Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac

Mingjiang Xu, Sahoko Matsuoka, Feng-Chun Yang, Yasuhiro Ebihara, Atsushi Manabe, Ryuhei Tanaka, Mitsuoki Eguchi, Shigetaka Asano, Tatsutoshi Nakahata, Kohichiro Tsuji

Research output: Contribution to journalArticle

74 Citations (Scopus)

Abstract

During mouse embryogenesis, primitive erythropoiesis occurs in blood islands of the yolk sac (YS) on the seventh day of gestation. This study demonstrated for the first time the presence of unique primitive megakaryocytic (Mk) progenitors in the early YS, which disappeared by 13.5 days postcoitum (dpc). When 7.5 dpc YS cells were incubated in the presence of stem cell factor (SCF), interleukin (IL)-3, IL-6, erythropoietin (EPO), thrombopoietin (TPO), and granulocyte colony-stimulating factor in methylcellulose clonal culture, not only erythroid bursts but also megakaryocyte colonies were observed. The megakaryocytes in the colonies matured to proplatelet stages and produced platelets as early as day 3 of culture, much earlier than those from adult bone marrow, although their ploidy class was lower. These megakaryocytes were stained with acetylcholine esterase, and expressed platelet glycoprotein (GP)Ibβ, GPIIIa, and platelet factor 4 by reverse transcription-polymerase chain reaction analysis. The analysis of hemoglobin types in erythrocytes obtained from hematopoietic multilineage colonies containing the megakaryocytes indicated that the Mk progenitors originated from primitive hematopoiesis. The primitive Mk progenitors formed colonies in the absence of any cytokines in fetal bovine serum (FBS)-containing culture, and SCF, IL-3, EPO, and TPO significantly enhanced the Mk colony formation. In FBS-free culture, however, no colony formation was induced without these cytokines. Because megakaryocytes were detected in 8.5-dpc YS, these unique primitive Mk progenitors may rapidly mature and give rise to platelets to prevent hemorrhage in the simultaneously developing blood vessels until definitive hematopoiesis begins to produce platelets.

Original languageEnglish (US)
Pages (from-to)2016-2022
Number of pages7
JournalBlood
Volume97
Issue number7
DOIs
StatePublished - Apr 1 2001
Externally publishedYes

Fingerprint

Yolk Sac
Megakaryocytes
Platelets
Thrombopoietin
Stem Cell Factor
Interleukin-3
Erythropoietin
Blood Platelets
Platelet Glycoprotein GPIb-IX Complex
Cytokines
Platelet Membrane Glycoproteins
Platelet Factor 4
Hematopoiesis
Methylcellulose
Polymerase chain reaction
Blood vessels
Granulocyte Colony-Stimulating Factor
Esterases
Transcription
Acetylcholine

ASJC Scopus subject areas

  • Hematology

Cite this

Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac. / Xu, Mingjiang; Matsuoka, Sahoko; Yang, Feng-Chun; Ebihara, Yasuhiro; Manabe, Atsushi; Tanaka, Ryuhei; Eguchi, Mitsuoki; Asano, Shigetaka; Nakahata, Tatsutoshi; Tsuji, Kohichiro.

In: Blood, Vol. 97, No. 7, 01.04.2001, p. 2016-2022.

Research output: Contribution to journalArticle

Xu, M, Matsuoka, S, Yang, F-C, Ebihara, Y, Manabe, A, Tanaka, R, Eguchi, M, Asano, S, Nakahata, T & Tsuji, K 2001, 'Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac', Blood, vol. 97, no. 7, pp. 2016-2022. https://doi.org/10.1182/blood.V97.7.2016
Xu, Mingjiang ; Matsuoka, Sahoko ; Yang, Feng-Chun ; Ebihara, Yasuhiro ; Manabe, Atsushi ; Tanaka, Ryuhei ; Eguchi, Mitsuoki ; Asano, Shigetaka ; Nakahata, Tatsutoshi ; Tsuji, Kohichiro. / Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac. In: Blood. 2001 ; Vol. 97, No. 7. pp. 2016-2022.
@article{a1c1fcf84a1f4565a1e8492eb6635240,
title = "Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac",
abstract = "During mouse embryogenesis, primitive erythropoiesis occurs in blood islands of the yolk sac (YS) on the seventh day of gestation. This study demonstrated for the first time the presence of unique primitive megakaryocytic (Mk) progenitors in the early YS, which disappeared by 13.5 days postcoitum (dpc). When 7.5 dpc YS cells were incubated in the presence of stem cell factor (SCF), interleukin (IL)-3, IL-6, erythropoietin (EPO), thrombopoietin (TPO), and granulocyte colony-stimulating factor in methylcellulose clonal culture, not only erythroid bursts but also megakaryocyte colonies were observed. The megakaryocytes in the colonies matured to proplatelet stages and produced platelets as early as day 3 of culture, much earlier than those from adult bone marrow, although their ploidy class was lower. These megakaryocytes were stained with acetylcholine esterase, and expressed platelet glycoprotein (GP)Ibβ, GPIIIa, and platelet factor 4 by reverse transcription-polymerase chain reaction analysis. The analysis of hemoglobin types in erythrocytes obtained from hematopoietic multilineage colonies containing the megakaryocytes indicated that the Mk progenitors originated from primitive hematopoiesis. The primitive Mk progenitors formed colonies in the absence of any cytokines in fetal bovine serum (FBS)-containing culture, and SCF, IL-3, EPO, and TPO significantly enhanced the Mk colony formation. In FBS-free culture, however, no colony formation was induced without these cytokines. Because megakaryocytes were detected in 8.5-dpc YS, these unique primitive Mk progenitors may rapidly mature and give rise to platelets to prevent hemorrhage in the simultaneously developing blood vessels until definitive hematopoiesis begins to produce platelets.",
author = "Mingjiang Xu and Sahoko Matsuoka and Feng-Chun Yang and Yasuhiro Ebihara and Atsushi Manabe and Ryuhei Tanaka and Mitsuoki Eguchi and Shigetaka Asano and Tatsutoshi Nakahata and Kohichiro Tsuji",
year = "2001",
month = "4",
day = "1",
doi = "10.1182/blood.V97.7.2016",
language = "English (US)",
volume = "97",
pages = "2016--2022",
journal = "Blood",
issn = "0006-4971",
publisher = "American Society of Hematology",
number = "7",

