Overexpression of HOXB4 Promotes Protection of Bone Marrow Mesenchymal Stem Cells Against Lipopolysaccharide-Induced Acute Lung Injury Partially Through the Activation of Wnt/β-Catenin Signaling

References

• Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA. 2016;315(8):801–810. doi:10.1001/jama.2016.0287
   PubMed Web of Science ®Google Scholar
• van der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis. 2008;8(1):32–43. doi:10.1016/S1473-3099(07)70265-7
   PubMed Web of Science ®Google Scholar
• Levi M, van der Poll T. Inflammation and coagulation. Crit Care Med. 2010;38(2 Suppl):S26–S34. doi:10.1097/CCM.0b013e3181c98d21
   PubMed Web of Science ®Google Scholar
• Hotchkiss RS, Nicholson DW. Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol. 2006;6(11):813–822. doi:10.1038/nri1943
   PubMed Web of Science ®Google Scholar
• Thompson BT, Chambers RC, Liu KD. Acute respiratory distress syndrome. N Engl J Med. 2017;377(6):562–572. doi:10.1056/NEJMra1608077
   PubMed Web of Science ®Google Scholar
• Millar FR, Summers C, Griffiths MJ, Toshner MR, Proudfoot AG. The pulmonary endothelium in acute respiratory distress syndrome: insights and therapeutic opportunities. Thorax. 2016;71(5):462–473. doi:10.1136/thoraxjnl-2015-207461
   PubMed Web of Science ®Google Scholar
• Huppert LA, Matthay MA, Ware LB. Pathogenesis of acute respiratory distress syndrome. Semin Respir Crit Care Med. 2019;40(1):31–39. doi:10.1055/s-0039-1683996
   PubMed Web of Science ®Google Scholar
• Huppert LA, Matthay MA. Alveolar fluid clearance in pathologically relevant conditions: in vitro and in vivo models of acute respiratory distress syndrome. Front Immunol. 2017;7(8):371.
   Google Scholar
• Fan E, Brodie D, Slutsky AS. Acute respiratory distress syndrome: advances in diagnosis and treatment. JAMA. 2018;319(7):698–710. doi:10.1001/jama.2017.21907
   PubMed Web of Science ®Google Scholar
• Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2(4):313–319. doi:10.1016/j.stem.2008.03.002
   PubMed Web of Science ®Google Scholar
• Gupta N, Su X, Popov B, Lee JW, Serikov V, Matthay MA. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol. 2007;179(3):1855–1863. doi:10.4049/jimmunol.179.3.1855
   PubMed Web of Science ®Google Scholar
• Gupta N, Krasnodembskaya A, Kapetanaki M, et al. Mesenchymal stem cells enhance survival and bacterial clearance in murine Escherichia coli pneumonia. Thorax. 2012;67(6):533–539. doi:10.1136/thoraxjnl-2011-201176
   PubMed Web of Science ®Google Scholar
• Lee JW, Krasnodembskaya A, McKenna DH, Song Y, Abbott J, Matthay MA. Therapeutic effects of human mesenchymal stem cells in ex vivo human lungs injured with live bacteria. Am J Respir Crit Care Med. 2013;187(7):751–760. doi:10.1164/rccm.201206-0990OC
   PubMed Web of Science ®Google Scholar
• Wilson JG, Liu KD, Zhuo H, et al. Mesenchymal stem (stromal) cells for treatment of ARDS: a phase 1 clinical trial. Lancet Respir Med. 2015;3(1):24–32. doi:10.1016/S2213-2600(14)70291-7
   PubMed Web of Science ®Google Scholar
• Liu KD, Wilson JG, Zhuo H, et al. Design and implementation of the START (STem cells for ARDS treatment) trial, a phase 1/2 trial of human mesenchymal stem/stromal cells for the treatment of moderate-severe acute respiratory distress syndrome. Ann Intensive Care. 2014;4:22. doi:10.1186/s13613-014-0022-z
   PubMed Web of Science ®Google Scholar
