MiR-142-3p Regulates the Formation and Differentiation of Hematopoietic Stem Cells in Vertebrates

Overview

Journal Cell Res

Specialty Cell Biology

Date 2013 Oct 30

PMID 24165894

Citations 48

Authors

Xinyan Lu

Xiajuan Li

Qiuping He

Jiao Gao

Ya Gao

Bing Liu

Feng Liu

Affiliations

Soon will be listed here.

Abstract

Previous studies on developmental hematopoiesis have mainly focused on signaling and transcription factors, while the appreciation of epigenetic regulation including that of microRNAs is recent. Here, we show that in zebrafish and mouse, miR-142-3p is specifically expressed in hematopoietic stem cells (HSCs). Knockdown of miR-142a-3p in zebrafish led to a reduced population of HSCs in the aorta-gonad-mesonephros (AGM) region as well as T-cell defects in the thymus. Mechanistically, miR-142a-3p regulates HSC formation and differentiation through the repression of interferon regulatory factor 7 (irf7)-mediated inflammation signaling. Finally, we show that miR-142-3p is also involved in the development of HSCs in mouse AGM, suggesting that it has a highly conserved role in vertebrates. Together, these findings unveil the pivotal roles that miR-142a-3p plays in the formation and differentiation of HSCs by repressing irf7 signaling.

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References

Kissa K, Herbomel P . Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature. 2010; 464(7285):112-5. DOI: 10.1038/nature08761. View

Dore L, Amigo J, Dos Santos C, Zhang Z, Gai X, Tobias J . A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci U S A. 2008; 105(9):3333-8. PMC: 2265118. DOI: 10.1073/pnas.0712312105. View

Pase L, Layton J, Kloosterman W, Carradice D, Waterhouse P, Lieschke G . miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood. 2008; 113(8):1794-804. PMC: 2647672. DOI: 10.1182/blood-2008-05-155812. View

Bertrand J, Chi N, Santoso B, Teng S, Stainier D, Traver D . Haematopoietic stem cells derive directly from aortic endothelium during development. Nature. 2010; 464(7285):108-11. PMC: 2858358. DOI: 10.1038/nature08738. View

North T, Goessling W, Peeters M, Li P, Ceol C, Lord A . Hematopoietic stem cell development is dependent on blood flow. Cell. 2009; 137(4):736-48. PMC: 2722870. DOI: 10.1016/j.cell.2009.04.023. View

Lechman E, Gentner B, van Galen P, Giustacchini A, Saini M, Boccalatte F . Attenuation of miR-126 activity expands HSC in vivo without exhaustion. Cell Stem Cell. 2012; 11(6):799-811. PMC: 3517970. DOI: 10.1016/j.stem.2012.09.001. View

Orkin S, Zon L . Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008; 132(4):631-44. PMC: 2628169. DOI: 10.1016/j.cell.2008.01.025. View

Wang H, Lee C, Qi C, Tailor P, Feng J, Abbasi S . IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood. 2008; 112(10):4028-38. PMC: 2581985. DOI: 10.1182/blood-2008-01-129049. View

Li L, Jin H, Xu J, Shi Y, Wen Z . Irf8 regulates macrophage versus neutrophil fate during zebrafish primitive myelopoiesis. Blood. 2010; 117(4):1359-69. DOI: 10.1182/blood-2010-06-290700. View

10.

OConnell R, Baltimore D . MicroRNAs and hematopoietic cell development. Curr Top Dev Biol. 2012; 99:145-74. DOI: 10.1016/B978-0-12-387038-4.00006-9. View

11.

Forman J, Coller H . The code within the code: microRNAs target coding regions. Cell Cycle. 2010; 9(8):1533-41. PMC: 2936675. DOI: 10.4161/cc.9.8.11202. View

12.

Hall C, Flores M, Oehlers S, Sanderson L, Lam E, Crosier K . Infection-responsive expansion of the hematopoietic stem and progenitor cell compartment in zebrafish is dependent upon inducible nitric oxide. Cell Stem Cell. 2012; 10(2):198-209. DOI: 10.1016/j.stem.2012.01.007. View

13.

Bartel D . MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-97. DOI: 10.1016/s0092-8674(04)00045-5. View

14.

Stainier D, Weinstein B, Detrich 3rd H, Zon L, Fishman M . Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development. 1995; 121(10):3141-50. DOI: 10.1242/dev.121.10.3141. View

15.

Ramkissoon S, Mainwaring L, Ogasawara Y, Keyvanfar K, McCoy Jr J, Sloand E . Hematopoietic-specific microRNA expression in human cells. Leuk Res. 2005; 30(5):643-7. DOI: 10.1016/j.leukres.2005.09.001. View

16.

Fredericksen B, Gale Jr M . West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J Virol. 2006; 80(6):2913-23. PMC: 1395472. DOI: 10.1128/JVI.80.6.2913-2923.2006. View

17.

Bissels U, Wild S, Tomiuk S, Hafner M, Scheel H, Mihailovic A . Combined characterization of microRNA and mRNA profiles delineates early differentiation pathways of CD133+ and CD34+ hematopoietic stem and progenitor cells. Stem Cells. 2011; 29(5):847-57. PMC: 3116150. DOI: 10.1002/stem.627. View

18.

Balaraman S, Tewary P, Singh V, Madhubala R . Leishmania donovani induces interferon regulatory factor in murine macrophages: a host defense response. Biochem Biophys Res Commun. 2004; 317(2):639-47. DOI: 10.1016/j.bbrc.2004.03.097. View

19.

North T, Goessling W, Walkley C, Lengerke C, Kopani K, Lord A . Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature. 2007; 447(7147):1007-11. PMC: 2775137. DOI: 10.1038/nature05883. View

20.

Ozato K, Tailor P, Kubota T . The interferon regulatory factor family in host defense: mechanism of action. J Biol Chem. 2007; 282(28):20065-9. DOI: 10.1074/jbc.R700003200. View