Skip to main content

Advertisement

Log in

Immunohistochemical Cross-Reactivity Between Arthrographis kalrae and Highly Pathogenic Coccidioides posadasii, Histoplasma capsulatum, and Paracoccidioides Fungal Species

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Recently, we have reported serological cross-reactivity between paracoccidioidomycosis ceti and paracoccidioidomycosis, histoplasmosis, and coccidioidomycosis. However, data on the interaction of Arthrographis kalrae with the above pathogenic fungal infections are lacking. A. kalrae is a widely occurring ascomycetous fungus; causes superficial and deep mycoses; shows thermally dependent dimorphism; and has a genomic profile related to the above-mentioned fungal species. Our study aims to investigate cross-reactivity using eight murine sera, obtained from experimental infection with two A. kalrae isolates. The murine sera were incubated with fungal cells of A. kalrae, Coccidioides posadasii, Histoplasma capsulatum, Paracoccidioides sp., and P. brasiliensis. Thirty murine sera, obtained from experimental infection with six isolates of H. capsulatum, sera from three cases of dolphin paracoccidioidomycosis ceti, two human sera from patients with paracoccidioidomycosis, and a serum sample from a healthy person with a history of coccidioidomycosis, were also incubated with A. kalrae fungal cells and the respective fungal cells that caused the infection as positive controls. Sera derived from the mice infected with A. kalrae reacted strongly when incubated with the Paracoccidioides sp., P. brasiliensis, and C. posadasii, but no positive reaction was observed against the fungal cells of H. capsulatum. The murine sera infected with three out of six isolates of H. capsulatum, and all cetacean and human serum samples reacted positively with the fungal cells of A. kalrae. The present study demonstrated serological cross-reactions among A. kalrae infection, coccidioidomycosis, paracoccidioidomycosis, paracoccidioidomycosis ceti, and histoplasmosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Vilela R. Mendoza: 9. Paracoccidioidomycosis ceti (Lacaziosis/Lobomycosis) in dolphins. In: Seyedmousavi S, de Hoog GS, Guillot J, Verweij PE, editors. Emerging and epizootic fungal infections in animals. Cham: Springer; 2018. p. 177–92.

    Chapter  Google Scholar 

  2. Nagashima LA, Akagi CY, Sano A, Álvares e Silva PL, Murata Y, Itano EN. Arthrographis kalrae soluble antigens present hemolytic and cytotoxic activities. Comp Immunol Microbiol Infect Dis. 2014;37:305–11.

    Article  PubMed  Google Scholar 

  3. Nagashima LA, Sano A, Araújoa EJA, Álvares e Silva PL, Assolini JP, Itano EN. Immunomodulation over the course of experimental Arthrographis kalrae infection in mice. Comp Immunol Microbiol Infect Dis. 2016;48:79–86.

    Article  PubMed  Google Scholar 

  4. Giraldo A, Gené A, Sutton DA, Madrid H, Cano J, Crous PW, Guarro J. Phylogenetic circumscription of Arthrographis (Eremomycetaceae, Dothideomycetes). Persoonia. 2014;32:102–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Pounder JI, Hansen D, Woods GL. Identification of Histoplasma capsulatum, Blastomyces dermatitidis, and Coccidioides species by repetitive-sequence-based PCR. J Clin Microbiol. 2006;44:2977–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Marin-Felix Y, Stchigel AM, Cano-Lira JF, Sanchis M, Mayayo E, Guarro J. Emmonsiellopsis, a new genus related to the thermally dimorphic fungi of the family Ajellomycetaceae. Mycoses. 2015;58:451–60.

    Article  CAS  PubMed  Google Scholar 

  7. Ueda K, Sano A, Yamate J, Itano EN, Kuwamura M, Izawa T, Tanaka M, Hasegawa Y, Chibana H, Izumisawa Y, Miyahara H, Uchida S. Two cases of lacaziosis in bottlenose dolphins (Tursiops truncatus) in Japan. Case Rep Vet Med. 2013;318548.

