Immunohistochemical Cross-Reactivity Between Arthrographis kalrae and Highly Pathogenic Coccidioides posadasii, Histoplasma capsulatum, and Paracoccidioides Fungal Species
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.
KeywordsArthrographis kalrae Coccidioidomycosis Histoplasmosis Paracoccidioidomycosis Paracoccidioidomycosis ceti
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.
Compliance with Ethical Standards
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.
- 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.Google Scholar
- 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.CrossRefGoogle 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.CrossRefGoogle 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).CrossRefGoogle 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.Google Scholar