An Acute Pathophysiology of Environmental Strains of Cryptococcus neoformans Isolated from a Park in Busan

  • Choi, Seok-Cheol (Department of Clinical Laboratory Science, College of Health Sciences, Catholic University of Pusan)
  • Received : 2010.07.09
  • Accepted : 2010.09.17
  • Published : 2010.09.30

Abstract

The present study was carried out to elucidate whether an environmental strain of Cryptococcus neoformans (environmental C. neoformans) isolated from an environmental source in a park of Busan has an acute pathophysiological effect in rats. On the second day after peritoneal inoculation of environmental C. neoformans, adverse effects occurred from the viewpoint of hematology and biochemistry. Eosinophil damages and crystal formations were found in the blood. Disturbances in cytokines production were observed in the cerebral and pulmonary tissues. Fungal budding existed in the brain, lung, liver and kidney. Tissue injury findings such as inflammation, leukocyte infiltration, bleeding, or degeneration were found in the brain, lung, liver and kidney. The present data suggest that the environmental C. neoformans can cause systematically harmful effects even for short periods of infection (two days of cryptococcal infection) and the adverse effects are summarized as immune derangements and biochemical and/or histological dysfunction and injury on major organ such as the brain, lung, liver and kidney in the immunocompetent hosts. Further studies should be focused on comparing the differences between environmental and clinical strains of C. neoformans.

