Contribution of signaling pathways associated with cellular senescence and regulatory non-coding RNAs to chronic obstructive pulmonary disease

Abstract

Chronic obstructive pulmonary disease (COPD) is a multifactorial disease of the respiratory system that affects the lung parenchyma and airways; it is one of the leading causes of death in the world, which explains the constant search for new approaches to diagnosis, treatment and prevention of the disease. COPD develops as a result of a complex interaction of molecular genetic factors, a network of epigenetic regulators, and environmental factors that are closely related to lifestyle. The molecular pathogenesis of COPD may include the mechanisms of alteration of the regulation of stressful reactions that prevent cellular senescence.

Non-coding RNAs play an important role in the regulation of various intracellular signaling pathways and is the most relevant subject of genetic studies of various pathological phenotypes. The expression profile of long non-coding RNA is often disregulated in various diseases. Information on the role of long non-coding RNA in the development of COPD is limited. Long non-coding RNA and the target-genes of signaling pathways involved in cellular senescence form a complex interactive network and may be targets for disease therapy.

The review presents the data concerning some aspects of the molecular pathogenesis of COPD, as well as role of long non-coding RNAs in the development of the COPD.

Keywords

chronic obstructive pulmonary disease / oxidative stress / cellular senescence / DNA damage / PI3K/AKT/mTOR signaling pathway / NRF2/KEAP1 signaling pathway / long non-coding RNAs (lncRNAs)

References

[1] Chuchalin AG, Avdeev SN, Aisanov ZR, et al. Federal Guidelines on diagnosis and treatment of chronic obstructive pulmonary disease. Pulmonology. 2022;32(3):356–392. (In Russ). doi: 10.18093/0869-0189-2022-32-3-356-392

[2] Чучалин А.Г., Авдеев С.Н., Айсанов З.Р., и др. Хроническая обструктивная болезнь легких: федеральные клинические рекомендации по диагностике и лечению // Пульмонология. 2022. Т. 32, № 3. С. 356–392. doi: 10.18093/0869-0189-2022-32-3-356-392

[3] Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: 2022 report [Internet]. [cited 2023 Feb 15]. Available from: https://goldcopd.org/2023-gold-report-2/

[4] Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: 2023 report [Internet]. [дата обращения: 15.02.2023]. Доступ по ссылке: https://goldcopd.org/2023-gold-report-2/

[5] Maselli DJ, Bhatt SP, Anzueto A, et al. Clinical epidemiology of COPD: insights from 10 years of the COPD gene study. Chest. 2019;156(2):228–238. doi: 10.1016/j.chest.2019.04.135

[6] Maselli D.J., Bhatt S.P., Anzueto A., et al. Clinical Epidemiology of COPD: Insights From 10 Years of the COPDGene Study // Chest. 2019. Vol. 156, N 2. P. 228–238. doi: 10.1016/j.chest.2019.04.135

[7] Chronic obstructive pulmonary disease (COPD). Geneva: World Health Organization; 2021 [internet]. [cited 2023 Feb 15]. Available from: https://www.who.int/news-room/fact-sheets/detail/chronic-obstructive-pulmonary-disease-(copd)

[8] Chronic obstructive pulmonary disease (COPD). Geneva: World Health Organization; 2021 [Internet]. [дата обращения: 15.02.2023]. Доступ по ссылке: https://www.who.int/news-room/fact-sheets/detail/chronic-obstructive-pulmonary-disease-(copd)

[9] Ragland MF, Benway CJ, Lutz SM, et al. Genetic advances in chronic obstructive pulmonary disease. Insights from COPD gene. Am J Respir Crit Care Med. 2019;200(6):677–690. doi: 10.1164/rccm.201808-1455SO

[10] Ragland M.F., Benway C.J., Lutz S.M., et al. Genetic advances in chronic obstructive pulmonary disease. Insights from COPDGene // Am J Respir Crit Care Med. 2019. Vol. 200, N 6. P. 677–690. doi: 10.1164/rccm.201808-1455SO

[11] Barnes PJ, Baker J, Donnelly LE. Cellular senescence as a mechanism and target in chronic lung diseases. Am J Respir Crit Care Med. 2019;200(5):556–564. doi:10.1164/rccm.201810-1975TR

[12] Barnes P.J., Baker J., Donnelly L.E. Cellular senescence as a mechanism and target in chronic lung diseases // Am J Respir Crit Care Med. 2019. Vol. 200, N 5. P. 556–564. doi: 10.1164/rccm.201810-1975TR

[13] Kan M, Shumyatcher M, Himes BE. Using omics approaches to understand pulmonary diseases. Respir Res. 2017;18(1):149. doi: 10.1186/s12931-017-0631-9

[14] Kan M., Shumyatcher M., Himes B.E. Using omics approaches to understand pulmonary diseases // Respir Res. 2017. Vol. 18, N 1. P. 149. doi: 10.1186/s12931-017-0631-9

[15] Balashenko NA, Dromashko SE. Long non-coding RNAs and their functions. Proceedings of the National Academy of Sciences of Belarus. Biological series. 2017;4:110–119. (In Russ).

[16] Балашенко Н.А., Дромашко С.Е. Длинные некодирующие РНК и их функции // Вес. Нац. акад. навук Беларусі. Сер. біял. навук. 2017. № 4. С. 110–119.

