Impact of Oncogenic Targets by Tumor-Suppressive miR-139-5p and miR-139-3p Regulation in Head and Neck Squamous Cell Carcinoma
We newly generated an RNA-sequencing-based microRNA (miRNA) expression signature of head and neck squamous cell carcinoma (HNSCC). Analysis of the signature revealed that both strands of some miRNAs, including miR-139-5p (the guide strand) and miR-139-3p (the passenger strand) of miR-139, were downr...
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| Veröffentlicht in: | International journal of molecular sciences 2021-09, Vol.22 (18), p.9947, Article 9947 |
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| creator | Koma, Ayaka Asai, Shunichi Minemura, Chikashi Oshima, Sachi Kinoshita, Takashi Kikkawa, Naoko Koshizuka, Keiichi Moriya, Shogo Kasamatsu, Atsushi Hanazawa, Toyoyuki Uzawa, Katsuhiro Seki, Naohiko |
| description | We newly generated an RNA-sequencing-based microRNA (miRNA) expression signature of head and neck squamous cell carcinoma (HNSCC). Analysis of the signature revealed that both strands of some miRNAs, including miR-139-5p (the guide strand) and miR-139-3p (the passenger strand) of miR-139, were downregulated in HNSCC tissues. Analysis of The Cancer Genome Atlas confirmed the low expression levels of miR-139 in HNSCC. Ectopic expression of these miRNAs attenuated the characteristics of cancer cell aggressiveness (e.g., cell proliferation, migration, and invasion). Our in silico analyses revealed a total of 28 putative targets regulated by pre-miR-139 (miR-139-5p and miR-139-3p) in HNSCC cells. Of these, the GNA12 (guanine nucleotide-binding protein subunit alpha-12) and OLR1 (oxidized low-density lipoprotein receptor 1) expression levels were identified as independent factors that predicted patient survival according to multivariate Cox regression analyses (p = 0.0018 and p = 0.0104, respectively). Direct regulation of GNA12 and OLR1 by miR-139-3p in HNSCC cells was confirmed through luciferase reporter assays. Moreover, overexpression of GNA12 and OLR1 was detected in clinical specimens of HNSCC through immunostaining. The involvement of miR-139-3p (the passenger strand) in the oncogenesis of HNSCC is a new concept in cancer biology. Our miRNA-based strategy will increase knowledge on the molecular pathogenesis of HNSCC. |
| doi_str_mv | 10.3390/ijms22189947 |
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Analysis of the signature revealed that both strands of some miRNAs, including miR-139-5p (the guide strand) and miR-139-3p (the passenger strand) of miR-139, were downregulated in HNSCC tissues. Analysis of The Cancer Genome Atlas confirmed the low expression levels of miR-139 in HNSCC. Ectopic expression of these miRNAs attenuated the characteristics of cancer cell aggressiveness (e.g., cell proliferation, migration, and invasion). Our in silico analyses revealed a total of 28 putative targets regulated by pre-miR-139 (miR-139-5p and miR-139-3p) in HNSCC cells. Of these, the GNA12 (guanine nucleotide-binding protein subunit alpha-12) and OLR1 (oxidized low-density lipoprotein receptor 1) expression levels were identified as independent factors that predicted patient survival according to multivariate Cox regression analyses (p = 0.0018 and p = 0.0104, respectively). Direct regulation of GNA12 and OLR1 by miR-139-3p in HNSCC cells was confirmed through luciferase reporter assays. Moreover, overexpression of GNA12 and OLR1 was detected in clinical specimens of HNSCC through immunostaining. The involvement of miR-139-3p (the passenger strand) in the oncogenesis of HNSCC is a new concept in cancer biology. Our miRNA-based strategy will increase knowledge on the molecular pathogenesis of HNSCC.</description><identifier>ISSN: 1661-6596</identifier><identifier>ISSN: 1422-0067</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms22189947</identifier><identifier>PMID: 34576110</identifier><language>eng</language><publisher>BASEL: Mdpi</publisher><subject>Binding sites ; Biochemistry & Molecular Biology ; Cancer ; Cell growth ; Cell proliferation ; Chemistry ; Chemistry, Multidisciplinary ; Ectopic expression ; expression signature ; Gene expression ; Genomes ; Guanine ; Guanine nucleotide-binding protein ; Head & neck cancer ; HNSCC ; Life Sciences & Biomedicine ; Medical prognosis ; Metastasis ; microRNA ; MicroRNAs ; miR-139-3p ; miR-139-5p ; miRNA ; Nucleotides ; Passengers ; Pathogenesis ; Physical Sciences ; Proteins ; Receptor density ; Science & Technology ; Squamous cell carcinoma ; tumor suppressor ; Tumorigenesis</subject><ispartof>International journal of molecular sciences, 2021-09, Vol.22 (18), p.9947, Article 9947</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). 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Analysis of the signature revealed that both strands of some miRNAs, including miR-139-5p (the guide strand) and miR-139-3p (the passenger strand) of miR-139, were downregulated in HNSCC tissues. Analysis of The Cancer Genome Atlas confirmed the low expression levels of miR-139 in HNSCC. Ectopic expression of these miRNAs attenuated the characteristics of cancer cell aggressiveness (e.g., cell proliferation, migration, and invasion). Our in silico analyses revealed a total of 28 putative targets regulated by pre-miR-139 (miR-139-5p and miR-139-3p) in HNSCC cells. Of these, the GNA12 (guanine nucleotide-binding protein subunit alpha-12) and OLR1 (oxidized low-density lipoprotein receptor 1) expression levels were identified as independent factors that predicted patient survival according to multivariate Cox regression analyses (p = 0.0018 and p = 0.0104, respectively). Direct regulation of GNA12 and OLR1 by miR-139-3p in HNSCC cells was confirmed through luciferase reporter assays. Moreover, overexpression of GNA12 and OLR1 was detected in clinical specimens of HNSCC through immunostaining. The involvement of miR-139-3p (the passenger strand) in the oncogenesis of HNSCC is a new concept in cancer biology. Our miRNA-based strategy will increase knowledge on the molecular pathogenesis of HNSCC.</description><subject>Binding sites</subject><subject>Biochemistry & Molecular Biology</subject><subject>Cancer</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Chemistry</subject><subject>Chemistry, Multidisciplinary</subject><subject>Ectopic expression</subject><subject>expression signature</subject><subject>Gene expression</subject><subject>Genomes</subject><subject>Guanine</subject><subject>Guanine nucleotide-binding protein</subject><subject>Head & neck cancer</subject><subject>HNSCC</subject><subject>Life Sciences & Biomedicine</subject><subject>Medical prognosis</subject><subject>Metastasis</subject><subject>microRNA</subject><subject>MicroRNAs</subject><subject>miR-139-3p</subject><subject>miR-139-5p</subject><subject>miRNA</subject><subject>Nucleotides</subject><subject>Passengers</subject><subject>Pathogenesis</subject><subject>Physical 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expression</topic><topic>Genomes</topic><topic>Guanine</topic><topic>Guanine nucleotide-binding protein</topic><topic>Head & neck cancer</topic><topic>HNSCC</topic><topic>Life Sciences & Biomedicine</topic><topic>Medical prognosis</topic><topic>Metastasis</topic><topic>microRNA</topic><topic>MicroRNAs</topic><topic>miR-139-3p</topic><topic>miR-139-5p</topic><topic>miRNA</topic><topic>Nucleotides</topic><topic>Passengers</topic><topic>Pathogenesis</topic><topic>Physical Sciences</topic><topic>Proteins</topic><topic>Receptor density</topic><topic>Science & Technology</topic><topic>Squamous cell carcinoma</topic><topic>tumor suppressor</topic><topic>Tumorigenesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Koma, Ayaka</creatorcontrib><creatorcontrib>Asai, Shunichi</creatorcontrib><creatorcontrib>Minemura, Chikashi</creatorcontrib><creatorcontrib>Oshima, Sachi</creatorcontrib><creatorcontrib>Kinoshita, 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miR-139-3p Regulation in Head and Neck Squamous Cell Carcinoma</atitle><jtitle>International journal of molecular sciences</jtitle><stitle>INT J MOL SCI</stitle><date>2021-09-14</date><risdate>2021</risdate><volume>22</volume><issue>18</issue><spage>9947</spage><pages>9947-</pages><artnum>9947</artnum><issn>1661-6596</issn><issn>1422-0067</issn><eissn>1422-0067</eissn><abstract>We newly generated an RNA-sequencing-based microRNA (miRNA) expression signature of head and neck squamous cell carcinoma (HNSCC). Analysis of the signature revealed that both strands of some miRNAs, including miR-139-5p (the guide strand) and miR-139-3p (the passenger strand) of miR-139, were downregulated in HNSCC tissues. Analysis of The Cancer Genome Atlas confirmed the low expression levels of miR-139 in HNSCC. Ectopic expression of these miRNAs attenuated the characteristics of cancer cell aggressiveness (e.g., cell proliferation, migration, and invasion). Our in silico analyses revealed a total of 28 putative targets regulated by pre-miR-139 (miR-139-5p and miR-139-3p) in HNSCC cells. Of these, the GNA12 (guanine nucleotide-binding protein subunit alpha-12) and OLR1 (oxidized low-density lipoprotein receptor 1) expression levels were identified as independent factors that predicted patient survival according to multivariate Cox regression analyses (p = 0.0018 and p = 0.0104, respectively). Direct regulation of GNA12 and OLR1 by miR-139-3p in HNSCC cells was confirmed through luciferase reporter assays. Moreover, overexpression of GNA12 and OLR1 was detected in clinical specimens of HNSCC through immunostaining. The involvement of miR-139-3p (the passenger strand) in the oncogenesis of HNSCC is a new concept in cancer biology. Our miRNA-based strategy will increase knowledge on the molecular pathogenesis of HNSCC.</abstract><cop>BASEL</cop><pub>Mdpi</pub><pmid>34576110</pmid><doi>10.3390/ijms22189947</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-7036-0859</orcidid><orcidid>https://orcid.org/0000-0002-0431-8337</orcidid><orcidid>https://orcid.org/0000-0003-4731-7956</orcidid><orcidid>https://orcid.org/0000-0001-8539-6240</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; MDPI - Multidisciplinary Digital Publishing Institute; Web of Science - Science Citation Index Expanded - 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; PubMed Central |
| subjects | Binding sites Biochemistry & Molecular Biology Cancer Cell growth Cell proliferation Chemistry Chemistry, Multidisciplinary Ectopic expression expression signature Gene expression Genomes Guanine Guanine nucleotide-binding protein Head & neck cancer HNSCC Life Sciences & Biomedicine Medical prognosis Metastasis microRNA MicroRNAs miR-139-3p miR-139-5p miRNA Nucleotides Passengers Pathogenesis Physical Sciences Proteins Receptor density Science & Technology Squamous cell carcinoma tumor suppressor Tumorigenesis |
| title | Impact of Oncogenic Targets by Tumor-Suppressive miR-139-5p and miR-139-3p Regulation in Head and Neck Squamous Cell Carcinoma |
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