Heat shock protein 72 enhances autophagy as a protective mechanism in lipopolysaccharide-induced peritonitis in rats

American Journal of Pathology

Volumn 179, Issue 6, 2011, Pages 2822-2834

  Li, Shu ^a   Zhou, Yi ^a   Fan, Jinjin ^a   Cao, Shirong ^a   Cao, Tao ^a   Huang, Fengxian ^a   Zhuang, Shougang ^b   Wang, Yihan ^c,d   Yu, Xueqing ^a   Mao, Haiping ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b BROWN UNIVERSITY   (United States)

^c Nephropathology Associates   (United States)

^d Laboratory for Kidney Pathology Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; HEAT SHOCK PROTEIN 72; LIPOPOLYSACCHARIDE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CULTURE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MESOTHELIUM CELL; NONHUMAN; PERITONEUM CELL; PERITONITIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; UPREGULATION;

ADENINE; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL SURVIVAL; CELLS, CULTURED; CHLOROQUINE; DITERPENES; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; GREEN FLUORESCENT PROTEINS; HSP72 HEAT-SHOCK PROTEINS; LIPOPOLYSACCHARIDES; LUMINESCENT AGENTS; MALE; MAP KINASE SIGNALING SYSTEM; PERITONEAL CAVITY; PERITONITIS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 81255214620     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.08.013     Document Type: Article

References (64)

