A fungal-binding agglutinin in the skin slime of Japanese flounder (Paralichthys olivaceus) is glyceraldehyde 3-phosphate dehydrogenase.
GAPDH
Japanese flounder
agglutinin
fungi
innate immunity
skin mucus
Journal
Microbiology and immunology
ISSN: 1348-0421
Titre abrégé: Microbiol Immunol
Pays: Australia
ID NLM: 7703966
Informations de publication
Date de publication:
24 Jun 2024
24 Jun 2024
Historique:
revised:
06
06
2024
received:
15
04
2024
accepted:
12
06
2024
medline:
26
6
2024
pubmed:
26
6
2024
entrez:
26
6
2024
Statut:
aheadofprint
Résumé
Agglutination of pathogenic microorganisms on the body surface is a significant phenomenon for the prevention of infection. In the present study, we show that an extract of the skin mucus from Japanese flounder (Paralichthys olivaceus) has agglutination activity against the yeast Saccharomyces cerevisiae. We purified this yeast-binding protein, which consists of an approximately 35-kDa homodimer, using affinity chromatography with yeast as a ligand. Multiple internal amino acid sequences of the protein, as determined using liquid chromatography with quadrupole time-of-flight tandem mass spectrometry, mapped to flounder glyceraldehyde 3-phosphate dehydrogenase (GAPDH). An anti-GAPDH antibody inhibited the yeast agglutination activity in the skin mucus extract and stained agglutinated yeast, indicating that flounder GAPDH could agglutinate yeast. The current study suggests that GAPDH, a well-known protein as the sixth enzyme in the glycolytic pathway, is a significant player in mucosal immunity in teleosts.
Identifiants
pubmed: 38923675
doi: 10.1111/1348-0421.13163
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : None
Informations de copyright
© 2024 The Societies and John Wiley & Sons Australia, Ltd.
Références
Tasumi S, Ohira T, Kawazoe I, Suetake H, Suzuki Y, Aida K. Primary structure and characteristics of a lectin from skin mucus of the Japanese eel Anguilla japonica. J Biol Chem. 2002;277:27305–27311.
Tasumi S, Yang WJ, Usami T, Tsutsui S, Ohira T, Kawazoe I, et al. Characteristics and primary structure of a galectin in the skin mucus of the Japanese eel, Anguilla japonica. Dev Comp Immunol. 2004;28:325–335.
Tsutsui S, Tasumi S, Suetake H, Suzuki Y. Lectins homologous to those of monocotyledonous plants in the skin mucus and intestine of pufferfish, Fugu rubripes. J Biol Chem. 2003;278:20882–20889.
Tsutsui S, Komatsu Y, Sugiura T, Araki K, Nakamura O. A unique epidermal mucus lectin identified from catfish (Silurus asotus): first evidence of intelectin in fish skin slime. J Biochem. 2011;150:501–514.
Xu Z, Parra D, Gómez D, Salinas I, Zhang YA, von Gersdorff Jorgensen L, et al. Teleost skin, an ancient mucosal surface that elicits gut‐like immune responses. Proc Nat Acad Sci. 2013;110:13097–13102.
Salinas I, Fernández‐Montero Á, Ding Y, Sunyer JO. Mucosal immunoglobulins of teleost fish: A decade of advances. Dev Comp Immunol. 2021;121:104079.
Shibuya K, Tsutsui S, Nakamura O. Fugu, Takifugu ruberipes, mucus keratins act as defense molecules against fungi. Mol Immunol. 2019;116:1–10.
Das S, Lyla PS, Khan SA. Marine microbial diversity and ecology: importance and future perspectives. Curr Sci. 2006;90:1325–1335.
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Nat Acad Sci. 2006;103:12115–12120.
Tsutsui S, Iwamoto K, Nakamura O, Watanabe T. Yeast‐binding C‐type lectin with opsonic activity from conger eel (Conger myriaster) skin mucus. Mol Immunol. 2007;44:691–702.
Dayhoff MO. Dehydrogenases. In: Dayhoff MO editor. Atlas of protein sequence and structure. 5th edn. Washington: National Biomedical Research Foundation; 1972. p. 141–144.
Meyer‐Siegler K, Mauro DJ, Seal G, Wurzer J, de Riel JK, Sirover MA. A human nuclear uracil DNA glycosylase is the 37‐kDa subunit of glyceraldehyde‐3‐phosphate dehydrogenase. Proc Nat Acad Sci. 1991;88:8460–8464.
Singh R, Green MR. Sequence‐specific binding of transfer RNA by Glyceraldehyde‐3‐Phosphate Dehydrogenase. Science. 1993;259:365–368.
Kumagai H, Sakai H. A porcine brain protein (35K Protein) which bundles microtubules and its identification as glyceraldehyde 3‐phosphate dehydrogenase1. J Biochem. 1983;93:1259–1269.
Robbins AR, Ward RD, Oliver C. A mutation in glyceraldehyde 3‐phosphate dehydrogenase alters endocytosis in CHO cells. J Cell Biol. 1995;130:1093–1104.
Ishitani R, Chuang DM. Glyceraldehyde‐3‐phosphate dehydrogenase antisense oligodeoxynucleotides protect against cytosine arabinonucleoside‐induced apoptosis in cultured cerebellar neurons. Proc Nat Acad Sci. 1996;93:9937–9941.
