Abstract
Laryngeal papillomas (LP) is a difficult disease to manage due to its frequent recurrence, airway compromise, and risk of cancer. Recently, growing evidence indicates the aberrant expression of OGFPD1, a stress granule protein, links closely to the development of tumorigenesis; however, little is known about its role in LP progression. Here, we investigated the tumor promoting action of OGFOD1 in LP. The transcriptional and translational levels of OGFOD1 were significantly up-regulated in LP tissues and cells. Moreover, OGFOD1 promoted viability and proliferation, and inhibited LP cells apoptosis. We further revealed that OGFOD1 was directly targeted by miR-1224-5p, which was significantly down-regulated in LP. Overexpression of the miR-1224-5p suppressed OGFOD1-induced cell proliferation and viability, and promoted apoptosis of LP. In accordance, knockdown of miR-1224-5p inversed the inhibitory effects. In confederation of the central involvement of OGFOD1 in LP progression, targeting the miR-1224-5p/OGFOD1 pathway might provide a novel strategy for LP treatment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anis MM, Razavi MM, Xiao X, Soliman AMS (2018) Association of gastroesophageal reflux disease and laryngeal cancer World J Otorhinolaryngol. Head Neck Surg 4:278–281. https://doi.org/10.1016/j.wjorl.2017.12.011
Carthew RW, Sontheimer EJ (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136:642–655. https://doi.org/10.1016/j.cell.2009.01.035
Croce CM (2009) Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704–714. https://doi.org/10.1038/nrg2634
Deng G, Sui G (2013) Noncoding RNA in oncogenesis: a new era of identifying key players. Int J Mol Sci 14:18319–18349. https://doi.org/10.3390/ijms140918319
Gordan JD, Simon MC (2007) Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr Opin Genet Dev 17:71–77. https://doi.org/10.1016/j.gde.2006.12.006
Guo L et al (2017) Hepatic neuregulin 4 signaling defines an endocrine checkpoint for steatosis-to-NASH progression. J Clin Invest 127:4449–4461. https://doi.org/10.1172/JCI96324
Katada C et al (2008) Narrow band imaging for detecting metachronous superficial oropharyngeal and hypopharyngeal squamous cell carcinomas after chemoradiotherapy for head and neck cancers. Laryngoscope 118:1787–1790. https://doi.org/10.1097/MLG.0b013e31817f4d22
Katsenos S, Becker HD (2011) Recurrent respiratory papillomatosis: a rare chronic disease, difficult to treat, with potential to lung cancer transformation: apropos of two cases and a brief literature review. Case Rep Oncol 4:162–171. https://doi.org/10.1159/000327094
Kim JH et al (2015) OGFOD1 is required for breast cancer cell proliferation and is associated with poor prognosis in breast cancer. Oncotarget 6:19528–19541. https://doi.org/10.18632/oncotarget.3683
Komlos KF et al (2012) Tumor-specific and gender-specific pre-vaccination distribution of human papillomavirus types 6 and 11 in anogenital warts and laryngeal papillomas: a study on 574 tissue specimens. J Med Virol 84:1233–1241. https://doi.org/10.1002/jmv.23318
Lee LA, Cheng AJ, Fang TJ, Huang CG, Liao CT, Chang JT, Li HY (2008) High incidence of malignant transformation of laryngeal papilloma in Taiwan. Laryngoscope 118:50–55. https://doi.org/10.1097/MLG.0b013e318155a288
Marina O et al (2010) Serologic markers of effective tumor immunity against chronic lymphocytic leukemia include nonmutated B-cell antigens. Cancer Res 70:1344–1355. https://doi.org/10.1158/0008-5472.CAN-09-3143
Niu Y et al (2011) Lipopolysaccharide-induced miR-1224 negatively regulates tumour necrosis factor-alpha gene expression by modulating Sp1. Immunology 133:8–20. https://doi.org/10.1111/j.1365-2567.2010.03374.x
Poetker DM, Sandler AD, Scott DL, Smith RJ, Bauman NM (2002) Survivin expression in juvenile-onset recurrent respiratory papillomatosis. Ann Otol Rhinol Laryngol 111:957–961. https://doi.org/10.1177/000348940211101101
