A small molecule inhibitor of PAI-1 protects against Doxorubicin-induced cellular senescence: molecular basis

Oncotarget

Volumn 7, Issue 45, 2016, Pages 72443-72457

  Ghosh, Asish K ^a   Rai, Rahul ^a   Park, Kitae E ^a   Eren, Mesut ^a   Miyata, Toshio ^b   Wilsbacher, Lisa D ^a   Vaughan, Douglas E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cardiomyocytes; Cellular senescence; Doxorubicin; Endothelial cells; Fibroblasts

Indexed keywords

CATALASE; DOXORUBICIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTECTIVE AGENT; PROTEIN P16; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN BINDING PROTEIN 3; TM 5441; TM 5484; UNCLASSIFIED DRUG; 4 AMINOBENZOIC ACID DERIVATIVE; ANTINEOPLASTIC ANTIBIOTIC; PIPERAZINE DERIVATIVE; PROTEASE NEXIN I; SERPINE2 PROTEIN, MOUSE; TM5441;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CANCER ADJUVANT THERAPY; CARDIAC MUSCLE CELL; CARDIOTOXICITY; CELL AGING; CELL PROTECTION; CELL STRESS; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; EMBRYO; ENDOTHELIUM CELL; ENZYME INDUCTION; HEART FIBROBLAST; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NEWBORN; NONHUMAN; PHARMACOLOGICAL BLOCKING; RAT; SENESCENCE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; FIBROBLAST; METABOLISM; PATHOLOGY; CELL DIVISION; MOLECULAR BIOLOGY; PROTEIN SYNTHESIS INHIBITION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOTOXICITY; CELLS, CULTURED; CELLULAR SENESCENCE; DOXORUBICIN; FIBROBLASTS; HUMANS; MICE; MYOCYTES, CARDIAC; PARA-AMINOBENZOATES; PIPERAZINES; RATS; SERPIN E2;

EID: 84995745327     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12494     Document Type: Article

References (39)

