Variants of MIRNA146A rs2910164 and MIRNA499 rs3746444 are associated with the development of cutaneous leishmaniasis caused by Leishmania guyanensis and with plasma chemokine IL-8
Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes includi...
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| Published in: | PLoS neglected tropical diseases Vol. 15; no. 9; p. e0009795 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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01-09-2021
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| Abstract | Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes including essential cellular functions. miR146-a acts as an inhibitor of interleukin 1 receptor associated kinase 1 (IRAK1) and tumour necrosis factor (TNF) receptor associated factor 6 (TRAF6) present in the toll-like receptors pathway while miR499a modulates TGF-β and TNF signalling pathways. Here, we investigated whether MIRNA146A rs2910164 and MIRNA499 rs3746444 variants are associated with the development of L. guyanensis (Lg)-cutaneous leishmaniasis (CL). The variants MIR146A rs2910164 and MIR499A rs3746444 were assessed in 850 patients with Lg-CL and 891 healthy controls by polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP). Plasma cytokines were measured using the BioPlex assay. Carriers of rs2910164 CC genotype have 30% higher odds of developing CL (ORadjage/sex = 1.3 [95%CI 0.9-1.8]; Padjage/sex 0.14) compared to individuals with the genotype GG (ORadjage/sex = 0.77 [95%CI 0.56-1.0]; Padjage/sex 0.14) if exposed to Lg-infection. Heterozygous GC individuals also showed lower odds of developing CL (ORadjage/sex = 0.77 [95%CI 0.5-1.1]; Padjage/sex 0.09). Homozygosity for the allele C is suggestive of an association with the development of Lg-CL among exposed individuals to Lg-infection. However, the odds of developing CL associated with the CC genotype was evident only in male individuals (ORadjage = 1.3 [95% CI = 0.9-2.0]; Padjage = 0.06). Individuals homozygous for the G allele tend to have higher plasma IL-8 and CCL5. Similarly, for the MIR499A rs3746444, an association with the G allele was only observed among male individuals (OR = 1.4 [1.0-1.9]; P = 0.009). In a dominant model, individuals with the G allele (GG-GA) when compared to the AA genotype reveals that carriers of the G allele have 40% elevated odds of developing Lg-CL (ORadjage = 1.4 [1.1-1.9]). Individuals with the GG genotype have higher odds of developing Lg-CL (ORadjage/sex = 2.0 [95%CI 0.83-5.0]; Padjage = 0.01. Individuals homozygous for the G allele have higher plasma IL-8. Genetic combinations of both variants revealed that male individuals exposed to Lg bearing three or four susceptible alleles have higher odds of developing Lg-CL (OR = 2.3 [95% CI 1.0-4.7]; p = 0.017). Both MIR146A rs2910164 and MIR499A rs3746444 are associated with the development of Lg-CL and this association is prevalent in male individuals. |
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| AbstractList | Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes including essential cellular functions. miR146-a acts as an inhibitor of interleukin 1 receptor associated kinase 1 (IRAK1) and tumour necrosis factor (TNF) receptor associated factor 6 (TRAF6) present in the toll-like receptors pathway while miR499a modulates TGF-β and TNF signalling pathways. Here, we investigated whether MIRNA146A rs2910164 and MIRNA499 rs3746444 variants are associated with the development of L. guyanensis (Lg)-cutaneous leishmaniasis (CL). The variants MIR146A rs2910164 and MIR499A rs3746444 were assessed in 850 patients with Lg-CL and 891 healthy controls by polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP). Plasma cytokines were measured using the BioPlex assay. Carriers of rs2910164 CC genotype have 30% higher odds of developing CL (ORadjage/sex = 1.3 [95%CI 0.9-1.8]; Padjage/sex 0.14) compared to individuals with the genotype GG (ORadjage/sex = 0.77 [95%CI 0.56-1.0]; Padjage/sex 0.14) if exposed to Lg-infection. Heterozygous GC individuals also showed lower odds of developing CL (ORadjage/sex = 0.77 [95%CI 0.5-1.1]; Padjage/sex 0.09). Homozygosity for the allele C is suggestive of an association with the development of Lg-CL among exposed individuals to Lg-infection. However, the odds of developing CL associated with the CC genotype was evident only in male individuals (ORadjage = 1.3 [95% CI = 0.9-2.0]; Padjage = 0.06). Individuals homozygous for the G allele tend to have higher plasma IL-8 and CCL5. Similarly, for the MIR499A rs3746444, an association with the G allele was only observed among male individuals (OR = 1.4 [1.0-1.9]; P = 0.009). In a dominant