Influence of SphK1 on Inflammatory Responses in Lipopolysaccharide-Challenged RAW 264.7 Cells.

ALI/ARDS LPS PI3K/AKT signaling pathway Sphingosine kinase 1 (SphK1)

Journal

Cell biochemistry and biophysics
ISSN: 1559-0283
Titre abrégé: Cell Biochem Biophys
Pays: United States
ID NLM: 9701934

Informations de publication

Date de publication:
22 Jun 2024
Historique:
accepted: 13 06 2024
medline: 23 6 2024
pubmed: 23 6 2024
entrez: 22 6 2024
Statut: aheadofprint

Résumé

Acute lung injury (ALI) and acute respiratory distress syndrome (ARDS) are serious respiratory disorders caused by a variety of intrapulmonary and extrapulmonary factors. Their incidence is increasing year by year, with high morbidity and mortality rates and lack of effective treatment. Inflammation plays a crucial role in ALI development, with sphingosine kinase 1 (SphK1) being a pivotal enzyme influencing sphingolipid metabolism and participating in inflammatory responses. However, the specific impact and the signaling pathway underlying SphK1 in lipopolysaccharide (LPS)-induced ALI/ARDS are poorly understood. This investigation aimed to explore the influence of SphK1 on inflammation and delve into the mechanistic aspects of inflammation in RAW 264.7 cells during LPS-induced ALI, which is of great importance in providing new targets and strategies for ALI/ARDS treatment.

