LYVE1 Marks the Divergence of Yolk Sac Definitive Hemogenic Endothelium from the Primitive Erythroid Lineage

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2016 Nov 24

PMID 27880904

Citations 42

Authors

Lydia K Lee

Yasamine Ghorbanian

Wenyuan Wang

Yanling Wang

Yeon Joo Kim

Irving L Weissman

Matthew A Inlay

Hanna K A Mikkola

Affiliations

Soon will be listed here.

Abstract

The contribution of the different waves and sites of developmental hematopoiesis to fetal and adult blood production remains unclear. Here, we identify lymphatic vessel endothelial hyaluronan receptor-1 (LYVE1) as a marker of yolk sac (YS) endothelium and definitive hematopoietic stem and progenitor cells (HSPCs). Endothelium in mid-gestation YS and vitelline vessels, but not the dorsal aorta and placenta, were labeled by Lyve1-Cre. Most YS HSPCs and erythro-myeloid progenitors were Lyve1-Cre lineage traced, but primitive erythroid cells were not, suggesting that they represent distinct lineages. Fetal liver (FL) and adult HSPCs showed 35%-40% Lyve1-Cre marking. Analysis of circulation-deficient Ncx1 concepti identified the YS as a major source of Lyve1-Cre labeled HSPCs. FL proerythroblast marking was extensive at embryonic day (E) 11.5-13.5, but decreased to hematopoietic stem cell (HSC) levels by E16.5, suggesting that HSCs from multiple sources became responsible for erythropoiesis. Lyve1-Cre thus marks the divergence between YS primitive and definitive hematopoiesis and provides a tool for targeting YS definitive hematopoiesis and FL colonization.

Citing Articles

Comprehensive analysis of myeloid reporter mice.

Wang Y, Dowling S, Rodriguez V, Maciuch J, Mayer M, Therron T bioRxiv. 2025; .

PMID: 40060446 PMC: 11888320. DOI: 10.1101/2025.02.24.639159.

Conversion of placental hemogenic endothelial cells to hematopoietic stem and progenitor cells.

Liang G, Liu S, Zhou C, Liu M, Zhang Y, Ma D Cell Discov. 2025; 11(1):9.

PMID: 39875377 PMC: 11775181. DOI: 10.1038/s41421-024-00760-2.

Mouse and human macrophages and their roles in cardiovascular health and disease.

Gallerand A, Han J, Ivanov S, Randolph G Nat Cardiovasc Res. 2024; 3(12):1424-1437.

PMID: 39604762 DOI: 10.1038/s44161-024-00580-3.

New insights into the endothelial origin of hematopoietic system inspired by "TIF" approaches.

Hou S, Guo X, Du J, Ding X, Ning X, Wang H Blood Sci. 2024; 6(4):e00199.

PMID: 39027902 PMC: 11254119. DOI: 10.1097/BS9.0000000000000199.

Self-Organization of Sinusoidal Vessels in Pluripotent Stem Cell-derived Human Liver Bud Organoids.

Saiki N, Nio Y, Yoneyama Y, Kawamura S, Iwasawa K, Kawakami E bioRxiv. 2024; .

PMID: 39005378 PMC: 11245015. DOI: 10.1101/2024.07.02.601804.

References

Rhodes K, Gekas C, Wang Y, Lux C, Francis C, Chan D . The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell. 2008; 2(3):252-63. PMC: 2888040. DOI: 10.1016/j.stem.2008.01.001. View

Beerman I, Bhattacharya D, Zandi S, Sigvardsson M, Weissman I, Bryder D . Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci U S A. 2010; 107(12):5465-70. PMC: 2851806. DOI: 10.1073/pnas.1000834107. View

Gordon E, Gale N, Harvey N . Expression of the hyaluronan receptor LYVE-1 is not restricted to the lymphatic vasculature; LYVE-1 is also expressed on embryonic blood vessels. Dev Dyn. 2008; 237(7):1901-9. DOI: 10.1002/dvdy.21605. View

Mikkola H, Klintman J, Yang H, Hock H, Schlaeger T, Fujiwara Y . Haematopoietic stem cells retain long-term repopulating activity and multipotency in the absence of stem-cell leukaemia SCL/tal-1 gene. Nature. 2003; 421(6922):547-51. DOI: 10.1038/nature01345. View

Inlay M, Serwold T, Mosley A, Fathman J, Dimov I, Seita J . Identification of multipotent progenitors that emerge prior to hematopoietic stem cells in embryonic development. Stem Cell Reports. 2014; 2(4):457-72. PMC: 3986503. DOI: 10.1016/j.stemcr.2014.02.001. View

Souroullas G, Salmon J, Sablitzky F, Curtis D, Goodell M . Adult hematopoietic stem and progenitor cells require either Lyl1 or Scl for survival. Cell Stem Cell. 2009; 4(2):180-6. PMC: 2672304. DOI: 10.1016/j.stem.2009.01.001. View

Growney J, Shigematsu H, Li Z, Lee B, Adelsperger J, Rowan R . Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood. 2005; 106(2):494-504. PMC: 1895175. DOI: 10.1182/blood-2004-08-3280. View

Mikkola H, Orkin S . The journey of developing hematopoietic stem cells. Development. 2006; 133(19):3733-44. DOI: 10.1242/dev.02568. View

Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe A, Speck N . Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996; 93(8):3444-9. PMC: 39628. DOI: 10.1073/pnas.93.8.3444. View

10.

Eilken H, Nishikawa S, Schroeder T . Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature. 2009; 457(7231):896-900. DOI: 10.1038/nature07760. View

11.

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

12.

Shivdasani R, Mayer E, Orkin S . Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature. 1995; 373(6513):432-4. DOI: 10.1038/373432a0. View

13.

Mouta Carreira C, Nasser S, Di Tomaso E, Padera T, Boucher Y, Tomarev S . LYVE-1 is not restricted to the lymph vessels: expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis. Cancer Res. 2001; 61(22):8079-84. View

14.

Chen M, Li Y, De Obaldia M, Yang Q, Yzaguirre A, Yamada-Inagawa T . Erythroid/myeloid progenitors and hematopoietic stem cells originate from distinct populations of endothelial cells. Cell Stem Cell. 2011; 9(6):541-52. PMC: 3576591. DOI: 10.1016/j.stem.2011.10.003. View

15.

McKinney-Freeman S, Naveiras O, Yates F, Loewer S, Philitas M, Curran M . Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells. Blood. 2009; 114(2):268-78. PMC: 2714203. DOI: 10.1182/blood-2008-12-193888. View

16.

Schledzewski K, Falkowski M, Moldenhauer G, Metharom P, Kzhyshkowska J, Ganss R . Lymphatic endothelium-specific hyaluronan receptor LYVE-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of.... J Pathol. 2006; 209(1):67-77. DOI: 10.1002/path.1942. View

17.

Zeigler B, Sugiyama D, Chen M, Guo Y, Downs K, Speck N . The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential. Development. 2006; 133(21):4183-92. DOI: 10.1242/dev.02596. View

18.

Van Handel B, Montel-Hagen A, Sasidharan R, Nakano H, Ferrari R, Boogerd C . Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell. 2012; 150(3):590-605. PMC: 3624753. DOI: 10.1016/j.cell.2012.06.026. View

19.

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

20.

Benz C, Copley M, Kent D, Wohrer S, Cortes A, Aghaeepour N . Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem Cell. 2012; 10(3):273-83. DOI: 10.1016/j.stem.2012.02.007. View