model, individuals with the G allele (GG-GA) when compared to the AA genotype reveals that carriers of the G allele have 40% elevated odds of developing Lg-CL (ORadjage = 1.4 [1.1-1.9]). Individuals with the GG genotype have higher odds of developing Lg-CL (ORadjage/sex = 2.0 [95%CI 0.83-5.0]; Padjage = 0.01. Individuals homozygous for the G allele have higher plasma IL-8. Genetic combinations of both variants revealed that male individuals exposed to Lg bearing three or four susceptible alleles have higher odds of developing Lg-CL (OR = 2.3 [95% CI 1.0-4.7]; p = 0.017). Both MIR146A rs2910164 and MIR499A rs3746444 are associated with the development of Lg-CL and this association is prevalent in male individuals. Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes including essential cellular functions. miR146-a acts as an inhibitor of interleukin 1 receptor associated kinase 1 (IRAK1) and tumour necrosis factor (TNF) receptor associated factor 6 (TRAF6) present in the toll-like receptors pathway while miR499a modulates TGF-[beta] and TNF signalling pathways. Here, we investigated whether MIRNA146A rs2910164 and MIRNA499 rs3746444 variants are associated with the development of L. guyanensis (Lg)-cutaneous leishmaniasis (CL). The variants MIR146A rs2910164 and MIR499A rs3746444 were assessed in 850 patients with Lg-CL and 891 healthy controls by polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP). Plasma cytokines were measured using the BioPlex assay. Carriers of rs2910164 CC genotype have 30% higher odds of developing CL (ORadj.sub.age/sex = 1.3 [95%CI 0.9-1.8]; Padj.sub.age/sex 0.14) compared to individuals with the genotype GG (ORadj.sub.age/sex = 0.77 [95%CI 0.56-1.0]; Padj.sub.age/sex 0.14) if exposed to Lg-infection. Heterozygous GC individuals also showed lower odds of developing CL (ORadj.sub.age/sex = 0.77 [95%CI 0.5-1.1]; Padj.sub.age/sex 0.09). Homozygosity for the allele C is suggestive of an association with the development of Lg-CL among exposed individuals to Lg-infection. However, the odds of developing CL associated with the CC genotype was evident only in male individuals (OR.sub.adjage = 1.3 [95% CI = 0.9-2.0]; P.sub.adjage = 0.06). Individuals homozygous for the G allele tend to have higher plasma IL-8 and CCL5. Similarly, for the MIR499A rs3746444, an association with the G allele was only observed among male individuals (OR = 1.4 [1.0-1.9]; P = 0.009). In a dominant model, individuals with the G allele (GG-GA) when compared to the AA genotype reveals that carriers of the G allele have 40% elevated odds of developing Lg-CL (ORadj.sub.age = 1.4 [1.1-1.9]). Individuals with the GG genotype have higher odds of developing Lg-CL (ORadj.sub.age/sex = 2.0 [95%CI 0.83-5.0]; P.sub.adjage = 0.01. Individuals homozygous for the G allele have higher plasma IL-8. Genetic combinations of both variants revealed that male individuals exposed to Lg bearing three or four susceptible alleles have higher odds of developing Lg-CL (OR = 2.3 [95% CI 1.0-4.7]; p = 0.017). Both MIR146A rs2910164 and MIR499A rs3746444 are associated with the development of Lg-CL and this association is prevalent in male individuals. Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes including essential cellular functions. miR146-a acts as an inhibitor of interleukin 1 receptor associated kinase 1 (IRAK1) and tumour necrosis factor (TNF) receptor associated factor 6 (TRAF6) present in the toll-like receptors pathway while miR499a modulates TGF-β and TNF signalling pathways. Here, we investigated whether MIRNA146A rs2910164 and MIRNA499 rs3746444 variants are associated with the development of L . guyanensis ( Lg )-cutaneous leishmaniasis (CL). The variants MIR146A rs2910164 and MIR499A rs3746444 were assessed in 850 patients with Lg -CL and 891 healthy controls by polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP). Plasma cytokines were measured using the BioPlex assay. Carriers of rs2910164 CC genotype have 30% higher odds of developing CL (ORadj age/sex = 1.3 [95%CI 0.9–1.8]; Padj age/sex 0.14) compared to individuals with the genotype GG (ORadj age/sex = 0.77 [95%CI 0.56–1.0]; Padj age/sex 0.14) if exposed to Lg -infection. Heterozygous GC individuals also showed lower odds of developing CL (ORadj age/sex = 0.77 [95%CI 0.5–1.1]; Padj age/sex 0.09). Homozygosity for the allele C is suggestive of an association with the development of Lg -CL among exposed individuals to Lg -infection. However, the odds of developing CL associated with the CC genotype was evident only in male individuals (OR adjage = 1.3 [95% CI = 0.9–2.0]; P adjage = 0.06). Individuals homozygous for the G allele tend to have higher plasma IL-8 and