The Role of the Microbiota in Myelopoiesis During Homeostasis and Inflammation

Overview

Journal Int Immunol

Specialty Allergy & Immunology

Date 2023 Jan 25

PMID 36694400

Authors

Yeji Kim

Nobuhiko Kamada

Affiliations

Soon will be listed here.

Abstract

The microbiota engages in the development and maintenance of the host immune system. The microbiota affects not only mucosal tissues where it localizes but also the distal organs. Myeloid cells are essential for host defense as first responders of the host immune system. Their generation, called myelopoiesis, is regulated by environmental signals, including commensal microbiota. Hematopoietic stem and progenitor cells in bone marrow can directly or indirectly sense microbiota-derived signals, thereby giving rise to myeloid cell lineages at steady-state and during inflammation. In this review, we discuss the role of commensal microorganisms in the homeostatic regulation of myelopoiesis in the bone marrow. We also outline the effects of microbial signals on myelopoiesis during inflammation and infection, with a particular focus on the development of innate immune memory. Studying the relationship between the microbiota and myelopoiesis will help us understand how the microbiota regulates immune responses at a systemic level beyond the local mucosa.

References

Tanoue T, Morita S, Plichta D, Skelly A, Suda W, Sugiura Y . A defined commensal consortium elicits CD8 T cells and anti-cancer immunity. Nature. 2019; 565(7741):600-605. DOI: 10.1038/s41586-019-0878-z. View

Hill D, Siracusa M, Abt M, Kim B, Kobuley D, Kubo M . Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med. 2012; 18(4):538-46. PMC: 3321082. DOI: 10.1038/nm.2657. View

Japp A, Hoffmann K, Schlickeiser S, Glauben R, Nikolaou C, Maecker H . Wild immunology assessed by multidimensional mass cytometry. Cytometry A. 2016; 91(1):85-95. DOI: 10.1002/cyto.a.22906. View

Stanley D, Mason L, Mackin K, Srikhanta Y, Lyras D, Prakash M . Translocation and dissemination of commensal bacteria in post-stroke infection. Nat Med. 2016; 22(11):1277-1284. DOI: 10.1038/nm.4194. View

Cheng N, He R, Tian J, Ye P, Ye R . Cutting edge: TLR2 is a functional receptor for acute-phase serum amyloid A. J Immunol. 2008; 181(1):22-6. PMC: 2464454. DOI: 10.4049/jimmunol.181.1.22. View

Chen J, Zhang S, Feng X, Wu Z, Dubois W, Thovarai V . Conventional Co-Housing Modulates Murine Gut Microbiota and Hematopoietic Gene Expression. Int J Mol Sci. 2020; 21(17). PMC: 7503692. DOI: 10.3390/ijms21176143. View

Foster S, Hargreaves D, Medzhitov R . Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature. 2007; 447(7147):972-8. DOI: 10.1038/nature05836. View

Serbina N, Hohl T, Cherny M, Pamer E . Selective expansion of the monocytic lineage directed by bacterial infection. J Immunol. 2009; 183(3):1900-10. PMC: 2753883. DOI: 10.4049/jimmunol.0900612. View

Balmer M, Schurch C, Saito Y, Geuking M, Li H, Cuenca M . Microbiota-derived compounds drive steady-state granulopoiesis via MyD88/TICAM signaling. J Immunol. 2014; 193(10):5273-83. DOI: 10.4049/jimmunol.1400762. View

10.

Pang W, Price E, Sahoo D, Beerman I, Maloney W, Rossi D . Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci U S A. 2011; 108(50):20012-7. PMC: 3250139. DOI: 10.1073/pnas.1116110108. View

11.

Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y, Narushima S . Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells. Cell. 2015; 163(2):367-80. PMC: 4765954. DOI: 10.1016/j.cell.2015.08.058. View

12.

Nardi K, Milia P, Eusebi P, Paciaroni M, Caso V, Agnelli G . Admission leukocytosis in acute cerebral ischemia: influence on early outcome. J Stroke Cerebrovasc Dis. 2011; 21(8):819-24. DOI: 10.1016/j.jstrokecerebrovasdis.2011.04.015. View

13.

Adami A, Bracken S, Guernsey L, Rafti E, Maas K, Graf J . Early-life antibiotics attenuate regulatory T cell generation and increase the severity of murine house dust mite-induced asthma. Pediatr Res. 2018; 84(3):426-434. PMC: 6258300. DOI: 10.1038/s41390-018-0031-y. View

14.

Hashimoto D, Chow A, Noizat C, Teo P, Beasley M, Leboeuf M . Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013; 38(4):792-804. PMC: 3853406. DOI: 10.1016/j.immuni.2013.04.004. View

15.

Quintin J, Saeed S, Martens J, Giamarellos-Bourboulis E, Ifrim D, Logie C . Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe. 2012; 12(2):223-32. PMC: 3864037. DOI: 10.1016/j.chom.2012.06.006. View

16.

Huggins M, Sjaastad F, Pierson M, Kucaba T, Swanson W, Staley C . Microbial Exposure Enhances Immunity to Pathogens Recognized by TLR2 but Increases Susceptibility to Cytokine Storm through TLR4 Sensitization. Cell Rep. 2019; 28(7):1729-1743.e5. PMC: 6703181. DOI: 10.1016/j.celrep.2019.07.028. View

17.

Yao Y, Jeyanathan M, Haddadi S, Barra N, Vaseghi-Shanjani M, Damjanovic D . Induction of Autonomous Memory Alveolar Macrophages Requires T Cell Help and Is Critical to Trained Immunity. Cell. 2018; 175(6):1634-1650.e17. DOI: 10.1016/j.cell.2018.09.042. View

18.

Magnusdottir S, Ravcheev D, de Crecy-Lagard V, Thiele I . Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet. 2015; 6:148. PMC: 4403557. DOI: 10.3389/fgene.2015.00148. View

19.

Griseri T, McKenzie B, Schiering C, Powrie F . Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23-driven chronic intestinal inflammation. Immunity. 2012; 37(6):1116-29. PMC: 3664922. DOI: 10.1016/j.immuni.2012.08.025. View

20.

Weaver L, Minichino D, Biswas C, Chu N, Lee J, Bittinger K . Microbiota-dependent signals are required to sustain TLR-mediated immune responses. JCI Insight. 2019; 4(1). PMC: 6485364. DOI: 10.1172/jci.insight.124370. View