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

[an error occurred while processing this directive]

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

• Research Article • Previous Articles Next Articles

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)

Abstract

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

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.

Figures/Tables 11

Table 1

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Table 2

Profiles of the top 50 genes with the most significant differences in D11_1"

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	↓

Table 2

Table 3

Profiles of the top 50 genes with the most significant differences in D12_1"

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	↓

Table 3

Table 4

Profiles of the top 50 genes with the most significant differences in D61_2"

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	↓

Table 4

Fig. 5

Table 5

Fig. 6

References 60

[1]	Wilmut I, Schnieke AE, Mcwhir J, Kind AJ, Campbell KH . Viable offspring derived from fetal and adult mammalian cells. Nature, 1997,385(6619):810-813. doi: 10.1038/385810a0 pmid: 9039911
[2]	Cibelli JB, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, de León FAP, Robl JM. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 1998,280(5367):1256-1258. pmid: 9596577
[3]	Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC . Pig cloning by microinjection of fetal fibroblast nuclei. Science, 2000,289(5482):1188-1190. pmid: 10947985
[4]	Liu Z, Cai YJ, Wang Y, Nie YH, Zhang CC, Xu YT, Zhang XT, Lu Y, Wang ZY, Poo M, Sun Q . Cloning of macaque monkeys by somatic cell nuclear transfer. Cell, 2018,172(4):881-887. doi: 10.1016/j.cell.2018.01.020 pmid: 29395327
[5]	Beyhan Z, Iager AE, Cibelli JB . Interspecies nuclear transfer: implications for embryonic stem cell biology. Cell Stem Cell, 2007,1(5):502-512. doi: 10.1016/j.stem.2007.10.009
[6]	Niemann H, Lucas-Hahn A . Somatic cell nuclear transfer cloning: practical applications and current legislation. Reprod Domest Anim, 2012,47(Suppl. 5):2-10.
[7]	Tachibana M, Amato P, Sparman M, Gutierrez N M, Tippner-Hedges R, Ma H, Kang E, Fulati A, Lee H S, Sritanaudomchai H, Masterson K, Larson J, Eaton D, Sadler-Fredd K, Battaglia D, Lee D, Wu D, Jensen J, Patton P, Gokhale S, Stouffer RL, Wolf D, Mitalipov S . Human embryonic stem cells derived by somatic cell nuclear transfer. Cell, 2013,153(6):1228-1238. doi: 10.1016/j.cell.2013.05.006
[8]	Ao Z, Wu X, Zhou J, Gu T, Wang XW, Shi JS, Zhao CF, Cai GY, Zheng EQ, Liu DW, Wu ZF, Li ZC . Cloned pig fetuses exhibit fatty acid deficiency from impaired placental transport. Mol Reprod Dev, 2019,86(11):1569-1581. pmid: 31347235
[9]	Liu Y, Li J, Løvendahl P, Schmidt M, Larsen K, Callesen H . In vitro manipulation techniques of porcine embryos: a meta-analysis related to transfers, pregnancies and piglets. Reprod Fertil Dev, 2015,27(3):429-439. doi: 10.1071/RD13329 pmid: 25482653
[10]	Jang G, Park ES, Cho JK, Bhuiyan MM, Lee BC, Kang SK, Hwang WS . Preimplantational embryo development and incidence of blastomere apoptosis in bovine somatic cell nuclear transfer embryos reconstructed with long-term cultured donor cells. Theriogenology, 2004,62(3-4):512-521. pmid: 15226007
[11]	Zhang DF, Liu D, Tang LL, Wang Y, Chen Y, Wang K, Wang GL, Schellander K, Cailu L . Effects of different donor cells on the development of nuclear-trans-ferred porcine embryos. Hereditas(Beijing), 2007,29(2):211-217.
	张德福, 刘东, 汤琳琳, 王英, 陈茵, 王凯, 王根林 , KARL Schellander, LIN Cailu. 不同供体细胞及其处理对猪核移植重构胚体外发育的影响. 遗传, 2007,29(2):211-217.
[12]	Ruan ZY, Zhao X, Li ZD, Qin XL, Shao QM, Ruan QY, Deng YF, Jiang JR, Huang B, Lu FH, Shi DS . Effect of sex differences in donor foetal fibroblast on the early development and DNA methylation status of buffalo (Bubalus bubalis) nuclear transfer embryos. Reprod Domest Anim, 2019,54(1):11-22. doi: 10.1111/rda.13286 pmid: 30051521
[13]	Rideout WR, Eggan K, Jaenisch R . Nuclear cloning and epigenetic reprogramming of the genome. Science, 2001,293(5532):1093-1098. doi: 10.1126/science.1063206 pmid: 11498580
[14]	Yang XQ, Wu ZF, Li ZC . Advances in epigenetic reprogramming of somatic cells nuclear transfer in mammals. Hereditas(Beijing), 2019,41(12):1099-1109.
	杨旭琼, 吴珍芳, 李紫聪 . 哺乳动物体细胞核移植表观遗传重编程研究进展. 遗传, 2019,41(12):1099-1109.
[15]	Zhai YH, Li W, Zhang ZR, Cao YQ, Wang ZZ, Zhang S, Li ZY . Epigenetic states of donor cells significantly affect the development of somatic cell nuclear transfer (SCNT) embryos in pigs. Mol Reprod Dev, 2018,85(1):26-37. doi: 10.1002/mrd.22935 pmid: 29205617
[16]	Yamanaka S . Elite and stochastic models for induced pluripotent stem cell generation. Nature, 2009,460(7251):49-52. doi: 10.1038/nature08180 pmid: 19571877
[17]	Inoue K, Ogonuki N, Mochida K, Yamamoto Y, Takano K, Kohda T, Ishino F, Ogura A . Effects of donor cell type and genotype on the efficiency of mouse somatic cell cloning. Biol Reprod, 2003,69(4):1394-1400. doi: 10.1095/biolreprod.103.017731 pmid: 12801984
[18]	Zhou C, Zhang JC, Zhang M, Wang DB, Ma Y, Wang Y, Wang YZ, Huang YM, Zhang Y . Transcriptional memory inherited from donor cells is a developmental defect of bovine cloned embryos. Faseb J, 2020,34(1):1637-1651. doi: 10.1096/fj.201900578RR pmid: 31914649
[19]	Picelli S, Faridani OR, Björklund AK, Winberg G, Sagasser S, Sandberg R . Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc, 2014,9(1):171-181. doi: 10.1038/nprot.2014.006 pmid: 24385147
[20]	Grubman A, Chew G, Ouyang JF, Sun GZ, Choo XY, Mclean C, Simmons RK, Buckberry S, Vargas-Landin DB, Poppe D, Pflueger J, Lister R, Rackham O, Petretto E, Polo JM . A single-cell atlas of entorhinal cortex from individuals with Alzheimer's disease reveals cell-type- specific gene expression regulation. Nat Neurosci, 2019,22(12):2087-2097 pmid: 31768052
[21]	Tang FC, Barbacioru C, Wang YZ, Nordman E, Lee C, Xu NN, Wang XH, Bodeau J, Tuch BB, Siddiqui A, Lao K , Surani MA. mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods, 2009,6(5):377-382. doi: 10.1038/nmeth.1315 pmid: 19349980
[22]	Kim D, Langmead B, Salzberg SL . HISAT: a fast spliced aligner with low memory requirements. Nat Methods, 2015,12(4):357-360. doi: 10.1038/nmeth.3317 pmid: 25751142
[23]	Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG . DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 2010,26(1):136-138. doi: 10.1093/bioinformatics/btp612
[24]	Young MD, Wakefield MJ, Smyth GK, Oshlack A . Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol, 2010,11(2):R14. doi: 10.1186/gb-2010-11-2-r14 pmid: 20132535
[25]	Robinson MD, Mccarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 2010,26(1):139-140. doi: 10.1093/bioinformatics/btp616 pmid: 19910308
[26]	Navin N, Hicks J . Future medical applications of single-cell sequencing in cancer. Genome Med, 2011,3(5):31. pmid: 21631906
[27]	Novick A, Weiner M . Enzyme induction as an all-or-none phenomenon. Proc Natl Acad Sci USA, 1957,43(7):553-566. pmid: 16590055
[28]	Coskun AF, Eser U, Islam S . Cellular identity at the single-cell level. Mol Biosyst, 2016,12(10):2965-2979. doi: 10.1039/c6mb00388e pmid: 27460751
[29]	Menon M, Mohammadi S, Davila-Velderrain J, Goods BA, Cadwell TD, Xing Y, Stemmer-Rachamimov A, Shalek AK, Love JC, Kellis M, Hafler BP . Single-cell transcriptomic atlas of the human retina identifies cell types associated with age-related macular degeneration. Nat Commun, 2019,10(1):4902. pmid: 31653841
[30]	Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S . Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 2007,131(5):861-872. doi: 10.1016/j.cell.2007.11.019 pmid: 18035408
[31]	Lowry WE, Richter L, Yachechko R, Pyle AD, Tchieu J, Sridharan R, Clark AT, Plath K . Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci USA, 2008,105(8):2883-2888. doi: 10.1073/pnas.0711983105 pmid: 18287077
[32]	Polo JM, Liu S, Figueroa M E, Kulalert W, Eminli S, Tan KY, Apostolou E, Stadtfeld M, Li YS, Shioda T, Natesan S, Wagers AJ, Melnick A, Evans T, Hochedlinger K . Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol, 2010,28(8):848-855. doi: 10.1038/nbt.1667 pmid: 20644536
[33]	Lai L, Tao T, Macháty Z, Kühholzer B, Sun QY, Park KW, Day BN, Prather RS . Feasibility of producing porcine nuclear transfer embryos by using G2/M-stage fetal fibroblasts as donors. Biol Reprod, 2001,65(5):1558-1564. doi: 10.1095/biolreprod65.5.1558 pmid: 11673275
[34]	Chesné P, Adenot PG, Viglietta C, Baratte M, Boulanger L, Renard JP . Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotechnol, 2002,20(4):366-369. doi: 10.1038/nbt0402-366 pmid: 11923842
[35]	Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G . Ubiquitin tag for sperm mitochondria. Nature, 1999,402(6760):371-372. doi: 10.1038/46466 pmid: 10586873
[36]	Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC . Pig cloning by microinjection of fetal fibroblast nuclei. Science, 2000,289(5482):1188-1190. doi: 10.1126/science.289.5482.1188 pmid: 10947985
[37]	Gupta S, Sahu D, Bomalaski JS, Frank I, Boorjian SA, Thapa P, Cheville J C, Hansel DE . Argininosuccinate Synthetase-1 (ASS1) loss in high-grade neuroendocrine carcinomas of the urinary bladder: implications for targeted therapy with ADI-PEG 20. Endocr Pathol, 2018,29(3):236-241. doi: 10.1007/s12022-018-9516-9 pmid: 29453600
[38]	Moren L, Perryman R, Crook T, Langer JK, Oneill K, Syed N, Antti H . Metabolomic profiling identifies distinct phenotypes for ASS1 positive and negative GBM. BMC Cancer, 2018,18(1):167. pmid: 29422017