1. Campisi J and d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell. Biol. 2007; 8:729-740
2. Muñoz-Espín D and Serrano M. Cellular senescence: from physiology to pathology. Nat. Rev. Mol Cell. Biol. 2014; 15:482-496
3. Blagosklonny MV. Geroconversion: irreversible step to cellular senescence. Cell Cycle. 2014;13:3628-3635
4. Leontieva OV and Blagosklonny MV. Gerosuppression in confluent cells. Aging (Albany NY). 2014; 6:1010-1018
5. Rodier F and Campisi J. Four faces of cellular senescence. J. Cell. Biol. 2011; 192:547-556
6. Campisi J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 2013; 75:685-705
7. Purcell M, Kruger A and Tainsky MA. (2014) Gene expression profiling of replicative and induced senescence. Cell Cycle. 2014; 13:3927-3937
8. Kortlever RM and Bernards R. Senescence, wound healing and cancer: the PAI-1 connection. Cell Cycle. 2006; 5, 2697-2703
9. Kortlever RM, Higgins PJ and Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat. Cell. Biol. 2006; 8:877-884
10. Kortlever RM, Nijwening JH and Bernards R. Transforming growth factor-beta requires its target plasminogen activator inhibitor-1 for cytostatic activity. J. Biol. Chem. 2008; 283:24308-24313
11. Elzi DJ, Lai Y, Song M, Hakala K, Weintraub ST and Shiio Y. Plasminogen activator inhibitor 1 insulin-like growth factor binding protein 3 cascade regulates stress-induced senescence. Proc Natl Acad Sci U S A. 2012; 109:12052-12057
12. Ghosh AK, Bradham WS, Gleaves LA, De Taeye B, Murphy SB, Covington JW and Vaughan DE. Genetic deficiency of plasminogen activator inhibitor-1 promotes cardiac fibrosis in aged mice involvement of constitutive transforming growth factor-beta signaling and endothelialto-mesenchymal transition. Circulation. 2010; 122:1200-1209
13. Ghosh AK and Vaughan DE. PAI-1 in tissue fibrosis. J. Cell. Physiol. 2012; 227:493-507
14. Ghosh AK, Murphy SB, Kishore R and Vaughan DE. Global gene expression profiling in PAI-1 knockout murine heart and kidney: molecular basis of cardiac-selective fibrosis. PLoS One. 2013; 8: e63825
15. Eren M, Boe AE, Murphy SB, Place AT, Nagpal V, Morales-Nebreda L, Urich D, Quaggin SE, Budinger GR, Mutlu GM, Miyata T and Vaughan DE. PAI-1-regulated extracellular proteolysis governs senescence and survival in Klotho mice. Proc. Natl. Acad. Sci. U S A. 2014; 111:7090-7095
16. Eren M, Boe AE, Klyachko EA and Vaughan DE. Role of plasminogen activator inhibitor-1 in senescence and aging. Semin. Thromb. Hemost. 2014; 40:645-651
17. Placencio VR, Ichimura A, Miyata T and DeClerck YA. Small Molecule Inhibitors of Plasminogen Activator Inhibitor-1 Elicit Anti-Tumorigenic and Anti-Angiogenic Activity. PLoS One. 2015; 10: e0133786
18. Ludke AR, Al-Shudiefat AA, Dhingra S, Jassal DS and Singal PK. A concise description of cardio-protective strategies in doxorubicin-induced cardiotoxicity. Can. J. Physiol. Pharmacol. 2009; 87, 756-763
19. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ and Moens AL. Doxorubicin induced cardiomyopathy: From molecular mechanisms to therapeutic strategies. J. Mol. Cell. Cardiol. 2012; 52:1213-1225
20. Giordano P, Molinari AC, Del Vecchio GC, Saracco P, Russo G, Altomare M, Perutelli P, Crescenzio N, Santoro N, Marchetti M, De Mattia D and Falanga A. Prospective study of hemostatic alterations in children with acute lymphoblastic leukemia. Am. J. Hematol. 2010; 85: 325-330
21. Venkatesan B, Prabhu SD, Venkatachalam K, Mummidi S, Valente AJ, Clark RA, Delafontaine P and Chandrasekar B. WNT1-inducible signaling pathway protein-1 activates diverse cell survival pathways and blocks doxorubicininduced cardiomyocyte death. Cell. Signal. 2010; 22:809-820
22. Poljsak B. Strategies for Reducing or Preventing the Generation of Oxidative Stress. Oxidative Medicine and Cellular Longevity, 2011; vol. 2011, ID 194586, 15 pages, doi:10.1155/2011/194586
23. Tilstra JS, Robinson AR, Wang J, Gregg SQ, Clauson CL, Reay DP, Nasto LA, St Croix CM, Usas A, Vo N, Huard J, Clemens PR, Stolz DB, Guttridge DC, Watkins SC, Garinis GA, Wang Y, Niedernhofer LJ and Robbins PD. NF-κB inhibition delays DNA damage-induced senescence and aging in mice. J. Clin. Invest. 2012; 122:2601-2612
24. Zhao W, Spitz DR, Oberley LW and Robbins ME. Redox modulation of the pro-fibrogenic mediator plasminogen activator inhibitor-1 following ionizing radiation. Cancer Res. 2001; 61:5537-5543
25. Kang YJ, Chen Y and Epstein PN. Suppression of doxorubicin cardiotoxicity by overexpression of catalase in the heart of transgenic mice. J. Biol. Chem. 1996; 271:12610-12616
26. Kang YJ, Sun X, Chen Y and Zhou Z. Inhibition of doxorubicin chronic toxicity in catalase overexpressing transgenic mouse hearts. Chem. Res. Toxicol. 2002; 15;1-6
27. Leontieva OV, Gudkov AV and Blagosklonny MV. Weak p53 permits senescence during cell cycle arrest. Cell Cycle. 2010; 9:4323-4327
28. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M and Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 2004; 114:1752-1761
29. Özcan S, Alessio N, Acar MB, Mert E, Omerli F, Peluso G and Galderisi U. Unbiased analysis of senescence associated secretory phenotype (SASP) to identify common components genotoxic stresses Aging (Albany NY). 2016; 8: 1316-1329
30. Li X, Lu Y, Liang K, Liu B and Fan Z. Differential responses to doxorubicin-induced phosphorylation and activation of Akt in human breast cancer cells. Breast Cancer Res.2005; 7:R589-R597. www.impactjournals.com/oncotarget72457Oncotarget
31. Spallarossa P, Altieri P, Garibaldi S, Ghigliotti G, Barisione C, Manca V, Fabbi P, Ballestrero A, Brunelli C and Barsotti A. Matrix metalloproteinase-2 and-9 are induced differently by doxorubicin in H9c2 cells: The role of MAP kinases and NAD(P)H oxidase. Cardiovasc. Res. 2006; 69: 736-745
32. Spallarossa P, Altieri P, Barisione C, Passalacqua M, Aloi C, Fugazza G, Frassoni F, Podesta M, Canepa M, Ghigliotti G and Brunelli C. P38 MAPK and JNK antagonistically control senescence and cytoplasmic p16INK4A expression in doxorubicin-treated endothelial progenitor cells. PLoS One. 2010; 5:e15583
33. Wold LE, Aberle NN and Ren J. Doxorubicin induces cardiomyocyte dysfunction via a p38 MAP kinasedependent oxidative stress mechanism. Cancer Detect. Prev. 2005; 29:294-299
34. Kim SY, Kim SJ, Kim BJ, Rah SY, Chung SM, Im MJ and Kim UH. Doxorubicin-induced reactive oxygen species generation and intracellular Ca2+ increase are reciprocally modulated in rat cardio-myocytes. Exp. Mol. Med. 2006; 38:535-545
35. Thandavarayan RA, Watanabe K, Sari FR, Ma M, Lakshmanan AP, Giridharan VV, Gurusamy N, Nishida H, Konishi T, Zhang S, Muslin AJ, Kodama M and Aizawa Y. Modulation of doxorubicin-induced cardiac dysfunction in dominant-negative p38alpha mitogen-activated protein kinase mice. Free Radic. Biol. Med. 2010; 49:1422-1431
36. Piegari E, De Angelis A, Cappetta D, Russo R, Esposito G, Costantino S, Graiani G, Frati C, Prezioso L, Berrino L, Urbanek K, Quaini F and Rossi F. Doxorubicin induces senescence and impairs function of human cardiac progenitor cells. Basic Res. Cardiol. 2013; 108:334-351
37. Watkins SJ, Borthwick GM and Arthur HM. The H9C2 cell line and primary neonatal cardiomyocyte cells show similar hypertrophic responses in vitro. In Vitro Cell. Dev. Biol. Anim. 2011; 47:125-131
38. Ahn K, Pan S, Beningo K and Hupe D. A permanent human cell line (EA.hy926) preserves the characteristics of endothelin converting enzyme from primary human umbilical vein endothelial cells. Life Sci. 1995; 56:2331-2341
39. Zhou M, Gu L, Li F, Zhu Y, Woods WG, Findley HW. DNA damage induces a novel p53-survivin signaling pathway regulating cell cycle and apoptosis in acute lymphoblastic leukemia cells. J Pharmacol Exp Ther. 2002;303:124-131