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Immunological Cross-Reactivity of Proteins Extracted from The Journal of Fungi Article Immunological Cross-Reactivity of Proteins Extracted from the Oomycete Pythium insidiosum and the Fungus Basidiobolus ranarum Compromises the Detection Specificity of Immunodiagnostic Assays for Pythiosis Tiwa Rotchanapreeda 1, Pattarana Sae-Chew 2 , Tassanee Lohnoo 2, Wanta Yingyong 2, Thidarat Rujirawat 2, Yothin Kumsang 2, Penpan Payattikul 2, Chalisa Jaturapaktrarak 2, Akarin Intaramat 3, Watcharapol Pathomsakulwong 4, Chompoonek Yurayart 5 and Theerapong Krajaejun 1,* 1 Department of Pathology, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok 10400, Thailand; [email protected] 2 Research Center, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok 10400, Thailand; [email protected] (P.S.-C.); [email protected] (T.L.); [email protected] (W.Y.); [email protected] (T.R.); [email protected] (Y.K.); [email protected] (P.P.); [email protected] (C.J.) 3 Translational Research Unit and Laboratory of Immunology, Chulabhorn Research Institute, Citation: Rotchanapreeda, T.; Bangkok 10210, Thailand; [email protected] 4 Equine Clinic, Kasetsart University Veterinary Teaching Hospital, Nakhon Pathom 73140, Thailand; Sae-Chew, P.; Lohnoo, T.; Yingyong, [email protected] W.; Rujirawat, T.; Kumsang, Y.; 5 Department of Microbiology and Immunology, Faculty of Veterinary Medicine, Kasetsart University, Payattikul, P.; Jaturapaktrarak, C.; Bangkok 10900, Thailand; [email protected] Intaramat, A.; Pathomsakulwong, W.; * Correspondence: [email protected] et al. Immunological Cross-Reactivity of Proteins Extracted from the Abstract: Pythiosis, a life-threatening disease caused by Pythium insidiosum, has been increasingly Oomycete Pythium insidiosum and the diagnosed worldwide. A recently developed immunochromatographic test (ICT) enables the rapid Fungus Basidiobolus ranarum diagnosis of pythiosis. During the 3-year clinical implementation of ICT in Thailand, we collected Compromises the Detection the laboratory reports of 38 animals with suspected pythiosis and detected ICT false-positive results Specificity of Immunodiagnostic Assays for Pythiosis. J. Fungi 2021, 7, in three horses and a dog with basidiobolomycosis. P. insidiosum and Basidiobolus ranarum cause infec- 474. https://doi.org/ tions with indistinguishable clinical and microscopic features. This study investigated cross-reactive 10.3390/jof7060474 antibodies by probing P. insidiosum and B. ranarum crude extracts and cell-free synthesized I06 protein (encoded in P. insidiosum genome, not other fungi) against a panel of pythiosis, basidiobolomycosis, Academic Editor: David S. Perlin rabbit anti-I06 peptide, and control sera by Western blot analyses. ICT false-positive results occurred from the cross-reactivity of anti-B. ranarum antibodies to the 15, 50, 60, and 120 kDa proteins of Received: 7 May 2021 P. insidiosum, not double infections caused by both pathogens. Notably, ICT could help to screen Accepted: 4 June 2021 pythiosis, and the positive test requires confirmation by culture or molecular method. The detection Published: 11 June 2021 specificity of ICT requires improvement. The crude extract containing multispecies antigens needs replacement with a refined P. insidiosum-specific protein. We proposed that the 55 kDa I06 protein is Publisher’s Note: MDPI stays neutral an excellent candidate for developing a more specific serodiagnostic test for pythiosis. with regard to jurisdictional claims in published maps and institutional affil- Keywords: pythiosis; Pythium insidiosum; Basidiobolus ranarum; cross-reactivity; serodiagnosis iations. 1. Introduction Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Detection of the pathogen-specific antibodies in a serum sample facilitates the accu- This article is an open access article rate diagnosis of many infectious diseases. Such an immunological method bypasses the distributed under the terms and routine, experience-required, and time-consuming microbiological techniques, i.e., cul- conditions of the Creative Commons ture and morphological examination. Several serodiagnostic assays have been developed Attribution (CC BY) license (https:// for the rapid diagnosis of pythiosis, a life-threatening infectious condition caused by the creativecommons.org/licenses/by/ fungus-like oomycete microorganism Pythium insidiosum, in humans and animals world- 4.0/). wide [1–12]. These assays include immunodiffusion (ID), Western blot (WB), enzyme-linked J. Fungi 2021, 7, 474. https://doi.org/10.3390/jof7060474 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 474 2 of 13 immunosorbent assay (ELISA), hemagglutination (HA), and an immunochromatographic test (ICT) [1–9]. The principle of these serological assays relies on