Comparative Analysis of Megakaryocyte and Platelet Transcriptome Changes in Acute Infection

doi:10.19586/j.2095-2341.2023.0011

Current Biotechnology ›› 2023, Vol. 13 ›› Issue (3): 465-472.DOI: 10.19586/j.2095-2341.2023.0011

• Articles • Previous Articles Next Articles

Comparative Analysis of Megakaryocyte and Platelet Transcriptome Changes in Acute Infection

Qinqin LIU¹^,²(), Baiming HUANG¹^,², Yezi MA¹^,², Cuicui LIU¹^,², Hongtao WANG¹^,², Jiaxi ZHOU¹^,²()

^1.State Key Laboratory of Experimental Hematology，National Clinical Research Center for Blood Diseases，Haihe Laboratory of Cell Ecosystem，Institute of Hematology & Blood Diseases Hospital，Chinese Academy of Medical Sciences & Peking Union Medical College，Tianjin 300020，China
^2.Tianjin Institutes of Health Science，Tianjin 301600，China

Received:2023-02-07 Accepted:2023-03-31 Online:2023-05-25 Published:2023-06-12
Contact: Jiaxi ZHOU

急性感染条件下巨核细胞与血小板转录组变化的对比分析

刘勤勤¹^,²(), 黄柏铭¹^,², 马叶子¹^,², 刘翠翠¹^,², 王洪涛¹^,², 周家喜¹^,²()

^1.中国医学科学院血液病医院（中国医学科学院血液学研究所），北京协和医学院，实验血液学国家重点实验室，国家血液系统疾病临床医学研究中心，细胞生态海河实验室，天津 300020
^2.天津医学健康研究院，天津 301600

通讯作者: 周家喜
作者简介:刘勤勤 E-mail: liuqinqin@ihcams.ac.cn；
基金资助:
中国医学科学院医学与健康科技创新工程项目(2021-I2M-1-073);天津市自然科学基金项目(20JCYBJC00240);天津市科技计划青年项目(22JCQNJC01270);细胞生态海河实验室“揭榜挂帅”项目(HH22KYZX0031)

Abstract

Abstract:

Megakaryocytes and platelets are a group of parent-offspring cells in hematopoietic system. In the classical mode， rare large megakaryocytes release abundant anuclear small platelets into the peripheral blood through the shear force of blood flow， participating in hemostasis and coagulation. In recent years， with the development of separation and sequencing technology， the exploration of the function and molecular characteristics of megakaryocyte and platelet has been deepening， but the relationship between the two on molecular level has not been analyzed in detail. Based on the transcriptome data of bone marrow megakaryocytes and platelets of mice infected by Escherichia coli reported by our group， this study compared the transcriptomic changes of megakaryocytes and platelets after acute infection. The results found that the change of megakaryocyte transcriptome after acute infection was weaker than that of platelets， and the involved genes were different. The genes up-regulated by both megakaryocytes and platelets after infection were mainly enriched by the function of antigen presentation. Besides，the number of genes up-regulated in platelet specifically was much higher than that in megakaryocyte， which mainly enrich the biology process of cell localization， transport， inflammatory reaction and platelet activation. This study provided data support for exploring the RNA inheritance relationship between megakaryocyte and platelet and the functional diversity of platelets.

Key words: megakaryocyte, platelet, acute infection, transcriptome

摘要：

巨核细胞与血小板是造血系统中一组独特的亲子细胞。经典模式下，数量少且体积大的巨核细胞借助血流剪切力释放大量体积小且无核的血小板进入外周血，参与机体止凝血等过程。近年来，随着细胞分离与组学技术的发展，领域内对于巨核细胞和血小板分子特征的探索不断深入，但目前对于两者在分子水平关系上的研究相对有限。利用近期报道的大肠杆菌急性感染条件下小鼠骨髓巨核细胞和血小板的转录组数据，对感染后巨核细胞和血小板转录组的变化进行了对比分析。结果发现，感染后巨核细胞转录组的变化程度弱于血小板，且二者变化的基因存在差异。感染后巨核细胞和血小板共同上调的基因主要富集了抗原呈递的功能。血小板特异性上调基因的数量远高于巨核细胞特异性上调的基因及二者共同上调的基因，主要富集了细胞定植、转运、炎症反应及血小板活化等生物学过程。研究结果为探究巨核细胞和血小板的RNA继承关系及血小板的功能多样性提供了重要的数据支撑。

关键词: 巨核细胞, 血小板, 急性感染, 转录组

CLC Number:

R394

Qinqin LIU, Baiming HUANG, Yezi MA, Cuicui LIU, Hongtao WANG, Jiaxi ZHOU. Comparative Analysis of Megakaryocyte and Platelet Transcriptome Changes in Acute Infection[J]. Current Biotechnology, 2023, 13(3): 465-472.

刘勤勤, 黄柏铭, 马叶子, 刘翠翠, 王洪涛, 周家喜. 急性感染条件下巨核细胞与血小板转录组变化的对比分析[J]. 生物技术进展, 2023, 13(3): 465-472.

Figures/Tables 4

Fig. 1 Transcriptome changes of bone marrow megakaryocytes after acute infection

Fig. 2 Effect of megakaryocyte transcriptome changes on platelet molecular characteristics in acute infection

Fig. 3 Comparative analysis of up-regulated genes in megakaryocytes and platelets under acute infection

Fig. 4 Comparative analysis of down-regulated genes in megakaryocytes and platelets under acute infection

References 27

1	EBAUGH F G, BIRD R M. The normal megakaryocyte concentration in aspirated human bone marrow[J]. Blood, 1951, 6(1): 75-80.
2	KOUPENOVA M, LIVADA A C, MORRELL C N. Platelet and megakaryocyte roles in innate and adaptive immunity[J]. Circ. Res., 2022, 130(2): 288-308.
3	BRAUN A, MAMMADOVA-BACH E. GALE force in platelet production[J]. Blood, 2023, 141(4): 330-331.
4	JUNT T, SCHULZE H, CHEN Z, et al.. Dynamic visualization of thrombopoiesis within bone marrow[J]. Science, 2007, 317(5845): 1767-1770.
5	LIU C, HUANG B, WANG H, et al.. The heterogeneity of megakaryocytes and platelets and implications for ex vivo platelet generation[J]. Stem Cells Transl. Med., 2021, 10(12): 1614-1620.
6	MARGRAF A, NUSSBAUM C, SPERANDIO M. Ontogeny of platelet function[J]. Blood Adv., 2019, 3(4): 692-703.
7	VIEIRA-DE-ABREU A, CAMPBELL R A, WEYRICH A S, et al.. Platelets: versatile effector cells in hemostasis, inflammation, and the immune continuum[J]. Semin. Immunopathol., 2012, 34(1): 5-30.
8	XU X R, ZHANG D, OSWALD B E, et al.. Platelets are versatile cells: new discoveries in hemostasis, thrombosis, immune responses, tumor metastasis and beyond[J]. Crit. Rev. Clin. Lab. Sci., 2016, 53(6): 409-430.
9	SHIRAKI R, INOUE N, KAWASAKI S, et al.. Expression of Toll-like receptors on human platelets[J]. Thromb. Res., 2004, 113(6): 379-385.
10	CUNIN P, NIGROVIC P A. Megakaryocytes as immune cells[J]. J. Leukocyte Biol., 2019, 105(6): 1111-1121.
11	ZUFFEREY A, SPECK E R, MACHLUS K R, et al.. Mature murine megakaryocytes present antigen-MHC class I molecules to T cells and transfer them to platelets[J]. Blood Adv., 2017, 1(20): 1773-1785.
12	BRAY P F, MCKENZIE S E, EDELSTEIN L C, et al.. The complex transcriptional landscape of the anucleate human platelet[J]. BMC Genomics, 2013, 14(1): 1-15.
13	HARRISON P, GOODALL A H. "Message in the platelet"--more than just vestigial mRNA![J]. Platelets, 2008, 19(6): 395-404.
14	HILLE L, CEDERQVIST M, HROMEK J, et al.. Evaluation of an alternative staining method using SYTO 13 to determine reticulated platelets[J]. Thromb. Haemost., 2019, 119(5): 779-785.
15	D'AMBROSI S, NILSSON R J, WURDINGER T. Platelets and tumor-associated RNA transfer[J]. Blood, 2021, 137(23): 3181-3191.
16	SUN Z Q, XIA M J, ZHENG L, et al.. The biological characteristics and transcriptome changes of platelets in the mouse peritonitis model[J]. Curr. Biotechnol., 2021, 11(3): 378-385.
17	LIU C, WU D, XIA M, et al.. Characterization of cellular heterogeneity and an immune subpopulation of human megakaryocytes[J/OL]. Adv. Sci., 2021, 8(15): e2100921[2021-05-26]. .
18	XIE X, SHI Q, WU P, et al.. Single-cell transcriptome profiling reveals neutrophil heterogeneity in homeostasis and infection[J]. Nat. Immunol., 2020, 21(9): 1119-1133.
19	JIANG H, YU Z, DING N, et al.. The role of AGK in thrombocytopoiesis and possible therapeutic strategies[J]. Blood, 2020, 136(1): 119-129.
20	EATON N, BOYD E K, BISWAS R, et al.. Endocytosis of the thrombopoietin receptor Mpl regulates megakaryocyte and erythroid maturation in mice[J/OL]. Front. Oncol., 2022, 12: 959806[2022-08-30]. .
21	MANNE B K, DENORME F, MIDDLETON E A, et al.. Platelet gene expression and function in patients with COVID-19[J]. Blood, 2020, 136(11): 1317-1329.
22	PARISER D N, HILT Z T, TURE S K, et al.. Lung megakaryocytes are immune modulatory cells[J/OL]. J. Clin. Invest., 2021, 131:1[2020-10-20]. .
23	YEUNG A K, VILLACORTA-MARTIN C, HON S, et al.. Lung megakaryocytes display distinct transcriptional and phenotypic properties[J]. Blood Adv., 2020, 4(24): 6204-6217.
24	孙志强,夏美娟,郑琳,等.小鼠腹膜炎模型下血小板的生物学特征及其转录组变化[J].生物技术进展,2021,11(3):378-385.
25	WANG H, HE J, XU C, et al.. Decoding human megakaryocyte development[J]. Cell Stem Cell, 2021, 28(3): 535-549.
26	SUN S, JIN C, SI J, et al.. Single-cell analysis of ploidy and the transcriptome reveals functional and spatial divergency in murine megakaryopoiesis[J]. Blood, 2021, 138(14): 1211-1224.
27	李敏敏,夏美娟,赵晶晶,等.人类胚胎期和成年期巨核细胞的分子特征比较[J].生物技术进展,2022,12(4):577-583.

