Comparative transcriptomic analysis of long noncoding RNAs in Leishmania-infected human macrophages
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Citações na Scopus
2
Tipo de produção
article
Data de publicação
2023
Título da Revista
ISSN da Revista
Título do Volume
Editora
FRONTIERS MEDIA SA
Autores
GONCALVES, Andre N. A.
FLOETER-WINTER, Lucile M.
NAKAYA, Helder I.
MUXEL, Sandra M.
Citação
FRONTIERS IN GENETICS, v.13, article ID 1051568, 17p, 2023
Resumo
It is well established that infection with Leishmania alters the host cell's transcriptome. Since mammalian cells have multiple mechanisms to control gene expression, different molecules, such as noncoding RNAs, can be involved in this process. MicroRNAs have been extensively studied upon Leishmania infection, but whether long noncoding RNAs (lncRNAs) are also altered in macrophages is still unexplored. We performed RNA-seq from THP-1-derived macrophages infected with Leishmania amazonensis (La), L. braziliensis (Lb), and L. infantum (Li), investigating a previously unappreciated fraction of macrophage transcriptome. We found that more than 24% of the total annotated transcripts and 30% of differentially expressed (DE) RNAs in Leishmania-infected macrophage correspond to lncRNAs. LncRNAs and protein coding RNAs with altered expression are similar among macrophages infected with the Leishmania species. Still, some species-specific alterations could occur due to distinct pathophysiology in which Li infection led to a more significant number of exclusively DE RNAs. The most represented classes among DE lncRNAs were intergenic and antisense lncRNAs. We also found enrichment for immune response-related pathways in the DE protein coding RNAs, as well as putative targets of the lncRNAs. We performed a coexpression analysis to explore potential cis regulation of coding and antisense noncoding transcripts. We identified that antisense lncRNAs are similarly regulated as its neighbor protein coding genes, such as the BAALC/BAALC-AS1, BAALC/BAALC-AS2, HIF1A/HIF1A-AS1, HIF1A/HIF1A-AS3 and IRF1/IRF1-AS1 pairs, which can occur as a species-specific modulation. These findings are a novelty in the field because, to date, no study has focused on analyzing lncRNAs in Leishmania-infected macrophage. Our results suggest that lncRNAs may account for a novel mechanism by which Leishmania can control macrophage function. Further research must validate putative lncRNA targets and provide additional prospects in lncRNA function during Leishmania infection.
Palavras-chave
gene expression, host-parasite interaction, lncRNA, THP-1, RNA-seq, transcriptomics, Leishmania, macrophage
Referências
- Aoki JI, 2019, SCI REP-UK, V9, DOI 10.1038/s41598-019-56305-1
- Barriocanal M, 2022, FRONT IMMUNOL, V13, DOI 10.3389/fimmu.2022.829335
- Bayer-Santos E, 2017, FRONT MICROBIOL, V8, DOI 10.3389/fmicb.2017.00474
- Bensaoud C, 2019, TRENDS PARASITOL, V35, P715, DOI 10.1016/j.pt.2019.06.012
- Bichiou H, 2021, FRONT CELL INFECT MI, V11, DOI 10.3389/fcimb.2021.748738
- Burza S, 2018, LANCET, V392, P951, DOI 10.1016/S0140-6736(18)31204-2
- Carlsen ED, 2013, INFECT IMMUN, V81, P3966, DOI 10.1128/IAI.00770-13
- Castro FF, 2017, MOL BIOCHEM PARASIT, V214, P69, DOI [10.1016/j.molblopara.2017.04.002, 10.1016/j.molbiopara.2017.04.002]
- Chen EY, 2013, BMC BIOINFORMATICS, V14, DOI 10.1186/1471-2105-14-128
- Chen JJ, 2004, NUCLEIC ACIDS RES, V32, P4812, DOI 10.1093/nar/gkh818
- Chen YG, 2017, NAT IMMUNOL, V18, P962, DOI 10.1038/ni.3771
- Colineau L, 2018, J BIOL CHEM, V293, P12805, DOI [10.1074/jbc.RA118.002462, 10.1074/jbc.ra118.002462]
- Das A, 2018, FRONT IMMUNOL, V9, DOI 10.3389/fimmu.2018.00022
- Dashti S, 2020, SCI REP-UK, V10, DOI 10.1038/s41598-020-76024-2
- de Lima DS, 2019, P NATL ACAD SCI USA, V116, P17121, DOI 10.1073/pnas.1822046116
- Di Fiore A, 2018, OXID MED CELL LONGEV, V2018, DOI 10.1155/2018/2018306
- Diotallevi A, 2018, FRONT MICROBIOL, V9, DOI 10.3389/fmicb.2018.01019
- Du Y, 2020, FRONT ONCOL, V10, DOI 10.3389/fonc.2020.580176
- Dumas C, 2006, EUKARYOT CELL, V5, P2033, DOI 10.1128/EC.00147-06
- Durinck S, 2009, NAT PROTOC, V4, P1184, DOI 10.1038/nprot.2009.97
- Ebert MS, 2007, NAT METHODS, V4, P721, DOI 10.1038/NMETH1079
- Favila MA, 2014, J IMMUNOL, V192, P5863, DOI 10.4049/jimmunol.1203230
- Fernandes JCR, 2019, NON-CODING RNA, V5, DOI 10.3390/ncrna5010017
- Fernandes MC, 2016, MBIO, V7, DOI 10.1128/mBio.00027-16
- Ferreira C, 2021, CURR OPIN MICROBIOL, V63, P231, DOI 10.1016/j.mib.2021.07.012
- Frohlich A, 2007, BLOOD, V109, P2023, DOI 10.1182/blood-2006-05-021600
- Gao R, 2022, BIOMED RES INT, V2022, DOI 10.1155/2022/5532118
- Gasparotto J, 2017, MEM I OSWALDO CRUZ, V112, P146, DOI 10.1590/0074-02760160403
- Gatto M, 2020, PLOS NEGLECT TROP D, V14, DOI 10.1371/journal.pntd.0007949
- Geraci NS, 2015, PARASITE IMMUNOL, V37, P43, DOI 10.1111/pim.12156
- Goncalves ANA, 2019, FRONT GENET, V10, DOI 10.3389/fgene.2019.00971
- Han YH, 2017, CELL REP, V20, P124, DOI 10.1016/j.celrep.2017.06.017
- Howe KL, 2021, NUCLEIC ACIDS RES, V49, pD884, DOI 10.1093/nar/gkaa942
- Hu GQ, 2013, NAT IMMUNOL, V14, P1190, DOI 10.1038/ni.2712
- Huang ZK, 2016, SCI REP-UK, V6, DOI 10.1038/srep19705
- Joung J, 2017, NATURE, V548, P343, DOI 10.1038/nature23451
- Kumar A, 2020, FRONT MICROBIOL, V11, DOI 10.3389/fmicb.2020.01716
- Langmead B, 2012, NAT METHODS, V9, P357, DOI [10.1038/NMETH.1923, 10.1038/nmeth.1923]
- Lemaire J, 2013, PLOS NEGLECT TROP D, V7, DOI 10.1371/journal.pntd.0002478
- Li NN, 2019, BIOMED PHARMACOTHER, V117, DOI 10.1016/j.biopha.2019.109015
- Li ZT, 2022, bioRxiv, DOI [10.1101/2022.06.03.494777, DOI 10.1101/2022.06.03.494777]
- Liao Y, 2014, BIOINFORMATICS, V30, P923, DOI 10.1093/bioinformatics/btt656
- Lin H, 2021, J ALLERGY CLIN IMMUN, V147, pAB242
- Liu JX, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.679658
- Lv WC, 2021, J CELL MOL MED, V25, P10403, DOI 10.1111/jcmm.16969
