Cell-surface anchoring of Listeria adhesion protein on L. monocytogenes is fastened by internalin B for pathogenesis

Dongqi Liu; Xingjian Bai; Harrison D.B. Helmick; Manalee Samaddar; Mary Anne Roshni Amalaradjou; Xilin Li; Shivendra Tenguria; Nicholas L.F. Gallina; Luping Xu; Rishi Drolia; Uma K. Aryal; Gustavo Marçal Schmidt Garcia Moreira; Michael Hust; Mohamed N. Seleem; Jozef L. Kokini; Raluca Ostafe; Abigail Cox; Arun K. Bhunia

Cell Reports (May 2023)

Cell-surface anchoring of Listeria adhesion protein on L. monocytogenes is fastened by internalin B for pathogenesis

Dongqi Liu,
Xingjian Bai,
Harrison D.B. Helmick,
Manalee Samaddar,
Mary Anne Roshni Amalaradjou,
Xilin Li,
Shivendra Tenguria,
Nicholas L.F. Gallina,
Luping Xu,
Rishi Drolia,
Uma K. Aryal,
Gustavo Marçal Schmidt Garcia Moreira,
Michael Hust,
Mohamed N. Seleem,
Jozef L. Kokini,
Raluca Ostafe,
Abigail Cox,
Arun K. Bhunia

Affiliations

Dongqi Liu: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA
Xingjian Bai: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA
Harrison D.B. Helmick: Department of Food Science, Purdue University, West Lafayette, IN, USA
Manalee Samaddar: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA
Mary Anne Roshni Amalaradjou: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Department of Animal Sciences, University of Connecticut, Storrs, CT, USA
Xilin Li: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA
Shivendra Tenguria: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA
Nicholas L.F. Gallina: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA
Luping Xu: Department of Food Science, Purdue University, West Lafayette, IN, USA
Rishi Drolia: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA; Department of Biological Science, Eastern Kentucky University, Richmond, KY, USA
Uma K. Aryal: Bindley Bioscience, Purdue University, West Lafayette, IN, USA; Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA
Gustavo Marçal Schmidt Garcia Moreira: Technische Universität Braunschweig University of Technology, Institute for Biochemistry, Biotechnology, and Bioinformatics, Spielmannstr. 7, 38106 Braunschweig, Germany
Michael Hust: Technische Universität Braunschweig University of Technology, Institute for Biochemistry, Biotechnology, and Bioinformatics, Spielmannstr. 7, 38106 Braunschweig, Germany
Mohamed N. Seleem: Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA; Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA
Jozef L. Kokini: Department of Food Science, Purdue University, West Lafayette, IN, USA
Raluca Ostafe: Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA
Abigail Cox: Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA
Arun K. Bhunia: Molecular Food Microbiology Laboratory, Department of Food Science, Purdue University, West Lafayette, IN, USA; Purdue Institute of Inflammation, Immunology, and Infectious Disease, West Lafayette, IN, USA; Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA; Corresponding author

Journal volume & issue: Vol. 42, no. 5
p. 112515

Abstract

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Summary: Listeria adhesion protein (LAP) is a secreted acetaldehyde alcohol dehydrogenase (AdhE) that anchors to an unknown molecule on the Listeria monocytogenes (Lm) surface, which is critical for its intestinal epithelium crossing. In the present work, immunoprecipitation and mass spectrometry identify internalin B (InlB) as the primary ligand of LAP (KD ∼ 42 nM). InlB-deleted and naturally InlB-deficient Lm strains show reduced LAP-InlB interaction and LAP-mediated pathology in the murine intestine and brain invasion. InlB-overexpressing non-pathogenic Listeria innocua also displays LAP-InlB interplay. In silico predictions reveal that a pocket region in the C-terminal domain of tetrameric LAP is the binding site for InlB. LAP variants containing mutations in negatively charged (E523S, E621S) amino acids in the C terminus confirm altered binding conformations and weaker affinity for InlB. InlB transforms the housekeeping enzyme, AdhE (LAP), into a moonlighting pathogenic factor by fastening on the cell surface.

CP: Microbiology

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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