1,023
Views
0
CrossRef citations to date
0
Altmetric
Review

Host-microbiota interaction in intestinal stem cell homeostasis

, , , , &
Article: 2353399 | Received 02 Feb 2024, Accepted 06 May 2024, Published online: 17 May 2024
 

ABSTRACT

Intestinal stem cells (ISCs) play a pivotal role in gut physiology by governing intestinal epithelium renewal through the precise regulation of proliferation and differentiation. The gut microbiota interacts closely with the epithelium through myriad of actions, including immune and metabolic interactions, which translate into tight connections between microbial activity and ISC function. Given the diverse functions of the gut microbiota in affecting the metabolism of macronutrients and micronutrients, dietary nutrients exert pronounced effects on host-microbiota interactions and, consequently, the ISC fate. Therefore, understanding the intricate host-microbiota interaction in regulating ISC homeostasis is imperative for improving gut health. Here, we review recent advances in understanding host-microbiota immune and metabolic interactions that shape ISC function, such as the role of pattern-recognition receptors and microbial metabolites, including lactate and indole metabolites. Additionally, the diverse regulatory effects of the microbiota on dietary nutrients, including proteins, carbohydrates, vitamins, and minerals (e.g. iron and zinc), are thoroughly explored in relation to their impact on ISCs. Thus, we highlight the multifaceted mechanisms governing host–microbiota interactions in ISC homeostasis. Insights gained from this review provide strategies for the development of dietary or microbiota-based interventions to foster gut health.

List of abbreviations

ACC1=

Acetyl-CoA-carboxylase

AHR=

Aryl hydrocarbon receptor

APC=

Adenomatous polyposis coli

BAs=

Bile acids

BMPs=

Bone morphogenetic proteins

BSH=

Bile salt hydrolase

CBCs=

Crypt-base columnar cells

CSL=

CBF-1/RBP-Jκ, Su(H), Lag-1

DCA=

Deoxycholic acid

Dkk1=

Dickkopf-related protein 1

DON=

Deoxynivalenol

ECs=

Enterocytes

EEs=

Enteroendocrine cells

EGF=

Epidermal growth factor

EGFR=

Epidermal growth factor receptor

ERK1/2=

Extracellular regulated kinase 1/2

FXR=

Farnesoid X receptor

GCPRs=

G protein-coupled receptors

HADCs=

Histone deacetylases

HCOs=

Human colonic organoids

HES=

Hairy and Enhancer of split

HFD=

High-fat diet

HIF-1α=

Hypoxia-inducible factor-1α

HIOs=

HPSC-derived small intestinal organoids

HMO=

Human milk oligosaccharides

HPSC=

Human pluripotent stem cell

ILC3=

innate lymphoid cells type 3

ISCs=

Intestinal stem cells

LCA=

Lithocholic acid

LGR5=

Leucine-rich repeat-containing G-protein-coupled receptor 5

LPS=

lipopolysaccharide

LTA=

Lipoteichoic acid

M3R=

muscarinic 3 receptor

MAMPs=

Microorganism-associated molecular patterns

MDP=

Muramyl dipeptide

MHE=

Mid-hindgut endoderm

NF-κB=

Nuclear factor κB

NICD=

Notch intracellular domain

NLRs=

Nucleotide-binding oligomerization domain (NOD)-like receptors

PG=

peptidoglycan

PGE2=

Prostaglandin E2

PPARα=

Peroxisome proliferator-activated receptor alpha

PPARδ=

Peroxisome proliferator-activated receptor delta

PRRs=

Pattern recognition receptors

rISCs=

Reserve intestinal stem cells

RNF43=

Ring finger protein 43

ROS=

Reactive oxygen species

SBAs=

Secondary bile acids

Se-Met=

Selenomethionine

SFCAs=

Short-chain fatty acids

TCFs=

T-cell factors

TGFα=

Transforming growth factor-a

TGR5=

Takeda G protein-coupled receptor 5

TLR2=

Toll-like receptor 2

TLR4=

Toll-like receptor 4

TLRs=

Toll-like receptors

Trp=

Tryptophan

YAP=

Yes-associated protein

ZNRF3=

ZNRF3

Acknowledgments

We extend our sincere admiration to the researchers in this field and within our laboratories for their unwavering dedication and hard work. We regret that we could not include citations of all the valuable works of scientists in this field owing to space constraints.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

WZ conceived and designed this review, edited the manuscript, and secured funding for the study. HW wrote the manuscript draft. CM participated in the concept development, edited and revised the manuscript. LX helped collect literature and draw the diagram. KY provided advice on the review structure. LS edited and proofread the manuscript. All authors contributed to the article and approved the final version of this manuscript.

Data Availability statement

Data sharing is not applicable to this article, as no datasets were generated or analyzed in the current study. were created using Figdraw software (www.figdraw.com).

Additional information

Funding

This work was supported by the National Natural Science Foundation of China [under Grant number 32030104] and the National Key R&D Program of China [under Grant number 2022YFD1300402].