- Maarouf M, 2019, CELL MICROBIOL, V21, DOI 10.1111/cmi.13036
- Mamani-Huanca M, 2021, INT J MOL SCI, V22, DOI 10.3390/ijms22136883
- Muxel SM, 2019, INT J MOL SCI, V20, DOI 10.3390/ijms20246248
- Maretti-Mira AC, 2012, PLOS NEGLECT TROP D, V6, DOI 10.1371/journal.pntd.0001816
- Maruyama SR, 2022, FRONT IMMUNOL, V13, DOI 10.3389/fimmu.2022.784463
- McCarthy DJ, 2012, NUCLEIC ACIDS RES, V40, P4288, DOI 10.1093/nar/gks042
- Menard KL, 2018, SCI REP-UK, V8, DOI 10.1038/s41598-018-33274-5
- Mesquita I, 2020, CELL REP, V30, P4052, DOI 10.1016/j.celrep.2020.02.098
- Moharrami NN, 2018, PLOS ONE, V13, DOI 10.1371/journal.pone.0207374
- Morita K, 2015, LEUKEMIA, V29, P2248, DOI 10.1038/leu.2015.137
- Muxel SM, 2018, FRONT MICROBIOL, V8, DOI 10.3389/fmicb.2017.02682
- Muxel SM, 2017, SCI REP-UK, V7, DOI 10.1038/srep44141
- Niu LM, 2020, SCI ADV, V6, DOI 10.1126/sciadv.aaz2059
- Novais FO, 2014, J INFECT DIS, V209, P1288, DOI 10.1093/infdis/jiu013
- Fortea JOY, 2009, BMC GENOMICS, V10, DOI 10.1186/1471-2164-10-119
- Otto NA, 2021, J IMMUNOL, V206, P827, DOI 10.4049/jimmunol.2000702
- Parmar N, 2018, J IMMUNOL, V201, P957, DOI 10.4049/jimmunol.1800062
- Paul S, 2020, 3 BIOTECH, V10, DOI 10.1007/s13205-020-02498-6
- Pinkney HR, 2020, NON-CODING RNA, V6, DOI 10.3390/ncrna6040049
- Ramos-Sanchez EM, 2022, FRONT CELL INFECT MI, V12, DOI 10.3389/fcimb.2022.826039
- Riege K, 2017, SCI REP-UK, V7, DOI 10.1038/srep40598
- Rinn JL, 2012, ANNU REV BIOCHEM, V81, P145, DOI 10.1146/annurev-biochem-051410-092902
- Ruy PD, 2019, RNA BIOL, V16, P639, DOI 10.1080/15476286.2019.1574161
- Sacks D, 2002, NAT REV IMMUNOL, V2, P845, DOI 10.1038/nri933
- Sacramento LA, 2020, PLOS PATHOG, V16, DOI 10.1371/journal.ppat.1008435
- Salloum T, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.702240
- Sanz CR, 2022, FRONT IMMUNOL, V12, DOI 10.3389/fimmu.2021.794627
- Schatz V, 2016, J IMMUNOL, V197, P4034, DOI 10.4049/jimmunol.1601080
- Soong L, 2012, FRONT IMMUNOL, V3, DOI 10.3389/fimmu.2012.00058
- Souza MD, 2021, FRONT CELL INFECT MI, V11, DOI 10.3389/fcimb.2021.687647
- Subramanian A, 2005, P NATL ACAD SCI USA, V102, P15545, DOI 10.1073/pnas.0506580102
- Tannahill GM, 2013, NATURE, V496, P238, DOI 10.1038/nature11986
- Vollmers AC, 2021, J BIOL CHEM, V296, DOI 10.1016/j.jbc.2021.100784
- Westermann AJ, 2016, NATURE, V529, P496, DOI 10.1038/nature16547
- Wheaton WW, 2011, AM J PHYSIOL-CELL PH, V300, pC385, DOI 10.1152/ajpcell.00485.2010
- Yang L, 2011, GENOME BIOL, V12, DOI 10.1186/gb-2011-12-2-r16
- Yang XF, 2016, SCI REP-UK, V6, DOI 10.1038/srep38963
- Yang ZY, 2007, J IMMUNOL, V178, P1077, DOI 10.4049/jimmunol.178.2.1077
- Zamboni DS, 2019, CURR OPIN MICROBIOL, V52, P70, DOI 10.1016/j.mib.2019.05.005
- Zhang XY, 2022, GENE THER, V29, P566, DOI 10.1038/s41434-020-00201-1
- Zhang Y, 2013, MOL CELL, V51, P792, DOI 10.1016/j.molcel.2013.08.017
- Zheng F, 2021, NAT COMMUN, V12, DOI 10.1038/s41467-021-21535-3