[17] Kopp F, Mendell JT. Functional classification and experimental dissection of long noncoding RNAs. Cell. 2018;172(3):393–407. doi: 10.1016/j.cell.2018.01.011

[18] Kopp F., Mendell J.T. Functional classification and experimental dissection of long noncoding RNAs // Cell. 2018. Vol. 172, N 3. P. 393–407. doi: 10.1016/j.cell.2018.01.011

[19] Puvvula PK. lncRNAs regulatory networks in cellular senescence. Int J Mol Sci. 2019;20(11):2615. doi: 10.3390/ijms20112615

[20] Puvvula P.K. lncRNAs regulatory networks in cellular senescence // Int J Mol Sci. 2019. Vol. 20, N 11. P. 2615. doi: 10.3390/ijms20112615

[21] Wu T, Du Y. lncRNAs: from basic research to medical application. Int J Biol Sci. 2017;13(3):295–307. doi: 10.7150/ijbs.16968

[22] Wu T., Du Y. lncRNAs: from basic research to medical application // Int J Mol Sci. 2017. Vol. 13, N 3. P. 295–307. doi: 10.7150/ijbs.16968

[23] Qu X, Dang X, Wang W, et al. Long noncoding RNAs and mRNA regulation in peripheral blood mononuclear cells of patients with chronic obstructive pulmonary disease. Mediators Inflamm. 2018;2018:7501851. doi: 10.1155/2018/7501851

[24] Qu X., Dang X., Wang W., et al. Long noncoding RNAs and mRNA regulation in peripheral blood mononuclear cells of patients with chronic obstructive pulmonary disease // Mediators Inflamm. 2018. Vol. 2018, P. 7501851. doi: 10.1155/2018/7501851

[25] Poulet C, Njock MS, Moermans C, et al. Exosomal long non-coding RNAs in lung diseases. Int J Mol Sci. 2020;21(10):3580. doi: 10.3390/ijms21103580

[26] Poulet C., Njock M.S., Moermans C., et al. Exosomal long non-coding rnas in lung diseases // Int J Mol Sci. 2020. Vol. 21, N 10. P. 3580. doi: 10.3390/ijms21103580

[27] Domej W, Oettl K, Renner W. Oxidative stress and free radicals in COPD-implications and relevance for treatment. Int J Chron Obstruct Pulmon Dis. 2014;9:1207–1224. doi: 10.2147/COPD.S51226

[28] Domej W., Oettl K., Renner W. Oxidative stress and free radicals in COPD-limplications and relevance for treatment // Int J Chron Obstruct Pulmon Dis. 2014. Vol. 9. P. 1207–1224. doi: 10.2147/COPD.S51226

[29] Choudhury G, MacNee W. Role of inflammation and oxidative stress in the pathology of ageing in COPD: potential therapeutic interventions. COPD. 2017;14(1):122–135. doi: 10.1080/15412555.2016.1214948

[30] Choudhury G., MacNee W. Role of inflammation and oxidative stress in the pathology of ageing in COPD: potential therapeutic interventions // COPD. 2017. Vol. 14, N 1. P. 122–135. doi: 10.1080/15412555.2016.1214948

[31] Barnes PJ. Senescence in COPD and its comorbidities. Annu Rev Physiol. 2017;79:517–539. doi: 10.1146/annurev-physiol-022516-034314

[32] Barnes P.J. Senescence in COPD and its comorbidities // Annu Rev Physiol. 2017. Vol. 79. P. 517–539. doi: 10.1146/annurev-physiol-022516-034314

[33] Hughes MJ, McGettrick HM, Sapey E. Shared mechanisms of multimorbidity in COPD, atherosclerosis and type-2 diabetes: the neutrophil as a potential inflammatory target. Eur Respir Rev. 2020;29(155):190102. doi: 10.1183/16000617.0102-2019

[34] Hughes M.J., McGettrick H.M., Sapey E. Shared mechanisms of multimorbidity in COPD, atherosclerosis and type-2 diabetes: the neutrophil as a potential inflammatory target // Eur Respir Rev. 2020. Vol. 29, N 155. P. 190102. doi: 10.1183/16000617.0102-2019

[35] Araya J, Kuwano K. Cellular senescence-an aging hallmark in chronic obstructive pulmonary disease pathogenesis. Respir Investig. 2022;60(1):33–44. doi: 10.1016/j.resinv.2021.09.003

[36] Araya J., Kuwano K. Cellular senescence-an aging hallmark in chronic obstructive pulmonary disease pathogenesis // Respir Investig. 2022. Vol. 60, N 1. P. 33–44. doi: 10.1016/j.resinv.2021.09.003

[37] Brandsma CA, de Vries M, Costa R, et al. Lung ageing and COPD: is there a role for ageing in abnormal tissue repair? Eur Respir Rev. 2017;26(146):170073. doi: 10.1183/16000617.0073-2017

[38] Brandsma C.A., de Vries M., Costa R., et al. Lung ageing and COPD: is there a role for ageing in abnormal tissue repair? // Eur Respir Rev. 2017. Vol. 26, N 146. P. 170073. doi: 10.1183/16000617.0073-2017

[39] Alder JK, Barkauskas CE, Limjunyawong N, et al. Telomere dysfunction causes alveolar stem cell failure. Proc Natl Acad Sci U S A. 2015;112(16):5099–5104. doi: 10.1073/pnas.1504780112

