Comparative transcriptomic analysis of long noncoding RNAs in Leishmania-infected human macrophages

Carregando...
Imagem de Miniatura
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
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
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
  1. Aoki JI, 2019, SCI REP-UK, V9, DOI 10.1038/s41598-019-56305-1
  2. Barriocanal M, 2022, FRONT IMMUNOL, V13, DOI 10.3389/fimmu.2022.829335
  3. Bayer-Santos E, 2017, FRONT MICROBIOL, V8, DOI 10.3389/fmicb.2017.00474
  4. Bensaoud C, 2019, TRENDS PARASITOL, V35, P715, DOI 10.1016/j.pt.2019.06.012
  5. Bichiou H, 2021, FRONT CELL INFECT MI, V11, DOI 10.3389/fcimb.2021.748738
  6. Burza S, 2018, LANCET, V392, P951, DOI 10.1016/S0140-6736(18)31204-2
  7. Carlsen ED, 2013, INFECT IMMUN, V81, P3966, DOI 10.1128/IAI.00770-13
  8. Castro FF, 2017, MOL BIOCHEM PARASIT, V214, P69, DOI [10.1016/j.molblopara.2017.04.002, 10.1016/j.molbiopara.2017.04.002]
  9. Chen EY, 2013, BMC BIOINFORMATICS, V14, DOI 10.1186/1471-2105-14-128
  10. Chen JJ, 2004, NUCLEIC ACIDS RES, V32, P4812, DOI 10.1093/nar/gkh818
  11. Chen YG, 2017, NAT IMMUNOL, V18, P962, DOI 10.1038/ni.3771
  12. Colineau L, 2018, J BIOL CHEM, V293, P12805, DOI [10.1074/jbc.RA118.002462, 10.1074/jbc.ra118.002462]
  13. Das A, 2018, FRONT IMMUNOL, V9, DOI 10.3389/fimmu.2018.00022
  14. Dashti S, 2020, SCI REP-UK, V10, DOI 10.1038/s41598-020-76024-2
  15. de Lima DS, 2019, P NATL ACAD SCI USA, V116, P17121, DOI 10.1073/pnas.1822046116
  16. Di Fiore A, 2018, OXID MED CELL LONGEV, V2018, DOI 10.1155/2018/2018306
  17. Diotallevi A, 2018, FRONT MICROBIOL, V9, DOI 10.3389/fmicb.2018.01019
  18. Du Y, 2020, FRONT ONCOL, V10, DOI 10.3389/fonc.2020.580176
  19. Dumas C, 2006, EUKARYOT CELL, V5, P2033, DOI 10.1128/EC.00147-06
  20. Durinck S, 2009, NAT PROTOC, V4, P1184, DOI 10.1038/nprot.2009.97
  21. Ebert MS, 2007, NAT METHODS, V4, P721, DOI 10.1038/NMETH1079
  22. Favila MA, 2014, J IMMUNOL, V192, P5863, DOI 10.4049/jimmunol.1203230
  23. Fernandes JCR, 2019, NON-CODING RNA, V5, DOI 10.3390/ncrna5010017
  24. Fernandes MC, 2016, MBIO, V7, DOI 10.1128/mBio.00027-16
  25. Ferreira C, 2021, CURR OPIN MICROBIOL, V63, P231, DOI 10.1016/j.mib.2021.07.012
  26. Frohlich A, 2007, BLOOD, V109, P2023, DOI 10.1182/blood-2006-05-021600
  27. Gao R, 2022, BIOMED RES INT, V2022, DOI 10.1155/2022/5532118
  28. Gasparotto J, 2017, MEM I OSWALDO CRUZ, V112, P146, DOI 10.1590/0074-02760160403
  29. Gatto M, 2020, PLOS NEGLECT TROP D, V14, DOI 10.1371/journal.pntd.0007949
  30. Geraci NS, 2015, PARASITE IMMUNOL, V37, P43, DOI 10.1111/pim.12156
  31. Goncalves ANA, 2019, FRONT GENET, V10, DOI 10.3389/fgene.2019.00971
  32. Han YH, 2017, CELL REP, V20, P124, DOI 10.1016/j.celrep.2017.06.017
  33. Howe KL, 2021, NUCLEIC ACIDS RES, V49, pD884, DOI 10.1093/nar/gkaa942
  34. Hu GQ, 2013, NAT IMMUNOL, V14, P1190, DOI 10.1038/ni.2712
  35. Huang ZK, 2016, SCI REP-UK, V6, DOI 10.1038/srep19705
  36. Joung J, 2017, NATURE, V548, P343, DOI 10.1038/nature23451
  37. Kumar A, 2020, FRONT MICROBIOL, V11, DOI 10.3389/fmicb.2020.01716
  38. Langmead B, 2012, NAT METHODS, V9, P357, DOI [10.1038/NMETH.1923, 10.1038/nmeth.1923]
  39. Lemaire J, 2013, PLOS NEGLECT TROP D, V7, DOI 10.1371/journal.pntd.0002478
  40. Li NN, 2019, BIOMED PHARMACOTHER, V117, DOI 10.1016/j.biopha.2019.109015
  41. Li ZT, 2022, bioRxiv, DOI [10.1101/2022.06.03.494777, DOI 10.1101/2022.06.03.494777]
