An ATP-binding cassette transporter G2 (CgABCG2) regulates the haemocyte proliferation by modulating the G1/S phase transition of cell cycle in oyster Crassostrea gigas

ATP-binding cassette transporter G2 (ABCG2) is a half-transporter of the G subfamily in ATP-binding cassette transporters (ABC transporter), which is involved in the regulation of multidrug-resistant, cell cycle, and cell proliferation. In the present study, a homologue of ABCG2 (named as CgABCG2) w...

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Veröffentlicht in:Fish & shellfish immunology 2023-05, Vol.136, p.108441-108441, Article 108441
Hauptverfasser: Yu, Simiao, Qiao, Xue, Yang, Ying, Gu, Xiaoyu, Sun, Wending, Liu, Xiyang, Zhang, Dan, Wang, Lingling, Song, Linsheng
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container_title Fish & shellfish immunology
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creator Yu, Simiao
Qiao, Xue
Yang, Ying
Gu, Xiaoyu
Sun, Wending
Liu, Xiyang
Zhang, Dan
Wang, Lingling
Song, Linsheng
description ATP-binding cassette transporter G2 (ABCG2) is a half-transporter of the G subfamily in ATP-binding cassette transporters (ABC transporter), which is involved in the regulation of multidrug-resistant, cell cycle, and cell proliferation. In the present study, a homologue of ABCG2 (named as CgABCG2) with the conserved AAA domain and ABC2 membrane domain was identified from the Pacific oyster Crassostrea gigas. The open reading frame (ORF) of CgABCG2 was of 1956 bp encoding a predicted polypeptide of 652 amino acids, which shared 56.7%–65.7% sequence similarities with previously identified ABCG2s from other animals. The mRNA transcripts of CgABCG2 were detected in all the tested tissues with higher expression levels in gonad and haemocytes (19.31-fold and 11.23-fold of that in adductor muscle respectively, p 
doi_str_mv 10.1016/j.fsi.2022.11.029
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In the present study, a homologue of ABCG2 (named as CgABCG2) with the conserved AAA domain and ABC2 membrane domain was identified from the Pacific oyster Crassostrea gigas. The open reading frame (ORF) of CgABCG2 was of 1956 bp encoding a predicted polypeptide of 652 amino acids, which shared 56.7%–65.7% sequence similarities with previously identified ABCG2s from other animals. The mRNA transcripts of CgABCG2 were detected in all the tested tissues with higher expression levels in gonad and haemocytes (19.31-fold and 11.23-fold of that in adductor muscle respectively, p &lt; 0.05). CgABCG2 was mainly distributed on the cell membrane of the haemocytes with a partial distribution in the cytoplasm and nucleus. After Vibrio splendidus stimulation, the mRNA expression level of CgABCG2 in haemocytes was significantly up-regulated at 3 h and 6 h, which was 5.22-fold and 8.60-fold (p &lt; 0.05) of that in control, respectively. After the expression of CgABCG2 was interfered by RNAi, the number of cells with EdU positive signals was reduced in both haemocytes and the potential hematopoietic sites. And the mRNA expression level of CgPCNA, CgGATA3, CgRunx, CgSCL and CgC-kit decreased significantly (p &lt; 0.05), which were about 0.66-, 0.37-, 0.32-, 0.50-, and 0.50-fold of that in the negative control group, respectively. While the mRNA expression level of CgCDK2 increased significantly (1.84-fold to that in control, p &lt; 0.05) and that of stem cell-related factor CgSOX2 did not change significantly in the si-CgABCG2 oysters. Moreover, the cell cycle of haemocytes was detected by flow cytometry, which was arrested at G0/G1 phase in the si-CgABCG2 oysters. All the results collectively suggested that CgABCG2 might involve the proliferation of haemocytes by regulating the expression of haematopoiesis related transcription factors and the G1/S phase transition of the cell cycle in oyster C. gigas. •A homologue of ATP-binding cassette transporter G2 (ABCG2) was identified in Pacific oyster C. gigas.•The mRNA expression of CgABCG2 in haemocytes was significantly up-regulated post V. splendidus stimulation.•The inhibition of CgABCG2 reduced the expressions of haematopoiesis related transcription factors.•The cell cycle was arrested at G0/G1 phase and the cell proliferation was reduced in the si-CgABCG2 oysters.</description><identifier>ISSN: 1050-4648</identifier><identifier>EISSN: 1095-9947</identifier><identifier>DOI: 10.1016/j.fsi.2022.11.029</identifier><identifier>PMID: 36403705</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>ABC transporters ; Animals ; ATP-Binding cassette transporter G2 ; Cell Cycle ; cell membranes ; Cell Proliferation ; Crassostrea - genetics ; Crassostrea gigas ; cytoplasm ; domain ; fish ; flow cytometry ; gene expression ; Haemocytes ; hematopoiesis ; hemocytes ; Hemocytes - metabolism ; Immunity, Innate - genetics ; immunology ; multiple drug resistance ; muscles ; oysters ; phase transition ; polypeptides ; Proliferation ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; S Phase ; shellfish ; subfamily ; Vibrio splendidus</subject><ispartof>Fish &amp; shellfish immunology, 2023-05, Vol.136, p.108441-108441, Article 108441</ispartof><rights>2022 Elsevier Ltd</rights><rights>Copyright © 2022 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c386t-eb183011a787f9abe2af9b9b5d1dae5671562d6c43624602e19052f662923bcf3</citedby><cites>FETCH-LOGICAL-c386t-eb183011a787f9abe2af9b9b5d1dae5671562d6c43624602e19052f662923bcf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1050464822007744$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36403705$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Simiao</creatorcontrib><creatorcontrib>Qiao, Xue</creatorcontrib><creatorcontrib>Yang, Ying</creatorcontrib><creatorcontrib>Gu, Xiaoyu</creatorcontrib><creatorcontrib>Sun, Wending</creatorcontrib><creatorcontrib>Liu, Xiyang</creatorcontrib><creatorcontrib>Zhang, Dan</creatorcontrib><creatorcontrib>Wang, Lingling</creatorcontrib><creatorcontrib>Song, Linsheng</creatorcontrib><title>An ATP-binding cassette transporter G2 (CgABCG2) regulates the haemocyte proliferation by modulating the G1/S phase transition of cell cycle in oyster Crassostrea gigas</title><title>Fish &amp; shellfish immunology</title><addtitle>Fish Shellfish Immunol</addtitle><description>ATP-binding cassette transporter G2 (ABCG2) is a half-transporter of the G subfamily in ATP-binding cassette transporters (ABC transporter), which is involved in the regulation of multidrug-resistant, cell cycle, and cell proliferation. In the present study, a homologue of ABCG2 (named as CgABCG2) with the conserved AAA domain and ABC2 membrane domain was identified from the Pacific oyster Crassostrea gigas. The open reading frame (ORF) of CgABCG2 was of 1956 bp encoding a predicted polypeptide of 652 amino acids, which shared 56.7%–65.7% sequence similarities with previously identified ABCG2s from other animals. The mRNA transcripts of CgABCG2 were detected in all the tested tissues with higher expression levels in gonad and haemocytes (19.31-fold and 11.23-fold of that in adductor muscle respectively, p &lt; 0.05). CgABCG2 was mainly distributed on the cell membrane of the haemocytes with a partial distribution in the cytoplasm and nucleus. After Vibrio splendidus stimulation, the mRNA expression level of CgABCG2 in haemocytes was significantly up-regulated at 3 h and 6 h, which was 5.22-fold and 8.60-fold (p &lt; 0.05) of that in control, respectively. After the expression of CgABCG2 was interfered by RNAi, the number of cells with EdU positive signals was reduced in both haemocytes and the potential hematopoietic sites. And the mRNA expression level of CgPCNA, CgGATA3, CgRunx, CgSCL and CgC-kit decreased significantly (p &lt; 0.05), which were about 0.66-, 0.37-, 0.32-, 0.50-, and 0.50-fold of that in the negative control group, respectively. While the mRNA expression level of CgCDK2 increased significantly (1.84-fold to that in control, p &lt; 0.05) and that of stem cell-related factor CgSOX2 did not change significantly in the si-CgABCG2 oysters. Moreover, the cell cycle of haemocytes was detected by flow cytometry, which was arrested at G0/G1 phase in the si-CgABCG2 oysters. All the results collectively suggested that CgABCG2 might involve the proliferation of haemocytes by regulating the expression of haematopoiesis related transcription factors and the G1/S phase transition of the cell cycle in oyster C. gigas. •A homologue of ATP-binding cassette transporter G2 (ABCG2) was identified in Pacific oyster C. gigas.•The mRNA expression of CgABCG2 in haemocytes was significantly up-regulated post V. splendidus stimulation.•The inhibition of CgABCG2 reduced the expressions of haematopoiesis related transcription factors.•The cell cycle was arrested at G0/G1 phase and the cell proliferation was reduced in the si-CgABCG2 oysters.</description><subject>ABC transporters</subject><subject>Animals</subject><subject>ATP-Binding cassette transporter G2</subject><subject>Cell Cycle</subject><subject>cell membranes</subject><subject>Cell Proliferation</subject><subject>Crassostrea - genetics</subject><subject>Crassostrea gigas</subject><subject>cytoplasm</subject><subject>domain</subject><subject>fish</subject><subject>flow cytometry</subject><subject>gene expression</subject><subject>Haemocytes</subject><subject>hematopoiesis</subject><subject>hemocytes</subject><subject>Hemocytes - metabolism</subject><subject>Immunity, Innate - genetics</subject><subject>immunology</subject><subject>multiple drug resistance</subject><subject>muscles</subject><subject>oysters</subject><subject>phase transition</subject><subject>polypeptides</subject><subject>Proliferation</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>S Phase</subject><subject>shellfish</subject><subject>subfamily</subject><subject>Vibrio splendidus</subject><issn>1050-4648</issn><issn>1095-9947</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUGP1CAYhhujcdfVH-DFcFwP7fJBS4d4mm10NNlEE9czofRrh0lbRmBM-o_8mVJn9KgnCHnehw_eLHsNtAAK4u5Q9MEWjDJWABSUySfZNVBZ5VKW9dN1X9G8FOXmKnsRwoFSKrigz7MrLkrKa1pdZz-3M9k-fslbO3d2HojRIWCMSKLXczg6H9GTHSO3zbC9b3bsLfE4nEYdMZC4R7LXODmzpMDRu9H26HW0bibtQibXreBqXckd3H0lx70OF7f9zbmeGBxHYhYzIrHpYAnrlY1Pg7gQPWoy2EGHl9mzXo8BX13Wm-zbh_ePzcf84fPuU7N9yA3fiJhjCxtOAXS9qXupW2S6l61sqw46jZWooRKsE6bkgpWCMgRJK9YLwSTjren5TXZ79qb3fD9hiGqyYR1Rz-hOQXGo-KYsJa_-i7I6kRIAaELhjBrvQvDYq6O3k_aLAqrWLtVBpS7V2qUCUKnLlHlz0Z_aCbu_iT_lJeDdGcD0Hz8sehWMxdlgZz2aqDpn_6H_Bd1Mr9g</recordid><startdate>20230501</startdate><enddate>20230501</enddate><creator>Yu, Simiao</creator><creator>Qiao, Xue</creator><creator>Yang, Ying</creator><creator>Gu, Xiaoyu</creator><creator>Sun, Wending</creator><creator>Liu, Xiyang</creator><creator>Zhang, Dan</creator><creator>Wang, Lingling</creator><creator>Song, Linsheng</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20230501</creationdate><title>An ATP-binding cassette transporter G2 (CgABCG2) regulates the haemocyte proliferation by modulating the G1/S phase transition of cell cycle in oyster Crassostrea gigas</title><author>Yu, Simiao ; Qiao, Xue ; Yang, Ying ; Gu, Xiaoyu ; Sun, Wending ; Liu, Xiyang ; Zhang, Dan ; Wang, Lingling ; Song, Linsheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c386t-eb183011a787f9abe2af9b9b5d1dae5671562d6c43624602e19052f662923bcf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>ABC transporters</topic><topic>Animals</topic><topic>ATP-Binding cassette transporter G2</topic><topic>Cell Cycle</topic><topic>cell membranes</topic><topic>Cell Proliferation</topic><topic>Crassostrea - genetics</topic><topic>Crassostrea gigas</topic><topic>cytoplasm</topic><topic>domain</topic><topic>fish</topic><topic>flow cytometry</topic><topic>gene expression</topic><topic>Haemocytes</topic><topic>hematopoiesis</topic><topic>hemocytes</topic><topic>Hemocytes - metabolism</topic><topic>Immunity, Innate - genetics</topic><topic>immunology</topic><topic>multiple drug resistance</topic><topic>muscles</topic><topic>oysters</topic><topic>phase transition</topic><topic>polypeptides</topic><topic>Proliferation</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>S Phase</topic><topic>shellfish</topic><topic>subfamily</topic><topic>Vibrio splendidus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Simiao</creatorcontrib><creatorcontrib>Qiao, Xue</creatorcontrib><creatorcontrib>Yang, Ying</creatorcontrib><creatorcontrib>Gu, Xiaoyu</creatorcontrib><creatorcontrib>Sun, Wending</creatorcontrib><creatorcontrib>Liu, Xiyang</creatorcontrib><creatorcontrib>Zhang, Dan</creatorcontrib><creatorcontrib>Wang, Lingling</creatorcontrib><creatorcontrib>Song, Linsheng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Fish &amp; shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Simiao</au><au>Qiao, Xue</au><au>Yang, Ying</au><au>Gu, Xiaoyu</au><au>Sun, Wending</au><au>Liu, Xiyang</au><au>Zhang, Dan</au><au>Wang, Lingling</au><au>Song, Linsheng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An ATP-binding cassette transporter G2 (CgABCG2) regulates the haemocyte proliferation by modulating the G1/S phase transition of cell cycle in oyster Crassostrea gigas</atitle><jtitle>Fish &amp; shellfish immunology</jtitle><addtitle>Fish Shellfish Immunol</addtitle><date>2023-05-01</date><risdate>2023</risdate><volume>136</volume><spage>108441</spage><epage>108441</epage><pages>108441-108441</pages><artnum>108441</artnum><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>ATP-binding cassette transporter G2 (ABCG2) is a half-transporter of the G subfamily in ATP-binding cassette transporters (ABC transporter), which is involved in the regulation of multidrug-resistant, cell cycle, and cell proliferation. In the present study, a homologue of ABCG2 (named as CgABCG2) with the conserved AAA domain and ABC2 membrane domain was identified from the Pacific oyster Crassostrea gigas. The open reading frame (ORF) of CgABCG2 was of 1956 bp encoding a predicted polypeptide of 652 amino acids, which shared 56.7%–65.7% sequence similarities with previously identified ABCG2s from other animals. The mRNA transcripts of CgABCG2 were detected in all the tested tissues with higher expression levels in gonad and haemocytes (19.31-fold and 11.23-fold of that in adductor muscle respectively, p &lt; 0.05). CgABCG2 was mainly distributed on the cell membrane of the haemocytes with a partial distribution in the cytoplasm and nucleus. After Vibrio splendidus stimulation, the mRNA expression level of CgABCG2 in haemocytes was significantly up-regulated at 3 h and 6 h, which was 5.22-fold and 8.60-fold (p &lt; 0.05) of that in control, respectively. After the expression of CgABCG2 was interfered by RNAi, the number of cells with EdU positive signals was reduced in both haemocytes and the potential hematopoietic sites. And the mRNA expression level of CgPCNA, CgGATA3, CgRunx, CgSCL and CgC-kit decreased significantly (p &lt; 0.05), which were about 0.66-, 0.37-, 0.32-, 0.50-, and 0.50-fold of that in the negative control group, respectively. While the mRNA expression level of CgCDK2 increased significantly (1.84-fold to that in control, p &lt; 0.05) and that of stem cell-related factor CgSOX2 did not change significantly in the si-CgABCG2 oysters. Moreover, the cell cycle of haemocytes was detected by flow cytometry, which was arrested at G0/G1 phase in the si-CgABCG2 oysters. All the results collectively suggested that CgABCG2 might involve the proliferation of haemocytes by regulating the expression of haematopoiesis related transcription factors and the G1/S phase transition of the cell cycle in oyster C. gigas. •A homologue of ATP-binding cassette transporter G2 (ABCG2) was identified in Pacific oyster C. gigas.•The mRNA expression of CgABCG2 in haemocytes was significantly up-regulated post V. splendidus stimulation.•The inhibition of CgABCG2 reduced the expressions of haematopoiesis related transcription factors.•The cell cycle was arrested at G0/G1 phase and the cell proliferation was reduced in the si-CgABCG2 oysters.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>36403705</pmid><doi>10.1016/j.fsi.2022.11.029</doi><tpages>1</tpages></addata></record>
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subjects ABC transporters
Animals
ATP-Binding cassette transporter G2
Cell Cycle
cell membranes
Cell Proliferation
Crassostrea - genetics
Crassostrea gigas
cytoplasm
domain
fish
flow cytometry
gene expression
Haemocytes
hematopoiesis
hemocytes
Hemocytes - metabolism
Immunity, Innate - genetics
immunology
multiple drug resistance
muscles
oysters
phase transition
polypeptides
Proliferation
RNA, Messenger - genetics
RNA, Messenger - metabolism
S Phase
shellfish
subfamily
Vibrio splendidus
title An ATP-binding cassette transporter G2 (CgABCG2) regulates the haemocyte proliferation by modulating the G1/S phase transition of cell cycle in oyster Crassostrea gigas
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