Identifiants

pubmed: 38909173
doi: 10.1007/s12013-024-01364-z
pii: 10.1007/s12013-024-01364-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Butt, Y., Kurdowska, A., & Allen, T. C. (2016). Acute lung injury: a clinical and molecular review. Archives of Pathology & Laboratory Medicine, 140(4), 345–350. https://doi.org/10.5858/arpa.2015-0519-RA .
doi: 10.5858/arpa.2015-0519-RA
Wang, C., Mei, X., Wu, Y., Yang, Y., & Zeng, Z. (2022). Cinobufagin alleviates lipopolysaccharide-induced acute lung injury by regulating autophagy through activation of the p53/mTOR pathway. Frontiers in Pharmacology, 13, 994625. https://doi.org/10.3389/fphar.2022.994625 .
doi: 10.3389/fphar.2022.994625 pubmed: 36518680 pmcid: 9742439
Ugwu, F. N., & Ho, J. (2019). Preclinical evidence of sphingosine kinase 1 inhibition in alleviation of intestinal epithelial injury in polymicrobial sepsis. Inflammation Research, 68(9), 723–726. https://doi.org/10.1007/s00011-019-01255-7 .
doi: 10.1007/s00011-019-01255-7 pubmed: 31154460
Khoei, S. G., Sadeghi, H., Samadi, P., Najafi, R., & Saidijam, M. (2021). Relationship between Sphk1/S1P and microRNAs in human cancers. Biotechnology and Applied Biochemistry, 68(2), 279–287. https://doi.org/10.1002/bab.1922 .
doi: 10.1002/bab.1922 pubmed: 32275078
Proia, R. L., & Hla, T. (2015). Emerging biology of sphingosine-1-phosphate: its role in pathogenesis and therapy. Journal of Clinical Investigation, 125(4), 1379–1387. https://doi.org/10.1172/jci76369 .
doi: 10.1172/jci76369 pubmed: 25831442 pmcid: 4409021
Chen, L., Li, L., Song, Y., & Lv, T. (2021). Blocking SphK1/S1P/S1PR1 signaling pathway alleviates lung injury caused by sepsis in acute ethanol intoxication mice. Inflammation, 44(6), 2170–2179. https://doi.org/10.1007/s10753-021-01490-3 .
doi: 10.1007/s10753-021-01490-3 pubmed: 34109517
Wang, Y., Wu, H., Deng, R., Dai, X. J., Bu, Y. H., Sun, M. H., Zhang, H., Wang, M. D., & Wang, R. H. (2021). Geniposide downregulates the VEGF/SphK1/S1P pathway and alleviates angiogenesis in rheumatoid arthritis in vivo and in vitro. Phytotherapy Research, 35(8), 4347–4362. https://doi.org/10.1002/ptr.7130 .
doi: 10.1002/ptr.7130 pubmed: 34152633
Yang, J., Wang, Y., Liu, H., Bi, J., & Lu, Y. (2017). C2-ceramide influences alveolar epithelial barrier function by downregulating Zo-1, occludin and claudin-4 expression. Toxicology Mechanisms and Methods, 27(4), 293–297. https://doi.org/10.1080/15376516.2017.1278812 .
doi: 10.1080/15376516.2017.1278812 pubmed: 28052715
Yan, C., Li, B., Liu, X., Deng, C., Cai, R., Shen, Y., & Tang, H. (2019). Involvement of multiple transcription factors in regulation of IL-β-induced MCP-1 expression in alveolar type II epithelial cells. Molecular Immunology, 111, 95–105. https://doi.org/10.1016/j.molimm.2019.04.013 .
doi: 10.1016/j.molimm.2019.04.013 pubmed: 31048100
Wolff, R. K., Brain, J. D., Patton, J. S., & Liggitt, D. (2016). Response to paper by Singh et al. “Hyperinsulinemia adversely affects lung structure and function”. American Journal of Physiology – Lung Cellular and Molecular Physiology, 311(1), L180–L182. https://doi.org/10.1152/ajplung.00187.2016 .
doi: 10.1152/ajplung.00187.2016 pubmed: 27407081
Yang, Y., Cheng, Y., Lian, Q. Q., Yang, L., Qi, W., Wu, D. R., Zheng, X., Liu, Y. J., Li, W. J., Jin, S. W., & Smith, F. G. (2013). Contribution of CFTR to alveolar fluid clearance by lipoxin A4 via PI3K/Akt pathway in LPS-induced acute lung injury. Mediators of Inflammation, 2013, 862628. https://doi.org/10.1155/2013/862628 .
doi: 10.1155/2013/862628 pubmed: 23766562 pmcid: 3671557
Zhong, R., Xia, T., Wang, Y., Ding, Z., Li, W., Chen, Y., Peng, M., Li, C., Zhang, H., & Shu, Z. (2022). Physalin B ameliorates inflammatory responses in lipopolysaccharide-induced acute lung injury mice by inhibiting NF-κB and NLRP3 via the activation of the PI3K/Akt pathway. Journal of Ethnopharmacology, 284, 114777. https://doi.org/10.1016/j.jep.2021.114777 .
doi: 10.1016/j.jep.2021.114777 pubmed: 34737012