[40] Alder J.K., Barkauskas C.E., Limjunyawong N., at al. Telomere dysfunction causes alveolar stem cell failure // Proc Natl Acad Sci U S A. 2015. Vol. 112, N 16. P. 5099–5104. doi: 10.1073/pnas.1504780112

[41] Woldhuis RR, Heijink IH, van den Berge M, et al. COPD-derived fibroblasts secrete higher levels of senescence-associated secretory phenotype proteins. Thorax. 2021;76(5):508–511. doi: 10.1136/thoraxjnl-2020-215114

[42] Woldhuis R.R., Heijink I.H., van den Berge M., at al. COPD-derived fibroblasts secrete higher levels of senescence-associated secretory phenotype proteins // Thorax. 2021. Vol. 76, N 5. P. 508–511. doi: 10.1136/thoraxjnl-2020-215114

[43] Birch J, Barnes PJ, Passos JF. Mitochondria, telomeres and cell senescence: Implications for lung ageing and disease. Pharmacol Ther. 2018;183:34–49. doi: 10.1016/j.pharmthera.2017.10.005

[44] Birch J., Barnes P.J., Passos J.F. Mitochondria, telomeres and cell senescence: Implications for lung ageing and disease // Pharmacol Ther. 2018. Vol. 183. P. 34–49. doi: 10.1016/j.pharmthera.2017.10.005

[45] Birch J, Anderson RK, Correia-Melo C, et al. DNA damage response at telomeres contributes to lung aging and chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol. 2015;309(10):L1124–L1137. doi: 10.1152/ajplung.00293.2015

[46] Birch J., Anderson R.K., Correia-Melo C., et al. DNA damage response at telomeres contributes to lung aging and chronic obstructive pulmonary disease // Am J Physiol Lung Cell Mol Physiol. 2015. Vol. 309, N 10. P. L1124–1137. doi: 10.1152/ajplung.00293.2015

[47] Stanley SE, Chen JJ, Podlevsky JD, et al. Telomerase mutations in smokers with severe emphysema. J Clin Invest. 2015;125(2):563–570. doi: 10.1172/JCI78554

[48] Stanley S.E., Chen J.J., Podlevsky J.D., et al. Telomerase mutations in smokers with severe emphysema // J Clin Invest. 2015. Vol. 125, N 2. P. 563–570. doi: 10.1172/JCI78554

[49] Chen R, Zhang K, Chen H, et al. Telomerase deficiency causes alveolar stem cell senescence-associated low-grade inflammation in lungs. J Biol Chem. 2015;290(52):30813–30829. doi: 10.1074/jbc.M115.681619

[50] Chen R., Zhang K., Chen H., et al. Telomerase deficiency causes alveolar stem cell senescence-associated low-grade inflammation in lungs // J Biol Chem. 2015. Vol. 290, N 52. P. 30813–30829. doi: 10.1074/jbc.M115.681619

[51] Müller L, Di Benedetto S, Pawelec G. The immune system and its dysregulation with aging. Subcell Biochem. 2019;91:21–43. doi: 10.1007/978-981-13-3681-2_2

[52] Müller L., Di Benedetto S., Pawelec G. The immune system and its dysregulation with aging // Subcell Biochem. 2019. Vol. 91. P. 21–43. doi: 10.1007/978-981-13-3681-2_2

[53] Ersahin T, Tuncbag N, Cetin-Atalay R. The PI3K/AKT/mTOR interactive pathway. Mol Biosyst. 2015;11(7):1946–1954. doi: 10.1039/c5mb00101c

[54] Ersahin T., Tuncbag N., Cetin-Atalay R. The PI3K/AKT/mTOR interactive pathway // Mol Biosyst. 2015. Vol. 11, N 7. P. 1946–1954. doi: 10.1039/c5mb00101c

[55] Johnson SC, Rabinovitch PS, Kaeberlein M. mTOR is a key modulator of ageing and age-related disease. Nature. 2013;493(7432):338–345. doi: 10.1038/nature11861

[56] Johnson S.C., Rabinovitch P.S., Kaeberlein M. mTOR is a key modulator of ageing and age-related disease // Nature. 2013. Vol. 493, N 7432. P. 338–345. doi: 10.1038/nature11861

[57] Carosi JM, Fourrier C, Bensalem J, Sargeant TJ. The mTOR-lysosome axis at the centre of ageing. FEBS Open Bio. 2022;12(4):739–757. doi: 10.1002/2211-5463.13347

[58] Carosi J.M., Fourrier C., Bensalem J., et al. The mTOR-lysosome axis at the centre of ageing // FEBS Open Bio. 2022. Vol. 12, N 4. P. 739–757. doi: 10.1002/2211-5463.13347

[59] Herranz N, Gallage S, Mellone M, et al. mTOR regulates MAPKAPK2 translation to control the senescence-associated secretory phenotype. Nat Cell Biol. 2015;17(9):1205–1217. Corrected and republished from: Nat Cell Biol. 2015;17(10):1370. doi: 10.1038/ncb3225

[60] Herranz N., Gallage S., Mellone M., et al. mTOR regulates MAPKAPK2 translation to control the senescence-associated secretory phenotype // Nat Cell Biol. 2015. Vol. 17, N 9. P. 1205–1217. Corrected and republished from: Nat. Cell Biol. 2015. Vol. 17, N 10. P. 1370. doi: 10.1038/ncb3225

[61] To Y, Ito K, Kizawa Y, et al. Targeting phosphoinositide-3-kinase-delta with theophylline reverses corticosteroid insensitivity in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010;182(7):897–904. doi: 10.1164/rccm.200906-0937OC

[62] To Y., Ito K., Kizawa Y., et al. Targeting phosphoinositide-3-kinase-delta with theophylline reverses corticosteroid insensitivity in chronic obstructive pulmonary disease // Am J Respir Crit Care Med. 2010. Vol. 182, N 7. P. 897–904. doi: 10.1164/rccm.200906-0937OC

[63] Mitani A, Ito K, Vuppusetty C, et al. Restoration of corticosteroid sensitivity in chronic obstructive pulmonary disease by inhibition of mammalian target of rapamycin. Am J Respir Crit Care Med. 2016;193(2):143–153. doi: 10.1164/rccm.201503-0593OC

[64] Mitani A., Ito K., Vuppusetty C., et al. Restoration of corticosteroid sensitivity in chronic obstructive pulmonary disease by inhibition of mammalian target of rapamycin // Am J Respir Crit Care Med. 2016. Vol. 193, N 2. P. 143–153. doi: 10.1164/rccm.201503-0593OC

[65] Worby CA, Dixon JE. PTEN. Annu Rev Biochem. 2014;83:641–669. doi: 10.1146/annurev-biochem-082411-113907

[66] Worby C.A., Dixon J.E. PTEN // Annu Rev Biochem. 2014. Vol. 83. P. 641–669. doi: 10.1146/annurev-biochem-082411-113907

[67] Wang CH, Wu SB, Wu YT, et al. Oxidative stress response elicited by mitochondrial dysfunction: implication in the pathophysiology of aging. Exp Biol Med (Maywood). 2013;238(5):450–460. doi: 10.1177/1535370213493069

[68] Wang C.H., Wu S.B., Wu Y.T., et al. Oxidative stress response elicited by mitochondrial dysfunction: implication in the pathophysiology of aging // Exp Biol Med. (Maywood). 2013. Vol. 238, N 5. P. 450–460. doi: 10.1177/1535370213493069

[69] Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012;489(7414):101–108. doi: 10.1038/nature11233

[70] Djebali S., Davis C.A., Merkel A., et al. Landscape of transcription in human cells // Nature. 2012. Vol. 489, N 7414. P. 101–108. doi: 10.1038/nature11233

[71] Mattick JS, Amaral PP, Carninci P, et al. Long non-coding RNAs: definitions, functions, challenges and recommendations. Nat Rev Mol Cell Biol. 2023;24(6):430–447. doi: 10.1038/s41580-022-00566-8

[72] Mattick J.S., Amaral P.P., Carninci P., et al. Long non-coding RNAs: definitions, functions, challenges and recommendations // Nat Rev Mol Cell Biol. 2023. Vol. 24, N 6. P. 430–447. doi: 10.1038/s41580-022-00566-8

[73] Dahariya S, Paddibhatla I, Kumar S, et al. Long non-coding RNA: classification, biogenesis and functions in blood cells. Mol Immunol. 2019;112:82–92. doi: 10.1016/j.molimm.2019.04.011

[74] Dahariya S., Paddibhatla I., Kumar S., et al. Long non-coding RNA: classification, biogenesis and functions in blood cells // Mol Immunol. 2019. Vol. 112. P. 82–92. doi: 10.1016/j.molimm.2019.04.011

[75] Nojima T, Proudfoot NJ. Mechanisms of lncRNA biogenesis as revealed by nascent transcriptomics. Nat Rev Mol Cell Biol. 2022;23(6):389–406. doi: 10.1038/s41580-021-00447-6

[76] Nojima T., Proudfoot N.J. Mechanisms of lncRNA biogenesis as revealed by nascent transcriptomics // Nat Rev Mol Cell Biol. 2022. Vol. 23. N 6. P. 389–406. doi: 10.1038/s41580-021-00447-6

[77] Derrien T, Johnson R, Bussotti G, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22(9):1775–1789. doi: 10.1101/gr.132159.111

[78] 39. Derrien T., Johnson R., Bussotti G., et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression // Genome Res. 2012. Vol. 22, N 9. P. 1775–1789. doi: 10.1101/gr.132159.111

[79] Jarroux J, Morillon A, Pinskaya M. History, discovery, and classification of lncRNAs. Adv Exp Med Biol. 2017;1008:1–46. doi: 10.1007/978-981-10-5203-3_1

[80] Jarroux J., Morillon A., Pinskaya M. History, discovery, and classification of lncRNAs // Adv Exp Med Biol. 2017. Vol. 1008. P. 1–46. doi: 10.1007/978-981-10-5203-3_1

[81] Bridges MC, Daulagala AC, Kourtidis A. LNCcation: lncRNA localization and function. J Cell Biol. 2021;220(2):e202009045. doi: 10.1083/jcb.202009045

[82] Bridges M.C., Daulagala A.C., Kourtidis A. LNCcation: lncRNA localization and function // J Cell Biol. 2021. Vol. 220, N 2. P. e202009045. doi: 10.1083/jcb.202009045

[83] Statello L, Guo CJ, Chen LL, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 2021;22(2):96–118. doi: 10.1038/s41580-020-00315-9

[84] Statello L., Guo C.J., Chen L.L., Huarte M. Gene regulation by long non-coding RNAs and its biological functions // Nat Rev Mol Cell Biol. 2021. Vol. 22. N 2. P. 96–118. doi: 10.1038/s41580-020-00315-9

[85] Deforges J, Reis RS, Jacquet P, et al. Control of cognate sense mRNA translation by cis-natural antisense RNAs. Plant Physiol. 2019;180(1):305–322. doi: 10.1104/pp.19.00043

[86] Deforges J., Reis R.S., Jacquet P., et al. Control of cognate sense mRNA translation by cis-natural antisense RNAs // Plant Physiol. 2019. Vol. 180. N 1. P. 305–322. doi: 10.1104/pp.19.00043

[87] Pisignano G, Ladomery M. Epigenetic regulation of alternative splicing: how lncRNAs tailor the message. Noncoding RNA. 2021;7(1):21. doi: 10.3390/ncrna7010021

[88] Pisignano G., Ladomery M. Epigenetic regulation of alternative splicing: how lncRNAs tailor the message // Noncoding RNA. 2021. Vol. 7, N 1. P. 21. doi: 10.3390/ncrna7010021

[89] Li C, Ni YQ, Xu H, et al. Roles and mechanisms of exosomal non-coding RNAs in human health and diseases. Signal Transduct Target Ther. 2021;6(1):383. doi: 10.1038/s41392-021-00779-x

[90] Li C., Ni Y.Q., Xu H., et al. Roles and mechanisms of exosomal non-coding RNAs in human health and diseases // Signal Transduct Target Ther. 2021. Vol. 6, N 1. P. 383. doi: 10.1038/s41392-021-00779-x

[91] Lei Y, Guo W, Chen B, et al. Tumor-released lncRNA H19 promotes gefitinib resistance via packaging into exosomes in non-small cell lung cancer. Oncol Rep. 2018;40(6):3438–3446. doi: 10.3892/or.2018.6762

[92] Lei Y., Guo W., Chen B., et al. Tumor-released lncRNA H19 promotes gefitinib resistance via packaging into exosomes in non-small cell lung cancer // Oncol Rep. 2018. Vol. 40, N 6. P. 3438–3446. doi: 10.3892/or.2018.6762

[93] Zhang R, Xia Y, Wang Z, et al. Serum long non coding RNA MALAT-1 protected by exosomes is up-regulated and promotes cell proliferation and migration in non-small cell lung cancer. Biochem Biophys Res Commun. 2017;490(2):406–414. doi: 10.1016/j.bbrc.2017.06.055

[94] Zhang R., Xia Y., Wang Z., et al. Serum long non coding RNA MALAT-1 protected by exosomes is up-regulated and promotes cell proliferation and migration in non-small cell lung cancer // Biochem Biophys Res Commun. 2017. Vol. 490, N 2. P. 406–414. doi: 10.1016/j.bbrc.2017.06.055

[95] Zhang C, Xu L, Deng G, et al. Exosomal HOTAIR promotes proliferation, migration and invasion of lung cancer by sponging miR-203. Sci China Life Sci. 2020;63(8):1265–1268. doi: 10.1007/s11427-019-1579-x

[96] Zhang C., Xu L., Deng G., et al. Exosomal HOTAIR promotes proliferation, migration and invasion of lung cancer by sponging miR-203 // Sci China Life Sci. 2020. Vol. 63, N 8. P. 1265–1268. doi: 10.1007/s11427-019-1579-x

[97] Loganathan T, Doss C GP. Non-coding RNAs in human health and disease: potential function as biomarkers and therapeutic targets. Funct Integr Genomics. 2023;23(1):33. doi: 10.1007/s10142-022-00947-4

[98] Loganathan T., Doss C.G.P. Non-coding RNAs in human health and disease: potential function as biomarkers and therapeutic targets // Funct Genomics. 2023. Vol. 23, N 1. P. 33. doi: 10.1007/s10142-022-00947-4

[99] Devadoss D, Long C, Langley RJ, et al. Long noncoding transcriptome in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2019;61(6):678–688. doi: 10.1165/rcmb.2019-0184TR

[100] Devadoss D., Long C., Langley R.J., et al. Long noncoding transcriptome in chronic obstructive pulmonary disease // Am J Respir Cell Mol Biol. 2019. Vol. 61, N 6. P. 678–688. doi: 10.1165/rcmb.2019-0184TR

[101] Wang X, Shen C, Zhu J, et al. Long noncoding RNAs in the regulation of oxidative stress. Oxid Med Cell Longev. 2019;2019:1318795. doi: 10.1155/2019/1318795

[102] Wang X., Shen C., Zhu J., et al. Long noncoding RNAs in the regulation of oxidative stress // Oxid Med Cell Longev. 2019. Vol. 2019. P. 1318795. doi: 10.1155/2019/1318795

[103] Zeng R, Zhang R, Song X, et al. The long non-coding RNA MALAT1 activates Nrf2 signaling to protect human umbilical vein endothelial cells from hydrogen peroxide. Biochem Biophys Res Commun. 2018;495(4):2532–2538. doi: 10.1016/j.bbrc.2017.12.105

