How are MCPIP1 and cytokines mutually regulated in cancer-related immunity?

doi:10.1007/s13238-020-00739-1

Protein Cell

2020, Vol. 11

Issue (12) : 881-893 https://doi.org/10.1007/s13238-020-00739-1

REVIEW

How are MCPIP1 and cytokines mutually regulated in cancer-related immunity?

Ruyi Xu^1,², Yi Li^1,², Yang Liu^1,², Jianwei Qu^1,², Wen Cao^1,², Enfan Zhang^1,², Jingsong He^1,²(

), Zhen Cai^1,²(

)

¹. Bone Marrow Transplantation Center, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310006, China
². Institution of Hematology, Zhejiang University, Hangzhou 310006, China

Download: PDF(1778 KB)
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

Cytokines are secreted by various cell types and act as critical mediators in many physiological processes, including immune response and tumor progression. Cytokines production is precisely and timely regulated by multiple mechanisms at different levels, ranging from transcriptional to post-transcriptional and posttranslational processes. Monocyte chemoattractant protein-1 induced protein 1 (MCPIP1), a potent immunosuppressive protein, was first described as a transcription factor in monocytes treated with monocyte chemoattractant protein-1 (MCP-1) and subsequently found to possess intrinsic RNase and deubiquitinase activities. MCPIP1 tightly regulates cytokines expression via various functions. Furthermore, cytokines such as interleukin 1 beta (IL-1B) and MCP-1 and inflammatory cytokines inducer lipopolysaccharide (LPS) strongly induce MCPIP1 expression. Mutually regulated MCPIP1 and cytokines form a complicated network in the tumor environment. In this review, we summarize how MCPIP1 and cytokines reciprocally interact and elucidate the effect of the network formed by these components in cancer-related immunity with aim of exploring potential clinical benefits of their mutual regulation.

Keywords MCPIP1 cytokines cancer-related immunity RNase deubiquitinase

Corresponding Author(s): Jingsong He,Zhen Cai

Online First Date: 14 September 2020 Issue Date: 22 December 2020

Cite this article:

Ruyi Xu,Yi Li,Yang Liu, et al. How are MCPIP1 and cytokines mutually regulated in cancer-related immunity?[J]. Protein Cell, 2020, 11(12): 881-893.

URL:

https://academic.hep.com.cn/pac/EN/10.1007/s13238-020-00739-1
https://academic.hep.com.cn/pac/EN/Y2020/V11/I12/881

1	AM Algra, PM Rothwell (2012) Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. Lancet Oncol 13(5):518–527 https://doi.org/10.1016/S1470-2045(12)70112-2
2	E Boratyn, I Nowak, I Horwacik, M Durbas, A Mistarz, M Kukla, P Kaczówka, M Łastowska, J Jura, H Rokita (2016) Monocyte chemoattractant protein-induced protein 1 overexpression modulates transcriptome, including microRNA, in human neuroblastoma cells. J Cell Biochem 117(3):694–707 https://doi.org/10.1002/jcb.25354
3	I Brana, A Calles, PM LoRusso, LK Yee, TA Puchalski, S Seetharam, B Zhong, CJ de Boer, J Tabernero, E Calvo (2015) Carlumab, an anti-CC chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: an open-label, multicenter phase 1b study. Target Oncol 10(1):111–123 https://doi.org/10.1007/s11523-014-0320-2
4	V Chitu, ER Stanley (2006) Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 18(1):39–48 https://doi.org/10.1016/j.coi.2005.11.006
5	SB Coffelt, KE De Visser (2014) Cancer: inflammation lights the way to metastasis. Nature 507(7490):48–49 https://doi.org/10.1038/nature13062
6	F Colotta, P Allavena, A Sica, C Garlanda, A Mantovani (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30(7):1073–1081 https://doi.org/10.1093/carcin/bgp127
7	S Costinean, SK Sandhu, IM Pedersen, E Tili, R Trotta, D Perrotti, D Ciarlariello, P Neviani, J Harb, LR Kauffmanet al. (2009) Src homology 2 domain–containing inositol-5-phosphatase and CCAAT enhancer-binding protein β are targeted by miR-155 in B cells of Eμ-MiR-155 transgenic mice. Blood JAmSoc Hematol 114(7):1374–1382 https://doi.org/10.1182/blood-2009-05-220814
8	LM Coussens, L Zitvogel, AK Palucka (2013) Neutralizing tumorpromoting chronic inflammation: a magic bullet? Science 339 (6117):286–291 https://doi.org/10.1126/science.1232227
9	L Deng, C Wang, E Spencer, L Yang, A Braun, J You, C Slaughter, C Pickart, ZJ Chen (2000) Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103(2):351–361 https://doi.org/10.1016/S0092-8674(00)00126-4
10	S Dhamija, R Winzen, A Doerrie, G Behrens, N Kuehne, C Schauerte, E Neumann, O Dittrich-Breiholz, M Kracht, H Holtmann (2013) Interleukin-17 (IL-17) and IL-1 activate translation of overlapping sets of mRNAs, including that of the negative regulator of inflammation, MCPIP1[J]. J Biol Chem 288(26):19250–19259 https://doi.org/10.1074/jbc.M113.452649
11	CI Diakos, KA Charles, DC McMillan, SJ Clarke (2014) Cancerrelated inflammation and treatment effectiveness. Lancet Oncol 15(11):e493–e503 https://doi.org/10.1016/S1470-2045(14)70263-3
12	E Dobosz, M Wilamowski, M Lech, B Bugara, J Jura, J Potempa, J Koziel (2016) MCPIP-1, alias regnase-1, controls epithelial inflammation by posttranscriptional regulation of IL-8 production [J]. J Innate Immun 8(6):564–578 https://doi.org/10.1159/000448038
13	M Dysthe, R Parihar (2020) Myeloid-derived suppressor cells in the tumor microenvironment. In: Tumor microenvironment 2020. Springer, Cham, pp 117–140 https://doi.org/10.1007/978-3-030-35723-8_8
14	E Elinav, R Nowarski, CA Thaiss, B Hu, C Jin, RA Flavell (2013) Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer 13(11):759 https://doi.org/10.1038/nrc3611
15	ME Fiori, S Di Franco, L Villanova, P Bianca, G Stassi, R De Maria (2019) Cancer-associated fibroblasts as abettors of tumor progression at the crossroads of EMT and therapy resistance. Mol Cancer 18(1):70 https://doi.org/10.1186/s12943-019-0994-2
16	J Folkman (2002) Role of angiogenesis in tumor growth and metastasis. In: Seminars in oncology. WB Saunders, vol 29(6), pp 15–18 https://doi.org/10.1053/sonc.2002.37263
17	M Fu, PJ Blackshear (2017) RNA-binding proteins in immune regulation: a focus on CCCH zinc finger proteins. Nat Rev Immunol 17(2):130 https://doi.org/10.1038/nri.2016.129
18	MR Galdiero, G Marone, A Mantovani (2018) Cancer inflammation and cytokines. Cold Spring Harb Perspect Biol 10(8):a028662 https://doi.org/10.1101/cshperspect.a028662
19	L Garderet, F Kuhnowski, B Berge, M Roussel, M Escoffre-Barbe, I Lafon, T Facon, X Leleu, L Karlin, A Perrotet al. (2018) Pomalidomide, cyclophosphamide, and dexamethasone for relapsed multiple myeloma. Blood 132(24):2555–2563 https://doi.org/10.1182/blood-2018-07-863829
20	AV Garg, N Amatya, K Chen, JA Cruz, P Grover, N Whibley, HR Conti, GH Mir, T Sirakova, EC Childset al. (2015) MCPIP1 endoribonuclease activity negatively regulates interleukin-17-mediated signaling and inflammation. Immunity 43(3):475–487 https://doi.org/10.1016/j.immuni.2015.07.021