Wu Y, Wu M, He G, Zhang X, Li W, Gao Y, et al. Glyceraldehyde‐3‐phosphate dehydrogenase: a universal internal control for Western blots in prokaryotic and eukaryotic cells. Anal Biochem. 2012;423:15–22.
Rajan B, Fernandes JM, Caipang CM, Kiron V, Rombout JH, Brinchmann MF. Proteome reference map of the skin mucus of Atlantic cod (Gadus morhua) revealing immune competent molecules. Fish Shellfish Immunol. 2011;2(31):224–231.
Cordero H, Brinchmann MF, Cuesta A, Meseguer J, Esteban MA. Skin mucus proteome map of European sea bass (Dicentrarchus labrax). Proteomics. 2015;15:4007–4020.
Jurado J, Fuentes‐Almagro CA, Guardiola FA, Cuesta A, Esteban MÁ, Prieto‐Álamo MJ. Proteomic profile of the skin mucus of farmed gilthead seabream (Sparus aurata). J Proteomics. 2015;120:21–34.
Sanahuja I, Ibarz A. Skin mucus proteome of gilthead sea bream: a non‐invasive method to screen for welfare indicators. Fish Shellfish Immunol. 2015;46:426–435.
Seo JK, Lee MJ, Go HJ, Park TH, Park NG. Purification and characterization of YFGAP, a GAPDH‐related novel antimicrobial peptide, from the skin of yellowfin tuna, Thunnus albacares. Fish Shellfish Immunol. 2012;33:743–752.
Tristan C, Shahani N, Sedlak TW, Sawa A. The diverse functions of GAPDH: Views from different subcellular compartments. Cell Signal. 2011;23:317–323.
Huitorel P, Pantaloni D. Bundling of microtubules by glyceraldehyde‐3‐phosphate dehydrogenase and its modulation by ATP. Eur J Biochem. 1985;150:265–269.
Durrieu C, Bernier‐Valentin F, Rousset B. Microtubules bind glyceraldehyde 3‐phosphate dehydrogenase and modulate its enzyme activity and quaternary structure. Arch Biochem Biophys. 1987;252:32–40.
Tisdale EJ, Kelly C, Artalejo CR. Glyceraldehyde‐3‐phosphate dehydrogenase interacts with Rab2 and plays an essential role in endoplasmic reticulum to Golgi transport exclusive of its glycolytic activity. J Biol Chem. 2004;279:54046–54052.
Mitsuzawa H, Kimura M, Kanda E, Ishihama A. Glyceraldehyde‐3‐phosphate dehydrogenase and actin associate with RNA polymerase II and interact with its Rpb7 subunit. FEBS Lett. 2005;579:48–52.
Jacquin MA, Chiche J, Zunino B, Bénéteau M, Meynet O, Pradelli LA, et al. GAPDH binds to active Akt, leading to Bcl‐xL increase and escape from caspase‐independent cell death. Cell Death Differ. 2013;20:1043–1054.
Raje CI, Kumar S, Harle A, Nanda JS, Raje M. The macrophage cell surface glyceraldehyde‐3‐phosphate dehydrogenase is a novel transferrin receptor. J Biol Chem. 2007;282:3252–3261.
Yamaji R, Chatani E, Harada N, Sugimoto K, Inui H, Nakano Y. Glyceraldehyde‐3‐phosphate dehydrogenase in the extracellular space inhibits cell spreading. Biochim Biophys Acta Gen Subj. 2005;1726:261–271.
Sugahara T, Shirahata S, Sasaki T, Murakami H. The mode of actions of glyceraldehyde‐3‐phosphate dehydrogenase identified as an immunoglobulin production stimulating factor. FEBS Lett. 1995;368:92–96.
Koster MI. Making an epidermis. Ann NY Acad Sci. 2009;1170:7–10.
Jin H, Song YP, Boel G, Kochar J, Pancholi V. Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J Mol Biol. 2005;350:27–41.
Antikainen J, Kupannen V, Lähteenmäki K, Korhonen TK. pH‐dependent association of enolase and glyceraldehyde‐3‐phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J Bacteriol. 2007;189:4539–4543.
Kinoshita H, Uchida H, Kawai Y, Kawasaki T, Wakahara N, Matsuo H, et al. Cell surface Lactobacillus plantarum LA 318 glyceraldehyde‐3‐phosphate dehydrogenase (GAPDH) adheres to human colonic mucin. J Appl Microbiol. 2008;104:1667–1674.
Kinoshita H, Wakahara N, Watanabe M, Kawasaki T, Matsuo H, Kawai Y, et al. Cell surface glyceraldehyde‐3‐phosphate dehydrogenase (GAPDH) of Lactobacillus plantarum LA 318 recognizes human A and B blood group antigens. Res Microbiol. 2008;159:685–691.
Pancholi V, Fischetti VA. A major surface protein on group A streptococci is a glyceraldehyde‐3‐phosphate‐dehydrogenase with multiple binding activity. J Exp Med. 1992;176:415–426.
Polderman‐Tijmes JJ, Jekel PA, de Vries EJ, van Merode AE, Floris R, van der Laan JM, et al. Cloning, Sequence Analysis, and Expression inEscherichia coliof the Gene Encoding an α‐Amino Acid Ester Hydrolase fromAcetobacter turbidans. Appl Environ Microbiol. 2002;68:211–218.
Winram SB, Lottenberg R. The plasmin‐binding protein Plr of group A streptococci is identified as glyceraldehyde‐3‐phosphate dehydrogenase. Microbiology. 1996;142:2311–2320.