1. J.H. Vernooy, M.A. Dentener, R.J. van Suylen, W.A. Buurman, and E.F. Wouters Intratracheal instillation of lipopolysaccharide in mice induces apoptosis in bronchial epithelial cells: no role for tumor necrosis factor-alpha and infiltrating neutrophils Am J Respir Cell Mol Biol 24 2001 569 576 (Pubitemid 32442764)
2. I. Bohlinger, M. Leist, F. Gantner, S. Angermuller, G. Tiegs, and A. Wendel DNA fragmentation in mouse organs during endotoxic shock Am J Pathol 149 1996 1381 1393 (Pubitemid 26337255)
3. X. Wang, B. Zingarelli, M. O'Connor, P. Zhang, A. Adeyemo, E.G. Kranias, Y. Wang, and G.C. Fan Overexpression of Hsp20 prevents endotoxin-induced myocardial dysfunction and apoptosis via inhibition of NF-kappaB activation J Mol Cell Cardiol 47 2009 382 390
4. M. Fujita, K. Kuwano, R. Kunitake, N. Hagimoto, H. Miyazaki, Y. Kaneko, M. Kawasaki, T. Maeyama, and N. Hara Endothelial cell apoptosis in lipopolysaccharide-induced lung injury in mice Int Arch Allergy Immunol 117 1998 202 208 (Pubitemid 28526168)
5. A. Haimovitz-Friedman, C. Cordon-Cardo, S. Bayoumy, M. Garzotto, M. McLoughlin, R. Gallily, C.K. Edwards 3rd, E.H. Schuchman, Z. Fuks, and R. Kolesnick Lipopolysaccharide induces disseminated endothelial apoptosis requiring ceramide generation J Exp Med 186 1997 1831 1841 (Pubitemid 27524593)
6. D.L. Hickson-Bick, C. Jones, and L.M. Buja Stimulation of mitochondrial biogenesis and autophagy by lipopolysaccharide in the neonatal rat cardiomyocyte protects against programmed cell death J Mol Cell Cardiol 44 2008 411 418
7. N. Meng, L. Wu, J. Gao, J. Zhao, L. Su, H. Su, S. Zhang, and J. Miao Lipopolysaccharide induces autophagy through BIRC2 in human umbilical vein endothelial cells J Cell Physiol 225 2010 174 179
8. K. Wang, I. Damjanov, and Y.J. Wan The protective role of pregnane X receptor in lipopolysaccharide/D-galactosamine-induced acute liver injury Lab Invest 90 2010 257 265
9. E.H. Carchman, J. Rao, P.A. Loughran, M.R. Rosengart, and B.S. Zuckerbraun Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice Hepatology 53 2011 2053 2062
10. Z. Xie, and D.J. Klionsky Autophagosome formation: core machinery and adaptations Nat Cell Biol 9 2007 1102 1109 (Pubitemid 47500484)
11. Y. Ohsumi Molecular dissection of autophagy: two ubiquitin-like systems Nat Rev Mol Cell Biol 2 2001 211 216 (Pubitemid 33675746)
12. K. Suzuki, T. Kirisako, Y. Kamada, N. Mizushima, T. Noda, and Y. Ohsumi The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation EMBO J 20 2001 5971 5981 (Pubitemid 33049272)
13. P. Boya, R.A. Gonzalez-Polo, N. Casares, J.L. Perfettini, P. Dessen, N. Larochette, D. Metivier, D. Meley, S. Souquere, T. Yoshimori, G. Pierron, P. Codogno, and G. Kroemer Inhibition of macroautophagy triggers apoptosis Mol Cell Biol 25 2005 1025 1040 (Pubitemid 40165810)
14. Y. Ishida, and K. Nagata Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress Autophagy 5 2009 1217 1219
15. R. Scherz-Shouval, H. Weidberg, C. Gonen, S. Wilder, Z. Elazar, and M. Oren p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation Proc Natl Acad Sci U S A 107 2010 18511 18516
16. J. Li, N. Hou, A. Faried, S. Tsutsumi, T. Takeuchi, and H. Kuwano Inhibition of autophagy by 3-MA enhances the effect of 5-FU-induced apoptosis in colon cancer cells Ann Surg Oncol 16 2009 761 771
17. S. Periyasamy-Thandavan, M. Jiang, Q. Wei, R. Smith, X.M. Yin, and Z. Dong Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells Kidney Int 74 2008 631 640
18. M. Jiang, K. Liu, J. Luo, and Z. Dong Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury Am J Pathol 176 2010 1181 1192
19. P.M. Yang, Y.L. Liu, Y.C. Lin, C.T. Shun, M.S. Wu, and C.C. Chen Inhibition of autophagy enhances anticancer effects of atorvastatin in digestive malignancies Cancer Res 70 2010 7699 7709
20. K. Degenhardt, R. Mathew, B. Beaudoin, K. Bray, D. Anderson, G. Chen, C. Mukherjee, Y. Shi, C. Gelinas, Y. Fan, D.A. Nelson, S. Jin, and E. White Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis Cancer Cell 10 2006 51 64
21. F. Li, H.P. Mao, K.L. Ruchalski, Y.H. Wang, W. Choy, J.H. Schwartz, and S.C. Borkan Heat stress prevents mitochondrial injury in ATP-depleted renal epithelial cells Am J Physiol Cell Physiol 283 2002 C917 C926
22. H.M. Beere, B.B. Wolf, K. Cain, D.D. Mosser, A. Mahboubi, T. Kuwana, P. Tailor, R.I. Morimoto, G.M. Cohen, and D.R. Green Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome Nat Cell Biol 2 2000 469 475
