Top

Inflammation Research

Published in:

01-07-2020 | Kidney Injury | Original Researh Article

SIKIAT1/miR-96/FOXA1 axis regulates sepsis-induced kidney injury through induction of apoptosis

Authors: Shijun Lu, Haibin Wu, Jianhua Xu, Zhaofeng He, Haiyan Li, Chao Ning

Published in: Inflammation Research | Issue 7/2020

Abstract

Objective and design

Nowadays, sepsis-induced acute kidney injury (AKI) has gradually become a global problem for its high incidence and increasing mortality. Previous study has reported lncRNA ENST00000452391.1 in sepsis patients. However, its potential biological function and downstream molecular mechanism are still mysterious.

Methods and results

Our study found that it was upregulated in sepsis-induced AKI patients, so it was identified as “sepsis-induced kidney injury associated transcript 1 (SIKIAT1)”. We used lipopolysaccharide (LPS) stimulated HK-2 cells as an in vitro model to demonstrated that SIKIAT1 acts as a ceRNA for miR-96-3p to enhance FOXA1 expression and promote HK-2 cell apoptosis.

Conclusion

Therefore, it could be a potential biomarker and therapeutic target for sepsis-induced AKI in the development of disease.

Available only for authorised users

Gao Y-L, Zhai J-H, Chai Y-F. Recent advances in the molecular mechanisms underlying pyroptosis in sepsis. Mediators Inflamm. 2018. https://doi.org/10.1155/2018/5823823.CrossRefPubMedPubMedCentral

Armstrong BA, Betzold RD, May AK. Sepsis and septic shock strategies. Surg Clin North Am. 2017;97(6):1339–79. https://doi.org/10.1016/j.suc.2017.07.003.CrossRefPubMed

Shankar-Hari M, Phillips GS, Levy ML, Seymour CW, Liu VX, Deutschman CS, et al. Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):775–87. https://doi.org/10.1001/jama.2016.0289.CrossRefPubMedPubMedCentral

Mårtensson J, Bellomo R. Sepsis-induced acute kidney injury. Crit Care Clin. 2015;31(4):649–60. https://doi.org/10.1016/j.ccc.2015.06.003.CrossRefPubMed

Gómez H, Kellum JA. Sepsis-induced acute kidney injury. Curr Opin Crit Care. 2016;22(6):546–53. https://doi.org/10.1097/MCC.0000000000000356.CrossRefPubMedPubMedCentral

Zarbock A, Gomez H, Kellum JA. Sepsis-induced acute kidney injury revisited: pathophysiology, prevention and future therapies. Curr Opin Crit Care. 2014;20(6):588–95. https://doi.org/10.1097/MCC.0000000000000153.CrossRefPubMedPubMedCentral

Gomez H, Ince C, De Backer D, Pickkers P, Payen D, Hotchkiss J, et al. A unified theory of sepsis-induced acute kidney injury: inflammation, microcirculatory dysfunction, bioenergetics, and the tubular cell adaptation to injury. Shock. 2014;41(1):3–11. https://doi.org/10.1097/SHK.0000000000000052.CrossRefPubMedPubMedCentral

Garofalo AM, Lorente-Ros M, Goncalvez G, Carriedo D, Ballén-Barragán A, Villar-Fernández A, et al. Histopathological changes of organ dysfunction in sepsis. Intensive Care Med Exp. 2019;7(Suppl 1):45. https://doi.org/10.1186/s40635-019-0236-3.CrossRefPubMedPubMedCentral

Hoste EAJ, Kellum JA, Selby NM, Zarbock A, Palevsky PM, Bagshaw SM, et al. Global epidemiology and outcomes of acute kidney injury. Nat Rev Nephrol. 2018;14(10):607–25. https://doi.org/10.1038/s41581-018-0052-0.CrossRefPubMed

10.

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

11.

Ferrè F, Colantoni A, Helmer-Citterich M. Revealing protein-lncRNA interaction. Brief Bioinform. 2016;17(1):106–16. https://doi.org/10.1093/bib/bbv031.CrossRefPubMed

12.

Valadkhan S, Gunawardane LS. lncRNA-mediated regulation of the interferon response. Virus Res. 2016;212:127–36. https://doi.org/10.1016/j.virusres.2015.09.023.CrossRefPubMed

13.

Kumar MM, Goyal R. LncRNA as a therapeutic target for angiogenesis. Curr Top Med Chem. 2017;17(15):1750–7. https://doi.org/10.2174/1568026617666161116144744.CrossRefPubMedPubMedCentral

14.

Peng WX, Koirala P, Mo YY. LncRNA-mediated regulation of cell signaling in cancer. Oncogene. 2017;36(41):5661–7. https://doi.org/10.1038/onc.2017.184.CrossRefPubMedPubMedCentral

15.

