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World Journal of Surgery

Published in:

01-07-2010

Histone Deacetylase Inhibitors Attenuate Acute Lung Injury During Cecal Ligation and Puncture-Induced Polymicrobial Sepsis

Authors: Li Zhang, Shengwei Jin, Changdong Wang, Rong Jiang, Jingyuan Wan

Published in: World Journal of Surgery | Issue 7/2010

Abstract

Background

The histone deacetylase (HDAC) inhibitors have emerged as the useful reagents that epigenetically modulate the expression of various genes. In the present study, the effects of HDAC inhibitors on the expression of inflammation-related genes and lung injury during sepsis were investigated.

Methods

Mice were pretreated with two structurally unrelated HDAC inhibitors, Trichostatin A (TSA) and sodium butyrate (SB). Thirty minutes later, mice underwent cecal ligation and puncture (CLP)-induced sepsis. Lung injury and the expression of inflammation-related molecules were determined. In addition, survival was assessed post-CLP.

Results

Our results indicated that administration of TSA or SB alleviated sepsis-induced lung injury. This was accompanied by reduced neutrophil infiltration, decreased intercellular adhesion molecule-1 (ICAM-1) and E-selectin expression in lung tissue, and lower interleukin-6 (IL-6) level in plasma. In addition, treatment with HDAC inhibitors significantly prolonged the survival time of CLP mice.

Conclusions

These data indicated that the HDAC inhibitors, based on modulating the key enzymes linked to acetylation modification, effectively attenuate intrapulmonary inflammatory response, thus significantly alleviating lung injury during sepsis.

Ware LB, Matthay MA (2000) The acute respiratory distress syndrome. N Engl J Med 342:1334–1349CrossRefPubMed

Phua J, Badia JR, Adhikari NK et al (2009) Has mortality from acute respiratory distress syndrome decreased over time?: a systematic review. Am J Respir Crit Care Med 179:220–227CrossRefPubMed

Balibrea JL, Arias-Díaz J (2003) Acute respiratory distress syndrome in the septic surgical patient. World J Surg 27:1275–1284CrossRefPubMed

Abraham E, Singer M (2007) Mechanisms of sepsis-induced organ dysfunction. Crit Care Med 35:2408–2416CrossRefPubMed

Kawai T, Akira S (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143:1–20CrossRefPubMed

Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8:349–361CrossRefPubMed

Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412CrossRefPubMed

Ito T (2007) Role of histone modification in chromatin dynamics. J Biochem 141:609–614CrossRefPubMed

Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12:142–148CrossRefPubMed

10.

Yang XJ, Seto E (2007) HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 26:5310–5318CrossRefPubMed

11.

Pan LN, Lu J, Huang B (2007) HDAC inhibitors: a potential new category of anti-tumor agents. Cell Mol Immunol 4:337–343PubMed

12.

Mehnert JM, Kelly WK (2007) Histone deacetylase inhibitors: biology and mechanism of action. Cancer J 13:23–29CrossRefPubMed

13.

Leoni F, Fossati G, Lewis EC et al (2005) The histone deacetylase inhibitor ITF2357 reduces production of pro-inflammatory cytokines in vitro and systemic inflammation in vivo. Mol Med 11:1–15CrossRefPubMed

14.

Choi JH, Oh SW, Kang MS et al (2005) Trichostatin A attenuates airway inflammation in mouse asthma model. Clin Exp Allergy 35:89–96CrossRefPubMed

15.

Glauben R, Batra A, Fedke I et al (2006) Histone hyperacetylation is associated with amelioration of experimental colitis in mice. J Immunol 176:5015–5022PubMed

16.

Lin HS, Hu CY, Chan HY et al (2007) Anti-rheumatic activities of histone deacetylase (HDAC) inhibitors in vivo in collagen-induced arthritis in rodents. Br J Pharmacol 150:862–872CrossRefPubMed

17.

Han SB, Lee JK (2009) Anti-inflammatory effect of Trichostatin-A on murine bone marrow-derived macrophages. Arch Pharm Res 32:613–624CrossRefPubMed

18.

Iwata K, Tomita K, Sano H et al (2002) Trichostatin A, a histone deacetylase inhibitor, down-regulates interleukin-12 transcription in SV-40-transformed lung epithelial cells. Cell Immunol 218:26–33CrossRefPubMed

19.

Li Y, Liu B, Zhao H et al (2009) Protective effect of suberoylanilide hydroxamic acid against LPS-induced septic shock in rodents. Shock 32:517–523CrossRefPubMed

20.

Sailhamer EA, Li Y, Smith EJ et al (2008) Acetylation: a novel method for modulation of the immune response following trauma/hemorrhage and inflammatory second hit in animals and humans. Surgery 144:204–216CrossRefPubMed

21.

Caldwell CC, Martignoni A, Leonis MA et al (2008) Ron receptor tyrosine kinase-dependent hepatic neutrophil recruitment and survival benefit in a murine model of bacterial peritonitis. Crit Care Med 36:1585–1593CrossRefPubMed

22.

Rittirsch D, Huber-Lang MS, Flierl MA et al (2009) Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc 4:31–36CrossRefPubMed

23.

van Griensven M, Probst C, Müller K et al (2006) Leukocyte-endothelial interactions via ICAM-1 are detrimental in polymicrobial sepsis. Shock 25:254–259CrossRefPubMed

24.

Rossi B, Constantin G (2008) Anti-selectin therapy for the treatment of inflammatory diseases. Inflamm Allergy Drug Targets 7:85–93CrossRefPubMed

25.

Yang XJ, Seto E (2008) Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31:449–461CrossRefPubMed

26.

Halili MA, Andrews MR, Sweet MJ et al (2009) Histone deacetylase inhibitors in inflammatory disease. Curr Top Med Chem 9:309–319CrossRefPubMed

27.

Blanchard F, Chipoy C (2005) Histone deacetylase inhibitors: new drugs for the treatment of inflammatory diseases? Drug Discov Today 10:197–204CrossRefPubMed

28.

Wagner JG, Roth RA (2000) Neutrophil migration mechanisms, with an emphasis on the pulmonary vasculature. Pharmacol Rev 52:349–374PubMed

29.

Zemans RL, Colgan SP, Downey GP (2009) Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 40:519–535CrossRefPubMed

30.

Reutershan J, Ley K (2004) Bench-to-bedside review: acute respiratory distress syndrome—how neutrophils migrate into the lung. Crit Care 8:453–461CrossRefPubMed

31.

Calandra T, Gerain J, Heumann D et al (1991) High circulating levels of interleukin-6 in patients with septic shock: evolution during sepsis, prognostic value, and interplay with other cytokines. Am J Med 91:23–29CrossRefPubMed

32.

Gårdlund B, Sjölin J, Nilsson A et al (1995) Plasma levels of cytokines in primary septic shock in humans: correlation with disease severity. J Infect Dis 172:296–301PubMed

33.

Damas P, Ledoux D, Nys M et al (1992) Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 215:356–362CrossRefPubMed

34.

Cao W, Bao C, Padalko E et al (2008) Acetylation of mitogen-activated protein kinase phosphatase-1 inhibits Toll-like receptor signaling. J Exp Med 205:1491–1503CrossRefPubMed

35.

Chen Lf, Fischle W, Verdin E et al (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293:1653–1657CrossRef

36.

Chen LF, Greene WC (2003) Regulation of distinct biological activities of the NF-kappaB transcription factor complex by acetylation. J Mol Med 81:549–557CrossRefPubMed

37.

Batta K, Das C, Gadad S et al (2007) Reversible acetylation of nonhistone proteins: role in cellular function and disease. Subcell Biochem 41:193–212CrossRefPubMed

38.

Das C, Kundu TK (2005) Transcriptional regulation by the acetylation of nonhistone proteins in humans—a new target for therapeutics. IUBMB Life 57:137–149CrossRefPubMed

39.

Esmon CT (2004) Why do animal models (sometimes) fail to mimic human sepsis? Crit Care Med 32:S219–S222CrossRefPubMed

Title: Histone Deacetylase Inhibitors Attenuate Acute Lung Injury During Cecal Ligation and Puncture-Induced Polymicrobial Sepsis
Authors: Li Zhang
Shengwei Jin
Changdong Wang
Rong Jiang
Jingyuan Wan
Publication date: 01-07-2010
Publisher: Springer-Verlag
Published in: World Journal of Surgery / Issue 7/2010
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI: https://doi.org/10.1007/s00268-010-0493-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Histone Deacetylase Inhibitors Attenuate Acute Lung Injury During Cecal Ligation and Puncture-Induced Polymicrobial Sepsis

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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