CCL5. Similarly, for the MIR499A rs3746444, an association with the G allele was only observed among male individuals (OR = 1.4 [1.0–1.9]; P = 0.009). In a dominant model, individuals with the G allele (GG-GA) when compared to the AA genotype reveals that carriers of the G allele have 40% elevated odds of developing Lg -CL (ORadj age = 1.4 [1.1–1.9]). Individuals with the GG genotype have higher odds of developing Lg -CL (ORadj age/sex = 2.0 [95%CI 0.83–5.0]; P adjage = 0.01. Individuals homozygous for the G allele have higher plasma IL-8. Genetic combinations of both variants revealed that male individuals exposed to Lg bearing three or four susceptible alleles have higher odds of developing Lg -CL (OR = 2.3 [95% CI 1.0–4.7]; p = 0.017). Both MIR146A rs2910164 and MIR499A rs3746444 are associated with the development of Lg -CL and this association is prevalent in male individuals. Leishmaniasis is caused by infection with Leishmania parasites. In regions with the presence of Leishmania parasites, all people do not develop the disease despite similar exposure. Only a proportion of inhabitants progress to the development of disease. Clinical manifestations depend on the vector and Leishmania species, as well the host genetic background and genetically determined immune responses. miRNAs play important roles in regulating gene expression and many biological processes including immune pathways. miR-146a targets TRAF6 and IRAK1 genes, that encode key adaptor molecules downstream of toll-like receptors (TLRs). TLRs are critical in immune response to Leishmania -infection. miR499-a modulates inflammation-related signalling pathways such as TGFβ, TNFα and TLR pathways. In this study, we showed that MIR146A and MIR499A variants are risk factors to developing cutaneous leishmaniasis caused by L . guyanensis in Amazonas state of Brazil. Individuals with these variants are susceptible to the development of CL. Leishmania are intracellular protozoan parasites that cause a wide spectrum of clinical manifestations in genetically susceptible individuals with an insufficient or balanced Th1 immune response to eliminate the parasite. MiRNAs play important regulatory role in numerous biological processes including essential cellular functions. miR146-a acts as an inhibitor of interleukin 1 receptor associated kinase 1 (IRAK1) and tumour necrosis factor (TNF) receptor associated factor 6 (TRAF6) present in the toll-like receptors pathway while miR499a modulates TGF-β and TNF signalling pathways. Here, we investigated whether MIRNA146A rs2910164 and MIRNA499 rs3746444 variants are associated with the development of L . guyanensis ( Lg )-cutaneous leishmaniasis (CL). The variants MIR146A rs2910164 and MIR499A rs3746444 were assessed in 850 patients with Lg -CL and 891 healthy controls by polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP). Plasma cytokines were measured using the BioPlex assay. Carriers of rs2910164 CC genotype have 30% higher odds of developing CL (ORadj age/sex = 1.3 [95%CI 0.9–1.8]; Padj age/sex 0.14) compared to individuals with the genotype GG (ORadj age/sex = 0.77 [95%CI 0.56–1.0]; Padj age/sex 0.14) if exposed to Lg -infection. Heterozygous GC individuals also showed lower odds of developing CL (ORadj age/sex = 0.77 [95%CI 0.5–1.1]; Padj age/sex 0.09). Homozygosity for the allele C is suggestive of an association with the development of Lg -CL among exposed individuals to Lg -infection. However, the odds of developing CL associated with the CC genotype was evident only in male individuals (OR adjage = 1.3 [95% CI = 0.9–2.0]; P adjage = 0.06). Individuals homozygous for the G allele tend to have higher plasma IL-8 and CCL5. Similarly, for the MIR499A rs3746444, an association with the G allele was only observed among male individuals (OR = 1.4 [1.0–1.9]; P = 0.009). In a dominant model, individuals with the G allele (GG-GA) when compared to the AA genotype reveals that carriers of the G allele have 40% elevated odds of developing Lg -CL (ORadj age = 1.4 [1.1–1.9]). Individuals with the GG genotype have higher odds of developing Lg -CL (ORadj age/sex = 2.0 [95%CI 0.83–5.0]; P adjage = 0.01. Individuals homozygous for the G allele have higher plasma IL-8. Genetic combinations of both variants revealed that male individuals exposed to Lg bearing three or four susceptible alleles have higher odds of developing Lg -CL (OR = 2.3 [95% CI 1.0–4.7]; p = 0.017). Both MIR146A rs2910164 and MIR499A rs3746444 are associated with the development of Lg -CL and this association is prevalent in male individuals. |
| Audience | Academic |