[104] Zeng R., Zhang R., Song X., et al. The long non-coding RNA MALAT1 activates Nrf2 signaling to protect human umbilical vein endothelial cells from hydrogen peroxide // Biochem Biophys Res Commun. 2018. Vol. 45, N 4. P. 2532–2538. doi: 10.1016/j.bbrc.2017.12.105

[105] Tano K, Onoguchi-Mizutani R, Yeasmin F, et al. Identification of minimal p53 promoter region regulated by MALAT1 in human lung adenocarcinoma cells. Front Genet. 2018;8:208. doi: 10.3389/fgene.2017.00208

[106] Tano K., Onoguchi-Mizutani R., Yeasmin F., et al. Identification of minimal p53 promoter region regulated by MALAT1 in human lung adenocarcinoma cells // Front Genet. 2018. Vol. 8, P. 208. doi: 10.3389/fgene.2017.00208

[107] Zhang X, He X, Liu Y, et al. MiR-101-3p inhibits the growth and metastasis of non-small cell lung cancer through blocking PI3K/AKT signal pathway by targeting MALAT-1. Biomed Pharmacother. 2017;93:1065–1073. doi: 10.1016/j.biopha.2017.07.005

[108] Zhang X., He X., Liu Y., et al. MiR-101-3p inhibits the growth and metastasis of non-small cell lung cancer through blocking PI3K/AKT signal pathway by targeting MALAT-1 // Biomed Pharmacother. 2017. N 93. P. 1065–1073. doi: 10.1016/j.biopha.2017.07.005

[109] Zhao S, Lin C, Yang T, et al. Expression of long non-coding RNA LUCAT1 in patients with chronic obstructive pulmonary disease and its potential functions in regulating cigarette smoke extract-induced 16HBE cell proliferation and apoptosis. J Clin Lab Anal. 2021;35(7):e23823. doi: 10.1002/jcla.23823

[110] Zhao S., Lin C., Yang T., et al. Expression of long non-coding RNA LUCAT1 in patients with chronic obstructive pulmonary disease and its potential functions in regulating cigarette smoke extract-induced 16HBE cell proliferation and apoptosis // J Clin Lab Anal. 2021. Vol. 35, N 7. P. e23823. doi: 10.1002/jcla.23823

[111] Ayesh S, Matouk I, Schneider T, et al. Possible physiological role of H19 RNA. Mol Carcinog. 2002;35(2):63–74. doi: 10.1002/mc.10075

[112] Ayesh S., Matouk I., Schneider T., et al. Possible physiological role of H19 RNA // Mol Carcinog. 2002. Vol. 35, N 2. P. 63–74. doi: 10.1002/mc.10075

[113] Xu JL, Hua T, Ding J, et al. FOXF2 aggravates the progression of non-small cell lung cancer through targeting lncRNA H19 to downregulate PTEN. Eur Rev Med Pharmacol Sci. 2019;23(24):10796–10802. doi: 10.26355/eurrev_201912_19782

[114] Xu J.L., Hua T., Ding J., et al. FOXF2 aggravates the progression of non-small cell lung cancer through targeting lncRNA H19 to downregulate PTEN // Eur Rev Med Pharmacol Sci. 2019. Vol. 23, N 24. P. 10796–10802. doi: 10.26355/eurrev_201912_19782

[115] Che J. Molecular mechanisms of the intracranial aneurysms and their association with the long noncoding ribonucleic acid ANRIL — a review of literature. Neurol India. 2017;65(4):718–728. doi: 10.4103/neuroindia.NI_1074_15

[116] Che J. Molecular mechanisms of the intracranial aneurysms and their association with the long noncoding ribonucleic acid ANRIL — a review of literature // Neurol India. 2017. Vol. 65, N 4. P. 718–728. doi: 10.4103/neuroindia.NI_1074_15

[117] Guo S, Zhang L, Zhang Y, et al. Long non-coding RNA TUG1 enhances chemosensitivity in non-small cell lung cancer by impairing microRNA-221-dependent PTEN inhibition. Aging (Albany NY). 2019;11(18):7553–7569. doi: 10.18632/aging.102271

[118] Guo S., Zhang L., Zhang Y., et al. Long non-coding RNA TUG1 enhances chemosensitivity in non-small cell lung cancer by impairing microRNA-221-dependent PTEN inhibition // Aging (Albany NY). 2019. Vol. 11, N 18. P. 7553–7569. doi: 10.18632/aging.102271

[119] Xia H, Xue J, Xu H, et al. Andrographolide antagonizes the cigarette smoke-induced epithelial-mesenchymal transition and pulmonary dysfunction through anti-inflammatory inhibiting HOTAIR. Toxicology. 2019;422:84–94. doi: 10.1016/j.tox.2019.05.009

[120] Xia H., Xue J., Xu H., et al. Andrographolide antagonizes the cigarette smoke-induced epithelial-mesenchymal transition and pulmonary dysfunction through anti-inflammatory inhibiting HOTAIR // Toxicology. 2019. N 422. P. 84–94. doi: 10.1016/j.tox.2019.05.009