Murphy MB, Medvedev AE. Long noncoding RNAs as regulators of Toll-like receptor signaling and innate immunity. J Leukoc Biol. 2016;99(6):839–50. https://doi.org/10.1189/jlb.2RU1215-575R.CrossRefPubMedPubMedCentral

16.

Mathy NW, Chen X-M. Long non-coding RNAs (lncRNAs) and their transcriptional control of inflammatory responses. J Biol Chem. 2017;292(30):12375–82. https://doi.org/10.1074/jbc.R116.760884.CrossRefPubMedPubMedCentral

17.

Liu X, Hong C, Wu S, Song S, Yang Z, Cao L, et al. Downregulation of lncRNA TUG1 contributes to the development of sepsis-associated acute kidney injury via regulating miR-142–3p/sirtuin 1 axis and modulating NF-κB pathway. J Cell Biochem. 2019. https://doi.org/10.1002/jcb.28409.CrossRefPubMedPubMedCentral

18.

Fu D, Zhou K, Liu J, Zheng P, Li P, Cheng W, et al. Long non-coding RNA PlncRNA-1 regulates cell proliferation, apoptosis, and autophagy in septic acute kidney injury by regulating BCL2. Int J Clin Exp Pathol. 2018;11(1):314–23.PubMedPubMedCentral

19.

Lorenzen JM, Schauerte C, Kielstein JT, Hübner A, Martino F, Fiedler J, et al. Circulating long noncoding RNATapSaki is a predictor of mortality in critically ill patients with acute kidney injury. Clin Chem. 2015;61(1):191–201. https://doi.org/10.1373/clinchem.2014.230359.CrossRefPubMed

20.

Dai Y, Liang Z, Li Y, Li C, Chen L. Circulating long noncoding rnas as potential biomarkers of sepsis: a preliminary study. Genet Test Mol Biomarkers. 2017;21(11):649–57. https://doi.org/10.1089/gtmb.2017.0061.CrossRefPubMed

21.

Chen L, Zhou Y, Li H. LncRNA, miRNA and lncRNA-miRNA interaction in viral infection. Virus Res. 2018;257:25–322. https://doi.org/10.1016/j.virusres.2018.08.018.CrossRefPubMed

22.

Wang L-X, Wan C, Dong Z-B, Wang B-H, Liu H-Y, Li Y. Integrative analysis of long noncoding RNA (lncRNA), microRNA (miRNA) and mRNA expression and construction of a competing endogenous RNA (ceRNA) network in metastatic melanoma. Med Sci Monit. 2019;25:2896–907. https://doi.org/10.12659/MSM.913881.CrossRefPubMedPubMedCentral

23.

Katoh M, Katoh M. Human FOX gene family (Review). Int J Oncol. 2004;25(5):1495–500.PubMed

24.

Hu Q, Luo Z, Xu T, Zhang J-Y, Zhu Y, Chen W-X, et al. FOXA1: a promising prognostic marker in breast cancer. Asian Pac J Cancer Prev. 2014;15(1):11–6. https://doi.org/10.7314/apjcp.2014.15.1.11.CrossRefPubMed

25.

Bernardo GM, Keri RA. FOXA1: a transcription factor with parallel functions in development and cancer. Biosci Rep. 2012;32(2):113–30. https://doi.org/10.1042/BSR20110046.CrossRefPubMedPubMedCentral

26.

Li C, Wu J, Li Y, Xing G. Cytoprotective effect of heat shock protein 27 against lipopolysaccharide-induced apoptosis of renal epithelial HK-2 cells. Cell Physiol Biochem. 2017;41(6):2211–20. https://doi.org/10.1159/000475636.CrossRefPubMed

27.

Song L, Wei X, Zhang B, Luo X, Liu J, Feng Y, et al. Role of Foxa1 in regulation of bcl2 expression during oxidative-stress-induced apoptosis in A549 type II pneumocytes. Cell Stress Chaperones. 2009;14(4):417–25. https://doi.org/10.1007/s12192-008-0095-4.CrossRefPubMedPubMedCentral

28.

Skube SJ, Katz SA, Chipman JG, Tignanelli CJ. Acute Kidney Injury and Sepsis. Surg Infect (Larchmt). 2018;19(2):216–24. https://doi.org/10.1089/sur.2017.261.CrossRef

29.

Aguirre-Allende I, Gallego-Otaegui L, Elosegui-Aguirrezabala JL, Placer-Galán C, Enriquez-Navascués JM. Laparoscopy-induced severe renal failure after appendectomy. J Surg Case Rep. 2019. https://doi.org/10.1093/jscr/rjz079.CrossRefPubMedPubMedCentral

30.