the specific binding of crude protein extracts (prepared from the in vitro growth of P. insidiosum) and their corresponding antibodies to differentiate pythiosis from other infectious diseases [4,13]. Compared to the other assays, ELISA and ICT show relatively higher assay efficiency and are commonly used for detecting the serum anti-P. insidiosum antibodies [1,2,4,9]. However, ICT is a more favorable test format because of its short turnaround time (i.e., 30 min) and user-friendly design (does not require any equipment) [1,2,4]. Inaccurate diagnosis could lead to delayed therapy and poor prognosis (i.e., losing an organ or life) in a patient with pythiosis. Rapid ICT result readout prompts a clinician to plan proper treatment for each pythiosis patient, which likely requires radical surgery (i.e., keratoplasty, enucleation, and limb amputation), as the conventional antimicrobial agents usually fail to fight against P. insidiosum [9–12,14,15]. ICT detected the anti-P. insidiosum antibodies in the first Thai case of animal pythiosis in 2017 [16]. Since then, the assay has assisted in diagnosing pythiosis in several centers in Thailand, including our allied laboratory at the Faculty of Veterinary Medicine, Kasetsart University. Confirmed cases of animal pythiosis have arisen because healthcare workers are more familiar with the disease, and diagnostic tools (i.e., culture, polymerase chain reaction (PCR), and ICT) have become widely available [2–4,6–9,17–20]. On several occasions, the antibody detection and the culture identification showed inconsistent findings (i.e., ICT was positive, but an organism other than P. insidiosum was isolated), indicating a false-positive serological result. The crude protein extract of P. insidiosum, commonly used to develop the serological assays [1–9,13], may share antigenic epitopes with another organism. The false-positive serological result could lead to an adverse consequence because the treatment of pythiosis and other mycoses are generally different (i.e., radical surgery for pythiosis and antimicrobial drug administration for other fungal infections). Here, we collected diagnostic laboratory data (including the culture and PCR reports) of the ICT-tested animals during the past 3 years and identified a fungal organism that might generate cross-reactive antibodies against P. insidiosum. In addition, we produced the 55 kDa immunoreactive OPEL-like I06 protein (uniquely presented in the genome of P. insidiosum but not the other medically important fungi) using the cell-free protein synthesis platform [21]. The synthesized I06 proteins, together with rabbit anti-I06 peptide antibodies and a panel of pythiosis and control sera, were employed to investigate the immunological cross-reactivity of P. insidiosum and another organism. The obtained information on the nature of the P. insidiosum antigens could be applied in developing a better serological assay to provide an accurate diagnosis for pythiosis. 2. Materials and Methods 2.1. Clinical Uses of ICT and Culture Method for Diagnosis of Animal Pythiosis ICT was implemented to rapidly detect the anti-P. insidiosum antibodies in the serum samples of 38 animals with clinically suspected pythiosis at the Department of Microbiology and Immunology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand, during the period between August 2017 and January 2021 (Table1). The assay was performed as previously described [2]. To summarize, an unknown serum, a positive control serum (from a culture-proven case of animal pythiosis), and a negative control serum (from a healthy animal) were diluted (1:5000) in 0.15× phosphate-buffered saline (0.15× PBS; 1.5 mM Na2HPO4, 0.27 mM KH2PO4, 20.55 mM NaCl, 0.405 mM KCl; pH 7.4). Each diluted serum sample (100 µL) was tested for anti-P. insidiosum antibodies using ICT. Experienced personnel read the ICT result within 30 min. J. Fungi 2021, 7, 474 3 of 13 Table 1. Laboratory test results of 38 animals with suspected pythiosis during the period between August 2018 and January 2021. Diagnostic Method Year Case ID Affected Animal Clinical Diagnosis Culture/Molecular ICT for Pythiosis Assay 2017 01 Dog Pythiosis Positive Pythium insidiosum 2017 02 Horse Pythiosis Positive Pythium insidiosum 2017 03 Horse Pythiosis Positive Pythium insidiosum 2017 04 Horse Pythiosis Positive Pythium insidiosum 2017 05 Horse Pythiosis Positive Pythium insidiosum 2017 06 Horse Fungal granuloma Weakly positive * Basidiobolus ranarum Guttural pouch 2018 07 Horse (Negative) Aspergillus flavus empyema 2018 08 Horse Chronic wound (Negative) Dark fungus 2018 09 Horse Pythiosis Positive Pythium insidiosum 2018 10 Horse Pythiosis Positive Pythium insidiosum 2018 11 Horse Habronemiasis Weakly positive * Nocardia species
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