[39]	Bang J, Lee E, Lee AR, Il Lee J, Choi SH, Seol D, Park C, Lee DR . The effect of cell penetrating peptide-conjugated coactivator-associated arginine methyltransferase 1 (CPP-CARM1) on the cloned mouse embryonic development. Sci Rep, 2018,8(1):16721. doi: 10.1038/s41598-018-35077-0 pmid: 30425285
[40]	Abdel-Hady AE, Beige J, Kreutz R, Bolbrinker J . Effect of UMOD genotype on long-term graft survival after kidney transplantation in patients treated with cyclosporine-based therapy. Pharmacogenomics J, 2018,18(2):227-231. pmid: 28418009
[41]	Bailie C, Kilner J, Maxwell AP, Mcknight AJ . Development of next generation sequencing panel for UMOD and association with kidney disease. PLoS One, 2017,12(6):e0178321. doi: 10.1371/journal.pone.0178321 pmid: 28609449
[42]	Davis D, Kannan M, Wattenberg B . Orm/ORMDL proteins: Gate guardians and master regulators. Adv Biol Regul, 2018,70:3-18. doi: 10.1016/j.jbior.2018.08.002 pmid: 30193828
[43]	Fava RA, Browning JL, Gatumu M, Skarstein K, Bolstad AI . LTBR-pathway in Sjogren's syndrome: CXCL13 levels and B-cell-enriched ectopic lymphoid aggregates in NOD mouse lacrimal glands are dependent on LTBR. Adv Exp Med Biol, 2011,691:383-390. doi: 10.1007/978-1-4419-6612-4_39 pmid: 21153342
[44]	Zhu QQ, Li N, Li F, Sang J, Deng H, Han QY, Lv Y, Li CY, Liu ZW . Association of LTBR polymorphisms with chronic hepatitis B virus infection and hepatitis B virus-related hepatocellular carcinoma. Int Immunopharmacol, 2017,49:126-131. doi: 10.1016/j.intimp.2017.05.031 pmid: 28575727
[45]	Sia D, Losic B, Moeini A, Cabellos L, Hao K, Revill K, Bonal D, Miltiadous O, Zhang ZY, Hoshida Y, Cornella H, Castillo-Martin M, Pinyol R, Kasai Y, Roayaie S, Thung S N, Fuster J, Schwartz ME, Waxman S, Cordon-Cardo C, Schadt E, Mazzaferro V, Llovet JM . Massive parallel sequencing uncovers actionable FGFR2-PPHLN1 fusion and ARAF mutations in intrahepatic cholangiocarcinoma. Nat Commun, 2015,6:6087. doi: 10.1038/ncomms7087 pmid: 25608663
[46]	Chung YG, Matoba S, Liu YT, Eum JH, Lu FL, Jiang W, Lee JE, Sepilian V, Cha KY, Lee DR, Zhang Y . Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell, 2015,17(6):758-766. doi: 10.1016/j.stem.2015.10.001 pmid: 26526725
[47]	Boone PM, Yuan B, Gu S, Ma ZW, Gambin T, Gonzaga-Jauregui C, Jain M, Murdock TJ, White JJ, Jhangiani SN, Walker K, Wang QY, Muzny DM, Gibbs RA, Hejtmancik JF, Lupski JR, Posey JE, Lewis RA . Hutterite-type cataract maps to chromosome 6p21.32- p21.31, cosegregates with a homozygous mutation in LEMD2, and is associated with sudden cardiac death. Mol Genet Genomic Med, 2016,4(1):77-94. doi: 10.1002/mgg3.181 pmid: 26788539
[48]	Mcgee LJ, Jiang AL, Lan Y. Golga5 is dispensable for mouse embryonic development and postnatal survival.Genesis, 2017, 55(7): 10. 1002/dvg. 23039.
[49]	O'Grady GL, Best HA, Sztal TE, Schartner V, Sanjuan-Vazquez M, Donkervoort S, Abath NO, Sutton RB, Ilkovski B, Romero NB, Stojkovic T, Dastgir J, Waddell L B, Boland A, Hu Y, Williams C, Ruparelia AA, Maisonobe T, Peduto AJ, Reddel SW, Lek M, Tukiainen T, Cummings BB, Joshi H, Nectoux J, Brammah S, Deleuze JF, Ing VO, Ramm G, Ardicli D, Nowak KJ, Talim B, Topaloglu H, Laing NG, North K N, Macarthur DG, Friant S, Clarke NF, Bryson-Richardson RJ, Bönnemann CG, Laporte J, Cooper ST,. Variants in the oxidoreductase PYROXD1 cause early-onset myopathy with internalized nuclei and myofibrillar disorganization. Am J Hum Genet, 2016,99(5):1086-1105. doi: 10.1016/j.ajhg.2016.09.005 pmid: 27745833
[50]	Al-Dabbagh N, Al-Shahrani H, Al-Dohayan N, Mustafa M, Arfin M, Al-Asmari AK . The SPARC-related modular calcium binding protein 2 (SMOC2) gene polymorphism in primary glaucoma: a case-control study. Clin Ophthalmol, 2017,11:549-555. doi: 10.2147/OPTH.S126459 pmid: 28356709
[51]	Huang XQ, Zhou ZQ, Zhang XF, Chen CL, Tang Y, Zhu Q, Zhang JH, Xia JC . Overexpression of SMOC2 attenuates the tumorigenicity of hepatocellular carcinoma cells and is associated with a positive postoperative prognosis in human hepatocellular carcinoma. J Cancer, 2017,8(18):3812-3827. doi: 10.7150/jca.20775 pmid: 29151969
[52]	Hagan N, Guarente J, Ellisor D, Zervas M . The temporal contribution of the Gbx2 lineage to cerebellar neurons. Front Neuroanat, 2017,11:50. doi: 10.3389/fnana.2017.00050 pmid: 28785208
[53]	Mallika C, Guo QX, Li JYH . Gbx2 is essential for maintaining thalamic neuron identity and repressing habenular characters in the developing thalamus. Dev Biol, 2015,407(1):26-39. doi: 10.1016/j.ydbio.2015.08.010 pmid: 26297811
[54]	Alber M, Kalscheuer VM, Marco E, Sherr E, Lesca G, Till M, Gradek G, Wiesener A, Korenke C, Mercier S, Becker F, Yamamoto T, Scherer SW, Marshall CR, Walker S, Dutta UR, Dalal A B, Suckow V, Jamali P, Kahrizi K, Najmabadi H, Minassian BA . ARHGEF9 disease: Phenotype clarification and genotype-phenotype correlation. Neurol Genet, 2017,3(3):e148. doi: 10.1212/NXG.0000000000000148 pmid: 28589176
[55]	Klein KM, Pendziwiat M, Eilam A, Gilad R, Blatt I, Rosenow F, Kanaan M, Helbig I, Afawi Z . The phenotypic spectrum of ARHGEF9 includes intellectual disability, focal epilepsy and febrile seizures. J Neurol, 2017,264(7):1421-1425. doi: 10.1007/s00415-017-8539-3 pmid: 28620718
[56]	Li HS, Song MM, Yang W, Cao P, Zheng L, Zuo YC . A Comparative analysis of single-cell transcriptome identifies reprogramming driver factors for efficiency improvement. Molecular Therapy - Nucleic Acids, 2020,19:1053-1064. doi: 10.1016/j.omtn.2019.12.035 pmid: 32045876
[57]	Inoue K, Ogonuki N, Mochida K, Yamamoto Y, Takano K, Kohda T, Ishino F, Ogura A . Effects of donor cell type and genotype on the efficiency of mouse somatic cell cloning. Biol Reprod, 2003,69(4):1394-1400. doi: 10.1095/biolreprod.103.017731 pmid: 12801984
[58]	Xie BT, Zhang H, Wei RY, Li QN, Weng XG, Kong QR, Liu ZH . Histone H3 lysine 27 trimethylation acts as an epigenetic barrier in porcine nuclear reprogramming. Reproduction, 2016,151(1):9-16. doi: 10.1530/REP-15-0338 pmid: 26515777
[59]	Matoba S, Liu YT, Lu FL, Iwabuchi KA, Shen L, Inoue A, Zhang Y . Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell, 2014,159(4):884-895. doi: 10.1016/j.cell.2014.09.055
[60]	Liu Y, Wu FR, Zhang L, Wu XQ, Li DK, Xin J, Xie J, Kong F, Wang WY, Wu QQ, Zhang D, Wang R, Gao SR, Li WY . Transcriptional defects and reprogramming barriers in somatic cell nuclear reprogramming as revealed by single-embryo RNA sequencing. BMC Genomics, 2018,19(1):734. doi: 10.1186/s12864-018-5091-1 pmid: 30305014