  8. Sacristán C, Réssio RA, Castilho P, Fernandes N, Costa-Silva S, Esperón F, Daura-Jorge FG, Groch KR, Kolesnikovas CK, Marigo J, Ott PH, Oliveira LR, Sánchez-Sarmiento AM, Simões-Lopes PC, Catão-Dias JL. Lacaziosis-like disease in Tursiops truncatus from Brazil: a histopathological and immunohistochemical approach. Dis Aquat Org. 2016;117:229–35.

    Article  CAS  PubMed  Google Scholar 

  9. Wheat J, Wheat H, Connolly P, Kleiman M, Supparatpinyo K, Nelson K, Bradsher R, Restrepo A. Cross-reactivity in Histoplasma capsulatum variety capsulatum antigen assays of urine samples from patients with endemic mycoses. Clin Infect Dis. 1997;24:1169–71.

    Article  CAS  PubMed  Google Scholar 

  10. Ferreira JB, Navarro IT, Freire RL, Oliveira GG, Omori AM, Belitardo DR, Itano EN, Camargo ZP, Ono MA. Evaluation of Paracoccidioides brasiliensis infection in dairy goats. Mycopathologia. 2013;176:95–9.

    Article  CAS  PubMed  Google Scholar 

  11. Shumoto G, Ueda K, Yamaguchi S, Kaneshima T, Konno T, Terashima Y, Yamamoto A, Nagashima LA, Itano EN, Sano A. Immunohistochemical cross-reactivity between Paracoccidioides sp. from dolphins and Histoplasma capsulatum. Mycopathologia. 2018;183:793–803.

    Article  CAS  PubMed  Google Scholar 

  12. Minakawa T, Ueda K, Tanaka M, Tanaka N, Kuwamura M, Izawa T, Konno T, Yamate J, Itano EN, Sano A, Wada S. Detection of multiple budding yeast cells and a partial sequence of 43-kDa glycoprotein coding gene of Paracoccidioides brasiliensis from a case of lacaziosis in a female Pacific white-sided dolphin (Lagenorhynchus obliquidens). Mycopathologia. 2016;181:523–9.

    Article  PubMed  Google Scholar 

  13. Sharmin S, Ohori A, Sano A, Kamei K, Yamaguchi M, Takeo K, Uno J, Nishimura K, Miyaji M. Histoplasma capsulatum variety duboisii isolated in Japan from an HIV-infected Ugandan patient. Nihon Ishinkin Gakkai Zasshi. 2003;44:299–306.

    Article  PubMed  Google Scholar 

  14. Turissini DA, Gomez OM, Teixeira MM, McEwen JG, Matute DR. Species boundaries in the human pathogen Paracoccidioides. Fungal Genet Biol. 2017;106:9–25.

    Article  PubMed  Google Scholar 

  15. Amper NA, Einstein HE, Galgiani JN, Pappagianis D, Wieden M. Chapter 2: coccidioidomycosis. In: Mandell GL, editor. Atlas of infectious diseases. Philadelphia: Current Medicine, Inc.; 2000. p. 24–41.

    Google Scholar 

  16. Sano A, Miyaji M, Kamei K, Mikami Y, Nishimura K. Reexamination of Coccidioides spp. reserved in the Research Center for Pathogenic Fungi and Microbial Toxicoses, Chiba University, based on a multiple gene analysis. Nippon Ishinkin Gakkai Zasshi. 2006;47:113–7 (Present name: Med Mycol J).

    Article  CAS  Google Scholar 

  17. Miyaji N, Nishimura K, Ajello L. Scanning electron microscope studies on the parasitic cycles of Coccidioides immitis. Mycopathologia. 1985;89:51–7.