23. V.L. Gabai, J.A. Yaglom, V. Volloch, A.B. Meriin, T. Force, M. Koutroumanis, B. Massie, D.D. Mosser, and M.Y. Sherman Hsp72-mediated suppression of c-Jun N-terminal kinase is implicated in development of tolerance to caspase-independent cell death Mol Cell Biol 20 2000 6826 6836
24. B. Bidmon, M. Endemann, K. Arbeiter, D. Ruffingshofer, H. Regele, K. Herkner, O. Eickelberg, and C. Aufricht Overexpression of HSP-72 confers cytoprotection in experimental peritoneal dialysis Kidney Int 66 2004 2300 2307 (Pubitemid 41115293)
25. Y. Zhou, H. Mao, S. Li, S. Cao, Z. Li, S. Zhuang, J. Fan, X. Dong, S.C. Borkan, Y. Wang, and X. Yu HSP72 inhibits Smad3 activation and nuclear translocation in renal epithelial-to-mesenchymal transition J Am Soc Nephrol 21 2010 598 609
26. H. Mao, Y. Wang, Z. Li, K.L. Ruchalski, X. Yu, J.H. Schwartz, and S.C. Borkan Hsp72 interacts with paxillin and facilitates the reassembly of focal adhesions during recovery from ATP depletion J Biol Chem 279 2004 15472 15480 (Pubitemid 38618947)
27. J.P. Rougier, P. Moullier, R. Piedagnel, and P.M. Ronco Hyperosmolality suppresses but TGF beta 1 increases MMP9 in human peritoneal mesothelial cells Kidney Int 51 1997 337 347 (Pubitemid 27064556)
28. T. Rampino, G. Cancarini, M. Gregorini, P. Guallini, M. Maggio, A. Ranghino, G. Soccio, and A. Dal Canton Hepatocyte growth factor/scatter factor released during peritonitis is active on mesothelial cells Am J Pathol 159 2001 1275 1285 (Pubitemid 32947957)
29. F. Zhu, T. Li, F. Qiu, J. Fan, Q. Zhou, X. Ding, J. Nie, and X. Yu Preventive effect of Notch signaling inhibition by a gamma-secretase inhibitor on peritoneal dialysis fluid-induced peritoneal fibrosis in rats Am J Pathol 176 2010 650 659
30. J. Nie, X. Dou, W. Hao, X. Wang, W. Peng, Z. Jia, W. Chen, X. Li, N. Luo, H.Y. Lan, and X.Q. Yu Smad7 gene transfer inhibits peritoneal fibrosis Kidney Int 72 2007 1336 1344 (Pubitemid 350126775)
31. H. Mao, Z. Li, Y. Zhou, Z. Li, S. Zhuang, X. An, B. Zhang, W. Chen, J. Nie, Z. Wang, S.C. Borkan, Y. Wang, and X. Yu HSP72 attenuates renal tubular cell apoptosis and interstitial fibrosis in obstructive nephropathy Am J Physiol Renal Physiol 295 2008 F202 F214
32. T.H. Leu, S. Charoenfuprasert, C.K. Yen, C.W. Fan, and M.C. Maa Lipopolysaccharide-induced c-Src expression plays a role in nitric oxide and TNFalpha secretion in macrophages Mol Immunol 43 2006 308 316 (Pubitemid 41668840)
33. S.H. Song, I.S. Kwak, B.Y. Yang, D.W. Lee, S.B. Lee, and M.Y. Lee Role of rosiglitazone in lipopolysaccharide-induced peritonitis: a rat peritoneal dialysis model Nephrology (Carlton) 14 2009 155 163
34. S. Suzuki, S. Maruyama, W. Sato, Y. Morita, F. Sato, Y. Miki, S. Kato, M. Katsuno, G. Sobue, Y. Yuzawa, and S. Matsuo Geranylgeranylacetone ameliorates ischemic acute renal failure via induction of Hsp70 Kidney Int 67 2005 2210 2220 (Pubitemid 41623382)
35. M.C. Maiuri, E. Zalckvar, A. Kimchi, and G. Kroemer Self-eating and self-killing: crosstalk between autophagy and apoptosis Nat Rev Mol Cell Biol 8 2007 741 752 (Pubitemid 47312826)
36. B. Levine, and J. Yuan Autophagy in cell death: an innocent convict? J Clin Invest 115 2005 2679 2688 (Pubitemid 41434392)
37. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J 19 2000 5720 5728
38. Yang Z, Klionsky DJ: Eaten alive: a history of macroautophagy, Nat Cell Biol 12:814822
39. K. Takahashi, M. Naito, S. Umeda, and L.D. Shultz The role of macrophage colony-stimulating factor in hepatic glucan-induced granuloma formation in the osteopetrosis mutant mouse defective in the production of macrophage colony-stimulating factor Am J Pathol 144 1994 1381 1392
40. H.L. Li, J. Suzuki, E. Bayna, F.M. Zhang, E. Dalle Molle, A. Clark, R.L. Engler, and W.Y. Lew Lipopolysaccharide induces apoptosis in adult rat ventricular myocytes via cardiac AT(1) receptors Am J Physiol Heart Circ Physiol 283 2002 H461 H467
41. W. Lieberthal Macroautophagy: a mechanism for mediating cell death or for promoting cell survival? Kidney Int 74 2008 555 557
42. Y. Wang, R. Singh, A.C. Massey, S.S. Kane, S. Kaushik, T. Grant, Y. Xiang, A.M. Cuervo, and M.J. Czaja Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus J Biol Chem 283 2008 4766 4777