  42. Liao Y, 2014, BIOINFORMATICS, V30, P923, DOI 10.1093/bioinformatics/btt656
  43. Lin H, 2021, J ALLERGY CLIN IMMUN, V147, pAB242
  44. Liu JX, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.679658
  45. Lv WC, 2021, J CELL MOL MED, V25, P10403, DOI 10.1111/jcmm.16969
  46. Maarouf M, 2019, CELL MICROBIOL, V21, DOI 10.1111/cmi.13036
  47. Mamani-Huanca M, 2021, INT J MOL SCI, V22, DOI 10.3390/ijms22136883
  48. Muxel SM, 2019, INT J MOL SCI, V20, DOI 10.3390/ijms20246248
  49. Maretti-Mira AC, 2012, PLOS NEGLECT TROP D, V6, DOI 10.1371/journal.pntd.0001816
  50. Maruyama SR, 2022, FRONT IMMUNOL, V13, DOI 10.3389/fimmu.2022.784463
  51. McCarthy DJ, 2012, NUCLEIC ACIDS RES, V40, P4288, DOI 10.1093/nar/gks042
  52. Menard KL, 2018, SCI REP-UK, V8, DOI 10.1038/s41598-018-33274-5
  53. Mesquita I, 2020, CELL REP, V30, P4052, DOI 10.1016/j.celrep.2020.02.098
  54. Moharrami NN, 2018, PLOS ONE, V13, DOI 10.1371/journal.pone.0207374
  55. Morita K, 2015, LEUKEMIA, V29, P2248, DOI 10.1038/leu.2015.137
  56. Muxel SM, 2018, FRONT MICROBIOL, V8, DOI 10.3389/fmicb.2017.02682
  57. Muxel SM, 2017, SCI REP-UK, V7, DOI 10.1038/srep44141
  58. Niu LM, 2020, SCI ADV, V6, DOI 10.1126/sciadv.aaz2059
  59. Novais FO, 2014, J INFECT DIS, V209, P1288, DOI 10.1093/infdis/jiu013
  60. Fortea JOY, 2009, BMC GENOMICS, V10, DOI 10.1186/1471-2164-10-119
  61. Otto NA, 2021, J IMMUNOL, V206, P827, DOI 10.4049/jimmunol.2000702
  62. Parmar N, 2018, J IMMUNOL, V201, P957, DOI 10.4049/jimmunol.1800062
  63. Paul S, 2020, 3 BIOTECH, V10, DOI 10.1007/s13205-020-02498-6
  64. Pinkney HR, 2020, NON-CODING RNA, V6, DOI 10.3390/ncrna6040049
  65. Ramos-Sanchez EM, 2022, FRONT CELL INFECT MI, V12, DOI 10.3389/fcimb.2022.826039
  66. Riege K, 2017, SCI REP-UK, V7, DOI 10.1038/srep40598
  67. Rinn JL, 2012, ANNU REV BIOCHEM, V81, P145, DOI 10.1146/annurev-biochem-051410-092902
  68. Ruy PD, 2019, RNA BIOL, V16, P639, DOI 10.1080/15476286.2019.1574161
  69. Sacks D, 2002, NAT REV IMMUNOL, V2, P845, DOI 10.1038/nri933
  70. Sacramento LA, 2020, PLOS PATHOG, V16, DOI 10.1371/journal.ppat.1008435
  71. Salloum T, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.702240
  72. Sanz CR, 2022, FRONT IMMUNOL, V12, DOI 10.3389/fimmu.2021.794627
  73. Schatz V, 2016, J IMMUNOL, V197, P4034, DOI 10.4049/jimmunol.1601080
  74. Soong L, 2012, FRONT IMMUNOL, V3, DOI 10.3389/fimmu.2012.00058
  75. Souza MD, 2021, FRONT CELL INFECT MI, V11, DOI 10.3389/fcimb.2021.687647
  76. Subramanian A, 2005, P NATL ACAD SCI USA, V102, P15545, DOI 10.1073/pnas.0506580102
  77. Tannahill GM, 2013, NATURE, V496, P238, DOI 10.1038/nature11986
  78. Vollmers AC, 2021, J BIOL CHEM, V296, DOI 10.1016/j.jbc.2021.100784
  79. Westermann AJ, 2016, NATURE, V529, P496, DOI 10.1038/nature16547
  80. Wheaton WW, 2011, AM J PHYSIOL-CELL PH, V300, pC385, DOI 10.1152/ajpcell.00485.2010
  81. Yang L, 2011, GENOME BIOL, V12, DOI 10.1186/gb-2011-12-2-r16
  82. Yang XF, 2016, SCI REP-UK, V6, DOI 10.1038/srep38963
  83. Yang ZY, 2007, J IMMUNOL, V178, P1077, DOI 10.4049/jimmunol.178.2.1077
  84. Zamboni DS, 2019, CURR OPIN MICROBIOL, V52, P70, DOI 10.1016/j.mib.2019.05.005
  85. Zhang XY, 2022, GENE THER, V29, P566, DOI 10.1038/s41434-020-00201-1
  86. Zhang Y, 2013, MOL CELL, V51, P792, DOI 10.1016/j.molcel.2013.08.017
  87. Zheng F, 2021, NAT COMMUN, V12, DOI 10.1038/s41467-021-21535-3