21	GL Gierach, JV Lacey, A Schatzkin, MF Leitzmann, D Richesson, AR Hollenbeck, LA Brinton (2008) Nonsteroidal anti-inflammatory drugs and breast cancer risk in the National Institutes of Health–AARP Diet and Health Study. Breast Cancer Res 10(2):R38 https://doi.org/10.1186/bcr2089
22	S Gordon, FO Martinez (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32(5):593–604 https://doi.org/10.1016/j.immuni.2010.05.007
23	J Houghton, C Stoicov, S Nomura, AB Rogers, J Carlson, H Li, X Cai, JG Fox, JR Goldenring, TC Wang (2004) Gastric cancer originating from bone marrow-derived cells. Science 306 (5701):1568–1571 https://doi.org/10.1126/science.1099513
24	S Huang, R Miao, Z Zhou, T Wang, J Liu, G Liu, YE Chen, HB Xin, J Zhang, M Fu (2013) MCPIP1 negatively regulates toll-like receptor 4 signaling and protects mice from LPS-induced septic shock. Cell Signal 25(5):1228–1234 https://doi.org/10.1016/j.cellsig.2013.02.009
25	S Huang, S Liu, JJ Fu, TT Wang, X Yao, A Kumar, G Liu, M Fu (2015) Monocyte chemotactic protein-induced protein 1 and 4 form a complex but act independently in regulation of interleukin-6 mRNA degradation. J Biol Chem 290(34):20782–20792 https://doi.org/10.1074/jbc.M114.635870
26	H Iwasaki, O Takeuchi, S Teraguchi, K Matsushita, T Uehata, K Kuniyoshi, T Satoh, T Saitoh, M Matsushita, DM Standleyet al. (2011) The IκB kinase complex regulates the stability of cytokineencoding mRNA induced by TLR–IL-1R by controlling degradation of regnase-1. Nat Immunol 12(12):1167 https://doi.org/10.1038/ni.2137
27	KM Jeltsch, D Hu, S Brenner, J Zöller, GA Heinz, D Nagel, KU Vogel, N Rehage, SC Warth, SL Edelmannet al. (2014) Cleavage of roquin and regnase-1 by the paracaspase MALT1 releases their cooperatively repressed targets to promote T H 17 differentiation. Nat Immunol 15(11):1079 https://doi.org/10.1038/ni.3008
28	H Jiang, X Lv, X Lei, Y Yang, X Yang, J Jiao (2016) Immune regulator MCPIP1 modulates TET expression during early neocortical development. Stem cell Rep 7(3):439–453 https://doi.org/10.1016/j.stemcr.2016.07.011
29	N Kapoor, J Niu, Y Saad, S Kumar, T Sirakova, E Becerra, X Li, PE Kolattukudy (2015) Transcription factors STAT6 and KLF4 implement macrophage polarization via the dual catalytic powers of MCPIP. J Immunol 194(12):6011–6023 https://doi.org/10.4049/jimmunol.1402797
30	M Karin, FR Greten (2005) NF-κB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5(10):749–759 https://doi.org/10.1038/nri1703
31	A Kasza, P Wyrzykowska, I Horwacik, P Tymoszuk, D Mizgalska, K Palmer, H Rokita, AD Sharrocks, J Jura (2010) Transcription factors Elk-1 and SRF are engaged in IL1-dependent regulation of ZC3H12A expression. BMC Mol Biol 11(1):14 https://doi.org/10.1186/1471-2199-11-14
32	M Leggas, KL Kuo, F Robert, G Cloud, M Deshazo, R Zhang, M Li, H Wang, S Davidson, J Rinehart (2009) Intensive anti-inflammatory therapy with dexamethasone in patients with non-small cell lung cancer: effect on chemotherapy toxicity and efficacy. Cancer Chemother Pharmacol 63(4):731–743 https://doi.org/10.1007/s00280-008-0767-x
33	M Li, W Cao, H Liu, W Zhang, X Liu, Z Cai, J Guo, X Wang, Z Hui, H Zhanget al. (2012) MCPIP1 down-regulates IL-2 expression through an ARE-independent pathway[J]. PLoS One 7(11): e49841 https://doi.org/10.1371/journal.pone.0049841
34	J Liang, J Wang, A Azfer, W Song, G Tromp, PE Kolattukudy, M Fu (2008) A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem 283(10):6337–6346 https://doi.org/10.1074/jbc.M707861200
35	J Liang, Y Saad, T Lei, J Wang, D Qi, Q Yang, PE Kolattukudy, M Fu (2010) MCP-induced protein 1 deubiquitinates TRAF proteins and negatively regulates JNK and NF-κB signaling. J Exp Med 207(13):2959–2973 https://doi.org/10.1084/jem.20092641
36	W Lu, H Ning, L Gu, H Peng, Q Wang, R Hou, M Fu, DF Hoft, J Liu (2016) MCPIP1 selectively destabilizes transcripts associated with an antiapoptotic gene expression program in breast cancer cells that can elicit complete tumor regression. Cancer Res 76(6):1429–1440 https://doi.org/10.1158/0008-5472.CAN-15-1115
37	S Maman, IP Witz (2018) A history of exploring cancer in context. Nat Rev Drug Discov 17(3):13–30 https://doi.org/10.1038/s41568-018-0006-7