[121] Dai Z, Liu X, Zeng H, Chen Y. Long noncoding RNA HOTAIR facilitates pulmonary vascular endothelial cell apoptosis via DNMT1 mediated hypermethylation of Bcl-2 promoter in COPD. Respir Res. 2022;23(1):356. doi: 10.1186/s12931-022-02234-z

[122] Dai Z., Liu X., Zeng H., Chen Y. Long noncoding RNA HOTAIR facilitates pulmonary vascular endothelial cell apoptosis via DNMT1 mediated hypermethylation of Bcl-2 promoter in COPD // Respir Res. 2022. Vol. 23, N 1. P. 356. doi: 10.1186/s12931-022-02234-z

[123] Yao Q, Zhang X, Chen D. Emerging roles and mechanisms of lncRNA FOXD3-AS1 in human diseases. Front Oncol. 2022;12:848296. doi: 10.3389/fonc.2022.848296

[124] Yao Q., Zhang X., Chen D. Emerging roles and mechanisms of lncRNA FOXD3-AS1 in human diseases // Front Oncol. 2022. N 12. P. 848296. doi: 10.3389/fonc.2022.848296

[125] Zhang D, Lee H, Haspel JA, Jin Y. Long noncoding RNA FOXD3-AS1 regulates oxidative stress-induced apoptosis via sponging microRNA-150. FASEB J. 2017;31(10):4472–4481. doi: 10.1096/fj.201700091R

[126] Zhang D., Lee H., Haspel J.A., Jin Y. Long noncoding RNA FOXD3-AS1 regulates oxidative stress-induced apoptosis via sponging microRNA-150 // FASEB J. 2017. Vol. 31, N 10. P. 4472–4481. doi: 10.1096/fj.201700091R

[127] Ghafouri-Fard S, Esmaeili M, Taheri M. H19 lncRNA: roles in tumorigenesis. Biomed Pharmacother. 2020;123:109774. doi: 10.1016/j.biopha.2019.109774

[128] Ghafouri-Fard S., Esmaeili M., Taheri M. H19 lncRNA: roles in tumorigenesis // Biomed Pharmacother. 2020. Vol. 123. P. 109774. doi: 10.1016/j.biopha.2019.109774

[129] Zhang E, Li W, Yin D, et al. c-Myc-regulated long non-coding RNA H19 indicates a poor prognosis and affects cell proliferation in non-small-cell lung cancer. Tumour Biol. 2016;37(3):4007–4015. Corrected and republished from: Tumour Biol. 2016;37(4):5653. doi: 10.1007/s13277-015-4185-5

[130] Zhang E., Li W., Yin D., et al. c-Myc-regulated long non-coding RNA H19 indicates a poor prognosis and affects cell proliferation in non-small-cell lung cancer // Tumour Biol. 2016. Vol. 37, N 3. P. 4007–4015. Corrected and republished from: Tumour Biol. 2016. Vol. 37, N 4. P. 5653. doi: 10.1007/s13277-015-4185-5

[131] Cai B, Ma W, Bi C, et al. Long noncoding RNA H19 mediates melatonin inhibition of premature senescence of c-kit(+) cardiac progenitor cells by promoting miR-675. J Pineal Res. 2016;61(1):82–95. doi: 10.1111/jpi.12331

[132] Cai B., Ma W., Bi C., et al. Long noncoding RNA H19 mediates melatonin inhibition of premature senescence of c-kit(+) cardiac progenitor cells by promoting miR-675 // J Pineal Res. 2016. Vol. 61, N 1. P. 82–95. doi: 10.1111/jpi.12331

[133] Borensztein M, Monnier P, Court F, et al. Myod and H19-Igf2 locus interactions are required for diaphragm formation in the mouse. Development. 2013;140(6):1231–1239. doi: 10.1242/dev.084665

[134] Borensztein M., Monnier P. Court F., et al. Myod and H19-Igf2 locus interactions are required for diaphragm formation in the mouse // Development. 2013. Vol. 140, N 6. P. 1231–1239. doi: 10.1242/dev.084665

[135] Shahdoust M, Hajizadeh E, Mozdarani H, Chehrei A. Finding genes discriminating smokers from non-smokers by applying a growing self-organizing clustering method to large airway epithelium cell microarray data. Asian Pac J Cancer Prev. 2013;14(1):111–116. doi: 10.7314/apjcp.2013.14.1.111

[136] Shahdoust M., Hajizadeh E., Mozdarani H., Chehrei A. Finding genes discriminating smokers from non-smokers by applying a growing self-organizing clustering method to large airway epithelium cell microarray data // Asian Pac J Cancer Prev. 2013. Vol. 14, N 1. P. 111–116. doi: 10.7314/apjcp.2013.14.1.111

[137] Kong Y, Hsieh CH, Alonso LC. ANRIL: A lncRNA at the CDKN2A/B locus with roles in cancer and metabolic disease. Front Endocrinol (Lausanne). 2018;9:405. doi: 10.3389/fendo.2018.00405

[138] Kong Y., Hsieh C.H., Alonso L.C. ANRIL: a lncRNA at the CDKN2A/B locus with roles in cancer and metabolic disease // Front Endocrinol (Lausanne). 2018. Vol. 9. P. 405. doi: 10.3389/fendo.2018.00405

