Cathelicidin PR-39 peptide inhibits hypoxia/reperfusion-induced kidney cell apoptosis by suppression of the endoplasmic reticulum-stress pathway

Acta Biochimica et Biophysica Sinica

Volumn 48, Issue 8, 2016, Pages 714-722

  Liu, Jing ^a   Xue, Wujun ^a   Xiang, Heli ^a   Zheng, Jin ^a   Zhao, Yanlong ^a   Jiao, Lizi ^a   Jiao, Zizhao ^a  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

anti apoptosis; ischemia reperfusion injury; kidney specific promoter (KSP); kidney derived HK 2 cells; PR 39

Indexed keywords

CATHELICIDIN;

3T3 CELL LINE; ANIMAL; APOPTOSIS; DRUG EFFECTS; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; HUMAN; HYPOXIA; KIDNEY; MOUSE; PATHOLOGY; REPERFUSION INJURY; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; APOPTOSIS; CATHELICIDINS; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA; KIDNEY; MICE; NIH 3T3 CELLS; REPERFUSION INJURY;

EID: 84984919780     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmw061     Document Type: Article

References (50)

1. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011, 121: 4210-4221.
2. Xie J, Guo Q. Apoptosis antagonizing transcription factor protects renal tubule cells against oxidative damage and apoptosis induced by ischemiareperfusion. J Am Soc Nephrol 2006, 17: 3336-3346.
3. Webb S, Dobb G. ARF, ATN or AKI? It's now acute kidney injury. Anaesth Intensive Care 2007, 35: 843-844.
4. Mehta RL, Kellum JA, Shah SV, Molitoris BA, Ronco C, Warnock DG, Levin A. Acute kidney injury network: report of an initiative to improve outcomes in acute kidney injury. Crit Care 2007, 11: R31.
5. Siew ED, Davenport A. The growth of acute kidney injury: a rising tide or just closer attention to detail? Kidney Int 2015, 87: 46-61.
6. Uchino S, Doig GS, Bellomo R, Morimatsu H, Morgera S, Schetz M, Tan I, et al. Diuretics and mortality in acute renal failure. Crit Care Med 2004, 32: 1669-1677.
7. Schrier RW, Wang W, Poole B, Mitra A. Acute renal failure: definitions, diagnosis, pathogenesis, and therapy. J Clin Invest 2004, 114: 5-14.
8. Chatterjee PK. Novel pharmacological approaches to the treatment of renal ischemia-reperfusion injury: a comprehensive review. Naunyn Schmiedebergs Arch Pharmacol 2007, 376: 1-43.
9. Venkataraman R, Kellum JA. Novel approaches to the treatment of acute renal failure. Expert Opin Investig Drugs 2003, 12: 1353-1366.
10. Tabara LC, Poveda J, Martin-Cleary C, Selgas R, Ortiz A, Sanchez-Nino MD. Mitochondria-targeted therapies for acute kidney injury. Expert Rev Mol Med 2014, 16: e13.
11. Havasi A, Borkan SC. Apoptosis and acute kidney injury. Kidney Int 2011, 80: 29-40.
12. Inagi R. Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 2010, 10: 156-165.
13. Linkermann A, Chen G, Dong G, Kunzendorf U, Krautwald S, Dong Z. Regulated cell death in AKI. J Am Soc Nephrol 2014, 25: 2689-2701.
14. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004, 75: 39-48.
15. Li J, Post M, Volk R, Gao Y, Li M, Metais C, Sato K, et al. PR39, a peptide regulator of angiogenesis. Nat Med 2000, 6: 49-55.
16. Bao J, Sato K, Li M, Gao Y, Abid R, Aird W, Simons M, et al. PR-39 and PR-11 peptides inhibit ischemia-reperfusion injury by blocking proteasome-mediated I kappa B alpha degradation. Am J Physiol Heart Circ Physiol 2001, 281: H2612-H2618.
17. Wu J, Parungo C, Wu G, Kang PM, Laham RJ, Sellke FW, Simons M, et al. PR39 inhibits apoptosis in hypoxic endothelial cells: role of inhibitor apoptosis protein-2. Circulation 2004, 109: 1660-1667.
18. Korthuis RJ, Gute DC, Blecha F Ross CR. PR-39, a proline/arginine-rich antimicrobial peptide, prevents postischemic microvascular dysfunction. Am J Physiol 1999, 277: H1007-H1013.
19. Zhou J, Li B, Peng C, Wang F, Fu Z, Zhou C, Hong D, et al. Inhibition of cervical cancer cell growth in vitro and in vivo by lentiviral-vector mediated shRNA targeting the common promoter of HPV16 E6 and E7 oncogenes. Antiviral Res 2013, 98: 305-313.
20. Tzvetkov MV, Meineke C, Oetjen E, Hirsch-Ernst K, Brockmoller J. Tissue-specific alternative promoters of the serotonin receptor gene HTR3B in human brain and intestine. Gene 2007, 386: 52-62.
21. Thomson RB, Igarashi P, Biemesderfer D, Kim R, Abu-Alfa A, Soleimani M, Aronson PS. Isolation and cDNA cloning of Ksp-cadherin, a novel kidneyspecific member of the cadherin multigene family. J Biol Chem 1995, 270: 17594-17601.
22. Thomson RB, Aronson PS. Immunolocalization of Ksp-cadherin in the adult and developing rabbit kidney. Am J Physiol 1999, 277: F146-F156.
