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Tumor-Associated Inhibition in Vitro Pathway and Resistance of Dendritic Cells to B Canonical Κ Promotes Activation of NF

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Tumor-Associated Inhibition in Vitro Pathway and Resistance of Dendritic Cells to B Canonical Κ Promotes Activation of NF Chromosome 1 Open Reading Frame 190 Promotes Activation of NF- κB Canonical Pathway and Resistance of Dendritic Cells to Tumor-Associated Inhibition In Vitro This information is current as of September 25, 2021. Zhizi Jing, Xin Yuan, Jing Zhang, Xin Huang, Zhiqian Zhang, Jingyi Liu, Miaomiao Zhang, Jiangbo Oyang, Yuan Zhang, Zhujun Zhang and Rongcun Yang J Immunol 2010; 185:6719-6727; Prepublished online 3 November 2010; Downloaded from doi: 10.4049/jimmunol.0903869 http://www.jimmunol.org/content/185/11/6719 http://www.jimmunol.org/ Supplementary http://www.jimmunol.org/content/suppl/2010/11/03/jimmunol.090386 Material 9.DC1 References This article cites 41 articles, 17 of which you can access for free at: http://www.jimmunol.org/content/185/11/6719.full#ref-list-1 Why The JI? Submit online. by guest on September 25, 2021 • 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 *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 All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Chromosome 1 Open Reading Frame 190 Promotes Activation of NF-kB Canonical Pathway and Resistance of Dendritic Cells to Tumor-Associated Inhibition In Vitro Zhizi Jing, Xin Yuan, Jing Zhang, Xin Huang, Zhiqian Zhang, Jingyi Liu, Miaomiao Zhang, Jiangbo Oyang, Yuan Zhang, Zhujun Zhang, and Rongcun Yang Tumor-associated dendritic cells (DCs) often induce T cell anergy or deletion and regulatory T cells instead of antitumor immunity. Although many tumor-associated Ags have been found, there is still no effective vaccine for cancer. Thus, novel rational strategies to enhance the immunogenicity of cancer-specific Ags are needed. Chromosome 1 open reading frame 190 (c1orf190), a gene that encodes a 239-aa hypothetical protein and contains multiple kinase phosphorylation sites, has a wide relationship with multiple signaling pathway molecules and can be regulated by multiple factors, such as TLR ligands. In this study, we demonstrate that Downloaded from c1orf190 can activate NF-kB, drive the production of cytokines, and promote the Ag-presenting function and the priming ability of DCs. Furthermore, c1orf190 can promote resistance of DCs to tumor-associated inhibition not only in the Ag-presenting function but also in the priming ability to induce Ag-specific T lymphocytes. Thus, c1orf190, an NF-kB activator, may be a candidate gene for regulating the function of DCs to resist tumor-associated factor-mediated dysfunction. We also found that c1orf190-mediated cytokine release is achieved by activating the canonical but not the noncanonical NF-kB pathway. The Journal of Immunology, 2010, 185: 6719–6727. http://www.jimmunol.org/ endritic cells (DCs) are key regulators of innate and vitro and in vivo (2–5). DC development and survival also requires adaptive immunity by selectively promoting or sup- distinct NF-kB subunits. For example, DC development is inhib- D pressing T cell responses (1). In addition to orchestrating ited in RelB-deficient mice (6) and in bone marrow cells infected essential aspects of the adaptive immune response, DCs produce with adenoviruses harboring an IkB repressor (7). proinflammatory cytokines, such as IL-1b, IL-6, and IL-12 to NF-kB, composed of NF-kB1 (p50), NF-kB2 (p52), RelA, regulate the functions of innate immune cells. DCs can be induced RelB, and c-Rel, plays a central role in regulating diverse biolog- from monocytes under certain conditions, including in the pres- ical processes (8–10), especially in inducing immune and inflam- ence of GM-CSF and various TLR ligands. Central to the im- matory responses and in regulating the expression of immune by guest on September 25, 2021 munologic function of DCs is that their maturation is induced by response genes associated with innate and adaptive immunity (11). TNF family members and TLR ligands. Activation of the canon- NF-kB can be activated in response to TNF-a, IL-1, TLR li- ical and the noncanonical NF-kB pathways is a common signaling gands, and various growth factors. Various external stimuli lead to response to these stimuli. A number of observations have dem- the phosphorylation of IkB by IKKs, which results in its ubiq- onstrated that the transcription factor NF-kB is essential for op- uitination and proteolytic degradation at the proteasome. NF-kBis timal DC maturation. Inhibition of NF-kB or its upstream acti- then released from IkB, translocates into the nucleus, binds to its vator IkB kinase (IKK)2 may block DC Ag presentation both in cognate DNA elements, and induces the transcription of various cytokines, receptors, and other proinflammatory genes (12, 13). NF-kB/IkB may directly respond to many independent signaling Department of Immunology, Nankai University School of Medicine and Key Labo- ratory of Bioactive Materials, Nankai University, Ministry of Education, People’s molecules, as reviewed by Verma and Stevenson (14). The mech- Republic of China anisms by which extracellular signals are transmitted to NF-kB Received for publication December 10, 2009. Accepted for publication September are still unclear despite intensive investigative efforts. Finding 22, 2010. a novel functional molecule that activates NF-kB transcription This work was supported in part by National Natural Science Foundation of China factor will cause an important consequence not only in under- Grants 30771967 and 30872315, the Ministry of Science and Technology (China) (863 Program, 2008AA02Z129), the National Key Basic Research and Development standing the NF-kB–activating pathways, but also in developing Program of China (973 Program, 2007CB914803), and by the National Key Scientific new adjuvants that enhance vaccine immunogenicity. Program of China (2011CB964902). Many kinases, such as protein kinase A, protein kinase C (PKC), Address correspondence and reprint requests to Dr. Rongcun Yang, Department of casein kinase II (CKII), glycogen synthase kinase-3b, T2K (TBK, Immunology, Nankai University School of Medicine, Nankai University, Tianjin 300071, People’s Republic of China. E-mail address: [email protected] NAK), and PI3K, have been shown to induce the phosphorylation The online version of this article contains supplemental material. of NF-kB directly or indirectly (8–10, 15, 16), which may be necessary for the transcriptional competence of NF-kB dimers by Abbreviations used in this paper: c1orf190, chromosome 1 open reading frame 190; CKII, casein kinase II; CRE, cAMP response element; DC, dendritic cell; FIV, feline facilitating their DNA binding, transcriptional coactivator recruit- immunodeficiency virus; GRE, glucocorticoid response element; HSE, heat shock ment, and acetylation. Chromosome 1 open reading frame 190 response element; IKK, IkB kinase; NBD, NF-kB essential modulator-binding do- main; NEMO, NF-kB essential modulator; NIK, NF-kB–induding kinase; PKC, pro- (c1orf190), a hypothetical protein, contains multiple CKII, PKC, tein kinase C; RLU, relative light unit; SEAP, secreted alkaline phosphatase; siIKKa, and cAMP- and cGMP-dependent protein kinase phosphorylation small interfering RNA for IkB kinase-a; siNIK, small interfering RNA for NF-kB– sites. In this study, we demonstrate that c1orf190 participates in inducing kinase; siRNA, small interfering RNA; SRE, serum response element. the activation of NF-kB, the induction of proinflammatory cyto- Copyright Ó 2010 by The American Association of Immunologists, Inc. 0022-1767/10/$16.00 kines, and in the Ag-presenting and priming function of DCs. www.jimmunol.org/cgi/doi/10.4049/jimmunol.0903869 6720 C1orf190 PROMOTES ACTIVATION OF NF-kB C1orf190 may be a candidate gene for regulating the function negative control p-TATA-like-SEAP reporter constructs were purchased of DCs. from BD Clontech (Palo Alto, CA) and used to cotransfect the cells with the plasmids. As described before (19), 293T cells were seeded in 96-well plates and cotransfected with c1orf190 construct combined with reporter Materials and Methods plasmids as indicated. Twenty-four hours after transfection with Lip- Preparation of monocyte-derived DCs ofectamine 2000, according to the manufacturer’s instructions, cells were treated with the indicated reagents or left untreated for 12 h. The samples Monocyte-derived DCs were prepared from monocytes according to our were harvested and processed as described above for determination of previously described protocol (17, 18). Briefly, after Ficoll-Hypaque sep- SEAP activity and normalized for the b-galactosidase activity (BD aration, peripheral blood cells were resuspended in RPMI 1640 medium Clontech). The amount of transfected DNA was equalized with empty supplemented with 10% FBS, 2 mM L-glutamine, and 1% penicillin- expression vectors, which were also used in the control, along with either streptomycin. The cells were incubated overnight at 37˚C, and the non- NF-kB or other SEAP reporter constructs. adherent cells were removed by gentle pipetting. The adherent cells were cultured in RPMI 1640 and supplemented with 10% FBS containing 1000 Small interfering RNA experiments U/ml GM-CSF (R&D Systems, Minneapolis, MN) and 1000 U/ml IL-4 (R&D Systems). After 6 d, floating DCs were harvested in PBS To knock down c1orf190, the small interfering RNA (siRNA) templates and cell morphology was determined by standard microscopic techniques. used to knock down the c1orf190 were selected and designed using the Phenotypes of DCs were analyzed by PE- or FITC-labeled anti-CD11c siRNA target finder (http://www.ambion.com/techlib/misc/siRNA_finder. (3.9), anti-human MHC class II-DR (L243), anti-human CD86 (IT2.2), html) (Supplemental Table II).
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