/10.1126/science.290.5495.1368