23. Thomson RB, Ward DC, Quaggin SE, Igarashi P, Muckler ZE, Aronson PS. cDNA cloning and chromosomal localization of the human and mouse isoforms of Ksp-cadherin. Genomics 1998, 51: 445-451.
24. Schievenbusch S, Strack I, Scheffler M, Nischt R, Coutelle O, Hosel M, Hallek M, et al. Combined paracrine and endocrine AAV9 mediated expression of hepatocyte growth factor for the treatment of renal fibrosis. Mol Ther 2010, 18: 1302-1309.
25. Pan C, Prentice H, Price AL, Wu JY. Beneficial effect of taurine on hypoxia-and glutamate-induced endoplasmic reticulum stress pathways in primary neuronal culture. Amino Acids 2012, 43: 845-855.
26. Tait SW, Parsons MJ, Llambi F, Bouchier-Hayes L, Connell S, Munoz-Pinedo C, Green DR. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev Cell 2010, 18: 802-813.
27. Sancho-Martinez SM, Lopez-Novoa JM, Lopez-Hernandez FJ. Pathophysiological role of different tubular epithelial cell death modes in acute kidney injury. Clin Kidney J 2015, 8: 548-559.
28. Linkermann A, De Zen F, Weinberg J, Kunzendorf U, Krautwald S. Programmed necrosis in acute kidney injury. Nephrol Dial Transplant 2012, 27: 3412-3419.
29. Gao H, Huang Z, Shi C, Li H. Construction and detection of the tissuespecific pINV-HPV16 E6/7 vector. Oncol Lett 2015, 9: 857-862.
30. Zhao W, Xu Y, Kong D, Liu R, Zhang Z, Jin C, Zhang Z, et al. Tissue-selective RNA interference in prostate cancer cell using prostate specific membrane antigen promoter/enhancer. Urol Oncol 2009, 27: 539-547.
31. Whyte DA, Li C, Thomson RB, Nix SL, Zanjani R, Karp SL, Aronson PS, et al. Ksp-cadherin gene promoter. I. Characterization and renal epithelial cell-specific activity. Am J Physiol 1999, 277: F587-F598.
32. Tian W, Li B, Zhang X, Dang W, Wang X, Tang H, Wang L, et al. Suppression of tumor invasion and migration in breast cancer cells following delivery of siRNA against Stat3 with the antimicrobial peptide PR39. Oncol Rep 2012, 28: 1362-1368.
33. Chan YR, Zanetti M, Gennaro R, Gallo RL. Anti-microbial activity and cell binding are controlled by sequence determinants in the anti-microbial peptide PR-39. J Invest Dermatol 2001, 116: 230-235.
34. Anbanandam A, Albarado DC, Tirziu DC, Simons M, Veeraraghavan S. Molecular basis for proline-and arginine-rich peptide inhibition of proteasome. J Mol Biol 2008, 384: 219-227.
35. Ramanathan B, Wu H, Ross CR. Blecha F. PR-39, a porcine antimicrobial peptide, inhibits apoptosis: involvement of caspase-3. Dev Comp Immunol 2004, 28: 163-169.
36. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403: 98-103.
37. Xu J, Hu H, Chen B, Yue R, Zhou Z, Liu Y, Zhang S, et al. Lycopene protects against hypoxia/reoxygenation injury by alleviating ER stress induced apoptosis in neonatal mouse cardiomyocytes. PLoS One 2015, 10: e0136443.
38. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002, 277: 34287-34294.
39. Di Sano F, Ferraro E, Tufi R, Achsel T, Piacentini M, Cecconi F. Endoplasmic reticulum stress induces apoptosis by an apoptosomedependent but caspase 12-independent mechanism. J Biol Chem 2006, 281: 2693-2700.
40. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005, 115: 2656-2664.
41. Momoi T. Caspases involved in ER stress-mediated cell death. J Chem Neuroanat 2004, 28: 101-105.
42. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011, 13: 184-190.
43. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002, 3: 401-410.
44. Hofmann K, Bucher P, Tschopp J. The CARD domain: a new apoptotic signalling motif. Trends Biochem Sci 1997, 22: 155-156.
45. Cheung HH, Lynn Kelly N, Liston P, Korneluk RG. Involvement of caspase-2 and caspase-9 in endoplasmic reticulum stress-induced apoptosis: a role for the IAPs. Exp Cell Res 2006, 312: 2347-2357.
46. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102: 33-42.
47. Rodriguez-Martinez S, Cancino-Diaz JC, Vargas-Zuniga LM, Cancino-Diaz ME. LL-37 regulates the overexpression of vascular endothelial growth factor (VEGF) and c-IAP-2 in human keratinocytes. Int J Dermatol 2008, 47: 457-462.
48. Bandurska K, Berdowska A, Barczynska-Felusiak R, Krupa P. Unique features of human cathelicidin LL-37. Biofactors 2015, 41: 289-300.
49. Iacob SA, Iacob DG. Antibacterial function of the human cathelicidin-18 peptide (LL-37) between theory and practice. Protein Pept Lett 2014, 21: 1247-1256.
50. Vazquez-Sanchez EA, Rodriguez-Romero M, Sanchez-Torres LE, Rodriguez-Martinez S, Cancino-Diaz JC, Rodriguez-Cortes O, Garcia-Lopez ES, et al. Peptidoglycan from Staphylococcus aureus has an antiapoptotic effect in HaCaT keratinocytes mediated by the production of the cellular inhibitor of apoptosis protein-2. Microbiol Immunol 2014, 58: 87-95.