猪耳成纤维细胞转录组异质性及对核移植胚胎发育的潜在影响

doi:10.16288/j.yczz.20-190

遗传 ›› 2020, Vol. 42 ›› Issue (9): 898-915.doi: 10.16288/j.yczz.20-190

猪耳成纤维细胞转录组异质性及对核移植胚胎发育的潜在影响

周俊¹, 赵成成¹, 吴霄¹, 石俊松², 周荣², 吴珍芳¹, 李紫聪¹()

^1. 华南农业大学动物科学院，国家生猪种业工程技术研究中心，广州 510642
^2. 广东温氏种猪科技有限公司，新兴 527400

收稿日期:2020-06-22 修回日期:2020-08-11 出版日期:2020-09-20 发布日期:2020-08-31
通讯作者: 李紫聪 E-mail:lizicongcong@163.com
作者简介:周俊,在读硕士研究生,专业方向：动物遗传育种与繁殖。E-mail: 374949357@qq.com
基金资助:
广东省乡村振兴战略专项(2018年)资助

Transcriptome heterogeneity of porcine ear fibroblast and its potential influence on embryo development in nuclear transplantation

Jun Zhou¹, Chengcheng Zhao¹, Xiao Wu¹, Junsong Shi², Rong Zhou², Zhenfang Wu¹, Zicong Li¹()

^1. National Engineering Research Center for Swine Breeding Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, China
^2. Guangdong Wenshi breeding pig Technology Co., Ltd，Xinxing 527400, China

Received:2020-06-22 Revised:2020-08-11 Online:2020-09-20 Published:2020-08-31
Contact: Li Zicong E-mail:lizicongcong@163.com
Supported by:
Supported by Guangdong Provincial Promotion Project on Preservation and Utilization of Local Breed of Livestock and Poultry (2018)

摘要/Abstract

摘要：

同一来源的供体细胞之间存在异质性。许多研究已经表明体细胞核移植(somatic cell nuclear transfer, SCNT)效率与供体细胞有关。然而,鲜有在单细胞水平分析供体细胞异质性对核移植效率的潜在影响。本研究利用单细胞转录组测序技术对同一来源且随机挑选的52个猪耳组织成纤维细胞进行测序分析。结果表明有48个单细胞的基因表达模式相似,4个单细胞(编号为D11_1、D12_1、DW61_2和DW99_2)的基因表达模式与其他单细胞存在较大的差异,并且不存在基因表达模式完全相同的两个单细胞。以基因表达模式相似的48个单细胞作为对照,进一步分析了单细胞D11_1、D12_1、DW61_2和DW99_2的差异基因表达模式：首先利用R语言筛选4个单细胞的差异表达基因,并对前50差异表达基因进行汇总;然后对差异表达基因进行GO富集分析和KEGG通路分析。富集分析发现差异表达基因的主要分子功能包括能量代谢、蛋白质代谢和细胞对刺激的反应等;主要通路包括KEGG中富集的与细胞周期、细胞代谢、DNA复制相关的通路。根据以上研究结果并结合SCNT研究进展讨论了4个单细胞的差异基因表达模式对核移植胚胎发育效率的潜在影响。本研究揭示了猪耳组织成纤维细胞的转录组异质性,并提供了分析精英供体细胞的一种有效方法,为提高克隆效率带来新的思路。

关键词: 猪, 体细胞核移植, 供体细胞, 异质性, 单细胞测序

Abstract:

There is heterogeneity among donor cells of the same source. Many studies have shown that donor cell affects the efficiency of somatic cell nuclear transfer (SCNT). However, the potential influence of donor cell heterogeneity on the efficiency of nuclear transplantation were rarely analyzed at the single-cell level. In this study, single-cell transcriptome sequencing was performed on 52 porcine ear fibroblasts randomly selected from the same source to compare their gene expression patterns. The results showed that 48 cells had similar gene expression patterns, whereas 4 cells (D11_1, D12_1, DW61_2, DW99_2) had significantly different gene expression patterns from those of other cells. There were no two cells with identical gene expression patterns. The gene expression patterns of D11_1, D12_1, DW61_2 and DW99_2 were analyzed, using the 48 cells with similar gene expression patterns as controls. Firstly, we used the R language statistics to select the differentially expressed genes in the 4 single cells, and identified the top 50 most significant differentially expressed genes. Then GO enrichment analysis and KEGG pathway analysis were performed on the differentially expressed genes. Enrichment analysis revealed that the main molecular functions of the differentially expressed genes included energy metabolism, protein metabolism and cell response to stimulation. The main pathways from KEGG enrichment were related to cell cycle, cell metabolism, and DNA replication. Finally, based on the above results and in consideration with the SCNT research progress, we discussed the potential effects of differential gene expression patterns of the 4 single cells on the embryonic development efficiency of nuclear transplantation. This study revealed transcriptional heterogeneity of porcine ear tissue fibroblasts and provided an effective method to analyze elite donor cells, thereby providing new ideas on improving the cloning efficiency of SCNT.

Key words: pigs, SCNT, donor cell, heterogeneity, single-cell sequencing

周俊, 赵成成, 吴霄, 石俊松, 周荣, 吴珍芳, 李紫聪. 猪耳成纤维细胞转录组异质性及对核移植胚胎发育的潜在影响[J]. 遗传, 2020, 42(9): 898-915.

Jun Zhou, Chengcheng Zhao, Xiao Wu, Junsong Shi, Rong Zhou, Zhenfang Wu, Zicong Li. Transcriptome heterogeneity of porcine ear fibroblast and its potential influence on embryo development in nuclear transplantation[J]. Hereditas(Beijing), 2020, 42(9): 898-915.

图/表 11

表1

图1

图2

图3

图4

表2

D11_1前50个差异最显著的基因信息"

基因	基因全称	表达情况
TMEM198	Transmembrane protein 198	↑
ALDOB	Aldolase, fructose-bisphosphate B	↑
UMOD	Uromodulin	↑
ASS1	Argininosuccinate synthase 1	↑
SLC5A12	Solute carrier family 5 member 12	↑
SLC34A1	Sus scrofa solute carrier family 34 member 1 (SLC34A1), mRNA	↑
AGR2	Anterior gradient protein 2 homolog precursor	↑
U6	U6 spliceosomal RNA	↑
BHMT	Betaine-homocysteine S-methyltransferase 1	↑
DDC	Dopa decarboxylase	↑
DAO	D-amino-acid oxidase	↑
SLC13A3	Solute carrier family 13 member 3	↑
CDH16	Cadherin 16	↑
CYP2D25	Vitamin D(3) 25-hydroxylase	↑
PPARGC1B	PPARG coactivator 1 beta	↑
FBP1	Fructose-1,6-bisphosphatase 1	↑
G6PC	Glucose-6-phosphatase	↑
CLDN2	Claudin-2	↑
DMGDH	Dimethylglycine dehydrogenase	↑
FMO1	Dimethylaniline monooxygenase [N-oxide-forming] 1	↑
UPP2	Uridine phosphorylase 2	↑
CYP4A24	Sus scrofa cytochrome P450,family 4,subfamily A,polypeptide 21 (CYP4A21), mRNA	↑
HNF4A	Hepatocyte nuclear factor 4-alpha	↑
ADSL	Adenylosuccinate lyase	↓
IGFBP6	Insulin-like growth factor-binding protein 6 precursor	↓
ORMDL2	ORMDL sphingolipid biosynthesis regulator 2	↓
MRPS35	Mitochondrial ribosomal protein S35	↓
TM7SF3	Transmembrane 7 superfamily member 3	↓
DERA	Deoxyribose-phosphate aldolase	↓
LTBR	Tumor necrosis factor receptor superfamily member 3 precursor	↓
TULP3	Tubby like protein 3	↓
PPHLN1	Periphilin 1	↓
PUS7L	Pseudouridylate synthase 7 like	↓
SLC38A1	Solute carrier family 38 member 1	↓
NEDD1	Neural precursor cell expressed, developmentally down-regulated 1	↓
SELENOO	Sus scrofa selenoprotein O (SELENOO), mRNA	↓
SLC35B3	Solute carrier family 35 member B3	↓
FAM8A1	Family with sequence similarity 8 member A1	↓
MBOAT1	Membrane bound O-acyltransferase domain containing 1	↓
novel gene	Lysosomal thioesterase PPT2 precursor	↓
MAN2A2	Mannosidase alpha class 2A member 2	↓
HMG20A	High mobility group 20A	↓
CSPG4	Chondroitin sulfate proteoglycan 4	↓
SRP54	Signal recognition particle 54	↓
FOS	Proto-oncogene c-Fos	↓
SPTLC2	Serine palmitoyltransferase long chain base subunit 2	↓
ATXN3	Ataxin-3	↓

表2

表3

D12_1前50个差异最显著的基因概况"

基因	基因全称	表达情况
PARVG	Gamma-parvin	↑
POU3F1	POU class 3 homeobox 1	↑
ASS1	Argininosuccinate synthase 1	↑
UMOD	Uromodulin	↑
PNMA2	Paraneoplastic Ma antigen 2	↑
ADGRG7	Adhesion G protein-coupled receptor G7	↑
KRT28	Keratin 28	↑
GSDMB	Gasdermin B	↑
U6	U6 spliceosomal RNA	↑
RNF223	Ring finger protein 223	↑
TBX10	T-box 10	↑
TMPRSS2	Transmembrane protease, serine 12	↑
HTR1E	5-hydroxytryptamine receptor 1E	↑
HIC2	HIC ZBTB transcriptional repressor 2	↑
SLC34A1	Sus scrofa solute carrier family 34 member 1 (SLC34A1), mRNA.	↑
ALDOB	Aldolase, fructose-bisphosphate B	↑
CSN1S1	Sus scrofa casein alpha s1 (CSN1S1), mRNA.	↑
SLC2A12	Solute carrier family 2 member 12	↑
CD53	CD53 molecule	↑
NAGA	Alpha-N-acetylgalactosaminidase precursor	↓
ADSL	Adenylosuccinate lyase	↓
C12orf4	Homolog isoform 2	↓
SLC35B3	Solute carrier family 35 member B3	↓
LEMD2	LEM domain containing 2	↓
GOLGA5	Golgin A5	↓
GSTA4	Glutathione S-transferase A4	↓
FAM98C	Family with sequence similarity 98 member C	↓
LDLRAP1	Low density lipoprotein receptor adaptor protein 1	↓
PLK3	Polo like kinase 3	↓
SMOC2	SPARC related modular calcium binding 2	↓
SPG21	Sus scrofa spastic paraplegia 21 (autosomal recessive, Mast syndrome) (SPG21), mRNA	↓
PCLAF	Sus scrofa PCNA-associated factor (LOC100514810), mRNA	↓
SERPIN2	Serpin family B member 2	↓
AEN	Apoptosis enhancing nuclease	↓
GCNT1	Glucosaminyl (N-acetyl) transferase 1, core 2	↓
PPP6C	Serine/threonine-protein phosphatase 6 catalytic subunit	↓
PCSK6	Proprotein convertase subtilisin/kexin type 6	↓
BOP1	Block of proliferation 1	↓
FAM49B	Protein FAM49B	↓
PLAT	Tissue-type plasminogen activator precursor	↓
SMOX	Spermine oxidase	↓
ASPN	Asporin precursor	↓
IL1R1	Interleukin 1 receptor type 1	↓

表3

表4

DW61_2前50个差异最显著的基因概况"

基因	基因全称	表达情况
NPPB	Natriuretic peptides B Brain natriuretic peptide 32 Brain natriuretic peptide 26	↑
GRIK2	Glutamate ionotropic receptor kainate type subunit 2	↑
PAX1	Paired box 1	↑
DOK5	Docking protein 5	↑
ANKR2	Ankyrin repeat domain 2	↑
SLC114	Solute carrier family 16 member 14	↑
GPR37	G protein-coupled receptor 37	↑
TRPV2	Transient receptor potential cation channel subfamily V member 2	↑
RHCE	Sus scrofa Rh blood group CcEe antigens (RHCE), mRNA.	↑
MFNG	MFNG O-fucosylpeptide 3-beta-N-acetylglucosaminyltransferase	↑
UBAPL	Ubiquitin associated protein 1 like	↑
ASPG	Asparaginase	↑
CRYBA1	Crystallin beta A1	↑
RECQL	ATP-dependent DNA helicase Q1	↓
RIMKLB	Ribosomal modification protein rimK like family member B	↓
C1R	Complement C1r	↓
WASHC4	WASH complex subunit 4	↓
GNPTAB	N-acetylglucosamine-1-phosphate transferase alpha and beta subunits	↓
SELENOO	Sus scrofa selenoprotein O (SELENOO), mRNA.	↓
MAN2A2	Mannosidase alpha class 2A member 2	↓
STRA6	Stimulated by retinoic acid 6	↓
ISLR	Immunoglobulin superfamily containing leucine rich repeat	↓
HECTD1	HECT domain E3 ubiquitin protein ligase 1	↓
C14orf119	Chromosome 14 open reading frame 119	↓
NFAT5	Nuclear factor of activated T-cells 5	↓
E2F4	E2F transcription factor 4	↓
INPP5B	Inositol polyphosphate-5-phosphatase B	↓
SMOC2	SPARC related modular calcium binding 2	↓
MTHFD1L	Methylenetetrahydrofolate dehydrogenase (NADP+ dependent) 1 like	↓
LATS1	Large tumor suppressor kinase 1	↓
ME2	Malic enzyme 2	↓
TRIP4	Thyroid hormone receptor interactor 4	↓
LEO1	LEO1 homolog, Paf1/RNA polymerase II complex component	↓
VPS39	VPS39, HOPS complex subunit	↓
DPP8	Dipeptidyl peptidase 8	↓
HACD3	3-hydroxyacyl-CoA dehydratase 3	↓
PRPF39	Pre-mRNA processing factor 39	↓

