Alteration of histone H3 lysine 9 dimethylation in peripheral white blood cells of septic patients with trauma and cancer

Jiang,Linghui; Wang,Yiqin; Zhu,Duming; Xue,Zhanggang; Mao,Hailei

doi:10.3892/mmr.2016.5958

Alteration of histone H3 lysine 9 dimethylation in peripheral white blood cells of septic patients with trauma and cancer

Authors:
- Linghui Jiang
- Yiqin Wang
- Duming Zhu
- Zhanggang Xue
- Hailei Mao
View Affiliations

Affiliations: Departments of Anesthesiology and Critical Care Medicine, Zhongshan Hospital, Fudan University, Shanghai 200032, P.R. China, State Key Laboratory of Molecular Biology and Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, P.R. China
Published online on: November 22, 2016 https://doi.org/10.3892/mmr.2016.5958
Pages: 5467-5474
Copyright: © Jiang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The present study aimed to investigate the clinical significance of histone methylation in sepsis. A total of 43 blood samples from trauma and esophageal cancer patients with or without sepsis were collected. Immunofluorescence staining of isolated peripheral white blood cells (WBCs) was conducted. Co‑stained 293T cells served as a reference, to allow the levels of histone methylation in different types of WBCs from patients to be determined. Immunostaining analyses revealed different levels of histone 3 lysine 9 dimethylation (H3K9me2) in neutrophils (Neu), lymphocytes (Lym), and monocytes (Mon) from trauma patients. Compared with trauma patients, the levels of H3K9me2 were elevated in the three types of WBCs from cancer patients. When combined with sepsis, trauma patients demonstrated increased H3K9me2 levels in Neu (P=0.0005) and Mon (P=0.0002), whereas cancer patients had a significant decrease of H3K9me2 levels in the three types of WBCs (Neu, P=0.0003; Lym, P=0.007; Mon, P=0.007). The H3K9me2 alterations in patients with trauma and cancer were different with the occurrence of sepsis. A larger cohort study is warranted to explore the diagnostic significance and prognostic implications of altered histone methylation in septic patients.

View Figures

View References

1	Soong J and Soni N: Sepsis: Recognition and treatment. Clin Med (Lond). 12:276–280. 2012. View Article : Google Scholar : PubMed/NCBI
2	An G, Namas RA and Vodovotz Y: Sepsis: From pattern to mechanism and back. Crit Rev Biomed Eng. 40:341–351. 2012. View Article : Google Scholar : PubMed/NCBI
3	Cavaillon JM, Adrie C, Fitting C and Adib-Conquy M: Reprogramming of circulatory cells in sepsis and SIRS. J Endotoxin Res. 11:311–320. 2005. View Article : Google Scholar : PubMed/NCBI
4	Chen S, Ma J, Wu F, Xiong LJ, Ma H, Xu W, Lv R, Li X, Villen J, Gygi SP, et al: The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev. 26:1364–1375. 2012. View Article : Google Scholar : PubMed/NCBI
5	De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, Austenaa L, Bucci G, Caganova M, Notarbartolo S, Casola S, et al: Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J. 28:3341–3352. 2009. View Article : Google Scholar : PubMed/NCBI
6	Chen X, El Gazzar M, Yoza BK and McCall CE: The NF-kappaB factor RelB and histone H3 lysine methyltransferase G9a directly interact to generate epigenetic silencing in endotoxin tolerance. J Biol Chem. 284:27857–27865. 2009. View Article : Google Scholar : PubMed/NCBI
7	De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G and Natoli G: The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell. 130:1083–1094. 2007. View Article : Google Scholar : PubMed/NCBI
8	Chan C, Li L, McCall CE and Yoza BK: Endotoxin tolerance disrupts chromatin remodeling and NF-kappaB transactivation at the IL-1beta promoter. J Immunol. 175:461–468. 2005. View Article : Google Scholar : PubMed/NCBI
9	Foster SL, Hargreaves DC and Medzhitov R: Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature. 447:972–978. 2007.PubMed/NCBI
10	Greer EL and Shi Y: Histone methylation: A dynamic mark in health, disease and inheritance. Nat Rev Genet. 13:343–357. 2012. View Article : Google Scholar : PubMed/NCBI
11	Strahl BD and Allis CD: The language of covalent histone modifications. Nature. 403:41–45. 2000. View Article : Google Scholar : PubMed/NCBI
12	Bannister AJ and Kouzarides T: Reversing histone methylation. Nature. 436:1103–1106. 2005. View Article : Google Scholar : PubMed/NCBI
13	Black JC, Van Rechem C and Whetstine JR: Histone lysine methylation dynamics: Establishment, regulation, and biological impact. Mol Cell. 48:491–507. 2012. View Article : Google Scholar : PubMed/NCBI
14	Bedford MT and Richard S: Arginine methylation an emerging regulator of protein function. Mol Cell. 18:263–272. 2005. View Article : Google Scholar : PubMed/NCBI
15	Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al: Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 448:553–560. 2007. View Article : Google Scholar : PubMed/NCBI
16	Vakoc CR, Mandat SA, Olenchock BA and Blobel GA: Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell. 19:381–391. 2005. View Article : Google Scholar : PubMed/NCBI
17	Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP and Workman JL: Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell. 123:581–592. 2005. View Article : Google Scholar : PubMed/NCBI
18	Cloos PA, Christensen J, Agger K, Maiolica A, Rappsilber J, Antal T, Hansen KH and Helin K: The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature. 442:307–311. 2006. View Article : Google Scholar : PubMed/NCBI
19	Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J and Zhang Y: The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature. 442:312–316. 2006. View Article : Google Scholar : PubMed/NCBI
20	Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA and Casero RA: Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 119:941–953. 2004. View Article : Google Scholar : PubMed/NCBI
21	Xiang S, Callaghan MM, Watson KG and Tong L: A different mechanism for the inhibition of the carboxyltransferase domain of acetyl-coenzyme A carboxylase by tepraloxydim. Proc Natl Acad Sci USA. 106:20723–20727. 2009. View Article : Google Scholar : PubMed/NCBI
22	Li Y, Reddy MA, Miao F, Shanmugam N, Yee JK, Hawkins D, Ren B and Natarajan R: Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem. 283:26771–26781. 2008. View Article : Google Scholar : PubMed/NCBI
23	Levy D, Kuo AJ, Chang Y, Schaefer U, Kitson C, Cheung P, Espejo A, Zee BM, Liu CL, Tangsombatvisit S, et al: Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling. Nat Immunol. 12:29–36. 2011. View Article : Google Scholar : PubMed/NCBI
24	El Gazzar M, Yoza BK, Chen X, Hu J, Hawkins GA and McCall CE: G9a and HP1 couple histone and DNA methylation to TNFalpha transcription silencing during endotoxin tolerance. J Biol Chem. 283:32198–32208. 2008. View Article : Google Scholar : PubMed/NCBI
25	Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL and Ramsay G: SCCM/ESICM/ACCP/ATS/SIS: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 2003. 31:1250–1256. 2003. View Article : Google Scholar
26	Knaus WA, Draper EA, Wagner DP and Zimmerman JE: APACHE II: A severity of disease classification system. Crit Care Med. 13:818–829. 1985. View Article : Google Scholar : PubMed/NCBI
27	Dominguez TE and Portnoy JD: Scoring for multiple organ dysfunction: Multiple organ dysfunction score, logistic organ dysfunction, or sequential organ failure assessment. Crit Care Med. 30:1913–1914. 2002. View Article : Google Scholar : PubMed/NCBI
28	Duncan EM, Muratore-Schroeder TL, Cook RG, Garcia BA, Shabanowitz J, Hunt DF and Allis CD: Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell. 135:284–294. 2008. View Article : Google Scholar : PubMed/NCBI
29	Adams-Cioaba MA, Krupa JC, Xu C, Mort JS and Min J: Structural basis for the recognition and cleavage of histone H3 by cathepsin L. Nat Commun. 2:1972011. View Article : Google Scholar : PubMed/NCBI
30	El Gazzar M, Yoza BK, Hu JY, Cousart SL and McCall CE: Epigenetic silencing of tumor necrosis factor alpha during endotoxin tolerance. J Biol Chem. 282:26857–26864. 2007. View Article : Google Scholar : PubMed/NCBI
31	El Gazzar M, Yoza BK, Chen X, Garcia BA, Young NL and McCall CE: Chromatin-specific remodeling by HMGB1 and linker histone H1 silences proinflammatory genes during endotoxin tolerance. Mol Cell Biol. 29:1959–1971. 2009. View Article : Google Scholar : PubMed/NCBI