Li, J., Song, Z., Wang, Y., Yin, Y., Liu, Y., Yuan, R., & Nan, X. (2016). Overexpression of SphK1 enhances cell proliferation and invasion in triple-negative breast cancer via the PI3K/AKT signaling pathway. Tumour Biology, 37(8), 10587–10593. https://doi.org/10.1007/s13277-016-4954-9 .
doi: 10.1007/s13277-016-4954-9 pubmed: 26857281
Geng, T., Sutter, A., Harland, M. D., Law, B. A., Ross, J. S., Lewin, D., Palanisamy, A., Russo, S. B., Chavin, K. D., & Cowart, L. A. (2015). SphK1 mediates hepatic inflammation in a mouse model of NASH induced by high saturated fat feeding and initiates proinflammatory signaling in hepatocytes. Journal of Lipid Research, 56(12), 2359–2371. https://doi.org/10.1194/jlr.M063511 .
doi: 10.1194/jlr.M063511 pubmed: 26482537 pmcid: 4655991
Vettorazzi, S., Bode, C., Dejager, L., Frappart, L., Shelest, E., Klaßen, C., Tasdogan, A., Reichardt, H. M., Libert, C., Schneider, M., Weih, F., Henriette Uhlenhaut, N., David, J. P., Gräler, M., Kleiman, A., & Tuckermann, J. P. (2015). Glucocorticoids limit acute lung inflammation in concert with inflammatory stimuli by induction of SphK1. Nature Communications, 6, 7796. https://doi.org/10.1038/ncomms8796 .
doi: 10.1038/ncomms8796 pubmed: 26183376
Maiti, A., Takabe, K., & Hait, N. C. (2017). Metastatic triple-negative breast cancer is dependent on SphKs/S1P signaling for growth and survival. Cellular Signalling, 32, 85–92. https://doi.org/10.1016/j.cellsig.2017.01.021 .
doi: 10.1016/j.cellsig.2017.01.021 pubmed: 28108260 pmcid: 5731460
Kim, E. S., Kim, J. S., Kim, S. G., Hwang, S., Lee, C. H., & Moon, A. (2011). Sphingosine 1-phosphate regulates matrix metalloproteinase-9 expression and breast cell invasion through S1P3-Gαq coupling. Journal of Cell Science, 124(Pt 13), 2220–2230. https://doi.org/10.1242/jcs.076794 .
doi: 10.1242/jcs.076794 pubmed: 21652634
Singh, S., Bodas, M., Bhatraju, N. K., Pattnaik, B., Gheware, A., Parameswaran, P. K., Thompson, M., Freeman, M., Mabalirajan, U., Gosens, R., Ghosh, B., Pabelick, C., Linneberg, A., Prakash, Y. S., & Agrawal, A. (2016). Hyperinsulinemia adversely affects lung structure and function. American Journal of Physiology – Lung Cellular Molecular Physiology, 310(9), L837–L845. https://doi.org/10.1152/ajplung.00091.2015 .
doi: 10.1152/ajplung.00091.2015 pubmed: 26919895 pmcid: 4867352
Xu, C. Q., Liu, B. J., Wu, J. F., Xu, Y. C., Duan, X. H., Cao, Y. X., & Dong, J. C. (2010). Icariin attenuates LPS-induced acute inflammatory responses: involvement of PI3K/Akt and NF-kappaB signaling pathway. European Journal of Pharmacology, 642(1-3), 146–153. https://doi.org/10.1016/j.ejphar.2010.05.012 .
doi: 10.1016/j.ejphar.2010.05.012 pubmed: 20519138
Cao, Y., Chen, J., Ren, G., Zhang, Y., Tan, X., & Yang, L. (2019). Punicalagin prevents inflammation in LPS-induced RAW 264.7 macrophages by inhibiting FoxO3a/autophagy signaling pathway. Nutrients, 11(11). https://doi.org/10.3390/nu11112794 .
Pyne, S., Lee, S. C., Long, J., & Pyne, N. J. (2009). Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signalling in health and disease. Cellular Signalling, 21(1), 14–21. https://doi.org/10.1016/j.cellsig.2008.08.008 .
doi: 10.1016/j.cellsig.2008.08.008 pubmed: 18768158
Albi, E., Alessenko, A., & Grösch, S. (2018). Sphingolipids in inflammation. Mediators of Inflammation, 2018, 7464702. https://doi.org/10.1155/2018/7464702 .
doi: 10.1155/2018/7464702 pubmed: 29853792 pmcid: 5960540
Ma, F., Liu, F., Ding, L., You, M., Yue, H., Zhou, Y., & Hou, Y. (2017). Anti-inflammatory effects of curcumin are associated with down regulating microRNA-155 in LPS-treated macrophages and mice. Pharmaceutical Biology, 55(1), 1263–1273. https://doi.org/10.1080/13880209.2017.1297838 .
doi: 10.1080/13880209.2017.1297838 pubmed: 28264607 pmcid: 6130682
Gabriel, T. L., Mirzaian, M., Hooibrink, B., Ottenhoff, R., van Roomen, C., Aerts, J., & van Eijk, M. (2017). Induction of Sphk1 activity in obese adipose tissue macrophages promotes survival. PLoS ONE, 12(7), e0182075. https://doi.org/10.1371/journal.pone.0182075 .
doi: 10.1371/journal.pone.0182075 pubmed: 28753653 pmcid: 5533446
Liu, J., & Jiang, B. (2020). Sphk1 promotes ulcerative colitis via activating JAK2/STAT3 signaling pathway. Human Cell, 33(1), 57–66. https://doi.org/10.1007/s13577-019-00283-z .
doi: 10.1007/s13577-019-00283-z pubmed: 31606874
Birkedal-Hansen, H. (1993). Role of cytokines and inflammatory mediators in tissue destruction. Journal of Periodontal Research, 28(6 Pt 2), 500–510. https://doi.org/10.1111/j.1600-0765.1993.tb02113.x .
doi: 10.1111/j.1600-0765.1993.tb02113.x pubmed: 8263720
Puneet, P., Yap, C. T., Wong, L., Lam, Y., Koh, D. R., Moochhala, S., Pfeilschifter, J., Huwiler, A., & Melendez, A. J. (2010). SphK1 regulates proinflammatory responses associated with endotoxin and polymicrobial sepsis. Science, 328(5983), 1290–1294. https://doi.org/10.1126/science.1188635 .
doi: 10.1126/science.1188635 pubmed: 20522778
van der Poll, T., Shankar-Hari, M., & Wiersinga, W. J. (2021). The immunology of sepsis. Immunity, 54(11), 2450–2464. https://doi.org/10.1016/j.immuni.2021.10.012 .
doi: 10.1016/j.immuni.2021.10.012 pubmed: 34758337
Chatterjee, K., Jana, S., Choudhary, P., & Swarnakar, S. (2018). Triumph and tumult of matrix metalloproteinases and their crosstalk with eicosanoids in cancer. Cancer and Metastasis Reviews, 37(2-3), 279–288. https://doi.org/10.1007/s10555-018-9756-7 .
doi: 10.1007/s10555-018-9756-7 pubmed: 30094569
Chen, X. L., Grey, J. Y., Thomas, S., Qiu, F. H., Medford, R. M., Wasserman, M. A., & Kunsch, C. (2004). Sphingosine kinase-1 mediates TNF-alpha-induced MCP-1 gene expression in endothelial cells: upregulation by oscillatory flow. American Journal of Physiology – Heart and Circulatory Physiology, 287(4), H1452–H1458. https://doi.org/10.1152/ajpheart.01101.2003 .
doi: 10.1152/ajpheart.01101.2003 pubmed: 15191888
Sukocheva, O. A., Lukina, E., McGowan, E., & Bishayee, A. (2020). Sphingolipids as mediators of inflammation and novel therapeutic target in inflammatory bowel disease. Advances in Protein Chemistry and Structural Biology, 120, 123–158. https://doi.org/10.1016/bs.apcsb.2019.11.003 .
doi: 10.1016/bs.apcsb.2019.11.003 pubmed: 32085881
Snider, A. J. (2013). Sphingosine kinase and sphingosine-1-phosphate: regulators in autoimmune and inflammatory disease. International Journal of Clinical Rheumatology, 8(4). https://doi.org/10.2217/ijr.13.40 .
Rosen, H., & Goetzl, E. J. (2005). Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nature Reviews Immunology, 5(7), 560–570. https://doi.org/10.1038/nri1650 .
doi: 10.1038/nri1650 pubmed: 15999095
Ersahin, T., Tuncbag, N., & Cetin-Atalay, R. (2015). The PI3K/AKT/mTOR interactive pathway. Molecular BioSystems, 11(7), 1946–1954. https://doi.org/10.1039/c5mb00101c .
doi: 10.1039/c5mb00101c pubmed: 25924008
Ma, C., Zhu, L., Wang, J., He, H., Chang, X., Gao, J., Shumin, W., & Yan, T. (2015). Anti-inflammatory effects of water extract of Taraxacum mongolicum hand.-Mazz on lipopolysaccharide-induced inflammation in acute lung injury by suppressing PI3K/Akt/mTOR signaling pathway. Journal of Ethnopharmacology, 168, 349–355. https://doi.org/10.1016/j.jep.2015.03.068 .
doi: 10.1016/j.jep.2015.03.068 pubmed: 25861954
Qu, L., Shi, K., Xu, J., Liu, C., Ke, C., Zhan, X., Xu, K., & Liu, Y. (2022). Atractylenolide-1 targets SPHK1 and B4GALT2 to regulate intestinal metabolism and flora composition to improve inflammation in mice with colitis. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 98, 153945. https://doi.org/10.1016/j.phymed.2022.153945 .
doi: 10.1016/j.phymed.2022.153945 pubmed: 35114452

Auteurs

Chao-Shun Wei (CS)

Medical College of Jishou University, Jishou, Hunan, 416000, PR China.

Lin-Li Song (LL)

Medical College of Jishou University, Jishou, Hunan, 416000, PR China.

Zi-Xi Peng (ZX)

Medical College of Jishou University, Jishou, Hunan, 416000, PR China.

Xiao-Li Wang (XL)

Medical College of Hunan Normal University, Changsha, Hunan, 410006, PR China. wangxiaolif@163.com.

Classifications MeSH