38	A Mantovani, P Allavena, A Sica, F Balkwill (2008) Cancer-related inflammation. Nature 454(7203):436–444 https://doi.org/10.1038/nature07205
39	E Marcuzzi, R Angioni, B Molon, B Calì (2019) Chemokines and chemokine receptors: orchestrating tumor metastasization. Int J Mol Sci 20(1):96 https://doi.org/10.3390/ijms20010096
40	P Marona, J Górka, Z Mazurek, W Wilk, J Rys, M Majka, J Jura, K Miekus (2017) MCPIP1 downregulation in clear cell renal cell carcinoma promotes vascularization and metastatic progression. Cancer Res 77(18):4905–4920 https://doi.org/10.1158/0008-5472.CAN-16-3190
41	K Matsushita, O Takeuchi, DM Standley, Y Kumagai, T Kawagoe, T Miyake, T Satoh, H Kato, T Tsujimura, H Nakamuraet al. (2009) Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature 458(7242):1185–1190 https://doi.org/10.1038/nature07924
42	R Miao, S Huang, Z Zhou, T Quinn, B Van Treeck, T Nayyar, D Dim, Z Jiang, CJ Papasian, Y Eugene Chenet al. (2013) Targeted disruption of MCPIP1/Zc3h12a results in fatal inflammatory disease. Immunol Cell Biol 91(5):368–376 https://doi.org/10.1038/icb.2013.11
43	T Mino, Y Murakawa, A Fukao, A Vandenbon, HH Wessels, D Ori, T Uehata, S Tartey, S Akira, Y Suzukiet al. (2015) Regnase-1 and roquin regulate a common element in inflammatory mRNAs by spatiotemporally distinct mechanisms. Cell 161(5):1058–1073 https://doi.org/10.1016/j.cell.2015.04.029
44	D Mizgalska, P Węgrzyn, K Murzyn, A Kasza, A Koj, J Jura, B Jarzab, J Jura (2009) Interleukin-1-inducible MCPIP protein has structural and functional properties of RNase and participates in degradation of IL-1β mRNA. FEBS J 276(24):7386–7399 https://doi.org/10.1111/j.1742-4658.2009.07452.x
45	L Monin, JE Gudjonsson, EE Childs, N Amatya, X Xing, AH Verma, BM Coleman, AV Garg, M Killeen, A Matherset al. (2017) MCPIP1/regnase-1 restricts IL-17A–and IL-17C–dependent skin inflammation. J Immunol 198(2):767–775 https://doi.org/10.4049/jimmunol.1601551
46	PJ Murray (2017) Macrophage polarization. Annu Rev Physiol 10 (79):541–566 https://doi.org/10.1146/annurev-physiol-022516-034339
47	PJ Murray, JE Allen, SK Biswas, EA Fisher, DW Gilroy, S Goerdt, S Gordon, JA Hamilton, LB Ivashkiv, T Lawrenceet al. (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41(1):14–20 https://doi.org/10.1016/j.immuni.2014.06.008
48	M Muzio, G Natoli, S Saccani, M Levrero, A Mantovani (1998) The human Toll signaling pathway: divergence of nuclear factor κB and JNK/SAPK activation upstream of tumor necrosis factor receptor–associated factor 6 (TRAF6). J Exp Med 187(12):2097–2101 https://doi.org/10.1084/jem.187.12.2097
49	J Niu, A Azfer, O Zhelyabovska, S Fatma, PE Kolattukudy (2008) Monocyte chemotactic protein (MCP)-1 promotes angiogenesis via a novel transcription factor, MCP-1-induced protein (MCPIP). J Biol Chem 283(21):14542–14551 https://doi.org/10.1074/jbc.M802139200
50	J Niu, Y Shi, J Xue, R Miao, S Huang, T Wang, J Wu, M Fu, ZH Wu (2013) USP10 inhibits genotoxic NF-κB activation by MCPIP1-facilitated deubiquitination of NEMO. The EMBO journal. 32(24):3206–3219 https://doi.org/10.1038/emboj.2013.247
51	G O’Boyle, JG Brain, JA Kirby, S Ali (2007) Chemokine-mediated inflammation: identification of a possible regulatory role for CCR2. Mol Immunol 44(8):1944–1953 https://doi.org/10.1016/j.molimm.2006.09.033
52	YT Oh, G Qian, J Deng, SY Sun (2018) Monocyte chemotactic protein-induced protein-1 enhances DR5 degradation and negatively regulates DR5 activation-induced apoptosis through its deubiquitinase function. Oncogene 37(25):3415–3425 https://doi.org/10.1038/s41388-018-0200-9
53	M Ono (2008) Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 99(8):1501–1506 https://doi.org/10.1111/j.1349-7006.2008.00853.x
54	AT Prach, TA MacDonald, DA Hopwood, DA Johnston (1997) Increasing incidence of Barrett’s oesophagus: education, enthusiasm, or epidemiology? The Lancet 350(9082):933 https://doi.org/10.1016/S0140-6736(05)63269-2
55	Y Qi, J Liang, ZG She, Y Cai, J Wang, T Lei, WB Stallcup, M Fu (2010) MCP-induced protein 1 suppresses TNFα-induced VCAM-1 expression in human endothelial cells[J]. FEBS Lett 584(14):3065–3072 https://doi.org/10.1016/j.febslet.2010.05.040
56	A Rodriguez, E Vigorito, S Clare, MV Warren, P Couttet, DR Soond, S Van Dongen, RJ Grocock, PP Das, EA Miskaet al. (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316(5824):608–611 https://doi.org/10.1126/science.1139253
57	PM Rothwell, M Wilson, JF Price, JF Belch, TW Meade, Z Mehta (2012) Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. The Lancet. 379(9826):1591–1601 https://doi.org/10.1016/S0140-6736(12)60209-8
58	A Roy, M Zhang, Y Saad, PE Kolattukudy (2013) Antidicer RNAse activity of monocyte chemotactic protein-induced protein-1 is critical for inducing angiogenesis. Am J Physiol Cell Physiol 305(10):C1021–C1032 https://doi.org/10.1152/ajpcell.00203.2013
59	S Singhal, J Stadanlick, MJ Annunziata, AS Rao, PS Bhojnagarwala, S O’Brien, EK Moon, E Cantu, G Danet-Desnoyers, HJ Raet al. (2019) Human tumor-associated monocytes/macrophages and their regulation of Tcell responses in early-stage lung cancer. Sci Transl Med 11(479):eaat1500 https://doi.org/10.1126/scitranslmed.aat1500
60	L Skalniak, D Mizgalska, A Zarebski, P Wyrzykowska, A Koj, J Jura (2009) Regulatory feedback loop between NF-κB and MCP-1-induced protein 1 RNase. FEBS J 276(20):5892–5905 https://doi.org/10.1111/j.1742-4658.2009.07273.x
61	L Skalniak, A Koj, J Jura (2013) Proteasome inhibitor MG-132 induces MCPIP 1 expression. FEBS J 280(11):2665–2674 https://doi.org/10.1111/febs.12264
62	SU Sønder, S Saret, W Tang, DE Sturdevant, SF Porcella, U Siebenlist (2011) IL-17-induced NF-κB activation via CIKS/Act1 physiologic significance and signaling mechanisms. J Biol Chem 286(15):12881–12890 https://doi.org/10.1074/jbc.M110.199547
63	O Stoeltzing, F Meric-Bernstam, LM Ellis (2006) Intracellular signaling in tumor and endothelial cells: the expected and yet again, the unexpected. Cancer Cell 10(2):89–91 https://doi.org/10.1016/j.ccr.2006.07.013
64	HI Suzuki, M Arase, H Matsuyama, YL Choi, T Ueno, H Mano, K Sugimoto, K Miyazono (2011) MCPIP1 ribonuclease antagonizes dicer and terminates microRNA biogenesis through precursor microRNA degradation. Mol Cell 44(3):424–436 https://doi.org/10.1016/j.molcel.2011.09.012
65	O Takeuchi (2018) Endonuclease regnase-1/monocyte chemotactic protein-1-induced protein-1 (MCPIP1) in controlling immune responses and beyond. Wiley Interdiscip Rev RNA 9(1):e1449 https://doi.org/10.1002/wrna.1449
66	T Uehata, H Iwasaki, A Vandenbon, K Matsushita, E Hernandez-Cuellar, K Kuniyoshi, T Satoh, T Mino, Y Suzuki, DM Standleyet al. (2013) Malt1-induced cleavage of regnase-1 in CD4+ helper T cells regulates immune activation. Cell 153(5):1036–1049 https://doi.org/10.1016/j.cell.2013.04.034
67	E Voronov, DS Shouval, Y Krelin, E Cagnano, D Benharroch, Y Iwakura, CA Dinarello, RN Apte (2003) IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci 100 (5):2645–2650 https://doi.org/10.1073/pnas.0437939100
68	TA Wynn, A Chawla, JW Pollard (2013) Macrophage biology in development, homeostasis and disease. Nature 496(7446):445–455 https://doi.org/10.1038/nature12034
69	C Xiao, L Srinivasan, DP Calado, HC Patterson, B Zhang, J Wang, JM Henderson, JL Kutok, K Rajewsky (2008) Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9(4):405–414 https://doi.org/10.1038/ni1575
70	J Xu, W Peng, Y Sun, X Wang, Y Xu, X Li, G Gao, Z Rao (2012a) Structural study of MCPIP1 N-terminal conserved domain reveals a PIN-like RNase. Nucleic Acids Res 40(14):6957–6965 https://doi.org/10.1093/nar/gks359
71	J Xu, S Fu, W Peng, Z Rao (2012b) MCP-1-induced protein-1, an immune regulator. Protein Cell 3(12):903–910 https://doi.org/10.1007/s13238-012-2075-9
72	R Xu, Y Li, H Yan, E Zhang, X Huang, Q Chen, J Chen, J Qu, Y Liu, J Heet al. (2019) CCL2 promotes macrophages-associated chemoresistance via MCPIP1 dual catalytic activities in multiple myeloma. Cell Death Dis 10(10):1–7 https://doi.org/10.1038/s41419-019-2012-4
73	H Yao, R Ma, L Yang, G Hu, X Chen, M Duan, Y Kook, F Niu, K Liao, M Fuet al. (2014) MiR-9 promotes microglial activation by targeting MCPIP1. Nat Commun 5(1):1–2 https://doi.org/10.1038/ncomms5386
74	Y Zheng, J Yang, J Qian, P Qiu, S Hanabuchi, Y Lu, Z Wang, Z Liu, H Li, J Heet al. (2013) PSGL-1/selectin and ICAM-1/CD18 interactions are involved in macrophage-induced drug resistance in myeloma. Leukemia 27(3):702–710 https://doi.org/10.1038/leu.2012.272
75	L Zhou, A Azfer, J Niu, S Graham, M Choudhury, FM Adamski, C Younce, PF Binkley, PE Kolattukudy (2006) Monocyte chemoattractant protein-1 induces a novel transcription factor that causes cardiac myocyte apoptosis and ventricular dysfunction. Circ Res 98(9):1177–1185 https://doi.org/10.1161/01.RES.0000220106.64661.71

[1]	Ting Shen, Huan Li, Yifan Song, Jun Yao, Miao Han, Ming Yu, Gang Wei, Ting Ni. Antisense transcription regulates the expression of sense gene via alternative polyadenylation[J]. Protein Cell, 2018, 9(6): 540-552.
[2]	Peipei Liu, Jinliang Huang, Qian Zheng, Leiming Xie, Xinping Lu, Jie Jin, Geng Wang. Mammalian mitochondrial RNAs are degraded in the mitochondrial intermembrane space by RNASET2[J]. Protein Cell, 2017, 8(10): 735-749.
[3]	Xiaojuan Chen,Xingxing Yang,Yang Zheng,Yudong Yang,Yaling Xing,Zhongbin Chen. SARS coronavirus papain-like protease inhibits the type I interferon signaling pathway through interaction with the STING-TRAF3-TBK1 complex[J]. Protein Cell, 2014, 5(5): 369-381.
[4]	Jiwei Xu, Sheng Fu, Wei Peng, Zihe Rao. MCP-1-induced protein-1, an immune regulator[J]. Prot Cell, 2012, 3(12): 903-910.
[5]	Priyanka Sathe, Li Wu. The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets[J]. Prot Cell, 2011, 2(8): 620-630.
[6]	Xiaoping Zhang, Pornpimon Angkasekwinai, Chen Dong, Hong Tang. Structure and function of interleukin-17 family cytokines[J]. Prot Cell, 2011, 2(1): 26-40.

Viewed

Full text

Abstract

Cited

Shared

Discussed