43. S. Gupta, A. Deepti, S. Deegan, F. Lisbona, C. Hetz, and A. Samali HSP72 protects cells from ER stress-induced apoptosis via enhancement of IRE1alpha-XBP1 signaling through a physical interaction PLoS Biol 8 2010 e1000410
44. D.D. Li, L.L. Wang, R. Deng, J. Tang, Y. Shen, J.F. Guo, Y. Wang, L.P. Xia, G.K. Feng, Q.Q. Liu, W.L. Huang, Y.X. Zeng, and X.F. Zhu The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agents-induced autophagy in cancer cells Oncogene 28 2009 886 898
45. H. Ren, K. Fu, C. Mu, B. Li, D. Wang, and G. Wang DJ-1, a cancer and Parkinson's disease associated protein, regulates autophagy through JNK pathway in cancer cells Cancer Lett 297 2010 101 108
46. Q. Cui, S. Tashiro, S. Onodera, M. Minami, and T. Ikejima Oridonin induced autophagy in human cervical carcinoma HeLa cells through Ras JNK, and P38 regulation J Pharmacol Sci 105 2007 317 325
47. Y. Ishii, J.M. Kwong, and J. Caprioli Retinal ganglion cell protection with geranylgeranylacetone, a heat shock protein inducer, in a rat glaucoma model Invest Ophthalmol Vis Sci 44 2003 1982 1992 (Pubitemid 36520289)
48. Y. Xu, S.O. Kim, Y. Li, and J. Han Autophagy contributes to caspase-independent macrophage cell death J Biol Chem 281 2006 19179 19187 (Pubitemid 44035422)
49. D. Hofius, T. Schultz-Larsen, J. Joensen, D.I. Tsitsigiannis, N.H. Petersen, O. Mattsson, L.B. Jorgensen, J.D. Jones, J. Mundy, and M. Petersen Autophagic components contribute to hypersensitive cell death in Arabidopsis Cell 137 2009 773 783
50. C. Veneault-Fourrey, M. Barooah, M. Egan, G. Wakley, and N.J. Talbot Autophagic fungal cell death is necessary for infection by the rice blast fungus Science 312 2006 580 583
51. A. Colell, J.E. Ricci, S. Tait, S. Milasta, U. Maurer, L. Bouchier-Hayes, P. Fitzgerald, A. Guio-Carrion, N.J. Waterhouse, C.W. Li, B. Mari, P. Barbry, D.D. Newmeyer, H.M. Beere, and D.R. Green GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation Cell 129 2007 983 997 (Pubitemid 46813151)
52. Y.T. Wu, H.L. Tan, Q. Huang, Y.S. Kim, N. Pan, W.Y. Ong, Z.G. Liu, C.N. Ong, and H.M. Shen Autophagy plays a protective role during zVAD-induced necrotic cell death Autophagy 4 2008 457 466 (Pubitemid 351705142)
53. P. James, C. Pfund, and E.A. Craig Functional specificity among Hsp70 molecular chaperones Science 275 1997 387 389 (Pubitemid 27051615)
54. I. Guzhova, and B. Margulis Hsp70 chaperone as a survival factor in cell pathology Int Rev Cytol 254 2006 101 149 (Pubitemid 44828728)
55. Y. Zhao, W. Wang, and L. Qian Hsp70 may protect cardiomyocytes from stress-induced injury by inhibiting Fas-mediated apoptosis Cell Stress Chaperones 12 2007 83 95 (Pubitemid 47403331)
56. Q. Yang, H. She, M. Gearing, E. Colla, M. Lee, J.J. Shacka, and Z. Mao Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy Science 323 2009 124 127
57. J.F. Dice Chaperone-mediated autophagy Autophagy 3 2007 295 299 (Pubitemid 46986334)
58. M.I. Hirsh, N. Hashiguchi, Y. Chen, L. Yip, and W.G. Junger Surface expression of HSP72 by LPS-stimulated neutrophils facilitates gammadeltaT cell-mediated killing Eur J Immunol 36 2006 712 721
59. D. Tang, R. Kang, W. Xiao, H. Wang, S.K. Calderwood, and X. Xiao The anti-inflammatory effects of heat shock protein 72 involve inhibition of high-mobility-group box 1 release and proinflammatory function in macrophages J Immunol 179 2007 1236 1244
60. Y. Wei, S. Pattingre, S. Sinha, M. Bassik, and B. Levine JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy Mol Cell 30 2008 678 688 (Pubitemid 351818252)
61. C. Li, E. Capan, Y. Zhao, J. Zhao, D. Stolz, S.C. Watkins, S. Jin, and B. Lu Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death J Immunol 177 2006 5163 5168 (Pubitemid 44527588)
62. T. Borsello, K. Croquelois, J.P. Hornung, and P.G. Clarke N-methyl-d-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway Eur J Neurosci 18 2003 473 485 (Pubitemid 37041099)
63. G. Jia, G. Cheng, D.M. Gangahar, and D.K. Agrawal Insulin-like growth factor-1 and TNF-alpha regulate autophagy through c-jun N-terminal kinase and Akt pathways in human atherosclerotic vascular smooth cells Immunol Cell Biol 84 2006 448 454 (Pubitemid 44286038)
64. K.J. Park, S.H. Lee, C.H. Lee, J.Y. Jang, J. Chung, M.H. Kwon, and Y.S. Kim Upregulation of Beclin-1 expression and phosphorylation of Bcl-2 and p53 are involved in the JNK-mediated autophagic cell death Biochem Biophys Res Commun 382 2009 726 729