    Article  CAS  PubMed  Google Scholar 

  18. Tristão FS, Leonello PC, Nagashima LA, Sano A, Ono MA, Itano EM. Carbohydrate-rich high-molecular-mass antigens are strongly recognized during experimental Histoplasma capsulatum infection. Rev Soc Bras Med Trop. 2012;45:232–7.

    Article  PubMed  Google Scholar 

  19. de Teixeira MM, Patané JS, Taylor ML, Gómez BL, Theodoro RC, de Hoog S, Engelthaler DM, Zancopé-Oliveira RM, Felipe MS, Barker BM. Worldwide phylogenetic distributions and population dynamics of the genus Histoplasma. PLoS Negl Trop Dis. 2016;10:e0004732.

    Article  PubMed Central  Google Scholar 

  20. Canteros CE, Madariaga MJ, Lee W, Rivas MC, Davel G, Iachini R. Endemic fungal pathogens in a rural setting of Argentina: seroepidemiological study in dogs. Rev Iberoam Micol. 2010;31(27):14–9.

    Article  Google Scholar 

  21. Jensen ED, Lipscomb T, Van Bonn B, Miller G, Fradkin JM, Ridgway SH. Disseminated histoplasmosis in an Atlantic bottlenose dolphin (Tursiops truncatus). J Zoo Wildl Med. 1998;29:456–60.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Drs. Katsuhiko Kamei (Medical Mycology Research Center, Chiba University, Chiba, Japan) and Yoshiteru Murata (Murata Animal Hospital, Mobara, Chiba, Japan) for donating the murine serum and tissue samples for our experiments, and to Drs. Kazuko Nishimura (Emeritus Professor, Medical Mycology Research Center, Chiba University, Chiba, Japan), Makoto Miyaji (Late Emeritus Professor, Medical Mycology Research Center, Chiba University, Chiba, Japan), and Kunie Iabuki Coelho Rabello (Emeritus Professor, Department of Pathology, Faculty of Medicine, State University of São Paulo, Botucatu, Brazil) for the paraffin-embedded tissue samples. We also sincerely thank Drs. Takashi Kaneshima (Ryukyu Animal Medical Center, Tomigusuku, Okinawa, Japan), Toshihiro Konno, Yoshie Terashima, and Atsushi Yamamoto (the United Graduate School of Agriculture Sciences, Kagoshima, University, Kagoshima, Japan) for their relentless encouragement and advice. We also thank Ms. Nanako Tomino (Under Graduate Student, Department of Animal Sciences, Faculty of Agriculture, University of the Ryukyus) for her helps on immune staining. This study was partly supported by JICA (Grant Number = J17-50165) awarded to Drs. Ayako Sano and Luciene Airy Nagashima; a special grant was given for women researchers from the United Graduate School of Agriculture Sciences, Kagoshima, University and a 2018 University of the Ryukyus Research Project Grant Program from the University of the Ryukyus for women researchers, Nishihara, Okinawa, Japan (No. 7, Project 18SP05107), to Dr. Ayako Sano. We would like to thank Editage (www.editage.jp) for English language editing and formatting of the article to comply with Mycopathologia journal standards.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ayako Sano.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and Animals Rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The usage of human sera was permitted by the ethic committee of University of the Ryukyus, No. 383 approved in November 24, 2017. Animal sera were derived from clinical samples, or previously permitted experimental infections, with permission No. 20020018 and No. 20050318 from Chiba University; therefore, our work did not qualify as an animal experiment according to the animal welfare committee of the University of the Ryukyus.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling editor: Mario Augusto Ono.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shumoto, G., Nagashima, L.A., Itano, E.N. et al. Immunohistochemical Cross-Reactivity Between Arthrographis kalrae and Highly Pathogenic Coccidioides posadasii, Histoplasma capsulatum, and Paracoccidioides Fungal Species. Mycopathologia 184, 393–402 (2019). https://doi.org/10.1007/s11046-019-00348-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-019-00348-5

Keywords

Navigation