High-dimensional analysis of intestinal immune cells during helminth infection

Single cell isolation from helminth-infected murine intestines has been notoriously difficult, due to the strong anti-parasite type 2 immune responses that drive mucus production, tissue remodeling and immune cell infiltration. Through the systematic optimization of a standard intestinal digestion p...

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Published ineLife Vol. 9
Main Authors Ferrer-Font, Laura, Mehta, Palak, Harmos, Phoebe, Schmidt, Alfonso J, Chappell, Sally, Price, Kylie M, Hermans, Ian F, Ronchese, Franca, le Gros, Graham, Mayer, Johannes U
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 11.02.2020
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
Animals
B cells
cell isolation
Confocal microscopy
Dimensional analysis
Duodenum
Duodenum - immunology
Duodenum - parasitology
EDTA
Experiments
Flow cytometry
Flow Cytometry - methods
H. polygyrus
Health aspects
helminth infection
Host-Parasite Interactions - immunology
Immune response
Immunology and Inflammation
Infections
intestinal immune cells
Intestine
Intestines
Isolation
Mice, Inbred C57BL
Microscopy
Nematospiroides dubius
Optimization
Parasites
Protocol
Tools and Resources
type 2 immunity
mouse
helminth infection
inflammation
cell isolation
H. polygyrus
intestinal immune cells
immunology
type 2 immunity
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Abstract Single cell isolation from helminth-infected murine intestines has been notoriously difficult, due to the strong anti-parasite type 2 immune responses that drive mucus production, tissue remodeling and immune cell infiltration. Through the systematic optimization of a standard intestinal digestion protocol, we were able to successfully isolate millions of immune cells from the heavily infected duodenum. To validate that these cells gave an accurate representation of intestinal immune responses, we analyzed them using a high-dimensional spectral flow cytometry panel and confirmed our findings by confocal microscopy. Our cell isolation protocol and high-dimensional analysis allowed us to identify many known hallmarks of anti-parasite immune responses throughout the entire course of helminth infection and has the potential to accelerate single-cell discoveries of local helminth immune responses that have previously been unfeasible.
AbstractList Single cell isolation from helminth-infected murine intestines has been notoriously difficult, due to the strong anti-parasite type 2 immune responses that drive mucus production, tissue remodeling and immune cell infiltration. Through the systematic optimization of a standard intestinal digestion protocol, we were able to successfully isolate millions of immune cells from the heavily infected duodenum. To validate that these cells gave an accurate representation of intestinal immune responses, we analyzed them using a high-dimensional spectral flow cytometry panel and confirmed our findings by confocal microscopy. Our cell isolation protocol and high-dimensional analysis allowed us to identify many known hallmarks of anti-parasite immune responses throughout the entire course of helminth infection and has the potential to accelerate single-cell discoveries of local helminth immune responses that have previously been unfeasible.
Single cell isolation from helminth-infected murine intestines has been notoriously difficult, due to the strong anti-parasite type 2 immune responses that drive mucus production, tissue remodeling and immune cell infiltration. Through the systematic optimization of a standard intestinal digestion protocol, we were able to successfully isolate millions of immune cells from the heavily infected duodenum. To validate that these cells gave an accurate representation of intestinal immune responses, we analyzed them using a high-dimensional spectral flow cytometry panel and confirmed our findings by confocal microscopy. Our cell isolation protocol and high-dimensional analysis allowed us to identify many known hallmarks of anti-parasite immune responses throughout the entire course of helminth infection and has the potential to accelerate single-cell discoveries of local helminth immune responses that have previously been unfeasible. Parasitic worms known as helminths represent an important health problem in large parts of Africa, South America and Asia. Once their larvae enter the body, they head to the gut where they mature into adults and start laying eggs. In areas with poor sanitation, these may then get passed on to other individuals. To defend the body, the immune system sends large numbers of immune cells to the gut, but it usually struggles to eliminate the parasites. Without deworming medication, the infection can last for many years. Scientists study helminth infections in the laboratory by using worms that naturally infect mice. Understanding exactly how the immune system responds to the infection is essential to grasp why it fails to clear the worms. However, it is difficult to extract immune cells from an infected gut, as the infection creates strong local responses – such as an intense ‘slime’ production to try to flush out the worms. The standard procedure to obtain immune cells from the gut consists of three steps: collecting a gut segment and washing it, stripping away the surface layers with chemicals, and finally using enzymes to digest the tissues, which are then filtered to obtain individual cells. However, this protocol is not able to extract cells during infection. Ferrer-Font et al. therefore methodically refined every step of this method, and finally succeeded in obtaining millions of immune cells from infected guts. For the first time, these cells could then be studied and identified using a new technology called spectral flow cytometry. Over 40 immune cell types were followed throughout the course of infection, revealing that many ‘first responders’ immune cells were recruited to the gut early on, when the worms were still larvae. However, these cells disappeared once the worms developed into adults. These findings were confirmed by microscopy, which also showed that the first responder cells were found around the developing larvae, likely attacking them. When the adult worms developed, these cells were replaced by other immune cells, which also decreased the longer the worms were present in the gut. This new extraction process established by Ferrer-Font et al. can also be paired with other technologies that can, for example, reveal which genes are turned on in individual cells. This could help map out exactly how the body fights helminth infections, and how to improve this response. The method could also be useful to extract immune cells from the gut in other challenging scenarios, such food allergies or inflammatory bowel disorders.
Audience Academic
Author Mehta, Palak
Price, Kylie M
le Gros, Graham
Ronchese, Franca
Chappell, Sally
Harmos, Phoebe
Ferrer-Font, Laura
Hermans, Ian F
Mayer, Johannes U
Schmidt, Alfonso J
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Keywords mouse
helminth infection
inflammation
cell isolation
H. polygyrus
intestinal immune cells
immunology
type 2 immunity
Language English
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Snippet Single cell isolation from helminth-infected murine intestines has been notoriously difficult, due to the strong anti-parasite type 2 immune responses that...
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proquest
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
SubjectTerms Animals
B cells
cell isolation
Confocal microscopy
Dimensional analysis
Duodenum
Duodenum - immunology
Duodenum - parasitology
EDTA
Experiments
Flow cytometry
Flow Cytometry - methods
H. polygyrus
Health aspects
helminth infection
Host-Parasite Interactions - immunology
Immune response
Immunology and Inflammation
Infections
intestinal immune cells
Intestine
Intestines
Isolation
Mice, Inbred C57BL
Microscopy
Nematospiroides dubius
Optimization
Parasites
Protocol
Tools and Resources
type 2 immunity
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Title High-dimensional analysis of intestinal immune cells during helminth infection
URI https://www.ncbi.nlm.nih.gov/pubmed/32041687
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Volume 9
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