[139] Cunnington MS, Santibanez Koref M, Mayosi BM, et al. Chromosome 9p21 SNPs associated with multiple disease phenotypes correlate with ANRIL expression. PLoS Genet. 2010;6(4):e1000899. doi: 10.1371/journal.pgen.1000899

[140] Cunnington M.S., Santibanez Koref M., Mayosi B.M., et al. Chromosome 9p21 SNPs associated with multiple disease phenotypes correlate with ANRIL expression // PLoS Genet. 2010. Vol. 6, N 4. P. e1000899. doi: 10.1371/journal.pgen.1000899

[141] Ge J, Geng S, Jiang H. Long noncoding RNAs antisense noncoding RNA in the INK4 locus (ANRIL) correlates with lower acute exacerbation risk, decreased inflammatory cytokines, and mild GOLD stage in patients with chronic obstructive pulmonary disease. J Clin Lab Anal. 2019;33(2):e22678. doi: 10.1002/jcla.22678

[142] Ge J., Geng S., Jiang H. Long noncoding RNAs antisense noncoding RNA in the INK4 locus (ANRIL) correlates with lower acute exacerbation risk, decreased inflammatory cytokines, and mild GOLD stage in patients with chronic obstructive pulmonary disease // J Clin Lab Anal. 2019. Vol. 33, N 2. P. e22678. doi: 10.1002/jcla.22678

[143] Khalil AM, Guttman M, Huarte M, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106(28):11667–11672. doi: 10.1073/pnas.0904715106

[144] Khalil A.M., Guttman M., Huarte M., et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression // Proc Natl Acad Sci U S A. 2009. Vol. 106, N 28. P. 11667–11672. doi: 10.1073/pnas.0904715106

[145] Li T, Liu Y, Xiao H, Xu G. Long non-coding RNA TUG1 promotes cell proliferation and metastasis in human breast cancer. Breast Cancer. 2017;24(4):535–543. doi: 10.1007/s12282-016-0736-x

[146] Li T., Liu Y., Xiao H., Xu G. Long non-coding RNA TUG1 promotes cell proliferation and metastasis in human breast cancer // Breast Cancer. 2017. Vol. 24, N 4. P. 535–543. doi: 10.1007/s12282-016-0736-x

[147] Gu W, Yuan Y, Wang L, et al. Long non-coding RNA TUG1 promotes airway remodelling by suppressing the miR-145-5p/DUSP6 axis in cigarette smoke-induced COPD. J Cell Mol Med. 2019;23(11):7200–7209. doi: 10.1111/jcmm.14389

[148] Gu W., Yuan Y., Wang L., et al. Long non-coding RNA TUG1 promotes airway remodelling by suppressing the miR-145-5p/DUSP6 axis in cigarette smoke-induced COPD // J Cell Mol Med. 2019. Vol. 23, N 11. P. 7200–7209. doi: 10.1111/jcmm.14389

[149] Tang W, Shen Z, Guo J, Sun S. Screening of long non-coding RNA and TUG1 inhibits proliferation with TGF-β induction in patients with COPD. Int J Chron Obstruct Pulmon Dis. 2016;11:2951–2964. doi: 10.2147/COPD.S109570

[150] Tang W., Shen Z., Guo J., Sun S. Screening of long non-coding RNA and TUG1 inhibits proliferation with TGF-β induction in patients with COPD // Int J Chron Obstruct Pulmon Dis. 2016. N 11. P. 2951–2964. doi: 10.2147/COPD.S109570

[151] Wu L, Murat P, Matak-Vinkovic D, et al. Binding interactions between long noncoding RNA HOTAIR and PRC2 proteins. Biochemistry. 2013;52(52):9519–9527. doi: 10.1021/bi401085h

[152] Wu L., Murat P., Matak-Vinkovic D., et al. Binding interactions between long noncoding RNA HOTAIR and PRC2 proteins // Biochemistry. 2013. Vol. 52, N 52. P. 9519–9527. doi: 10.1021/bi401085h

[153] Rinn JL, Kertesz M, Wang JK, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007;129(7):1311–1323. doi: 10.1016/j.cell.2007.05.022

[154] Rinn J.L., Kertesz M., Wang J.K., et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs // Cell. 2007. Vol. 129, N 7. P. 1311–1323. doi: 10.1016/j.cell.2007.05.022

[155] Zimta AA, Tigu AB, Braicu C, et al. An emerging class of long non-coding RNA With oncogenic role arises from the snoRNA host genes. Front Oncol. 2020;10:389. doi: 10.3389/fonc.2020.00389

[156] Zimta A.A., Tigu A.B., Braicu C., et al. An emerging class of long non-coding RNA with oncogenic role arises from the snoRNA host genes // Front Oncol. 2020. Vol. 10. P. 389. doi: 10.3389/fonc.2020.00389

[157] Shen Q, Zheng J, Wang X, et al. lncRNA SNHG5 regulates cell apoptosis and inflammation by miR-132/PTEN axis in COPD. Biomed Pharmacother. 2020;126:110016. doi: 10.1016/j.biopha.2020.110016

[158] Shen Q., Zheng J., Wang X., et al. lncRNA SNHG5 regulates cell apoptosis and inflammation by miR-132/PTEN axis in COPD // Biomed Pharmacother. 2020. N 126. P. 110016. doi: 10.1016/j.biopha.2020.110016

RIGHTS & PERMISSIONS

Eco-Vector