• Zheng G, Huang L, Tong H, et al. Treatment of acute respiratory distress syndrome with allogeneic adipose-derived mesenchymal stem cells: a randomized, placebo-controlled pilot study. Respir Res. 2014;15(1):39. doi:10.1186/1465-9921-15-39
   PubMed Web of Science ®Google Scholar
• Lopes-Pacheco M, Robba C, Rocco PRM, Pelosi P. Current understanding of the therapeutic benefits of mesenchymal stem cells in acute respiratory distress syndrome. Cell Biol Toxicol. 2020;36(1):83–102. doi:10.1007/s10565-019-09493-5
   PubMed Web of Science ®Google Scholar
• Sengupta V, Sengupta S, Lazo A, Woods P, Nolan A, Bremer N. Exosomes derived from bone marrow mesenchymal stem cells as treatment for severe COVID-19. Stem Cells Dev. 2020;29(12):747–754. doi:10.1089/scd.2020.0080
   PubMed Web of Science ®Google Scholar
• Leng Z, Zhu R, Hou W, et al. Transplantation of ACE2- mesenchymal stem cells improves the outcome of patients with COVID-19 pneumonia. Aging Dis. 2020;11(2):216–228. doi:10.14336/AD.2020.0228
   PubMed Web of Science ®Google Scholar
• Antonchuk J, Sauvageau G, Humphries RK. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell. 2002;109(1):39–45. doi:10.1016/S0092-8674(02)00697-9
   PubMed Web of Science ®Google Scholar
• Grässel S, Stöckl S, Jenei-Lanzl Z. Isolation, culture, and osteogenic/chondrogenic differentiation of bone marrow-derived mesenchymal stem cells. Methods Mol Biol. 2012;879:203–267.
   PubMedGoogle Scholar
• Li B, Zhang H, Zeng M, et al. Bone marrow mesenchymal stem cells protect alveolar macrophages from lipopolysaccharide-induced apoptosis partially by inhibiting the Wnt/β-catenin pathway. Cell Biol Int. 2015;39(2):192–200. doi:10.1002/cbin.10359
   PubMed Web of Science ®Google Scholar
• Zeng M, Chen Q, Ge S, et al. Overexpression of FoxM1 promotes differentiation of bone marrow mesenchymal stem cells into alveolar type II cells through activating Wnt/β-catenin signalling. Biochem Biophys Res Commun. 2020;528(2):311–317. doi:10.1016/j.bbrc.2020.05.042
   PubMed Web of Science ®Google Scholar
• Huang C, Zheng H, He W, et al. Ghrelin ameliorates the human alveolar epithelial A549 cell apoptosis induced by lipopolysaccharide. Biochem Biophys Res Commun. 2016;474(1):83–90. doi:10.1016/j.bbrc.2016.04.074
   PubMed Web of Science ®Google Scholar
• Chen HR, Chuang YC, Lin YS, et al. Dengue virus nonstructural protein 1 induces vascular leakage through macrophage migration inhibitory factor and autophagy. PLoS Negl Trop Dis. 2016;10(7):e0004828. doi:10.1371/journal.pntd.0004828
   PubMed Web of Science ®Google Scholar
• Mei SH, Haitsma JJ, Dos Santos CC, et al. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med. 2010;182(8):1047–1057. doi:10.1164/rccm.201001-0010OC
   PubMed Web of Science ®Google Scholar
• Timmers L, Lim SK, Hoefer IE, et al. Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction. Stem Cell Res. 2011;6(3):206–214. doi:10.1016/j.scr.2011.01.001
   PubMed Web of Science ®Google Scholar
• Tanrıverdi AK, Polat O, Elçin AE, et al. Mesenchymal stem cell transplantation in polytrauma: evaluation of bone and liver healing response in an experimental rat model. Eur J Trauma Emerg Surg. 2020;46(1):53–64. doi:10.1007/s00068-019-01101-9
   PubMed Web of Science ®Google Scholar
• Wong AP, Dutly AE, Sacher A, et al. Targeted cell replacement with bone marrow cells for airway epithelial regeneration. Am J Physiol Lung Cell Mol Physiol. 2007;293(3):L740–L752. doi:10.1152/ajplung.00050.2007
   PubMed Web of Science ®Google Scholar
• Liechty KW, MacKenzie TC, Shaaban AF, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000;6(11):1282–1286. doi:10.1038/81395