Qian J et al (2015) MiR-1224-5p acts as a tumor suppressor by targeting CREB1 in malignant gliomas. Mol Cell Biochem 403:33–41. https://doi.org/10.1007/s11010-015-2334-1
Ren HB, Shi XJ, Li Y (2016) Reduction of p38 mitogen-activated protein kinase and cyclooxygenase-2 signaling by isoflurane inhibits proliferation and apoptosis evasion in human papillomavirus-infected laryngeal papillomas. Exp Ther Med 12:3425–3432. https://doi.org/10.3892/etm.2016.3776
Saito K, Adachi N, Koyama H, Matsushita M (2010) OGFOD1, a member of the 2-oxoglutarate and iron dependent dioxygenase family, functions in ischemic signaling. FEBS Lett 584:3340–3347. https://doi.org/10.1016/j.febslet.2010.06.015
Semenza GL (2019) pharmacologic targeting of hypoxia-inducible factors. Annu Rev Pharmacol Toxicol 59:379–403. https://doi.org/10.1146/annurev-pharmtox-010818-021637
Singleton RS et al (2014) OGFOD1 catalyzes prolyl hydroxylation of RPS23 and is involved in translation control and stress granule formation. Proc Natl Acad Sci USA 111:4031–4036. https://doi.org/10.1073/pnas.1314482111
Steinberg BM, Meade R, Kalinowski S, Abramson AL (1990) Abnormal differentiation of human papillomavirus-induced laryngeal papillomas. Arch Otolaryngol 116:1167–1171
Sun LC et al (2015) cMyc-mediated activation of serine biosynthesis pathway is critical for cancer progression under nutrient deprivation conditions. Cell Res 25:429–444. https://doi.org/10.1038/cr.2015.33
Vancurova I, Wu R, Miskolci V, Sun S (2002) Increased p50/p50 NF- B activation in human papillomavirus type 6- or type 11-induced laryngeal papilloma tissue. J Virol 76:1533–1536. https://doi.org/10.1128/jvi.76.3.1533-1536.2002
Watanabe A, Tsujie H, Taniguchi M, Hosokawa M, Fujita M, Sasaki S (2006) Laryngoscopic detection of pharyngeal carcinoma in situ with narrowband imaging. Laryngoscope 116:650–654. https://doi.org/10.1097/01.mlg.0000204304.38797.34
Wehner KA, Schutz S, Sarnow P (2010) OGFOD1, a novel modulator of eukaryotic translation initiation factor 2alpha phosphorylation and the cellular response to stress. Mol Cell Biol 30:2006–2016. https://doi.org/10.1128/MCB.01350-09
White NMA, Fatoohi E, Metias M, Jung K, Stephan C, Yousef GM (2011) Metastamirs: a stepping stone towards improved cancer management. Nat Rev Clin Oncol 8:75–84. https://doi.org/10.1038/nrclinonc.2010.173
Wu QY et al (2357https) miR-1224-5p mediates mitochondrial damage to affect silica-induced pulmonary fibrosis by targeting BECN1. Int J Mol Sci 18:2357. https://doi.org/10.3390/ijms18112357
Yamamoto K, Ito S, Hanafusa H, Shimizu K, Ouchida M (2015) Uncovering direct targets of MiR-19a involved in lung cancer progression. PLoS ONE ONE 10:e0137887. https://doi.org/10.1371/journal.pone.0137887
Yu SN et al (2010) miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Can Res 70:6015–6025. https://doi.org/10.1158/0008-5472.Can-09-4531
Zhang P, Yao Q, Lu L, Li Y, Chen PJ, Duan C (2014) Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep 6:1110–1121. https://doi.org/10.1016/j.celrep.2014.02.011
Zhang P, Cao L, Fan P, Mei Y, Wu M (2016) LncRNA-MIF, a c-Myc-activated long non-coding RNA, suppresses glycolysis by promoting Fbxw7-mediated c-Myc degradation. EMBO Rep 17:1204–1220. https://doi.org/10.15252/embr.201642067
Funding
None.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care were followed. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent has derived from all participants.
Additional information
Communicated by Stefan Hohmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yin, D., Wang, Q., Wang, S. et al. OGFOD1 negatively regulated by miR-1224-5p promotes proliferation in human papillomavirus-infected laryngeal papillomas. Mol Genet Genomics 295, 675–684 (2020). https://doi.org/10.1007/s00438-020-01649-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-020-01649-x