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

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	↓

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

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 11

References 60

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Xi Han, Fucheng Luo. Application of single-cell RNA sequencing in probing oligodendroglia heterogeneity and neurological disorders [J]. Hereditas(Beijing), 2023, 45(3): 198-211.
[2]	Beiping Zeng, Hongen Xu, Lu Mao, Wenxue Tang. Molecular diagnosis of hereditary deafness and application of stepwise testing strategy [J]. Hereditas(Beijing), 2023, 45(1): 29-41.
[3]	Zhuo Wang, Xiaohan Shen, Qihui Shi. Advances in single-cell whole genome sequencing technology and its application in biomedicine [J]. Hereditas(Beijing), 2021, 43(2): 108-117.
[4]	Baosong Xing, Jing Wang, Junfeng Chen, Qiang Ma, Qiaoling Ren, Jiaqing Zhang, Hua Zhang, Liushuai Hua, Jiajie Sun, Hai Cao. Analysis of differentially expressed circRNAs in longissimus muscle between castrated and intact male pigs [J]. Hereditas(Beijing), 2021, 43(11): 1066-1077.
[5]	Liang Qu, Su Li, Huaji Qiu. Applications of single-cell RNA sequencing in virology [J]. Hereditas(Beijing), 2020, 42(3): 269-277.
[6]	Qiang Zhang, Mingliang Gu. Single-cell sequencing and its application in breast cancer [J]. Hereditas(Beijing), 2020, 42(3): 250-268.
[7]	Zheng Ao, Xiang Chen, Zhenfang Wu, Zicong Li. Progress on abnormal development of cloned pigs generated by somatic cell transfer nuclear [J]. Hereditas(Beijing), 2020, 42(10): 993-1003.
[8]	Jianxin Mo,Haoqiang Wang,Guangyan Huang,Gengyuan Cai,Zhenfang Wu,Xianwei Zhang. Heterogenous expression and enzymatic property analysis of microbial-derived pectinases in pig PK15 cells [J]. Hereditas(Beijing), 2019, 41(8): 736-745.
[9]	Baojun Wu,Zhuo Wang,Yu Dong,Yuliang Deng,Qihui Shi. Identification and single-cell sequencing analysis of rare tumor cells in malignant pleural effusion of lung cancer patients [J]. Hereditas(Beijing), 2019, 41(2): 175-184.
[10]	Xuqiong Yang, Zhenfang Wu, Zicong Li. Advances in epigenetic reprogramming of somatic cells nuclear transfer in mammals [J]. Hereditas(Beijing), 2019, 41(12): 1099-1109.
[11]	Youwang Lu,Kunhua Wang. Research progress on genetic heterogeneity between primary and paired metastatic colorectal cancer [J]. Hereditas(Beijing), 2017, 39(6): 482-490.
[12]	Zheng Ao, Dewu Liu, Gengyuan Cai, Zhenfang Wu, Zicong Li. Placental developmental defects in cloned mammalian animals [J]. HEREDITAS(Beijing), 2016, 38(5): 402-410.
[13]	Linqi Wang. Adaptation strategies: how environmental fungi become fatal? [J]. HEREDITAS(Beijing), 2015, 37(5): 436-441.
[14]	Jing Liu, Yanan Wang, Yaqi Sun, Hongyang Wang, Chao Wang, Zhongzhen Peng, Bang Liu. Investigation of genes within copy number variation regions in pig chromosome 13 and analysis of the genetic law [J]. HEREDITAS, 2014, 36(4): 354-359.
[15]	Ji Huili, Lu Shengsheng, Pan Dengke. Epigenetic reprogramming by somatic cell nuclear transfer: questions and potential solutions [J]. HEREDITAS(Beijing), 2014, 36(12): 1211-1218.