}

TY - JOUR

T1 - Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac

AU - Xu, Mingjiang

AU - Matsuoka, Sahoko

AU - Yang, Feng-Chun

AU - Ebihara, Yasuhiro

AU - Manabe, Atsushi

AU - Tanaka, Ryuhei

AU - Eguchi, Mitsuoki

AU - Asano, Shigetaka

AU - Nakahata, Tatsutoshi

AU - Tsuji, Kohichiro

PY - 2001/4/1

Y1 - 2001/4/1

N2 - During mouse embryogenesis, primitive erythropoiesis occurs in blood islands of the yolk sac (YS) on the seventh day of gestation. This study demonstrated for the first time the presence of unique primitive megakaryocytic (Mk) progenitors in the early YS, which disappeared by 13.5 days postcoitum (dpc). When 7.5 dpc YS cells were incubated in the presence of stem cell factor (SCF), interleukin (IL)-3, IL-6, erythropoietin (EPO), thrombopoietin (TPO), and granulocyte colony-stimulating factor in methylcellulose clonal culture, not only erythroid bursts but also megakaryocyte colonies were observed. The megakaryocytes in the colonies matured to proplatelet stages and produced platelets as early as day 3 of culture, much earlier than those from adult bone marrow, although their ploidy class was lower. These megakaryocytes were stained with acetylcholine esterase, and expressed platelet glycoprotein (GP)Ibβ, GPIIIa, and platelet factor 4 by reverse transcription-polymerase chain reaction analysis. The analysis of hemoglobin types in erythrocytes obtained from hematopoietic multilineage colonies containing the megakaryocytes indicated that the Mk progenitors originated from primitive hematopoiesis. The primitive Mk progenitors formed colonies in the absence of any cytokines in fetal bovine serum (FBS)-containing culture, and SCF, IL-3, EPO, and TPO significantly enhanced the Mk colony formation. In FBS-free culture, however, no colony formation was induced without these cytokines. Because megakaryocytes were detected in 8.5-dpc YS, these unique primitive Mk progenitors may rapidly mature and give rise to platelets to prevent hemorrhage in the simultaneously developing blood vessels until definitive hematopoiesis begins to produce platelets.

AB - During mouse embryogenesis, primitive erythropoiesis occurs in blood islands of the yolk sac (YS) on the seventh day of gestation. This study demonstrated for the first time the presence of unique primitive megakaryocytic (Mk) progenitors in the early YS, which disappeared by 13.5 days postcoitum (dpc). When 7.5 dpc YS cells were incubated in the presence of stem cell factor (SCF), interleukin (IL)-3, IL-6, erythropoietin (EPO), thrombopoietin (TPO), and granulocyte colony-stimulating factor in methylcellulose clonal culture, not only erythroid bursts but also megakaryocyte colonies were observed. The megakaryocytes in the colonies matured to proplatelet stages and produced platelets as early as day 3 of culture, much earlier than those from adult bone marrow, although their ploidy class was lower. These megakaryocytes were stained with acetylcholine esterase, and expressed platelet glycoprotein (GP)Ibβ, GPIIIa, and platelet factor 4 by reverse transcription-polymerase chain reaction analysis. The analysis of hemoglobin types in erythrocytes obtained from hematopoietic multilineage colonies containing the megakaryocytes indicated that the Mk progenitors originated from primitive hematopoiesis. The primitive Mk progenitors formed colonies in the absence of any cytokines in fetal bovine serum (FBS)-containing culture, and SCF, IL-3, EPO, and TPO significantly enhanced the Mk colony formation. In FBS-free culture, however, no colony formation was induced without these cytokines. Because megakaryocytes were detected in 8.5-dpc YS, these unique primitive Mk progenitors may rapidly mature and give rise to platelets to prevent hemorrhage in the simultaneously developing blood vessels until definitive hematopoiesis begins to produce platelets.

UR - http://www.scopus.com/inward/record.url?scp=0035313155&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0035313155&partnerID=8YFLogxK

U2 - 10.1182/blood.V97.7.2016

DO - 10.1182/blood.V97.7.2016

M3 - Article

C2 - 11264166

AN - SCOPUS:0035313155

VL - 97

SP - 2016

EP - 2022

JO - Blood

JF - Blood

SN - 0006-4971

IS - 7

ER -