Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age

Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen inte...

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Vydáno v:	Infection and immunity Ročník 86; číslo 11
Hlavní autoři:	Barrila, Jennifer, Crabbé, Aurélie, Yang, Jiseon, Franco, Karla, Nydam, Seth D, Forsyth, Rebecca J, Davis, Richard R, Gangaraju, Sandhya, Ott, C Mark, Coyne, Carolyn B, Bissell, Mina J, Nickerson, Cheryl A
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States 01.11.2018
Témata:	Cellular Microenvironment History, 20th Century History, 21st Century Host-Pathogen Interactions Humans Intestinal Mucosa - physiology Models, Biological Organ Culture Techniques - history Organ Culture Techniques - methods Organoids Tissue Engineering - history Tissue Engineering - methods RWV 3D host-pathogen interactions mechanotransduction rotating wall vessel gut-on-a-chip 3-D organ-on-a-chip host-microbe interaction organoid
ISSN:	1098-5522, 1098-5522
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Abstract	Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). A major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologies provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments.
AbstractList	Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). A major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologies provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments.Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). A major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologies provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments. Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). A major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologies provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments.
Author	Crabbé, Aurélie Nydam, Seth D Franco, Karla Yang, Jiseon Forsyth, Rebecca J Barrila, Jennifer Bissell, Mina J Coyne, Carolyn B Davis, Richard R Nickerson, Cheryl A Gangaraju, Sandhya Ott, C Mark
Author_xml	– sequence: 1 givenname: Jennifer orcidid: 0000-0002-6597-3001 surname: Barrila fullname: Barrila, Jennifer organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 2 givenname: Aurélie orcidid: 0000-0003-3084-4418 surname: Crabbé fullname: Crabbé, Aurélie organization: Laboratory of Pharmaceutical Microbiology, Ghent University, Ghent, Belgium – sequence: 3 givenname: Jiseon surname: Yang fullname: Yang, Jiseon organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 4 givenname: Karla surname: Franco fullname: Franco, Karla organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 5 givenname: Seth D surname: Nydam fullname: Nydam, Seth D organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 6 givenname: Rebecca J surname: Forsyth fullname: Forsyth, Rebecca J organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 7 givenname: Richard R surname: Davis fullname: Davis, Richard R organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 8 givenname: Sandhya surname: Gangaraju fullname: Gangaraju, Sandhya organization: Center for Immunotherapy, Vaccines and Virotherapy, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA – sequence: 9 givenname: C Mark surname: Ott fullname: Ott, C Mark organization: Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, Texas, USA – sequence: 10 givenname: Carolyn B orcidid: 0000-0002-1884-6309 surname: Coyne fullname: Coyne, Carolyn B organization: Department of Pediatrics, University of Pittsburgh, Pittsburgh, Pennsylvania, USA – sequence: 11 givenname: Mina J surname: Bissell fullname: Bissell, Mina J organization: Division Biological Systems and Engineering, Lawrence Berkeley National Laboratory, Berkeley, California, USA – sequence: 12 givenname: Cheryl A orcidid: 0000-0002-9804-9739 surname: Nickerson fullname: Nickerson, Cheryl A email: Cheryl.Nickerson@asu.edu organization: School of Life Sciences, Arizona State University, Tempe, Arizona, USA
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SubjectTerms	Cellular Microenvironment History, 20th Century History, 21st Century Host-Pathogen Interactions Humans Intestinal Mucosa - physiology Models, Biological Organ Culture Techniques - history Organ Culture Techniques - methods Organoids Tissue Engineering - history Tissue Engineering - methods
Title	Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age
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