Keywords

References

  1. Ahn IS, Kim HG, Ryu JS, Kim L, Kwak SM, Lee HL, Yoon YH, Cho JH. A case of pulmonary cryptococcosis with non-small cell lung cancer in idiopathic CD4+ T-lymphocytopenia. Yonsei Med J. 2005. 46: 173-176. https://doi.org/10.3349/ymj.2005.46.1.173
  2. Archer GT. Mechanism of eosinophilia and mast cell disruption in rats infected with the parasite Amplicaecum robertsi. Paihology 1969. 1: 133-140.
  3. Arora S, Hermandez Y, Erb-Downward JR, McDonald RA, Toews GB, Huffinagle GB. Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. J Immunol. 2005. 174: 6346-6356.
  4. Brandt ME, Hutwagener LC, Klug LA, Baughman WS, Rimland D, Graviss EA, Hamill RJ, Thomas C, Pappas PG, Reingold AL, Pinner RW. Molecular subtype distribution of Cryptococcus neoformans in four areas of the United States. Cryptococcal Disease Active Surveillance Group. J Clin Microbiol. 1996. 34: 912-917.
  5. Castro AG, Esaguy N, Macedo PM, Aguas AP, Silva MT. Live but not heat-killed mycobacteria cause rapid chemotaxis of large numbers of eosinophils in vivo and are ingested by the attracted granulocytes. Infect Immun. 1991. 59: 3009-3014.
  6. Chevion S, Moran DS, Heled Y, Shani Y, Regev G, Abbou B, Berenshtein E, Stadtman ER, Epstein Y. Plasma antioxidant status and cell injury after severe physical exercise. Proc Natl Acad Sci USA. 2003. 100: 5119-5123. https://doi.org/10.1073/pnas.0831097100
  7. Chiapello LS, Baronetti JL, Aoki MP, Gea S, Rubinstein H, Masih T. Immunosuppression, interleukin-10 synthesis and apoptosis are induced in rats inoculated with Cryptococcus neoformans glucuronoxylomannan. Immunology 2004. 113: 392-400. https://doi.org/10.1111/j.1365-2567.2004.01970.x
  8. Cline MJ, Hanifin J, Lehrer RJ. Phagocytosis by human eosinophils. Blood 1968.32: 922-934.
  9. Davis WB, Fells GA, Sun XH, Gadek JE, Venet A, Crystal RG. Eosinophil-Mediated injury to lung parenchymal cells and interstitial matrix. A possible role for eosinophils in chronic inflammatory disorders of the lower respiratory tract. J Clin Invest. 1984.74: 269-278. https://doi.org/10.1172/JCI111411
  10. El-Hashimi W. Charcot-Leyden clystals. Formation from primate and lack of formation from nonprimate eosinophils. Am J Pathol. 1971. 65: 311-324.
  11. Ernst JF, Tielker D. Responses to hypoxia in fungal pathogens. Cell Microbiol. 2009. 11: 183-190. https://doi.org/10.1111/j.1462-5822.2008.01259.x
  12. Fabian I, Kletter Y; Bleiberg I, Gadish M, Naparsteck E, Slavin S. Effect of exogenous recombinant human granulocyte and granulocyte-macrophage colony-stimulating factor on neutrophil function following allogeneic bone marrow transplantation. Exp Hematol 1991.19: 868-873.
  13. Huffnagle GB, Toews GB, Burdick MD, Boyd MB, McAllister KS, McDonald RA, Kunkel SL, Strieter RM. Afferent phase production of TNF-alpha is required for the development of protective T cell immunity to Cryptococcus neoformans. J Immunol. 1996.157: 4529-4536.
  14. Huffnagle GB, Boyd MB, Street NE, Lipscomb MF. IL-5 is required for eosinophil recruitment, crystal deposition, and mononuclear cell recruitment during a pulmonary Cryptococcus neoformans infection in genetically susceptible mice (C57BL/6). J Immunol. 1998. 160: 2393-2400.
  15. Huffnagle GB, Strieter RM, Standiford TJ, McDonald RA, Burdick MD, Kunkel SL, Toews GB. The role of monocyte chemotactic protein-1 (MCP-1) in the recruitment of monocytes and CD4+ T cells during a pulmonary Cryptococcus neoformans infection. J Immunol. 1995. 155: 4790-4797.
  16. Huffnagle GB, Stricter RM, Standiford TJ, McDonald RA, Burdick MD, Kunkel SL, Toews GB. The role of monocyte chemotactic protein-1 (MCP-1) in the recruitment of monocytes and CD4+ T cells during a pulmonary Cryptococcus neoformans infection. J Immunol. 1995. 155: 4790-4797.
  17. Hwang SM, Oh KS, Lee KW. Serotype and enzymatic profile of Cryptococcus neoformans isolates from clinical and environmental sources in Korea. Kor J Microbiol. 2006. 42: 257-264.
  18. Levitz SM, Farrell TP. Growth inhibition of Cryptococcus neoformans by cultured human monocytes: role of the capsule, opsonins, the culture surface, and cytokines. Infect Immun. 1990. 58: 1201-1209.
  19. Liu PY, Yang Y, Shi ZY. Cryptococcal liver abscess: a case report of successful treatment with amphotericin-B and literature review. Jpn J Infect Dis. 2009. 62: 59-60.
  20. Mawhorter SD, Kazura JW, Boom WH. Human eosinophils as antigen-presenting cells: relative efficiency for superantigenand antigen-induced CD4+ T-cell proliferation. Immunology 1994. 81: 584-591.
  21. Mitchell TG, Perfect JR. Cryptococcosis in the era of AIDS-100 years atter the discovery of Cryptococcus neoformans. Clin Microbiol Rev. 1995. 8: 515-548.
  22. Murphy JW. Cryptococcal immunity and immunostimulation. Adv Exp Med Biol. 1992. 319: 225-230. https://doi.org/10.1007/978-1-4615-3434-1_23
  23. Nara S, Sano T, Ojima H, Onaya H, Ikeda M, Morizane C, Esaki M, Sakamoto Y, Shimada K, Kosuge T. Liver cryptococcosis manifesting as obstructive jaundice in a young immuno-competent man: report of a case. Surg Today 2008. 38: 271-274 https://doi.org/10.1007/s00595-007-3605-6
  24. Oh KS, Hwang SM. Isolation and characterization of Cyptococcus neoformans from enivronmental sources in Busan. Mycobiology 2005. 33: 188-193. https://doi.org/10.4489/MYCO.2005.33.4.188
  25. Olszweski MA, Huffinagle GB, Traynor TR, McDonald RA, Cook DN, Toews GB. Regulatory effects of macrophage inflammatory protein lalpha/CCL3 on the development of immunity to Cryptococcus neoformans depend on expression of early inflammatory cytokines. Infect Immun. 2001. 69: 6256-6263. https://doi.org/10.1128/IAI.69.10.6256-6263.2001
  26. Piratvisuth T, Siripaitoon P, Sriplug H, Ovartlamporn B. Findings and benefit of liver biopsies in 46 patients infected with human immunodeficiency virus. J Gastroenterol Hepatol. 1999. 14: 146-149.
  27. Rozenbaum R, Goncalves AJ. Clinical epidemiological study of 171 cases of cryptococcosis. Clin Infect Dis. 1994. 18: 369-380. https://doi.org/10.1093/clinids/18.3.369
  28. Shaw RJ, Walsh GM, Cromwell O, Moqbel R, Spry CJ, Kay AB. Activated human eosinophils generate SRS-A leukotrienes following IgG-dependent stimulation. Nature 1985. 316: 150-152. https://doi.org/10.1038/316150a0
  29. Spessotto P, Dri P, Bulla R, Zabucchi G, Patriarca P. Human eosinophil peroxidase enhances tumor necrosis factor and hydrogen peroxide release by human monocyte-derived macrophages. Eur J Immunol. 1995. 25: 1366-1373. https://doi.org/10.1002/eji.1830250535
  30. Strazzullo P, Barba G, Cappuecio FP, Siani A, Trevisan M, Farinaro E, Pagano E, Barbato A, Iacone R, Galletti F. Altered renal sodium handling in men with abdominal adiposity: a link to hypertension. Hypertens. 2001. 19: 2157-2164. https://doi.org/10.1097/00004872-200112000-00007
  31. Todd R, Donoff BR, Chiang T, Chou MY, Elovic A, Gallagher GT, Wong DT. The eosinophil as a cellular source of transforming growth factor alpha in healing cutaneous wounds. Am J Pathol. 1991. 138: 1307-1313.
  32. Tomassini M, Tsicopoulos A, Tai PC, Gruart V, Tonnel AB, Prin L, Capron A, Capron M. Release of granule proteins by eosinophils from allergic and nonallergic patients with eosinophilia on immunoglobulin-dependent activation. J Allergy Clin Immunol. 1991. 88: 365-375. https://doi.org/10.1016/0091-6749(91)90099-A
  33. Waring WS, Webb DJ, Maxwell SR Sytemic uric acid administration increases serum antioxidant capacity in healthy volunteers. J Cardiovasc Pharmacol. 2001. 38: 365-371. https://doi.org/10.1097/00005344-200109000-00005
  34. Weller PF, Goetzl EJ, Austen KF. Identification of human eosinophil lysophospholipase as the constituent of Charcot- Leyden crystals. Proc Natl Acad Sci USA. 1980. 77: 7440-7743. https://doi.org/10.1073/pnas.77.12.7440
  35. Wormley FL Jr, Perfect JR, Steele C, Cox GM. Protection against cryptococcosis by using a murine gamma interferon-producing Cryptococcus neoformans strain. Infect Immun. 2007. 75: 1453-1462. https://doi.org/10.1128/IAI.00274-06
  36. Yamamoto S, Khido K, Sato A. Isolation of C. neoformans from pulmonary granuloma of a cat and from pigeon droppings. Jpn J Vet Sci. 1957. 19: 179-189. https://doi.org/10.1292/jvms1939.19.179
  37. Yauch LE, Mansour MK, Levitz SM. Receptor-mediated clearance of Cryptococcus neoformans capsular polysaccharide in vivo. Infect Immun. 2005. 73: 8429-8432. https://doi.org/10.1128/IAI.73.12.8429-8432.2005
  38. Zaragoza O, Rodrigues ML, de Jesus M, Frases S, Dadachova E, Casadevall A. The capsule of the fungal pathogen Cryptococcus neoformans. Adv Appl Microbiol. 2009. 68: 133-216. https://doi.org/10.1016/S0065-2164(09)01204-0