Cell penetrating peptides coupled to an endothelial nitric oxide synthase sequence alter endothelial permeability

References

• Derakhshankhah H, Jafari S. Cell penetrating peptides: a concise review with emphasis on biomedical applications. Biomed Pharmacother. 2018;108:1–12. doi:10.1016/j.biopha.2018.09.097.
   PubMed Web of Science ®Google Scholar
• Schmidt N, Mishra A, Lai GH, Wong GC. Arginine-rich cell-penetrating peptides. FEBS Lett. 2010;584(9):1806–1813. doi:10.1016/j.febslet.2009.11.046.
   PubMed Web of Science ®Google Scholar
• Wang YF, Xu X, Fan X, Zhang C, Wei Q, Wang X, Guo W, Xing W, Yu J, Yan J-L, et al. A cell-penetrating peptide suppresses inflammation by inhibiting NF-kappaB signaling. Mol Ther. 2011;19(10):1849–1857. doi:10.1038/mt.2011.82.
   PubMed Web of Science ®Google Scholar
• Rudd KE, Johnson SC, Agesa KM, Shackelford KA, Tsoi D, Kievlan DR, Colombara DV, Ikuta KS, Kissoon N, Finfer S, et al. Global, regional, and national sepsis incidence and mortality, 1990-2017: analysis for the Global Burden of Disease Study. Lancet. 2020;395(10219):200–211. doi:10.1016/S0140-6736(19)32989-7.
   PubMed Web of Science ®Google Scholar
• Joffre J, Hellman J, Ince C, Ait-Oufella H. Endothelial responses in sepsis. Am J Respir Crit Care Med. 2020;202(3):361–370. doi:10.1164/rccm.201910-1911TR.
   PubMed Web of Science ®Google Scholar
• Lambden S. Bench to bedside review: therapeutic modulation of nitric oxide in sepsis-an update. Intensive Care Med Exp. 2019;7(1):64. doi:10.1186/s40635-019-0274-x.
   PubMed Web of Science ®Google Scholar
• Coletta C, Modis K, Olah G, Brunyanszki A, Herzig DS, Sherwood ER, Ungvári Z, Szabo C, et al. Endothelial dysfunction is a potential contributor to multiple organ failure and mortality in aged mice subjected to septic shock: preclinical studies in a murine model of cecal ligation and puncture. Crit Care. 2014;18(5):511. doi:10.1186/s13054-014-0511-3.
   PubMed Web of Science ®Google Scholar
• Koch SR, Choi H, Mace EH, Stark RJ. Toll-like receptor 3-mediated inflammation by p38 is enhanced by endothelial nitric oxide synthase knockdown. Cell Commun Signal. 2019;17(1):33. doi:10.1186/s12964-019-0345-3.
   PubMedGoogle Scholar
• Stark RJ, Koch SR, Choi H, Mace EH, Dikalov SI, Sherwood ER, Lamb FS. Endothelial nitric oxide synthase modulates Toll-like receptor 4–mediated IL-6 production and permeability via nitric oxide-independent signaling. FASEB J. 2018;32(2):945–956. doi:10.1096/fj.201700410R.
   PubMed Web of Science ®Google Scholar
• Chrestensen CA, McMurry JL, Salerno JC. MAP kinases bind endothelial nitric oxide synthase. FEBS Open Bio. 2012;2(1):51–55. doi:10.1016/j.fob.2012.02.002.
   PubMedGoogle Scholar
• Konduri GG, Afolayan AJ, Eis A, Pritchard KA Jr., Teng RJ. Interaction of endothelial nitric oxide synthase with mitochondria regulates oxidative stress and function in fetal pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2015;309(9):L1009–17. doi:10.1152/ajplung.00386.2014.
   PubMed Web of Science ®Google Scholar
• Bernatchez P, Sharma A, Bauer PM, Marin E, Sessa WC. A noninhibitory mutant of the caveolin-1 scaffolding domain enhances eNOS-derived NO synthesis and vasodilation in mice. J Clin Invest. 2011;121(9):3747–3755. doi:10.1172/JCI44778.
   PubMed Web of Science ®Google Scholar
• Ryu J, Han K, Park J, Choi SY. Enhanced uptake of a heterologous protein with an HIV-1 Tat protein transduction domains (PTD) at both termini. Mol Cells. 2003;16:385–391.
   PubMed Web of Science ®Google Scholar
• Vignon P, Laterre PF, Daix T, Francois B. New agents in development for sepsis: any reason for hope? Drugs. 2020;80(17):1751–1761. doi:10.1007/s40265-020-01402-z.
   PubMed Web of Science ®Google Scholar
• Tanoue T, Nishida E. Molecular recognitions in the MAP kinase cascades. Cell Signal. 2003;15(5):455–462. doi:10.1016/S0898-6568(02)00112-2.
   PubMed Web of Science ®Google Scholar
• Gao S, Chen J, Brodsky SV, Huang H, Adler S, Lee JH, Dhadwal N, Cohen-Gould L, Gross SS, Goligorsky MS, et al. Docking of endothelial nitric oxide synthase (eNOS) to the mitochondrial outer membrane: a pentabasic amino acid sequence in the autoinhibitory domain of eNOS targets a proteinase K-cleavable peptide on the cytoplasmic face of mitochondria. J Biol Chem. 2004;279(16):15968–15974. doi:10.1074/jbc.M308504200.
   PubMed Web of Science ®Google Scholar
• Camara AKS, Zhou Y, Wen PC, Tajkhorshid E, Kwok WM. Mitochondrial VDAC1: a key gatekeeper as potential therapeutic target. Front Physiol. 2017;8:460. doi:10.3389/fphys.2017.00460.
   PubMed Web of Science ®Google Scholar
• Han YJ, Hu WY, Piano M, de Lanerolle P. Regulation of myosin light chain kinase expression by angiotensin II in hypertension. Am J Hypertens. 2008;21(8):860–865. doi:10.1038/ajh.2008.199.
   PubMed Web of Science ®Google Scholar
• Shen Q, Rigor RR, Pivetti CD, Wu MH, Yuan SY. Myosin light chain kinase in microvascular endothelial barrier function. Cardiovasc Res. 2010;87(2):272–280. doi:10.1093/cvr/cvq144.
   PubMed Web of Science ®Google Scholar
• Van Roey K, Uyar B, Weatheritt RJ, Dinkel H, Seiler M, Budd A, Gibson TJ, Davey NE, et al. Short linear motifs: ubiquitous and functionally diverse protein interaction modules directing cell regulation. Chem Rev. 2014;114(13):6733–6778. doi:10.1021/cr400585q.
   PubMed Web of Science ®Google Scholar
• Ricard N, Scott RP, Booth CJ, Velazquez H, Cilfone NA, Baylon JL, Gulcher JR, Quaggin SE, Chittenden TW, Simons M, et al. Endothelial ERK1/2 signaling maintains integrity of the quiescent endothelium. J Exp Med. 2019;216(8):1874–1890. doi:10.1084/jem.20182151.
   PubMed Web of Science ®Google Scholar
• Miller MR, Koch SR, Choi H, Lamb FS, Stark RJ. Apoptosis signal-regulating kinase 1 (ASK1) inhibition reduces endothelial cytokine production without improving permeability after toll-like receptor 4 (TLR4) challenge. Transl Res. 2021;235:115–128. doi:10.1016/j.trsl.2021.04.001.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Zhang M, Zhao Y, Chen J, Li B, Cai W. JNK inhibitor SP600125 protects against lipopolysaccharide-induced acute lung injury via upregulation of claudin-4. Exp Ther Med. 2014;8(1):153–158. doi:10.3892/etm.2014.1684.
   PubMed Web of Science ®Google Scholar
• Zhai Z, Ni X, Jin C, Ren W, Li J, Deng J, Deng B, Yin Y. Cecropin A modulates tight junction-related protein expression and enhances the barrier function of porcine intestinal epithelial cells by suppressing the MEK/ERK pathway. Int J Mol Sci. 2018;19(7):1941. doi:10.3390/ijms19071941.
   Web of Science ®Google Scholar
• Bechara C, Sagan S. Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett. 2013;587(12):1693–1702. doi:10.1016/j.febslet.2013.04.031.
   PubMed Web of Science ®Google Scholar
• Caesar CE, Esbjorner EK, Lincoln P, Norden B. Membrane interactions of cell-penetrating peptides probed by tryptophan fluorescence and dichroism techniques: correlations of structure to cellular uptake. Biochemistry. 2006;45(24):7682–7692. doi:10.1021/bi052095t.
   PubMed Web of Science ®Google Scholar
• Nakase I, Niwa M, Takeuchi T, Sonomura K, Kawabata N, Koike Y, Takehashi M, Tanaka S, Ueda K, Simpson JC, et al. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther. 2004;10(6):1011–1022. doi:10.1016/j.ymthe.2004.08.010.
   PubMed Web of Science ®Google Scholar
• Stark R, Choi H, Koch S, Lamb F, Sherwood E. Monophosphoryl lipid A inhibits the cytokine response of endothelial cells challenged with LPS. Innate Immun. 2015;21(6):565–574. doi:10.1177/1753425914564172.
   PubMed Web of Science ®Google Scholar
• Console S, Marty C, Garcia-Echeverria C, Schwendener R, Ballmer-Hofer K. Antennapedia and HIV transactivator of transcription (TAT) “protein transduction domains” promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J Biol Chem. 2003;278(37):35109–35114. doi:10.1074/jbc.M301726200.
   PubMed Web of Science ®Google Scholar
• Nookala AR, Kumar A. Molecular mechanisms involved in HIV-1 Tat-mediated induction of IL-6 and IL-8 in astrocytes. J Neuroinflammation. 2014;11(1):214. doi:10.1186/s12974-014-0214-3.
   PubMedGoogle Scholar
• Ben Haij N, Planes R, Leghmari K, Serrero M, Delobel P, Izopet J, BenMohamed L, Bahraoui E. HIV-1 tat protein induces production of proinflammatory cytokines by human dendritic cells and Monocytes/Macrophages through engagement of TLR4-MD2-CD14 complex and activation of NF-kappaB pathway. PLoS One. 2015;10(6):e0129425. doi:10.1371/journal.pone.0129425.
   PubMed Web of Science ®Google Scholar
• Splith K, Neundorf I. Antimicrobial peptides with cell-penetrating peptide properties and vice versa. Eur Biophys J. 2011;40(4):387–397. doi:10.1007/s00249-011-0682-7.
   PubMed Web of Science ®Google Scholar
• Rusnati M, Presta M. HIV-1 Tat protein and endothelium: from protein/cell interaction to AIDS-associated pathologies. Angiogenesis. 2002;5(3):141–151. doi:10.1023/A:1023892223074.
   PubMedGoogle Scholar