| Author | de Mesquita, Tirza Gabrielle Ramos Neto, José Pereira de Moura Gomes, Lissianne Augusta Matos de Souza, Mara Lúcia Gomes Queiroz, Krys Layane Guimarães Duarte de Lacerda, Thais Carneiro Júnior, Cláudio Marcello da Silveira Junior, José do Espírito Santo Guerra, Marcus Vinitius de Farias Ramasawmy, Rajendranath |
| AuthorAffiliation | 3 Programa de Pós-Graduação em Imunologia Básica e Aplicada, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil 1 Programa de Pós-Graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, Amazonas, Brazil Centro de Pesquisa Gonçalo Moniz-FIOCRUZ/BA, BRAZIL 6 Genomic Health Surveillance Network: Optimization of Assistance and Research in The State of Amazonas–REGESAM, Manaus, Amazonas, Brazil 2 Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil 5 Faculdade de Ciências Farmacêuticas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil 4 Faculdade de Medicina Nilton Lins, Universidade Nilton Lins, Manaus, Amazonas, Brazil |
| AuthorAffiliation_xml | – name: 4 Faculdade de Medicina Nilton Lins, Universidade Nilton Lins, Manaus, Amazonas, Brazil – name: 3 Programa de Pós-Graduação em Imunologia Básica e Aplicada, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil – name: 2 Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil – name: 5 Faculdade de Ciências Farmacêuticas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil – name: Centro de Pesquisa Gonçalo Moniz-FIOCRUZ/BA, BRAZIL – name: 1 Programa de Pós-Graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, Amazonas, Brazil – name: 6 Genomic Health Surveillance Network: Optimization of Assistance and Research in The State of Amazonas–REGESAM, Manaus, Amazonas, Brazil |
| Author_xml | – sequence: 1 givenname: Tirza Gabrielle Ramos orcidid: 0000-0001-5896-1005 surname: de Mesquita fullname: de Mesquita, Tirza Gabrielle Ramos organization: Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil – sequence: 2 givenname: José do Espírito Santo surname: Junior fullname: Junior, José do Espírito Santo organization: Faculdade de Medicina Nilton Lins, Universidade Nilton Lins, Manaus, Amazonas, Brazil – sequence: 3 givenname: Thais Carneiro surname: de Lacerda fullname: de Lacerda, Thais Carneiro organization: Faculdade de Medicina Nilton Lins, Universidade Nilton Lins, Manaus, Amazonas, Brazil – sequence: 4 givenname: Krys Layane Guimarães Duarte surname: Queiroz fullname: Queiroz, Krys Layane Guimarães Duarte organization: Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil – sequence: 5 givenname: Cláudio Marcello da Silveira surname: Júnior fullname: Júnior, Cláudio Marcello da Silveira organization: Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil – sequence: 6 givenname: José Pereira de Moura orcidid: 0000-0003-2177-7292 surname: Neto fullname: Neto, José Pereira de Moura organization: Faculdade de Ciências Farmacêuticas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil – sequence: 7 givenname: Lissianne Augusta Matos surname: Gomes fullname: Gomes, Lissianne Augusta Matos organization: Faculdade de Medicina Nilton Lins, Universidade Nilton Lins, Manaus, Amazonas, Brazil – sequence: 8 givenname: Mara Lúcia Gomes orcidid: 0000-0002-4273-2678 surname: de Souza fullname: de Souza, Mara Lúcia Gomes organization: Fundação de Medicina Tropical Doutor Heitor Vieira Dourado, Manaus, Amazonas, Brazil – sequence: 9 givenname: Marcus Vinitius de Farias surname: Guerra fullname: Guerra, Marcus Vinitius de Farias organization: Genomic Health Surveillance Network: Optimization of Assistance and Research in The State of Amazonas-REGESAM, Manaus, Amazonas, Brazil – sequence: 10 givenname: Rajendranath orcidid: 0000-0002-0538-0773 surname: Ramasawmy fullname: Ramasawmy, Rajendranath organization: Genomic Health Surveillance Network: Optimization of Assistance and Research in The State of Amazonas-REGESAM, Manaus, Amazonas, Brazil |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34543271$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2021 Public Library of Science 2021 de Mesquita et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 de Mesquita et al 2021 de Mesquita et al |
| Copyright_xml | – notice: COPYRIGHT 2021 Public Library of Science – notice: 2021 de Mesquita et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2021 de Mesquita et al 2021 de Mesquita et al |
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| DOI | 10.1371/journal.pntd.0009795 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. |
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| Title | Variants of MIRNA146A rs2910164 and MIRNA499 rs3746444 are associated with the development of cutaneous leishmaniasis caused by Leishmania guyanensis and with plasma chemokine IL-8 |
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