   PubMed Web of Science ®Google Scholar
• Morrison TJ, Jackson MV, Cunningham EK, et al. Mesenchymal stromal cells modulate macrophages in clinically relevant lung injury models by extracellular vesicle mitochondrial transfer. Am J Respir Crit Care Med. 2017;196(10):1275–1286. doi:10.1164/rccm.201701-0170OC
   PubMed Web of Science ®Google Scholar
• Phinney DG, Di Giuseppe M, Njah J, et al. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs. Nat Commun. 2015;6:8472. doi:10.1038/ncomms9472
   PubMed Web of Science ®Google Scholar
• Zhu YG, Feng XM, Abbott J, et al. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells. 2014;32(1):116–125. doi:10.1002/stem.1504
   PubMed Web of Science ®Google Scholar
• Fan R, Bonde S, Gao P, et al. Dynamic HoxB4-regulatory network during embryonic stem cell differentiation to hematopoietic cells. Blood. 2012;119(19):e139–e147. doi:10.1182/blood-2011-12-396754
   PubMed Web of Science ®Google Scholar
• Wang L, Menendez P, Shojaei F, et al. Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med. 2005;201(10):1603–1614. doi:10.1084/jem.20041888
   PubMed Web of Science ®Google Scholar
• Lee GS, Kim BS, Sheih JH, Moore M. Forced expression of HoxB4 enhances hematopoietic differentiation by human embryonic stem cells. Mol Cells. 2008;25(4):487–493.
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17(1):9–26. doi:10.1016/j.devcel.2009.06.016
   PubMed Web of Science ®Google Scholar
• Liebner S, Corada M, Bangsow T, et al. Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol. 2008;183(3):409–417. doi:10.1083/jcb.200806024
   PubMed Web of Science ®Google Scholar
• Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007;19(2):150–158. doi:10.1016/j.ceb.2007.02.007
   PubMed Web of Science ®Google Scholar
• Maretto S, Cordenonsi M, Dupont S, et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci USA. 2003;100(6):3299–3304. doi:10.1073/pnas.0434590100
   PubMed Web of Science ®Google Scholar
• Zhang W, Zhang Y, Guo X, et al. Sirt1 protects endothelial cells against LPS-induced barrier dysfunction. Oxid Med Cell Longev. 2017;2017:4082102. doi:10.1155/2017/4082102
   PubMed Web of Science ®Google Scholar
• Li B, Zeng M, He W, et al. Ghrelin protects alveolar macrophages against lipopolysaccharide-induced apoptosis through growth hormone secretagogue receptor 1a-dependent c-Jun N-terminal kinase and Wnt/-catenin signaling and suppresses lung inflammation. Endocrinology. 2015;156(1):203–217. doi:10.1210/en.2014-1539
   PubMed Web of Science ®Google Scholar
• Li Y, Shi J, Yang J, et al. A Wnt/β-catenin negative feedback loop represses TLR-triggered inflammatory responses in alveolar epithelial cells. Mol Immunol. 2014;59(2):128–135. doi:10.1016/j.molimm.2014.02.002
   PubMed Web of Science ®Google Scholar
• Cai SX, Liu AR, Chen S, et al. Activation of Wnt/β-catenin signalling promotes mesenchymal stem cells to repair injured alveolar epithelium induced by lipopolysaccharide in mice. Stem Cell Res Ther. 2015;6(1):65. doi:10.1186/s13287-015-0060-y
   PubMed Web of Science ®Google Scholar
• Zhang J, Shao Y, He D, Zhang L, Xu G, Shen J. Evidence that bone marrow-derived mesenchymal stem cells reduce epithelial permeability following phosgene-induced acute lung injury via activation of wnt3a protein-induced canonical wnt/β-catenin signaling. Inhal Toxicol. 2016;28(12):572–579. doi:10.1080/08958378.2016.1228720