表4

图5

表5

图6

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序号	样品编号	序号	样品编号	序号	样品编号
1	D1_1	19	D31_1	37	DW22_2
2	D1_3	20	D32_3	38	DW24_1
3	D8_2	21	D33_1	39	DW31_1
4	D9_2	22	D36_3	40	DW36_1
5	D11_1	23	D37_3	41	DW36_2
6	D12_1	24	D40_2	42	DW41_2
7	D12_2	25	D40_3	43	DW45_1
8	D13_1	26	D43_3	44	DW45_2
9	D18_3	27	D44_1	45	DW58_2
10	D20_1	28	D45_3	46	DW61_1
11	D21_1	29	D48_1	47	DW61_2
12	D22_1	30	D52_3	48	DW69_1
13	D23_3	31	D63_1	49	DW69_2
14	D25_1	32	D63_2	50	DW73-1
15	D26_1	33	D64_1	51	DW99_1
16	D27_1	34	D66_1	52	DW99_2
17	D28_1	35	DW16_1
18	D28_2	36	DW22_1

基因	基因全称	表达情况
GBX2	Gastrulation brain homeobox 2	↑
PCDH12	Protocadherin 12	↑
ARHGEF9	Cdc42 guanine nucleotide exchange factor 9	↑
TRAM1L1	Translocation associated membrane protein 1-like 1	↑
U6	U6 spliceosomal RNA	↑
DMTN	Dematin actin binding protein	↑
CEP72	Centrosomal protein 72	↑
YBX2	Y-box binding protein 2	↑
ZNF768	Zinc finger protein 768	↑
NOTCH4	Neurogenic locus notch homolog protein 4 precursor	↑
GARNL3	GTPase activating Rap/RanGAP domain like 3	↑
MTBP	MDM2 binding protein	↑
UHRF1	Ubiquitin like with PHD and ring finger domains 1	↑
PACSIN2	Protein kinase C and casein kinase substrate in neurons 2	↑
EP300	E1A binding protein p300	↓
ADSL	Adenylosuccinate lyase	↓
PWP1	PWP1 homolog, endonuclein	↓
IGFBP6	Insulin-like growth factor-binding protein 6 precursor	↓
MMP19	Matrix metallopeptidase 19	↓
ESYT1	Extended synaptotagmin 1	↓
SMARCC2	SWI/SNF related, matrix associated, actin dependent regulator of chromatin subfamily c member 2	↓
PTGES3	Prostaglandin E synthase 3	↓
MON2	MON2 homolog, regulator of endosome-to-Golgi trafficking	↓
XPOT	Exportin for tRNA	↓
TMEM19	Transmembrane protein 19	↓
TBC1D15	TBC1 domain family member 15	↓
DNM1L	Dynamin 1 like	↓
FAR2	Fatty acyl-CoA reductase 2	↓
ARNTL2	Aryl hydrocarbon receptor nuclear translocator like 2	↓
TM7SF3	Transmembrane 7 superfamily member 3	↓
FGFR1OP2	FGFR1 oncogene partner 2	↓
AEBP2	AE binding protein 2	↓
LRP6	LDL receptor related protein 6	↓
C1R	Complement C1r	↓
NOP2	Sus scrofa NOP2 nucleolar protein (NOP2), mRNA	↓

猪耳成纤维细胞转录组异质性及对核移植胚胎发育的潜在影响

Transcriptome heterogeneity of porcine ear fibroblast and its potential influence on embryo development in nuclear transplantation

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