Regulation of DNA methylation on key parasitism genes of Cysticercus cellulosae revealed by integrative epigenomic-transcriptomic analyses.


Journal

Hereditas
ISSN: 1601-5223
Titre abrégé: Hereditas
Pays: England
ID NLM: 0374654

Informations de publication

Date de publication:
12 Aug 2021
Historique:
received: 05 08 2020
accepted: 02 08 2021
entrez: 13 8 2021
pubmed: 14 8 2021
medline: 24 12 2021
Statut: epublish

Résumé

The life cycle of Taenia solium is characterized by different stages of development, requiring various kinds of hosts that can appropriately harbor the eggs (proglottids), the oncospheres, the larvae and the adults. Similar to other metazoan pathogens, T. solium undergoes transcriptional and developmental regulation via epigenetics during its complex lifecycle and host interactions. In the present study, we integrated whole-genome bisulfite sequencing and RNA-seq technologies to characterize the genome-wide DNA methylation and its effect on transcription of Cysticercus cellulosae of T. solium. We confirm that the T. solium genome in the cysticercus stage is epigenetically modified by DNA methylation in a pattern similar to that of other invertebrate genomes, i.e., sparsely or moderately methylated. We also observed an enrichment of non-CpG methylation in defined genetic elements of the T. solium genome. Furthermore, an integrative analysis of both the transcriptome and the DNA methylome indicated a strong correlation between these two datasets, suggesting that gene expression might be tightly regulated by DNA methylation. Importantly, our data suggested that DNA methylation might play an important role in repressing key parasitism-related genes, including genes encoding excretion-secretion proteins, thereby raising the possibility of targeting DNA methylation processes as a useful strategy in therapeutics of cysticercosis.

Sections du résumé

BACKGROUND BACKGROUND
The life cycle of Taenia solium is characterized by different stages of development, requiring various kinds of hosts that can appropriately harbor the eggs (proglottids), the oncospheres, the larvae and the adults. Similar to other metazoan pathogens, T. solium undergoes transcriptional and developmental regulation via epigenetics during its complex lifecycle and host interactions.
RESULT RESULTS
In the present study, we integrated whole-genome bisulfite sequencing and RNA-seq technologies to characterize the genome-wide DNA methylation and its effect on transcription of Cysticercus cellulosae of T. solium. We confirm that the T. solium genome in the cysticercus stage is epigenetically modified by DNA methylation in a pattern similar to that of other invertebrate genomes, i.e., sparsely or moderately methylated. We also observed an enrichment of non-CpG methylation in defined genetic elements of the T. solium genome. Furthermore, an integrative analysis of both the transcriptome and the DNA methylome indicated a strong correlation between these two datasets, suggesting that gene expression might be tightly regulated by DNA methylation. Importantly, our data suggested that DNA methylation might play an important role in repressing key parasitism-related genes, including genes encoding excretion-secretion proteins, thereby raising the possibility of targeting DNA methylation processes as a useful strategy in therapeutics of cysticercosis.

Identifiants

pubmed: 34384501
doi: 10.1186/s41065-021-00195-9
pii: 10.1186/s41065-021-00195-9
pmc: PMC8361615
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

28

Subventions

Organisme : the National Key Research and Development Program of China
ID : 2017YFD0501303
Organisme : the National Natural Science Foundation of China
ID : NSFC 31960707, 31160504, 31460658
Organisme : the Inner Mongolia Provincial Natural Science Foundation
ID : 2017MS0321

Informations de copyright

© 2021. The Author(s).

Références

Curr Protoc Bioinformatics. 2009 Mar;Chapter 4:Unit 4.10
pubmed: 19274634
Nat Rev Genet. 2010 Mar;11(3):204-20
pubmed: 20142834
Oncotarget. 2012 Apr;3(4):462-74
pubmed: 22577155
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W293-7
pubmed: 16845012
Nature. 2007 Sep 13;449(7159):248-51
pubmed: 17713477
Genome Biol. 2012 Oct 17;13(10):R100
pubmed: 23075480
Nature. 2000 Nov 30;408(6812):538-40
pubmed: 11117732
Proc Natl Acad Sci U S A. 2013 May 21;110(21):8627-31
pubmed: 23641003
Development. 2004 Dec;131(24):6033-9
pubmed: 15537686
PLoS Negl Trop Dis. 2021 Mar 23;15(3):e0009234
pubmed: 33755677
Cell. 2014 Mar 13;156(6):1286-1297
pubmed: 24630728
BMC Bioinformatics. 2009 Jul 27;10:232
pubmed: 19635165
Folia Parasitol (Praha). 2012 Dec;59(4):255-63
pubmed: 23327006
Mol Biochem Parasitol. 2004 Jan;133(1):115-24
pubmed: 14668018
Microbes Infect. 2000 Dec;2(15):1875-90
pubmed: 11165932
Nat Biotechnol. 2010 May;28(5):511-5
pubmed: 20436464
Nat Biotechnol. 2010 May;28(5):516-20
pubmed: 20436463
Mol Biol Evol. 1987 Jul;4(4):406-25
pubmed: 3447015
Trends Parasitol. 2016 Jul;32(7):515-521
pubmed: 27142564
Parasitol Int. 2006;55 Suppl:S127-30
pubmed: 16337432
BMC Genomics. 2013 Jul 09;14:462
pubmed: 23837670
Proc Natl Acad Sci U S A. 2010 May 11;107(19):8689-94
pubmed: 20395551
Science. 2008 Apr 25;320(5875):489-92
pubmed: 18436779
Genome Res. 2009 Jun;19(6):959-66
pubmed: 19273618
Nat Genet. 2007 Jan;39(1):61-9
pubmed: 17128275
Nature. 2008 Mar 13;452(7184):215-9
pubmed: 18278030
Bioinformatics. 2009 May 1;25(9):1105-11
pubmed: 19289445
FEBS Lett. 1997 Nov 3;417(1):48-52
pubmed: 9395072
BMC Genomics. 2017 Feb 27;18(1):204
pubmed: 28241794
Nat Genet. 2009 Jun;41(6):696-702
pubmed: 19412177
J Immunol. 2018 Jul 1;201(1):124-133
pubmed: 29752313
Int J Parasitol. 2021 Jul;51(8):685-692
pubmed: 33753094
Gigascience. 2018 Jan 1;7(1):1-6
pubmed: 29220494
Cell. 1979 Aug;17(4):889-901
pubmed: 487434
PLoS Biol. 2010 Nov 02;8(11):e1000506
pubmed: 21072239
Genome Res. 2011 Nov;21(11):1841-50
pubmed: 21940836
Science. 2010 May 14;328(5980):916-9
pubmed: 20395474
Nucleic Acids Res. 1990 Oct 25;18(20):6097-100
pubmed: 2172928
Genes Dev. 1997 Sep 15;11(18):2383-95
pubmed: 9308966
Nat Genet. 2007 Apr;39(4):457-66
pubmed: 17334365
Science. 2006 Jan 20;311(5759):395-8
pubmed: 16424344
Bull Pan Am Health Organ. 1993;27(4):397-403
pubmed: 8312963
Nat Commun. 2011 Aug 09;2:424
pubmed: 21829186
Exp Parasitol. 2005 May;110(1):1-11
pubmed: 15884156
Proteomics. 2012 Jun;12(11):1860-9
pubmed: 22623400
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
PLoS Pathog. 2018 Jun 28;14(6):e1007107
pubmed: 29953544
Mol Biochem Parasitol. 2009 Sep;167(1):1-11
pubmed: 19406170
Exp Parasitol. 2012 Jan;130(1):78-85
pubmed: 22075212
Nature. 2015 Jan 15;517(7534):321-6
pubmed: 25592537
Comput Appl Biosci. 1992 Jun;8(3):275-82
pubmed: 1633570

Auteurs

Xinrui Wang (X)

College of Animal Science and Technology, Inner Mongolia University for Nationalities, Tongliao, 028000, Inner Mongolia, China.

Weiyi Song (W)

College of Animal Science and Technology, Inner Mongolia University for Nationalities, Tongliao, 028000, Inner Mongolia, China.

Guanyu Ji (G)

Shenzhen E-GENE Technology Co., LTD, B3301, Life Science Park, Shenzhen City Construction Investment Development Creative Factory, Julongshan A Road, Pingshan District, Shenzhen, 518083, China.

Yining Song (Y)

College of Animal Science and Technology, Inner Mongolia University for Nationalities, Tongliao, 028000, Inner Mongolia, China.

Xiaolei Liu (X)

Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun, 130000, China.

Xuenong Luo (X)

Lanzhou Institute of Veterinary Medicine, Chinese Academy of Agricultural Sciences, Lanzhou, 730000, China.

Mingyuan Liu (M)

College of Animal Science and Technology, Inner Mongolia University for Nationalities, Tongliao, 028000, Inner Mongolia, China. liumy@jlu.edu.cn.
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun, 130000, China. liumy@jlu.edu.cn.

Shumin Sun (S)

College of Animal Science and Technology, Inner Mongolia University for Nationalities, Tongliao, 028000, Inner Mongolia, China. shums1975@163.com.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH