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Bacterial DNA and Lipopolysaccharide Induce Synergistic Production of TNF- Α Through a Post-Transcriptional Mechanism

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Bacterial DNA and Lipopolysaccharide Induce Synergistic Production of TNF- Α Through a Post-Transcriptional Mechanism Bacterial DNA and Lipopolysaccharide Induce Synergistic Production of TNF- α Through a Post-Transcriptional Mechanism This information is current as Jian Jun Gao, Qiao Xue, Christopher J. Papasian and David of September 23, 2021. C. Morrison J Immunol 2001; 166:6855-6860; ; doi: 10.4049/jimmunol.166.11.6855 http://www.jimmunol.org/content/166/11/6855 Downloaded from References This article cites 39 articles, 19 of which you can access for free at: http://www.jimmunol.org/content/166/11/6855.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 23, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2001 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Bacterial DNA and Lipopolysaccharide Induce Synergistic Production of TNF-␣ Through a Post-Transcriptional Mechanism1 Jian Jun Gao,* Qiao Xue,* Christopher J. Papasian,* and David C. Morrison2*† LPS is well recognized for its potent capacity to activate mouse macrophages to produce TNF-␣, an important inflammatory mediator in bacterial infection-related diseases such as septic shock. We demonstrate here that while inducing only low levels of TNF-␣ alone, DNA from both Gram-negative and Gram-positive bacteria synergizes with subthreshold concentrations of LPS (0.3 ng/ml) to induce TNF-␣ in the RAW 264.7 macrophage-like cell line. The bacterial DNA effects are mimicked by synthetic CpG-containing oligodeoxynucleotides, but not non-CpG-containing oligodeoxynucleotides. Pretreatment of macrophages with either DNA for 2–8 h inhibits macrophage TNF-␣ production in responses to DNA/LPS. However, when pretreatment was Downloaded from extended to 24 h, DNA/LPS synergy on TNF-␣ is further enhanced. RT-PCR analysis indicates that mRNA levels of the TNF-␣ gene, however, are not synergistically induced by bacterial DNA and LPS. Analyses of the half-life of TNF-␣ mRNA indicate that TNF-␣ message has a longer half-life in bacterial DNA- and LPS-treated macrophages than that in bacterial DNA- or LPS-treated macrophages. These findings indicate that the temporally controlled, synergistic induction of TNF-␣ by bacterial DNA and LPS is not mediated at the transcriptional level. Instead, this synergy may occur via a post-transcriptional mechanism. The Journal of Immunology, 2001, 166: 6855–6860. http://www.jimmunol.org/ ecent data indicate that purified bacterial DNA can acti- inducer of mouse macrophage activation, resulting in production vate macrophages and other inflammatory cells (reviewed of many inflammatory mediators, including TNF-␣, that play a key R in Refs. 1 and 2). Macrophages stimulated with bacterial role in the development of septic shock (reviewed in Refs. 18 and DNA reportedly produce proinflammatory cytokines such as 19). The induction of TNF-␣ secretion from mouse macrophages TNF-␣ (3, 4), IL- 1 (4), IL-6 (5), IL-12 (6–8), IFN-␣␤ (9, 10), in response to LPS stimulation is controlled at transcriptional, IFN-␥ (9), and the reactive nitrogen intermediate, NO (11, 12). post-transcriptional, and translational levels (17, 20, 21). Subtle structural differences between bacterial and eukaryotic DNA In this communication we explore the mechanisms by which apparently account for the ability of bacterial DNA to serve as an LPS and bacterial DNA act synergistically to activate macro- by guest on September 23, 2021 immune-activating agent. Specifically, bacterial DNA is thought to phages. We present in vitro data demonstrating that bacterial DNA activate inflammatory cells because of its high content of short se- acts synergistically with substimulatory concentrations of LPS to quences with unmethylated CpG dinucleotides (13). In mammalian enhance TNF-␣ secretion by the murine RAW 264.7 macrophage- DNA, CpG-containing sequences occur at a much lower frequency like cell line. The observed synergy depends upon the presence of than in bacterial DNA, and the cytosine present in CpG dinucleoti- unmethylated CpG residues in DNA and is also dependent upon des of mammalian DNA is usually methylated (14, 15). the temporal order of treatment by LPS and bacterial DNA. En- In vivo studies support the concept that bacterial DNA is an hanced TNF-␣ secretion by RAW 264.7 cells simultaneously ex- important proinflammatory stimulus, as bacterial DNA has been posed to bacterial DNA and LPS is not accompanied by enhanced shown to trigger septic shock in D-galactosamine treated mice. transcription of the TNF-␣ gene. Analyses of the half-life of (16). Also of interest is the finding that bacterial DNA acts syn- TNF-␣ in differentially treated macrophages suggest that bacterial ergistically with LPS to induce TNF-␣ production in vivo, result- DNA and LPS act synergistically to enhance TNF-␣ production ing in lethal shock in mice (11, 17). The molecular mechanism(s) through a post-transcriptional event. by which bacterial DNA acts synergistically with LPS to induce TNF-␣ production remains to be determined. LPS, a constituent of the Gram-negative bacterial cell wall, is well known as a potent Materials and Methods Materials *Department of Basic Medical Sciences, University of Missouri, and †Saint Luke’s Hospital, Kansas City, MO 64111 Purified LPS from Escherichia coli O111: B4 was obtained from List Bi- ological Laboratories (Campbell, CA). E. coli strain B genomic DNA, Received for publication February 2, 2001. Accepted for publication March 21, 2001. salmon sperm genomic DNA, and RNase-free DNase I were purchased The costs of publication of this article were defrayed in part by the payment of page from Sigma (St. Louis, MO). Synthetic oligodeoxynucleotides (ODNs;3 charges. This article must therefore be hereby marked advertisement in accordance T3, 5Ј-AACGTT AACGTT AACGTT-3Ј; C3, 5Ј-CCATGGCCATGGC with 18 U.S.C. Section 1734 solely to indicate this fact. CATGG-3Ј) were obtained from Sigma-Genosys (The Woodlands, TX). 1 This work was supported by National Institutes of Health Grants AI23447, AI44936, The endotoxin levels in these ODNs are Ͻ0.01 ng/␮g of DNA based upon and AI46493, and an unrestricted Medical Research Grant from Merck & Co. (West the Limulus amebocyte lysate assay. Point, PA). D.C.M. is supported in part by a Westport Anesthesia Service/State of Missouri Endowed Chair in Research. 2 Address correspondence and reprint requests to Dr. David C. Morrison, Office of Research Administration, Room 3112, Main Hospital, Saint Luke’s Hospital of Kan- sas City, 4401 Wornall Road, Kansas City, MO 64111. E-mail address: 3 Abbreviations used in this paper: ODN, oligodeoxynucleotide; UTR, untranslated [email protected] region. Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 6856 REGULATION OF TNF-␣ GENE BY CpG DNA AND LPS Culture of macrophages To determine whether the ability of E. coli DNA to act syner- The murine macrophage-like cell line RAW 264.7 (American Type Culture gistically with LPS was applicable to other bacterial species, we Collection, Manassas, VA) was used in all the studies described here. Mac- repeated the above experiments with DNA purified from the rophages were cultured in RPMI 1640 medium (Life Technologies, Grand Gram-positive bacteria, S. aureus. S. aureus DNA alone induced Island, NY) supplemented with 100 U/ml of penicillin, 100 ␮g/ml of strep- RAW cells to produce only low levels (Ͻ2000 pg/ml) of TNF-␣ Ͻ tomycin, and 10% heat-inactivated FBS (endotoxin content of 0.06 ng/ (Fig. 1B, Œ). However, in the presence of a subthreshold LPS ml; Sigma) at 37°C in a humidified, 5% CO2 environment. Before being stimulated, macrophages were seeded into culture plates and cultured stimulus (0.3 ng/ml), S. aureus DNA induced a greatly enhanced overnight. DNA manipulation E. coli DNA and salmon sperm DNA (Sigma) were further purified by two-step CsCl ultracentrifugation. DNA from Staphylococcus aureus was extracted exactly as described by Dyer and Iandolo (22). DNA digestion was performed using RNase-free DNase I (2 U/␮g of DNA) in buffer (pH 7.6) containing 20 mM Tris-HCl and 20 mM MgCl2 at 37°C for 3 h. The endotoxin levels in these DNA preparations were Ͻ0.001 ng/␮gofDNA according to the Limulus amebocyte lysate assay. TNF-␣ analysis After 20 h of stimulation, TNF-␣ production in macrophage culture super- Downloaded from natants was analyzed using the ELISA Duoset kit (purchased from R&D Systems, Minneapolis, MN). The protocol from the manufacturer was fol- lowed exactly for the assay. All data for TNF-␣ represent the average of duplicate samples Ϯ SEM. Each experiment was repeated at least twice. RNA isolation and RT-PCR analysis RAW 264.7 macrophages were stimulated for various periods of time with http://www.jimmunol.org/ different combinations of stimuli as described in Results. Total RNA from macrophages was isolated using TRIzol reagent (Life Technologies) ac- cording to the manufacturer’s instructions. A total of 1 ␮g of RNA from each sample was used for RT-PCR using the One-Step RT-PCR kit from Qiagen (Valencia, CA) according to the manufacturer’s protocols. The se- quences of the specific primers used in these studies are: mouse TNF-␣ sense, 5Ј-GGC AGG TCT ACT TTG GAG TCA TTG C-3Ј; mouse TNF-␣ antisense, 5Ј-ACA TTC GAG GCT CCA GTG AAT TCG G-3Ј; mouse ␤-actin sense, 5Ј-TGT GAT GGT GGG AAT GGG TCA G-3Ј; and mouse ␤-actin antisense, 5Ј-TTT GAT GTC ACG CAC GAT TTC C-3Ј.
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