A novel proteolysis-resistant cyclic helix B peptide ameliorates kidney ischemia reperfusion injury

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 11, 2014, Pages 2306-2317

  Yang, Cheng ^a,b   Xu, Zhongliang ^c   Zhao, Zitong ^a,b   Li, Long ^a,b   Zhao, Tian ^a,b   Peng, Dian ^c   Xu, Ming ^a,b   Rong, Ruiming ^a,b   Long, Ya Qiu ^c   Zhu, Tongyu ^a,b  

^a FUDAN UNIVERSITY   (China)

^b Shanghai Key Laboratory of Organ Transplantation   (China)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

Apoptosis; Autophagy; Cyclic helix B peptide; Inflammation; Kidney ischemia reperfusion injury; Metabolic stability

Indexed keywords

COMPLEMENT COMPONENT C3; CYCLIC HELIX B PEPTIDE; CYCLOPEPTIDE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; SULFIDE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; EPITHELIUM CELL; IN VITRO STUDY; KIDNEY FUNCTION; KIDNEY ISCHEMIA; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RENAL PROTECTION; REPERFUSION; REPERFUSION INJURY; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

EID: 84907986089     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.09.001     Document Type: Article

References (37)

1. Velly L., Pellegrini L., Guillet B., Bruder N., Pisano P. Erythropoietin 2nd cerebral protection after acute injuries: a double-edged sword?. Pharmacol. Ther. 2010, 128:445-459.
2. Brines M., Patel N.S., Villa P., Brines C., Mennini T., De Paola M., Erbayraktar Z., Erbayraktar S., Sepodes B., Thiemermann C., Ghezzi P., Yamin M., Hand C.C., Xie Q.W., Coleman T., Cerami A. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10925-10930.
3. Yang C., Zhao T., Lin M., Zhao Z., Hu L., Jia Y., Xue Y., Xu M., Tang Q., Yang B., Rong R., Zhu T. Helix B surface peptide administered after insult of ischemia reperfusion improved renal function, structure and apoptosis through beta common receptor/erythropoietin receptor and PI3K/Akt pathway in a murine model. Exp. Biol. Med. (Maywood) 2013, 238:111-119.
4. van Rijt W.G., Nieuwenhuijs-Moeke G.J., van Goor H., Jespersen B., Ottens P.J., Ploeg R.J., Leuvenink H.G. ARA290, a non-erythropoietic EPO derivative, attenuates renal ischemia/reperfusion injury. J. Transl. Med. 2013, 11:9.
5. Brines M., Cerami A. The receptor that tames the innate immune response. Mol. Med. 2012, 18:486-496.
6. Long Y.Q., Guo R., Luo J.H., Yang D., Roller P.P. Potentiating effect of distant sites in non-phosphorylated cyclic peptide antagonists of the Grb2-SH2 domain. Biochem. Biophys. Res. Commun. 2003, 310:334-340.
7. Song Y.L., Peach M.L., Roller P.P., Qiu S., Wang S., Long Y.Q. Discovery of a novel nonphosphorylated pentapeptide motif displaying high affinity for Grb2-SH2 domain by the utilization of 3'-substituted tyrosine derivatives. J. Med. Chem. 2006, 49:1585-1596.
8. Long Y.Q., Xue T., Song Y.L., Liu Z.L., Huang S.X., Yu Q. Synthesis and utilization of chiral alpha-methylated alpha-amino acids with a carboxyalkyl side chain in the design of novel Grb2-SH2 peptide inhibitors free of phosphotyrosine. J. Med. Chem. 2008, 51:6371-6380.
9. Kinsey G.R., Sharma R., Huang L., Li L., Vergis A.L., Ye H., Ju S.T., Okusa M.D. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J. Am. Soc. Nephrol. 2009, 20:1744-1753.
10. Yang B., Jain S., Pawluczyk I.Z., Imtiaz S., Bowley L., Ashra S.Y., Nicholson M.L. Inflammation and caspase activation in long-term renal ischemia/reperfusion injury and immunosuppression in rats. Kidney Int. 2005, 68:2050-2067.
11. Yang J., Ahn H.N., Chang M., Narasimhan P., Chan P.H., Song Y.S. Complement component 3 inhibition by an antioxidant is neuroprotective after cerebral ischemia and reperfusion in mice. J. Neurochem. 2013, 124:523-535.
12. Hanidziar D., Koulmanda M. Inflammation and the balance of Treg and Th17 cells in transplant rejection and tolerance. Curr. Opin. Organ Transplant. 2010, 15:411-415.
13. Wang Z., Choi M.E. Autophagy in kidney health and disease. Antioxid. Redox Signal. 2014, 20:519-537.
14. Kaushal G.P. Autophagy protects proximal tubular cells from injury and apoptosis. Kidney Int. 2012, 82:1250-1253.
15. Zou M.H., Xie Z. Regulation of interplay between autophagy and apoptosis in the diabetic heart: new role of AMPK. Autophagy 2013, 9:624-625.
16. Ueba H., Brines M., Yamin M., Umemoto T., Ako J., Momomura S., Cerami A., Kawakami M. Cardioprotection by a nonerythropoietic, tissue-protective peptide mimicking the 3D structure of erythropoietin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14357-14362.
17. Zhao Z., Yang C., Wang L., Li L., Zhao T., Hu L., Rong R., Xu M., Zhu T. The regulatory T cell effector soluble fibrinogen-like protein 2 induces tubular epithelial cell apoptosis in renal transplantation. Exp. Biol. Med. (Maywood) 2014, 239:193-201.
18. Yang C., Jia Y., Zhao T., Xue Y., Zhao Z., Zhang J., Wang J., Wang X., Qiu Y., Lin M., Zhu D., Qi G., Tang Q., Rong R., Xu M., Ni S., Lai B., Nicholson M.L., Zhu T., Yang B. Naked caspase 3 small interfering RNA is effective in cold preservation but not in autotransplantation of porcine kidneys. J. Surg. Res. 2013, 181:342-354.
19. Li P., Roller P.P. Cyclization strategies in peptide derived drug design. Curr. Top. Med. Chem. 2002, 2:325-341.
20. Shepherd N.E., Hoang H.N., Abbenante G., Fairlie D.P. Single turn peptide alpha helices with exceptional stability in water. J. Am. Chem. Soc. 2005, 127:2974-2983.
21. Lee J.W., Park S., Takahashi Y., Wang H.G. The association of AMPK with ULK1 regulates autophagy. PLoS One 2010, 5:e15394.
22. Yokoyama T., Kondo Y., Kondo S. Roles of mTOR and STAT3 in autophagy induced by telomere 3' overhang-specific DNA oligonucleotides. Autophagy 2007, 3:496-498.
23. Codogno P., Meijer A.J. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 2005, 12:1509-1518.
24. McVicar C.M., Hamilton R., Colhoun L.M., Gardiner T.A., Brines M., Cerami A., Stitt A.W. Intervention with an erythropoietin-derived peptide protects against neuroglial and vascular degeneration during diabetic retinopathy. Diabetes 2011, 60:2995-3005.
25. Swartjes M., Morariu A., Niesters M., Brines M., Cerami A., Aarts L., Dahan A. ARA290, a peptide derived from the tertiary structure of erythropoietin, produces long-term relief of neuropathic pain: an experimental study in rats and beta-common receptor knockout mice. Anesthesiology 2011, 115:1084-1092.
26. Schmidt R.E., Feng D., Wang Q., Green K.G., Snipes L.L., Yamin M., Brines M. Effect of insulin and an erythropoietin-derived peptide (ARA290) on established neuritic dystrophy and neuronopathy in Akita (Ins2 Akita) diabetic mouse sympathetic ganglia. Exp. Neurol. 2011, 232:126-135.
27. Aboye T.L., Camarero J.A. Biological synthesis of circular polypeptides. J. Biol. Chem. 2012, 287:27026-27032.
28. Suh Y., Afaq F., Khan N., Johnson J.J., Khusro F.H., Mukhtar H. Fisetin induces autophagic cell death through suppression of mTOR signaling pathway in prostate cancer cells. Carcinogenesis 2010, 31:1424-1433.
29. Ahn Y.J., Kim H., Lim H., Lee M., Kang Y., Moon S., Kim H.S., Kim H.H. AMP-activated protein kinase: implications on ischemic diseases. BMB Rep. 2012, 45:489-495.
30. Seo-Mayer P.W., Thulin G., Zhang L., Alves D.S., Ardito T., Kashgarian M., Caplan M.J. Preactivation of AMPK by metformin may ameliorate the epithelial cell damage caused by renal ischemia. Am. J. Physiol. Renal Physiol. 2011, 301:F1346-F1357.
31. Takagi H., Matsui Y., Hirotani S., Sakoda H., Asano T., Sadoshima J. AMPK mediates autophagy during myocardial ischemia in vivo. Autophagy 2007, 3:405-407.
32. Pastor-Soler N.M., Hallows K.R. AMP-activated protein kinase regulation of kidney tubular transport. Curr. Opin. Nephrol. Hypertens. 2012, 21:523-533.
33. Watanabe K., Tsubata T. Autophagy connects antigen receptor signaling to costimulatory signaling in B lymphocytes. Autophagy 2009, 5:108-110.
34. Kono H., Fujii H., Ogiku M., Hosomura N., Amemiya H., Tsuchiya M., Hara M. Role of IL-17A in neutrophil recruitment and hepatic injury after warm ischemia-reperfusion mice. J. Immunol. 2011, 187:4818-4825.
35. Suzuki S., Inaba K., Konno H. Ischemic preconditioning in hepatic ischemia and reperfusion. Curr. Opin. Organ Transplant. 2008, 13:142-147.
36. Luan H.F., Zhao Z.B., Zhao Q.H., Zhu P., Xiu M.Y., Ji Y. Hydrogen sulfide postconditioning protects isolated rat hearts against ischemia and reperfusion injury mediated by the JAK2/STAT3 survival pathway. Braz. J. Med. Biol. Res. 2012, 45:898-905.
37. Wang J., Ouyang C., Chen X., Fu B., Lu Y., Hong Q. STAT3 inhibits apoptosis of human renal tubular epithelial cells induced by ATP depletion/recovery. Nephron Exp. Nephrol. 2008, 108:e11-e18.