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Histoplasma Capsulatum: Mechanisms for Pathogenesis

  • Jamie Mittal
  • Maria G. Ponce
  • Inessa Gendlina
  • Joshua D. NosanchukEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 422)

Abstract

Histoplasmosis, caused by the dimorphic environmental fungus Histoplasma capsulatum, is a major mycosis on the global stage. Acquisition of the fungus by mammalian hosts can be clinically silent or it can lead to life-threatening systemic disease, which can occur in immunologically intact or deficient hosts, albeit severe disease is more likely in the setting of compromised cellular immunity. H. capsulatum yeast cells are highly adapted to the mammalian host as they can effectively survive within intracellular niches in select phagocytic cells. Understanding the biological response by both the host and H. capsulatum will facilitate improved approaches to prevent and/or modify disease. This review presents our current understanding of the major pathogenic mechanisms involved in histoplasmosis.

Keywords

Histoplasma capsulatum Histoplasmosis Intracellular survival Virulence Microbial pathogenesis 

References

  1. Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, Zancope-Oliveira RM, Almeida IC, Nosanchuk JD (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10(8):1695–1710.  https://doi.org/10.1111/j.1462-5822.2008.01160.xPubMedPubMedCentralCrossRefGoogle Scholar
  2. Allen HL, Deepe GS (2006) B cells and CD4-CD8- T cells are key regulators of the severity of reactivation histoplasmosis. J Immunol 177(3):1763–1771PubMedCrossRefGoogle Scholar
  3. Allendoerfer R, Deepe GS (1998) Blockade of endogenous TNF-alpha exacerbates primary and secondary pulmonary histoplasmosis by differential mechanisms. J Immunol 160(12):6072–6082PubMedGoogle Scholar
  4. Armstrong PA, Jackson BR, Haselow D, Fields V, Ireland M, Austin C, Signs K, Fialkowski V, Patel R, Ellis P, Iwen PC, Pedati C, Gibbons-Burgener S, Anderson J, Dobbs T, Davidson S, McIntyre M, Warren K, Midla J, Luong N, Benedict K (2018) Multistate epidemiology of histoplasmosis, United States, 2011–2014. Emerg Infect Dis 24(3):425–431.  https://doi.org/10.3201/eid2403.171258PubMedPubMedCentralCrossRefGoogle Scholar
  5. Arrigoni MG, Bernatz PE, Donoghue FE (1971) Broncholithiasis. J Thorac Cardiovasc Surg 62(2):231–237PubMedGoogle Scholar
  6. Assi M, Lakkis IE, Wheat LJ (2011) Cross-reactivity in the Histoplasma antigen enzyme immunoassay caused by sporotrichosis. Clin Vaccine Immunol 18(10):1781–1782.  https://doi.org/10.1128/cvi.05017-11PubMedPubMedCentralCrossRefGoogle Scholar
  7. Azar MM, Hage CA (2017) Laboratory diagnostics for histoplasmosis. J Clin Microbiol 55(6):1612–1620.  https://doi.org/10.1128/jcm.02430-16PubMedPubMedCentralCrossRefGoogle Scholar
  8. Baddley JW, Winthrop KL, Patkar NM, Delzell E, Beukelman T, Xie F, Chen L, Curtis JR (2011) Geographic distribution of endemic fungal infections among older persons, United States. Emerg Infect Dis 17(9):1664–1669.  https://doi.org/10.3201/eid1709.101987PubMedPubMedCentralCrossRefGoogle Scholar
  9. Batanghari JW, Deepe GS, Di Cera E, Goldman WE (1998) Histoplasma acquisition of calcium and expression of CBP1 during intracellular parasitism. Mol Microbiol 27(3):531–539PubMedCrossRefGoogle Scholar
  10. Baum GL, Schwarz J (1957) The history of histoplasmosis, 1906 to 1956. N Engl J Med 256(6):253–258.  https://doi.org/10.1056/nejm195702072560605PubMedCrossRefGoogle Scholar
  11. Beyhan S, Gutierrez M, Voorhies M, Sil A (2013) A temperature-responsive network links cell shape and virulence traits in a primary fungal pathogen. PLoS Biol 11(7):e1001614.  https://doi.org/10.1371/journal.pbio.1001614PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bullock WE, Wright SD (1987) Role of the adherence-promoting receptors, CR3, LFA-1, and p150,95, in binding of Histoplasma capsulatum by human macrophages. J Exp Med 165(1):195–210PubMedCrossRefGoogle Scholar
  13. Cain JA, Deepe GS (1998) Evolution of the primary immune response to Histoplasma capsulatum in murine lung. Infect Immun 66(4):1473–1481PubMedPubMedCentralGoogle Scholar
  14. Carreto-Binaghi LE, Aliouat eM, Taylor ML (2016) Surfactant proteins, SP-A and SP-D, in respiratory fungal infections: their role in the inflammatory response. Respir Res 17(1):66.  https://doi.org/10.1186/s12931-016-0385-9
  15. Casadevall A, Pirofski LA (2003) The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 1(1):17–24.  https://doi.org/10.1038/nrmicro732PubMedCrossRefGoogle Scholar