[1]	Yifei CAI, Yezi MA, Meijuan XIA, Cuicui LIU, Hongtao WANG, Jiaxi ZHOU. Analysis of Molecular Characteristics of Megakaryocytes Between Embryonic Aorta-gonad-mesonephros and Adult Bone Marrow [J]. Current Biotechnology, 2025, 15(4): 702-710.
[2]	AYELHAN·Haysa, Fei JIAO, Hong LIU, ANASI·Hudelati, Yubang SHEN. Integrating GWAS and Transcriptome Profiling to Identify SNP Markers Linked to High-temperature Tolerance in Esox lucius [J]. Current Biotechnology, 2025, 15(3): 432-445.
[3]	Zhuoying LIU, Xiaojin ZHOU, Yanli HUANG, Sen PANG. Joint Transcriptome Analysis of Maize Under Salt Stress and MeJA Treatment [J]. Current Biotechnology, 2025, 15(2): 263-275.
[4]	Yezi MA, Meijuan XIA, Cuicui LIU, Hongtao WANG, Jiaxi ZHOU. Comparative Analysis of Platelet Transcriptome and Proteome Changes in SARS-CoV2 Omicron Infection [J]. Current Biotechnology, 2024, 14(4): 649-656.
[5]	Hui ZHANG, Bobo LIU, Fengmei LI, Jian CUI. Study on the Involvement of Auxin Signaling Pathway in Response to Powdery Mildew Stress in Pumpkin [J]. Current Biotechnology, 2024, 14(3): 433-441.
[6]	Hongmei QIAO. Transcriptome Analysis of the Terrestrial Plant Carallia brachiata from Rhizophoraceae [J]. Current Biotechnology, 2024, 14(2): 228-236.
[7]	Caihong WANG, Yuhan SHAO, Mengyuan JIANG. The Mechanisms of IL-17 Inhibiting Pseudomonas aeruginosa Infection on Lung Epithelial Cells [J]. Current Biotechnology, 2024, 14(2): 304-311.
[8]	Di WANG, Yanhong ZHAO, Yipeng LIANG, Haoze SONG, Lihong SHI, Jingyuan TONG. Research on the Function of CXCL2 During Megakaryocyte Differentiation [J]. Current Biotechnology, 2023, 13(2): 257-263.
[9]	Minmin LI, Meijuan XIA, Jingjing ZHAO, Xiaoyuan CHEN, Cuicui LIU, Pei SU, Hongtao WANG, Jiaxi ZHOU. Comparison of the Molecular Characteristics of Human Megakaryocytes Between Embryonic Stage and Adult Stage [J]. Current Biotechnology, 2022, 12(4): 577-583.
[10]	Dongao LI, Huiquan LIU, Qinhu WANG. Research Progress on Wheat Transcriptomes Responsive to Fusarium graminearum Infection [J]. Current Biotechnology, 2021, 11(5): 610-617.
[11]	SUN Zhiqiang, XIA Meijuan, ZHENG Lin, ZHAO Jingjing, SU Pei, WANG Hongtao, ZHOU Jiaxi, LIU Cuicui^* . The Biological Characteristics and Transcriptome Changes of Platelets in the Mouse Peritonitis Model [J]. Curr. Biotech., 2021, 11(3): 378-385.
[12]	XING Hengte, QIU Bo^*. Progress on the Application of Platelet-rich Plasma Injection in Knee Osteoarthritis [J]. Curr. Biotech., 2021, 11(2): 163-169.
[13]	FANG Hanshun1,2, XIE Yongdun2, ZENG Weiwei2, GUO Huijun2, XIONG Hongchun2, ZHAO Linshu2, GU Jiayu2, XU Yanhao1, LIU Luxiang2. The Transcriptome Analysis of Wheat Dwarf Mutant jm22d Responding to GA Treatment [J]. Curr. Biotech., 2020, 10(5): 503-516.

Comparative Analysis of Megakaryocyte and Platelet Transcriptome Changes in Acute Infection

急性感染条件下巨核细胞与血小板转录组变化的对比分析

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 4

References 27

Related Articles 13

Recommended Articles

Metrics

Comments