   PubMed Web of Science ®Google Scholar
• Villar J, Cabrera NE, Casula M, et al. WNT/β-catenin signaling is modulated by mechanical ventilation in an experimental model of acute lung injury. Intensive Care Med. 2011;37(7):1201–1209. doi:10.1007/s00134-011-2234-0
   PubMed Web of Science ®Google Scholar
• Monick MM, Carter AB, Robeff PK, Flaherty DM, Peterson MW, Hunninghake GW. Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of beta-catenin. J Immunol. 2001;166(7):4713–4720. doi:10.4049/jimmunol.166.7.4713
   PubMed Web of Science ®Google Scholar
• Lee H, Bae S, Choi BW, Yoon Y. WNT/β-catenin pathway is modulated in asthma patients and LPS-stimulated RAW264.7 macrophage cell line. Immunopharmacol Immunotoxicol. 2012;34(1):56–65. doi:10.3109/08923973.2011.574704
   PubMed Web of Science ®Google Scholar
• Gong K, Zhou F, Huang H, Gong Y, Zhang L. Suppression of GSK3β by ERK mediates lipopolysaccharide induced cell migration in macrophage through β-catenin signaling. Protein Cell. 2012;3(10):762–768. doi:10.1007/s13238-012-2058-x
   PubMed Web of Science ®Google Scholar
• Cheng L, Zhao Y, Qi D, Li W, Wang D. Wnt/β-catenin pathway promotes acute lung injury induced by LPS through driving the Th17 response in mice. Biochem Biophys Res Commun. 2018;495(2):1890–1895. doi:10.1016/j.bbrc.2017.12.058
   PubMed Web of Science ®Google Scholar
• Sun Z, Gong X, Zhu H, et al. Inhibition of Wnt/β-catenin signaling promotes engraftment of mesenchymal stem cells to repair lung injury. J Cell Physiol. 2014;229(2):213–224. doi:10.1002/jcp.24436
   PubMed Web of Science ®Google Scholar
• Villar J, Cabrera-Benítez NE, Ramos-Nuez A, et al. Early activation of pro-fibrotic WNT5A in sepsis-induced acute lung injury. Crit Care. 2014;18(5):568. doi:10.1186/s13054-014-0568-z
   PubMed Web of Science ®Google Scholar
• Ma B, Hottiger MO. Crosstalk between Wnt/β-catenin and NF-κB signaling pathway during inflammation. Front Immunol. 2016;7:378. doi:10.3389/fimmu.2016.00378
   PubMed Web of Science ®Google Scholar
• McNeill H, Woodgett JR. When pathways collide: collaboration and connivance among signalling proteins in development. Nat Rev Mol Cell Biol. 2010;11(6):404–413. doi:10.1038/nrm2902
   PubMed Web of Science ®Google Scholar
• Blumenthal A, Ehlers S, Lauber J, et al. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood. 2006;108(3):965–973. doi:10.1182/blood-2005-12-5046
   PubMed Web of Science ®Google Scholar
• Mastri M, Lin H, Lee T. Enhancing the efficacy of mesenchymal stem cell therapy. World J Stem Cells. 2014;6(2):82–93. doi:10.4252/wjsc.v6.i2.82
   PubMedGoogle Scholar
• Kumar S, Chanda D, Ponnazhagan S. Therapeutic potential of genetically modified mesenchymal stem cells. Gene Ther. 2008;15(10):711–715. doi:10.1038/gt.2008.35
   PubMed Web of Science ®Google Scholar
• Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73(10):1907–1920. doi:10.1016/j.jprot.2010.06.006
   PubMed Web of Science ®Google Scholar
• Zhou H, Li X, Yin Y, et al. The proangiogenic effects of extracellular vesicles secreted by dental pulp stem cells derived from periodontally compromised teeth. Stem Cell Res Ther. 2020;11(1):110. doi:10.1186/s13287-020-01614-w
   PubMed Web of Science ®Google Scholar
• Lei D, Yang WT, Zheng PS. HOXB4 inhibits the proliferation and tumorigenesis of cervical cancer cells by downregulating the activity of Wnt/β-catenin signaling pathway. Cell Death Dis. 2021;12(1):105. doi:10.1038/s41419-021-03411-6
   PubMed Web of Science ®Google Scholar