  16. Chakrabarti A, Slavin MA (2011) Endemic fungal infections in the Asia-Pacific region. Med Mycol 49(4):337–344.  https://doi.org/10.3109/13693786.2010.551426PubMedCrossRefGoogle Scholar
  17. Chao LY, Rine J, Marletta MA (2008) Spectroscopic and kinetic studies of Nor1, a cytochrome P450 nitric oxide reductase from the fungal pathogen Histoplasma capsulatum. Arch Biochem Biophys 480(2):132–137.  https://doi.org/10.1016/j.abb.2008.09.001PubMedPubMedCentralCrossRefGoogle Scholar
  18. Clark R, Kupper T (2005) Old meets new: the interaction between innate and adaptive immunity. J Invest Dermatol 125(4):629–637.  https://doi.org/10.1111/j.0022-202X.2005.23856.xPubMedCrossRefGoogle Scholar
  19. Cleare LG, Zamith-Miranda D, Nosanchuk JD (2017) Heat shock proteins in Histoplasma and Paracoccidioides. Clin Vaccine Immunol 24(11).  https://doi.org/10.1128/cvi.00221-17
  20. Clemons KV, Darbonne WC, Curnutte JT, Sobel RA, Stevens DA (2000) Experimental histoplasmosis in mice treated with anti-murine interferon-gamma antibody and in interferon-gamma gene knockout mice. Microbes Infect 2(9):997–1001PubMedCrossRefGoogle Scholar
  21. Clemons KV, Lutz JE, Stevens DA (2001) Efficacy of interferon-gamma and amphotericin B for the treatment of systemic murine histoplasmosis. Microbes Infect 3(1):3–10PubMedCrossRefGoogle Scholar
  22. Cohen NR, Tatituri RV, Rivera A, Watts GF, Kim EY, Chiba A, Fuchs BB, Mylonakis E, Besra GS, Levitz SM, Brigl M, Brenner MB (2011) Innate recognition of cell wall β-glucans drives invariant natural killer T cell responses against fungi. Cell Host Microbe 10(5):437–450.  https://doi.org/10.1016/j.chom.2011.09.011PubMedPubMedCentralCrossRefGoogle Scholar
  23. Colombo AL, Tobón A, Restrepo A, Queiroz-Telles F, Nucci M (2011) Epidemiology of endemic systemic fungal infections in Latin America. Med Mycol 49(8):785–798.  https://doi.org/10.3109/13693786.2011.577821PubMedCrossRefGoogle Scholar
  24. Dade J, DuBois JC, Pasula R, Donnell AM, Caruso JA, Smulian AG, Deepe GS (2016) HcZrt2, a zinc responsive gene, is indispensable for the survival of Histoplasma capsulatum in vivo. Med Mycol 54(8):865–875.  https://doi.org/10.1093/mmy/myw045PubMedPubMedCentralCrossRefGoogle Scholar
  25. Darling ST (1906) A protozoön general infection producing pseudotubercles in the lungs and focal necroses in the liver, spleen and lymphnodes. J Am Med Assoc XLVI 17:1283–1285.  https://doi.org/10.1001/jama.1906.62510440037003CrossRefGoogle Scholar
  26. Davis AM, Pierson RN, Loyd JE (2001) Mediastinal fibrosis. Semin Respir Infect 16(2):119–130PubMedCrossRefGoogle Scholar
  27. Deepe GS (2005) Modulation of infection with Histoplasma capsulatum by inhibition of tumor necrosis factor-alpha activity. Clin Infect Dis 41(Suppl 3):S204–S207.  https://doi.org/10.1086/429999PubMedCrossRefGoogle Scholar
  28. Deepe GS (2007) Tumor necrosis factor-alpha and host resistance to the pathogenic fungus, Histoplasma capsulatum. J Investig Dermatol Symp Proc 12(1):34–37.  https://doi.org/10.1038/sj.jidsymp.5650026PubMedCrossRefGoogle Scholar
  29. Deepe GS, Buesing WR (2012) Deciphering the pathways of death of Histoplasma capsulatum-infected macrophages: implications for the immunopathogenesis of early infection. J Immunol 188(1):334–344.  https://doi.org/10.4049/jimmunol.1102175PubMedCrossRefGoogle Scholar
  30. Deepe GS, Gibbons RS (2008) TNF-alpha antagonism generates a population of antigen-specific CD4+ CD25+ T cells that inhibit protective immunity in murine histoplasmosis. J Immunol 180(2):1088–1097PubMedPubMedCentralCrossRefGoogle Scholar
  31. Deepe GS, Gibbons RS, Smulian AG (2008) Histoplasma capsulatum manifests preferential invasion of phagocytic subpopulations in murine lungs. J Leukoc Biol 84(3):669–678.  https://doi.org/10.1189/jlb.0308154PubMedPubMedCentralCrossRefGoogle Scholar
  32. Edwards JA, Alore EA, Rappleye CA (2011) The yeast-phase virulence requirement for α-glucan synthase differs among Histoplasma capsulatum chemotypes. Eukaryot Cell 10(1):87–97.  https://doi.org/10.1128/ec.00214-10PubMedPubMedCentralCrossRefGoogle Scholar
  33. Eissenberg LG, Goldman WE (1987) Histoplasma capsulatum fails to trigger release of superoxide from macrophages. Infect Immun 55(1):29–34PubMedPubMedCentralGoogle Scholar
  34. Eissenberg LG, Schlesinger PH, Goldman WE (1988) Phagosome-lysosome fusion in P388D1 macrophages infected with Histoplasma capsulatum. J Leukoc Biol 43(6):483–491PubMedCrossRefGoogle Scholar
  35. Elansari R, Abada R, Rouadi S, Roubal M, Mahtar M (2016) Histoplasma capsulatum sinusitis: possible way of revelation to the disseminated form of histoplasmosis in HIV patients: case report and literature review. Int J Surg Case Rep 24:97–100.  https://doi.org/10.1016/j.ijscr.2016.03.010PubMedPubMedCentralCrossRefGoogle Scholar
  36. English BC, Van Prooyen N, Örd T, Sil A (2017) The transcription factor CHOP, an effector of the integrated stress response, is required for host sensitivity to the fungal intracellular pathogen Histoplasma capsulatum. PLoS Pathog 13(9):e1006589.  https://doi.org/10.1371/journal.ppat.1006589PubMedPubMedCentralCrossRefGoogle Scholar
  37. Galetta D, Pelosi G, Nebuloni M, Spaggiari L (2007) Challenging diagnosis of an unusual solitary pulmonary nodule. Thorac Cardiovasc Surg 55(2):123–125.  https://doi.org/10.1055/s-2006-924407PubMedCrossRefGoogle Scholar
  38. Garfoot AL, Rappleye CA (2016) Histoplasma capsulatum surmounts obstacles to intracellular pathogenesis. FEBS J 283(4):619–633.  https://doi.org/10.1111/febs.13389PubMedCrossRefGoogle Scholar
  39. Garfoot AL, Zemska O, Rappleye CA (2014) Histoplasma capsulatum depends on de novo vitamin biosynthesis for intraphagosomal proliferation. Infect Immun 82(1):393–404.  https://doi.org/10.1128/iai.00824-13PubMedPubMedCentralCrossRefGoogle Scholar
  40. Garfoot AL, Shen Q, Wüthrich M, Klein BS, Rappleye CA (2016) The Eng1 β-Glucanase enhances Histoplasma Virulence by reducing β-Glucan exposure. MBio 7(2):e01388–e01315.  https://doi.org/10.1128/mBio.01388-15PubMedPubMedCentralCrossRefGoogle Scholar
  41. Garfoot AL, Dearing KL, VanSchoiack AD, Wysocki VH, Rappleye CA (2017) Eng1 and Exg8 Are the Major β-Glucanases Secreted by the Fungal Pathogen. J Biol Chem 292(12):4801–4810.  https://doi.org/10.1074/jbc.M116.762104PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gildea LA, Morris RE, Newman SL (2001) Histoplasma capsulatum yeasts are phagocytosed via very late antigen-5, killed, and processed for antigen presentation by human dendritic cells. J Immunol 166(2):1049–1056PubMedCrossRefGoogle Scholar
  43. Gildea LA, Ciraolo GM, Morris RE, Newman SL (2005) Human dendritic cell activity against Histoplasma capsulatum is mediated via phagolysosomal fusion. Infect Immun 73(10):6803–6811.  https://doi.org/10.1128/iai.73.10.6803-6811.2005PubMedPubMedCentralCrossRefGoogle Scholar
  44. Gomez FJ, Allendoerfer R, Deepe GS (1995) Vaccination with recombinant heat shock protein 60 from Histoplasma capsulatum protects mice against pulmonary histoplasmosis. Infect Immun 63(7):2587–2595PubMedPubMedCentralGoogle Scholar
  45. Gomez FJ, Pilcher-Roberts R, Alborzi A, Newman SL (2008) Histoplasma capsulatum cyclophilin A mediates attachment to dendritic cell VLA-5. J Immunol 181(10):7106–7114PubMedCrossRefGoogle Scholar
  46. Goodwin RA, Snell JD (1969) The enlarging histoplasmoma. Concept of a tumor-like phenomenon encompassing the tuberculoma and coccidioidoma. Am Rev Respir Dis 100(1):1–12.  https://doi.org/10.1164/arrd.1969.100.1.1PubMedCrossRefGoogle Scholar
  47. Goodwin RA, Owens FT, Snell JD, Hubbard WW, Buchanan RD, Terry RT, Des Prez RM (1976) Chronic pulmonary histoplasmosis. Medicine (Baltimore) 55(6):413–452CrossRefGoogle Scholar
  48. Gray PW, Flaggs G, Leong SR, Gumina RJ, Weiss J, Ooi CE, Elsbach P (1989) Cloning of the cDNA of a human neutrophil bactericidal protein. Structural and functional correlations. J Biol Chem 264(16):9505–9509PubMedGoogle Scholar
  49. Guimarães AJ, Nosanchuk JD, Zancopé-Oliveira RM (2006) Diagnosis of histoplasmosis. Braz J Microbiol 37(1):1–13.  https://doi.org/10.1590/s1517-83822006000100001PubMedPubMedCentralCrossRefGoogle Scholar
  50. Guimarães AJ, Hamilton AJ, de M Guedes HL, Nosanchuk JD, Zancopé-Oliveira RM (2008) Biological function and molecular mapping of M antigen in yeast phase of Histoplasma capsulatum. PloS one 3(10):e3449.  https://doi.org/10.1371/journal.pone.0003449PubMedPubMedCentralCrossRefGoogle Scholar
  51. Guimarães AJ, Frases S, Gomez FJ, Zancopé-Oliveira RM, Nosanchuk JD (2009) Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun 77(4):1357–1367.  https://doi.org/10.1128/IAI.01443-08PubMedPubMedCentralCrossRefGoogle Scholar
  52. Guimarães AJ, Frases S, Pontes B, de Cerqueira MD, Rodrigues ML, Viana NB, Nimrichter L, Nosanchuk JD (2011a) Agglutination of Histoplasma capsulatum by IgG monoclonal antibodies against Hsp60 impacts macrophage effector functions. Infect Immun 79(2):918–927.  https://doi.org/10.1128/iai.00673-10PubMedCrossRefGoogle Scholar
  53. Guimarães AJ, Nakayasu ES, Sobreira TJ, Cordero RJ, Nimrichter L, Almeida IC, Nosanchuk JD (2011b) Histoplasma capsulatum heat-shock 60 orchestrates the adaptation of the fungus to temperature stress. PLoS ONE 6(2):e14660.  https://doi.org/10.1371/journal.pone.0014660PubMedPubMedCentralCrossRefGoogle Scholar
  54. Han S, Mallampalli RK (2015) The role of surfactant in lung disease and host defense against pulmonary infections. Ann Am Thorac Soc 12(5):765–774.  https://doi.org/10.1513/AnnalsATS.201411-507FRPubMedPubMedCentralCrossRefGoogle Scholar
  55. Heninger E, Hogan LH, Karman J, Macvilay S, Hill B, Woods JP, Sandor M (2006) Characterization of the Histoplasma capsulatum-induced granuloma. J Immunol 177(5):3303–3313PubMedPubMedCentralCrossRefGoogle Scholar
  56. Histoplasmosis Risk & Prevention. Centers for Disease Control and Prevention. https://www.cdc.gov/fungal/diseases/histoplasmosis/risk-prevention.html#one. Accessed 16 May 2018
  57. Holbrook ED, Smolnycki KA, Youseff BH, Rappleye CA (2013) Redundant catalases detoxify phagocyte reactive oxygen and facilitate Histoplasma capsulatum pathogenesis. Infect Immun 81(7):2334–2346.  https://doi.org/10.1128/iai.00173-13PubMedPubMedCentralCrossRefGoogle Scholar
  58. Holt PG, Schon-Hegrad MA (1987) Localization of T cells, macrophages and dendritic cells in rat respiratory tract tissue: implications for immune function studies. Immunology 62(3):349–356PubMedPubMedCentralGoogle Scholar
  59. Howard DH, Rafie R, Tiwari A, Faull KF (2000) Hydroxamate siderophores of Histoplasma capsulatum. Infect Immun 68(4):2338–2343PubMedPubMedCentralCrossRefGoogle Scholar
  60. Huffnagle GB, Noverr MC (2008) GI microbiota and regulation of the immune system. In: Advances in experimental medicine and biology, vol 635. Springer Science + Business Media; Landes Bioscience, New York; Austin, TXGoogle Scholar
  61. Hutton JP, Durham JB, Miller DP, Everett ED (1985) Hyphal forms of Histoplasma capsulatum. A common manifestation of intravascular infections. Arch Pathol Lab Med 109(4):330–332PubMedGoogle Scholar
  62. Hwang LH, Mayfield JA, Rine J, Sil A (2008) Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization. PLoS Pathog 4(4):e1000044.  https://doi.org/10.1371/journal.ppat.1000044PubMedPubMedCentralCrossRefGoogle Scholar
  63. Isaac DT, Coady A, Van Prooyen N, Sil A (2013) The 3-hydroxy-methylglutaryl coenzyme A lyase HCL1 is required for macrophage colonization by human fungal pathogen Histoplasma capsulatum. Infect Immun 81(2):411–420.  https://doi.org/10.1128/iai.00833-12PubMedPubMedCentralCrossRefGoogle Scholar
  64. Isaac DT, Berkes CA, English BC, Murray DH, Lee YN, Coady A, Sil A (2015) Macrophage cell death and transcriptional response are actively triggered by the fungal virulence factor Cbp1 during H. capsulatum infection. Mol Microbiol 98(5):910–929.  https://doi.org/10.1111/mmi.13168PubMedPubMedCentralCrossRefGoogle Scholar
  65. Joffe LS, Nimrichter L, Rodrigues ML, Del Poeta M (2016) Potential roles of fungal extracellular vesicles during infection. mSphere 1(4).  https://doi.org/10.1128/msphere.00099-16
  66. Johnson CH, Klotz MG, York JL, Kruft V, McEwen JE (2002) Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148(Pt 4):1129–1142.  https://doi.org/10.1099/00221287-148-4-1129PubMedCrossRefGoogle Scholar
  67. 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(12):3383–3401PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kataria YP, Campbell PB, Burlingham BT (1981) Acute pulmonary histoplasmosis presenting as adult respiratory distress syndrome: effect of therapy on clinical and laboratory features. South Med J 74(5):534–537, 542PubMedCrossRefGoogle Scholar
  69. Kauffman CA (2007) Histoplasmosis: a clinical and laboratory update. Clin Microbiol Rev 20(1):115–132.  https://doi.org/10.1128/cmr.00027-06PubMedPubMedCentralCrossRefGoogle Scholar
  70. Knox KS, Hage CA (2010) Histoplasmosis. Proc Am Thorac Soc 7(3):169–172.  https://doi.org/10.1513/pats.200907-069ALPubMedCrossRefGoogle Scholar
  71. Kroetz DN, Deepe GS (2012) CCR5 deficiency mitigates the deleterious effects of tumor necrosis factor α antagonism in murine histoplasmosis. J Infect Dis 205(6):955–963.  https://doi.org/10.1093/infdis/jir869PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kwon-Chung KJ, Weeks RJ, Larsh HW (1974) Studies on Emmonsiella capsulata (Histoplasma capsulatum). II. Distribution of the two mating types in 13 endemic states of the United States. Am J Epidemiol 99(1):44–49PubMedCrossRefGoogle Scholar
  73. Lane TE, Wu-Hsieh BA, Howard DH (1991) Iron limitation and the gamma interferon-mediated antihistoplasma state of murine macrophages. Infect Immun 59(7):2274–2278PubMedPubMedCentralGoogle Scholar
  74. Lane TE, Wu-Hsieh BA, Howard DH (1994) Antihistoplasma effect of activated mouse splenic macrophages involves production of reactive nitrogen intermediates. Infect Immun 62(5):1940–1945PubMedPubMedCentralGoogle Scholar
  75. Larrabee WF, Ajello L, Kaufman L (1978) An epidemic of histoplasmosis on the Isthmus of Panama. Am J Trop Med Hyg 27(2 Pt 1):281–285PubMedCrossRefGoogle Scholar
  76. Lázár-Molnár E, Gácser A, Freeman GJ, Almo SC, Nathenson SG, Nosanchuk JD (2008) The PD-1/PD-L costimulatory pathway critically affects host resistance to the pathogenic fungus Histoplasma capsulatum. Proc Natl Acad Sci U S A 105(7):2658–2663.  https://doi.org/10.1073/pnas.0711918105PubMedPubMedCentralCrossRefGoogle Scholar
  77. Le Cabec V, Carréno S, Moisand A, Bordier C, Maridonneau-Parini I (2002) Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. J Immunol 169(4):2003–2009PubMedCrossRefGoogle Scholar
  78. Leach MD, Cowen LE (2013) Surviving the heat of the moment: a fungal pathogens perspective. PLoS Pathog 9(3):e1003163.  https://doi.org/10.1371/journal.ppat.1003163PubMedPubMedCentralCrossRefGoogle Scholar
  79. Lee JH, Slifman NR, Gershon SK, Edwards ET, Schwieterman WD, Siegel JN, Wise RP, Brown SL, Udall JN, Braun MM (2002) Life-threatening histoplasmosis complicating immunotherapy with tumor necrosis factor alpha antagonists infliximab and etanercept. Arthritis Rheum 46(10):2565–2570.  https://doi.org/10.1002/art.10583PubMedCrossRefGoogle Scholar
  80. Lenhart SW, National Institute for Occupational Safety and Health., National Center for Infectious Diseases (U.S.) (2004) Histoplasmosis: protecting workers at risk. DHHS publication, vol (NIOSH) 2005-109, Rev. edn. U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control and Prevention; National Center for Infectious Diseases, Cincinnati, OH; Atlanta, GAGoogle Scholar
  81. Limper AH, Knox KS, Sarosi GA, Ampel NM, Bennett JE, Catanzaro A, Davies SF, Dismukes WE, Hage CA, Marr KA, Mody CH, Perfect JR, Stevens DA, Group ATSFW (2011) An official American Thoracic Society statement: treatment of fungal infections in adult pulmonary and critical care patients. Am J Respir Crit Care Med 183(1):96-128.  https://doi.org/10.1164/rccm.2008-740stPubMedCrossRefGoogle Scholar
  82. Long KH, Gomez FJ, Morris RE, Newman SL (2003) Identification of heat shock protein 60 as the ligand on Histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages. J Immunol 170(1):487–494PubMedCrossRefGoogle Scholar
  83. Lopes LC, Guimarães AJ, de Cerqueira MD, Gómez BL, Nosanchuk JD (2010) A Histoplasma capsulatum-specific IgG1 isotype monoclonal antibody, H1C, to a 70-kilodalton cell surface protein is not protective in murine histoplasmosis. Clin Vaccine Immunol 17(7):1155–1158.  https://doi.org/10.1128/cvi.00033-10PubMedPubMedCentralCrossRefGoogle Scholar
  84. Loulergue P, Bastides F, Baudouin V, Chandenier J, Mariani-Kurkdjian P, Dupont B, Viard JP, Dromer F, Lortholary O (2007) Literature review and case histories of Histoplasma capsulatum var. duboisii infections in HIV-infected patients. Emerg Infect Dis 13(11):1647–1652.  https://doi.org/10.3201/eid1311.070665PubMedPubMedCentralCrossRefGoogle Scholar
  85. Manos NE, Ferebee SH, Kerschbaum WF (1956) Geographic variation in the prevalence of histoplasmin sensitivity. Dis Chest 29(6):649–668PubMedCrossRefGoogle Scholar
  86. Maresca B, Kobayashi GS (1989) Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol Rev 53(2):186–209PubMedPubMedCentralGoogle Scholar
  87. Marion CL, Rappleye CA, Engle JT, Goldman WE (2006) An alpha-(1,4)-amylase is essential for alpha-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol Microbiol 62(4):970–983.  https://doi.org/10.1111/j.1365-2958.2006.05436.xPubMedCrossRefGoogle Scholar
  88. Matos Baltazar L, Nakayasu ES, Sobreira TJ, Choi H, Casadevall A, Nimrichter L, Nosanchuk JD (2016) Antibody binding alters the characteristics and contents of extracellular vesicles released by Histoplasma capsulatum. mSphere 1(2).  https://doi.org/10.1128/msphere.00085-15
  89. McCormack FX, Gibbons R, Ward SR, Kuzmenko A, Wu H, Deepe GS (2003) Macrophage-independent fungicidal action of the pulmonary collectins. J Biol Chem 278(38):36250–36256.  https://doi.org/10.1074/jbc.M303086200PubMedCrossRefGoogle Scholar
  90. McLeod DS, Mortimer RH, Perry-Keene DA, Allworth A, Woods ML, Perry-Keene J, McBride WJ, Coulter C, Robson JM (2011) Histoplasmosis in Australia: report of 16 cases and literature review. Medicine (Baltimore) 90(1):61–68.  https://doi.org/10.1097/MD.0b013e318206e499CrossRefGoogle Scholar
  91. Medoff G, Kobayashi GS, Painter A, Travis S (1987) Morphogenesis and pathogenicity of Histoplasma capsulatum. Infect Immun 55(6):1355–1358PubMedPubMedCentralGoogle Scholar
  92. Missall TA, Lodge JK, McEwen JE (2004) Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukaryot Cell 3(4):835–846.  https://doi.org/10.1128/ec.3.4.835-846.2004PubMedPubMedCentralCrossRefGoogle Scholar
  93. Nacher M, Adenis A, Blanchet D, Vantilcke V, Demar M, Basurko C, Gaubert-Maréchal E, Dufour J, Aznar C, Carme B, Couppié P (2014) Risk factors for disseminated histoplasmosis in a cohort of HIV-infected patients in French Guiana. PLoS Negl Trop Dis 8(1):e2638.  https://doi.org/10.1371/journal.pntd.0002638PubMedPubMedCentralCrossRefGoogle Scholar
  94. Nadel JA, Murray JF, Mason RJ (2005) Murray and Nadel’s textbook of respiratory medicine, 4th edn. Elsevier Saunders, Philadelphia, PAGoogle Scholar
  95. Nakamura LT, Wu-Hsieh BA, Howard DH (1994) Recombinant murine gamma interferon stimulates macrophages of the RAW cell line to inhibit intracellular growth of Histoplasma capsulatum. Infect Immun 62(2):680–684PubMedPubMedCentralGoogle Scholar
  96. Nayak A, Dodagatta-Marri E, Tsolaki AG, Kishore U (2012) An insight into the diverse roles of surfactant proteins, SP-A and SP-D in innate and adaptive immunity. Front Immunol 3:131.  https://doi.org/10.3389/fimmu.2012.00131PubMedPubMedCentralCrossRefGoogle Scholar
  97. Nemecek JC, Wüthrich M, Klein BS (2006) Global control of dimorphism and virulence in fungi. Science 312(5773):583–588.  https://doi.org/10.1126/science.1124105PubMedCrossRefGoogle Scholar
  98. Newman SL, Bucher C, Rhodes J, Bullock WE (1990) Phagocytosis of Histoplasma capsulatum yeasts and microconidia by human cultured macrophages and alveolar macrophages. Cellular cytoskeleton requirement for attachment and ingestion. J Clin Investig 85(1):223–230.  https://doi.org/10.1172/jci114416PubMedCrossRefGoogle Scholar
  99. Newman SL, Gootee L, Gabay JE (1993) Human neutrophil-mediated fungistasis against Histoplasma capsulatum. Localization of fungistatic activity to the azurophil granules. J Clin Investig 92(2):624–631.  https://doi.org/10.1172/jci116630PubMedCrossRefGoogle Scholar
  100. Newman SL, Gootee L, Brunner G, Deepe GS (1994) Chloroquine induces human macrophage killing of Histoplasma capsulatum by limiting the availability of intracellular iron and is therapeutic in a murine model of histoplasmosis. J Clin Investig 93(4):1422–1429.  https://doi.org/10.1172/jci117119PubMedCrossRefGoogle Scholar
  101. Newman SL, Gootee L, Gabay JE, Selsted ME (2000) Identification of constituents of human neutrophil azurophil granules that mediate fungistasis against Histoplasma capsulatum. Infect Immun 68(10):5668–5672PubMedPubMedCentralCrossRefGoogle Scholar
  102. Newman SL, Bhugra B, Holly A, Morris RE (2005) Enhanced killing of Candida albicans by human macrophages adherent to type 1 collagen matrices via induction of phagolysosomal fusion. Infect Immun 73(2):770–777.  https://doi.org/10.1128/iai.73.2.770-777.2005PubMedPubMedCentralCrossRefGoogle Scholar
  103. Newman SL, Gootee L, Hilty J, Morris RE (2006) Human macrophages do not require phagosome acidification to mediate fungistatic/fungicidal activity against Histoplasma capsulatum. J Immunol 176(3):1806–1813PubMedCrossRefGoogle Scholar
  104. Newman SL, Lemen W, Smulian AG (2011) Dendritic cells restrict the transformation of Histoplasma capsulatum conidia into yeasts. Med Mycol 49(4):356–364.  https://doi.org/10.3109/13693786.2010.531295PubMedCrossRefGoogle Scholar
  105. 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(12):4880–4885.  https://doi.org/10.1073/pnas.0710448105PubMedPubMedCentralCrossRefGoogle Scholar
  106. Nittler MP, Hocking-Murray D, Foo CK, Sil A (2005) Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Mol Biol Cell 16(10):4792–4813.  https://doi.org/10.1091/mbc.E05-05-0434PubMedPubMedCentralCrossRefGoogle Scholar
  107. Nosanchuk JD, Gacser A (2008) Histoplasma capsulatum at the host-pathogen interface. Microbes Infect 10(9):973–977.  https://doi.org/10.1016/j.micinf.2008.07.011PubMedPubMedCentralCrossRefGoogle Scholar
  108. Nosanchuk JD, Steenbergen JN, Shi L, Deepe GS, Casadevall A (2003) Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J Clin Investig 112(8):1164–1175.  https://doi.org/10.1172/jci19361PubMedCrossRefGoogle Scholar
  109. Nosanchuk JD, Zancopé-Oliveira RM, Hamilton AJ, Guimarães AJ (2012) Antibody therapy for histoplasmosis. Front Microbiol 3:21.  https://doi.org/10.3389/fmicb.2012.00021PubMedPubMedCentralCrossRefGoogle Scholar
  110. Peebles RS, Carpenter CT, Dupont WD, Loyd JE (2000) Mediastinal fibrosis is associated with human leukocyte antigen-A2. Chest 117(2):482–485PubMedCrossRefGoogle Scholar
  111. Pitangui NeS, Sardi JeC, Voltan AR, Dos Santos CT, da Silva JeF, da Silva RA, Souza FO, Soares CP, Rodríguez-Arellanes G, Taylor ML, Mendes-Giannini MJ, Fusco-Almeida AM (2015) An intracellular arrangement of Histoplasma capsulatum yeast-aggregates generates nuclear damage to the cultured murine alveolar macrophages. Front Microbiol 6:1526.  https://doi.org/10.3389/fmicb.2015.01526
  112. 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(1):153–165.  https://doi.org/10.1111/j.1365-2958.2004.04131.xPubMedCrossRefGoogle Scholar
  113. Retallack DM, Woods JP (1999) Molecular epidemiology, pathogenesis, and genetics of the dimorphic fungus Histoplasma capsulatum. Microbes Infect 1(10):817–825PubMedCrossRefGoogle Scholar
  114. Rizzi MD, Batra PS, Prayson R, Citardi MJ (2006) Nasal histoplasmosis. Otolaryngol Head Neck Surg 135(5):803–804.  https://doi.org/10.1016/j.otohns.2005.02.017PubMedCrossRefGoogle Scholar
  115. Rodrigues ML, Nakayasu ES, Oliveira DL, Nimrichter L, Nosanchuk JD, Almeida IC, Casadevall A (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7(1):58–67.  https://doi.org/10.1128/ec.00370-07PubMedCrossRefGoogle Scholar
  116. Rosenthal J, Brandt KD, Wheat LJ, Slama TG (1983) Rheumatologic manifestations of histoplasmosis in the recent Indianapolis epidemic. Arthritis Rheum 26(9):1065–1070PubMedCrossRefGoogle Scholar
  117. Sacco M, Medoff G, Lambowitz AM, Kumar BV, Kobayashi GS, Painter A (1983) Sulfhydryl induced respiratory “shunt” pathways and their role in morphogenesis in the fungus Histoplasma capsulatum. J Biol Chem 258(13):8223–8230PubMedGoogle Scholar
  118. Sebghati TS, Engle JT, Goldman WE (2000) Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290(5495):1368–1372PubMedCrossRefGoogle Scholar
  119. Sepúlveda VE, Márquez R, Turissini DA, Goldman WE, Matute DR (2017) Genome sequences reveal cryptic speciation in the human pathogen. MBio 8(6).  https://doi.org/10.1128/mbio.01339-17
  120. Sertl K, Takemura T, Tschachler E, Ferrans VJ, Kaliner MA, Shevach EM (1986) Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J Exp Med 163(2):436–451PubMedCrossRefGoogle Scholar
  121. Shi L, Albuquerque PC, Lazar-Molnar E, Wang X, Santambrogio L, Gácser A, Nosanchuk JD (2008) A monoclonal antibody to Histoplasma capsulatum alters the intracellular fate of the fungus in murine macrophages. Eukaryot Cell 7(7):1109–1117.  https://doi.org/10.1128/ec.00036-08PubMedPubMedCentralCrossRefGoogle Scholar
  122. Strasser JE, Newman SL, Ciraolo GM, Morris RE, Howell ML, Dean GE (1999) Regulation of the macrophage vacuolar ATPase and phagosome-lysosome fusion by Histoplasma capsulatum. J Immunol 162(10):6148–6154PubMedGoogle Scholar
  123. Svirbely JR, Ayers LW, Buesching WJ (1985) Filamentous Histoplasma capsulatum endocarditis involving mitral and aortic valve porcine bioprostheses. Arch Pathol Lab Med 109(3):273–276PubMedGoogle Scholar
  124. Symptoms of Histoplasmosis. Centers for Disease Control and Prevention. https://www.cdc.gov/fungal/diseases/histoplasmosis/symptoms/. Accessed 6 May 2018
  125. Taylor ML, Espinosa-Schoelly ME, Iturbe R, Rico B, Casasola J, Goodsaid F (1989) Evaluation of phagolysosome fusion in acridine orange stained macrophages infected with Histoplasma capsulatum. Clin Exp Immunol 75(3):466–470PubMedPubMedCentralGoogle Scholar
  126. Tewari RP, Von Behren LA (2000) Immune responses in histoplasmosis, a prototype of respiratory mycoses. Indian J Chest Dis Allied Sci 42(4):265–269PubMedGoogle Scholar
  127. Thind SK, Taborda CP, Nosanchuk JD (2015) Dendritic cell interactions with Histoplasma and Paracoccidioides. Virulence 6(5):424–432.  https://doi.org/10.4161/21505594.2014.965586PubMedPubMedCentralCrossRefGoogle Scholar
  128. Timmerman MM, Woods JP (1999) Ferric reduction is a potential iron acquisition mechanism for Histoplasma capsulatum. Infect Immun 67(12):6403–6408PubMedPubMedCentralGoogle Scholar
  129. Timmerman MM, Woods JP (2001) Potential role for extracellular glutathione-dependent ferric reductase in utilization of environmental and host ferric compounds by Histoplasma capsulatum. Infect Immun 69(12):7671–7678.  https://doi.org/10.1128/iai.69.12.7671-7678.2001PubMedPubMedCentralCrossRefGoogle Scholar
  130. Tristão FS, Leonello PC, Nagashima LA, Sano A, Ono MA, Itano EN (2012) Carbohydrate-rich high-molecular-mass antigens are strongly recognized during experimental Histoplasma capsulatum infection. Rev Soc Bras Med Trop 45(2):232–237PubMedPubMedCentralCrossRefGoogle Scholar
  131. van de Wetering JK, van Remoortere A, Vaandrager AB, Batenburg JJ, van Golde LM, Hokke CH, van Hellemond JJ (2004) Surfactant protein D binding to terminal alpha1-3-linked fucose residues and to Schistosoma mansoni. Am J Respir Cell Mol Biol 31(5):565–572.  https://doi.org/10.1165/rcmb.2004-0105OCPubMedCrossRefGoogle Scholar
  132. Vargas G, Rocha JD, Oliveira DL, Albuquerque PC, Frases S, Santos SS, Nosanchuk JD, Gomes AM, Medeiros LC, Miranda K, Sobreira TJ, Nakayasu ES, Arigi EA, Casadevall A, Guimaraes AJ, Rodrigues ML, Freire-de-Lima CG, Almeida IC, Nimrichter L (2015) Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell Microbiol 17(3):389–407.  https://doi.org/10.1111/cmi.12374PubMedCrossRefGoogle Scholar
  133. 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(38):14573–14578.  https://doi.org/10.1073/pnas.0806221105PubMedPubMedCentralCrossRefGoogle Scholar
  134. Wheat LJ, Stein L, Corya BC, Wass JL, Norton JA, Grider K, Slama TG, French ML, Kohler RB (1983) Pericarditis as a manifestation of histoplasmosis during two large urban outbreaks. Medicine (Baltimore) 62(2):110–119CrossRefGoogle Scholar
  135. Wheat LJ, Wass J, Norton J, Kohler RB, French ML (1984) Cavitary histoplasmosis occurring during two large urban outbreaks. Analysis of clinical, epidemiologic, roentgenographic, and laboratory features. Medicine (Baltimore) 63(4):201–209CrossRefGoogle Scholar
  136. Wheat LJ, Freifeld AG, Kleiman MB, Baddley JW, McKinsey DS, Loyd JE, Kauffman CA, America IDSo (2007) Clinical practice guidelines for the management of patients with histoplasmosis: 2007 update by the Infectious Diseases Society of America. Clin Infect Dis 45(7):807–825.  https://doi.org/10.1086/521259PubMedCrossRefGoogle Scholar
  137. Wheat LJ, Azar MM, Bahr NC, Spec A, Relich RF, Hage C (2016) Histoplasmosis. Infect Dis Clin North Am 30(1):207–227.  https://doi.org/10.1016/j.idc.2015.10.009PubMedPubMedCentralCrossRefGoogle Scholar
  138. Winters MS, Spellman DS, Chan Q, Gomez FJ, Hernandez M, Catron B, Smulian AG, Neubert TA, Deepe GS (2008) Histoplasma capsulatum proteome response to decreased iron availability. Proteome Sci 6:36.  https://doi.org/10.1186/1477-5956-6-36PubMedPubMedCentralCrossRefGoogle Scholar
  139. Woods JP (2016) Revisiting old friends: Developments in understanding Histoplasma capsulatum pathogenesis. J Microbiol 54(3):265–276.  https://doi.org/10.1007/s12275-016-6044-5PubMedCrossRefGoogle Scholar
  140. Woods JP, Retallack DM, Heinecke EL, Goldman WE (1998) Rare homologous gene targeting in Histoplasma capsulatum: disruption of the URA5Hc gene by allelic replacement. J Bacteriol 180(19):5135–5143PubMedPubMedCentralGoogle Scholar
  141. Youseff BH, Holbrook ED, Smolnycki KA, Rappleye CA (2012) Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8(5):e1002713.  https://doi.org/10.1371/journal.ppat.1002713PubMedPubMedCentralCrossRefGoogle Scholar
  142. Zamith-Miranda D, Nimrichter L, Rodrigues ML, Nosanchuk JD (2018) Fungal extracellular vesicles: modulating host-pathogen interactions by both the fungus and the host. Microbes Infect.  https://doi.org/10.1016/j.micinf.2018.01.011PubMedCrossRefPubMedCentralGoogle Scholar
  143. Zerbe CS, Holland SM (2005) Disseminated histoplasmosis in persons with interferon-gamma receptor 1 deficiency. Clin Infect Dis 41(4):e38–e41.  https://doi.org/10.1086/432120PubMedCrossRefGoogle Scholar
  144. Zhou P, Freidag BL, Caldwell CC, Seder RA (2001) Perforin is required for primary immunity to Histoplasma capsulatum. J Immunol 166(3):1968–1974PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jamie Mittal
    • 1
  • Maria G. Ponce
    • 1
  • Inessa Gendlina
    • 2
  • Joshua D. Nosanchuk
    • 2
    • 3
    Email author
  1. 1.Department of Medicine (Infectious Diseases)Montefiore Medical CenterBronxUSA
  2. 2.Department of Medicine (Infectious Diseases)Albert Einstein College of MedicineBronxUSA
  3. 3.Department of Microbiology and ImmunologyAlbert Einstein College of MedicineBronxUSA

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