Ren G-L, Zhu J, Li J, Meng X-M. Noncoding RNAs in acute kidney injury. J Cell Physiol. 2019;234(3):2266–76. https://doi.org/10.1002/jcp.27203.CrossRefPubMed

31.

Liu Z, Wang Y, Shu S, Cai J, Tang C, Dong Z. Non-coding RNAs in kidney injury and repair. Am J Physiol Cell Physiol. 2019;317(2):C177–C188188. https://doi.org/10.1152/ajpcell.00048.2019.CrossRefPubMed

32.

Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge R-M, Chang HY. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife. 2013. https://doi.org/10.7554/eLife.00762.CrossRefPubMedPubMedCentral

33.

Gomez JA, Wapinski OL, Yang YW, Bureau J-F, Gopinath S, Monack DM, et al. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-γ locus. Cell. 2013;152(4):743–54. https://doi.org/10.1016/j.cell.2013.01.015.CrossRefPubMedPubMedCentral

34.

Cui H, Xie N, Tan Z, Banerjee S, Thannickal VJ, Abraham E, et al. The human long noncoding RNA lnc-IL7R regulates the inflammatory response. Eur J Immunol. 2014;44(7):2085–95. https://doi.org/10.1002/eji.201344126.CrossRefPubMedPubMedCentral

35.

Imamura K, Imamachi N, Akizuki G, Kumakura M, Kawaguchi A, Nagata K, et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell. 2014;53(3):393–406. https://doi.org/10.1016/j.molcel.2014.01.009.CrossRefPubMed

36.

Li Z, Chao T-C, Chang K-Y, Lin N, Patil VS, Shimizu C, et al. The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL. Proc Natl Acad Sci USA. 2014;111(3):1002–7. https://doi.org/10.1073/pnas.1313768111.CrossRefPubMed

37.

Iiott NE, Heward JA, Roux B, Tsitsiou E, Fenwick PS, Lenzi L, et al. Long non-coding RNAs and enhancer RNAs regulate the lipopolysaccharide-induced inflammatory response in human monocytes. Nat Commun. 2014;5:3979. https://doi.org/10.1038/ncomms4979.CrossRefPubMedPubMedCentral

38.

Singh KK, Matkar PN, Muhammad S, Quan A, Gupta V, Teoh H, et al. Investigation of novel LPS-induced differentially expressed long non-coding RNAs in endothelial cells. Mol Cell Biochem. 2016;421(1–2):157–68. https://doi.org/10.1007/s11010-016-2797-8.CrossRefPubMed

39.

Tay Y, Rinn J, Pandolfi PP. The multilayered complexity of ceRNA crosstalk and competition. Nature. 2014;505(7483):344–52. https://doi.org/10.1038/nature12986.CrossRefPubMedPubMedCentral

40.

Yin Y, Gao H, Guo J, Gao Y. Effect of circular RNA UBAP2 silencing on proliferation and invasion of human lung cancer A549 cells and its mechanism. Zhongguo Fei Ai Za Zhi. 2017;20(12):800–7. https://doi.org/10.3779/j.issn.1009-3419.2017.12.02.CrossRefPubMed

41.

Gou L, Zou H, Li B. Long noncoding RNA MALAT1 knockdown inhibits progression of anaplastic thyroid carcinoma by regulating miR-200a-3p/FOXA1. Cancer Biol Ther. 2019;20(11):1355–65. https://doi.org/10.1080/15384047.2019.1617567.CrossRefPubMed

Title: SIKIAT1/miR-96/FOXA1 axis regulates sepsis-induced kidney injury through induction of apoptosis
Authors: Shijun Lu
Haibin Wu
Jianhua Xu
Zhaofeng He
Haiyan Li
Chao Ning
Publication date: 01-07-2020
Publisher: Springer International Publishing
Keywords: Kidney Injury
Acute Kidney Injury
Septicemia
Septicemia
Acute Kidney Injury
Published in: Inflammation Research / Issue 7/2020
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI: https://doi.org/10.1007/s00011-020-01350-0

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objective and design

Methods and results

Conclusion

Please log in to get access to this content

Other articles of this Issue 7/2020

Hydrogen attenuates sepsis-associated encephalopathy by NRF2 mediated NLRP3 pathway inactivation

Hepatitis B virus X protein promotes liver cell pyroptosis under oxidative stress through NLRP3 inflammasome activation

Jumonji domain containing-3 (JMJD3) inhibition attenuates IL-1β-induced chondrocytes damage in vitro and protects osteoarthritis cartilage in vivo

SARS-CoV-2-mediated inflammatory response in lungs: should we look at RAGE?

CHRFAM7A reduces monocyte/macrophage migration and colony formation in vitro

SARS-CoV-2 will continue to circulate in the human population: an opinion from the point of view of the virus-host relationship

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage