SKAP2 suppresses inflammation-mediated tumorigenesis by regulating SHP-1 and SHP-2.
Journal
Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
19
07
2021
accepted:
09
12
2021
revised:
01
12
2021
pubmed:
18
1
2022
medline:
11
3
2022
entrez:
17
1
2022
Statut:
ppublish
Résumé
Inflammatory bowel diseases, like ulcerative colitis and Crohn's disease are frequently accompanied by colorectal cancers. However, the mechanisms underlying colitis-associated cancers are not fully understood. Src Kinase Associated Phosphoprotein 2 (SKAP2), a substrate of Src family kinases, is highly expressed in macrophages. Here, we examined the effects of SKAP2 on inflammatory responses in a mouse model of tumorigenesis with colitis induced by azoxymethane/dextran sulfate sodium. SKAP2 knockout increased the severity of colitis and tumorigenesis, as well as lipopolysaccharide (LPS) induced acute inflammation. SKAP2 attenuated inflammatory signaling in macrophages induced by uptake of cancer cell-derived exosomes. SKAP2
Identifiants
pubmed: 35034964
doi: 10.1038/s41388-021-02153-1
pii: 10.1038/s41388-021-02153-1
doi:
Substances chimiques
PTPN6 protein, human
EC 3.1.3.48
Protein Tyrosine Phosphatase, Non-Receptor Type 6
EC 3.1.3.48
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1087-1099Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Bourette RP, Thérier J, Mouchiroud G. Macrophage colony-stimulating factor receptor induces tyrosine phosphorylation of SKAP55R adaptor and its association with actin. Cell Signal. 2005;17:941–9.
pubmed: 15894167
doi: 10.1016/j.cellsig.2004.11.009
Reinhold A, Reimann S, Reinhold D, Schraven B, Togni M. Expression of SKAP-HOM in DCs is required for an optimal immune response in vivo. J Leukoc Biol. 2009;86:61–71.
pubmed: 19369640
doi: 10.1189/jlb.0608344
Swanson KD, Tang Y, Ceccarelli DF, Poy F, Sliwa JP, Neel BG, et al. The Skap-hom dimerization and PH domains comprise a 3’-phosphoinositide-gated molecular switch. Mol Cell. 2008;32:564–75.
pubmed: 19026786
pmcid: 2628593
doi: 10.1016/j.molcel.2008.09.022
Tanaka M, Shimamura S, Kuriyama S, Maeda D, Goto A, Aiba N. SKAP2 Promotes Podosome Formation to Facilitate Tumor-Associated Macrophage Infiltration and Metastatic Progression. Cancer Res. 2016;76:358–69.
pubmed: 26577701
doi: 10.1158/0008-5472.CAN-15-1879
Boras M, Volmering S, Bokemeyer A, Rossaint J, Block H, Bardel B, et al. Skap2 is required for β(2) integrin-mediated neutrophil recruitment and functions. J Exp Med. 2017;214:851–74.
pubmed: 28183734
pmcid: 5339670
doi: 10.1084/jem.20160647
Shaban L, Nguyen GT, Mecsas-Faxon BD, Swanson KD, Tan S, Mecsas J. Yersinia pseudotuberculosis YopH targets SKAP2-dependent and independent signaling pathways to block neutrophil antimicrobial mechanisms during infection. PLoS Pathog. 2020;16:e1008576.
pubmed: 32392230
pmcid: 7241846
doi: 10.1371/journal.ppat.1008576
Nguyen GT, Shaban L, Mack M, Swanson KD, Bunnell SC, Sykes DB, et al. SKAP2 is required for defense against K. pneumoniae infection and neutrophil respiratory burst. Elife 2020;9:e56656.
pubmed: 32352382
pmcid: 7250567
doi: 10.7554/eLife.56656
Timms JF, Swanson KD, Marie-Cardine A, Raab M, Rudd CE, Schraven B, et al. SHPS-1 is a scaffold for assembling distinct adhesion-regulated multi-protein complexes in macrophages. Curr Biol. 1999;9:927–30.
pubmed: 10469599
doi: 10.1016/S0960-9822(99)80401-1
Alenghat FJ, Baca QJ, Rubin NT, Pao LI, Matozaki T, Lowell CA, et al. Macrophages require Skap2 and Sirpα for integrin-stimulated cytoskeletal rearrangement. J Cell Sci. 2012;125:5535–45.
pubmed: 22976304
pmcid: 3561861
Shi L, Han X, Li JX, Liao YT, Kou FS, Wang ZB, et al. Identification of differentially expressed genes in ulcerative colitis and verification in a colitis mouse model by bioinformatics analyses. World J Gastroenterol. 2020;26:5983–96.
pubmed: 33132649
pmcid: 7584051
doi: 10.3748/wjg.v26.i39.5983
Yashiro M. Ulcerative colitis-associated colorectal cancer. World J Gastroenterol. 2014;20:16389–97.
pubmed: 25469007
pmcid: 4248182
doi: 10.3748/wjg.v20.i44.16389
Snider AJ, Bialkowska AB, Ghaleb AM, Yang VW, Obeid LM, Hannun YA. Murine model for colitis-associated cancer of the colon. Methods Mol Biol. 2016;1438:245–54.
pubmed: 27150094
pmcid: 5657253
doi: 10.1007/978-1-4939-3661-8_14
Waldner MJ, Neurath MF. Mechanisms of immune signaling in colitis-associated cancer. Cell Mol Gastroenterol Hepatol. 2015;1:6–16.
pubmed: 28247866
doi: 10.1016/j.jcmgh.2014.11.006
Fukata M, Hernandez Y, Conduah D, Cohen J, Chen A, Breglio K, et al. Innate immune signaling by Toll-like receptor-4 (TLR4) shapes the inflammatory microenvironment in colitis-associated tumors. Inflamm Bowel Dis. 2009;15:997–1006.
pubmed: 19229991
doi: 10.1002/ibd.20880
Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, et al. LPS-induced cytokine production in human monocytes and macrophages. Crit Rev Immunol. 2011;31:379–446.
pubmed: 22142165
doi: 10.1615/CritRevImmunol.v31.i5.20
Hoogland IC, Houbolt C, van Westerloo DJ, van Gool WA, van de Beek D. Systemic inflammation and microglial activation: systematic review of animal experiments. J Neuroinflammation. 2015;12:114.
pubmed: 26048578
pmcid: 4470063
doi: 10.1186/s12974-015-0332-6
Corrin B. Lung pathology in septic shock. J Clin Pathol. 1980;33:891–4.
pubmed: 7430404
pmcid: 1146256
doi: 10.1136/jcp.33.9.891
Chattopadhyay S, Sen GC. Tyrosine phosphorylation in toll-like receptor signaling. Cytokine Growth Factor Rev. 2014;25:533–41.
pubmed: 25022196
pmcid: 4254339
doi: 10.1016/j.cytogfr.2014.06.002
Antwi-Baffour SS. Molecular characterisation of plasma membrane-derived vesicles. J Biomed Sci. 2015;22:68.
pubmed: 26259622
pmcid: 4532247
doi: 10.1186/s12929-015-0174-7
Ciardiello C, Cavallini L, Spinelli C, Yang J, Reis-Sobreiro M, de Candia P, et al. Focus on extracellular vesicles: new frontiers of cell-to-cell communication in cancer. Int J Mol Sci. 2016;17:175.
pubmed: 26861306
pmcid: 4783909
doi: 10.3390/ijms17020175
Qian Z, Shen Q, Yang X, Qiu Y, Zhang W. The role of extracellular vesicles: an epigenetic view of the cancer microenvironment. Biomed Res Int. 2015;2015:649161.
pubmed: 26582468
pmcid: 4637039
doi: 10.1155/2015/649161
Steinbichler TB, Dudás J, Riechelmann H, Skvortsova II. The role of exosomes in cancer metastasis. Semin Cancer Biol. 2017;44:170–81.
pubmed: 28215970
doi: 10.1016/j.semcancer.2017.02.006
Paschon V, Takada SH, Ikebara JM, Sousa E, Raeisossadati R, Ulrich H, et al. Interplay between exosomes, microRNAs and toll-like receptors in brain disorders. Mol Neurobiol. 2016;53:2016–28.
pubmed: 25862375
doi: 10.1007/s12035-015-9142-1
Zhang X, Shi H, Yuan X, Jiang P, Qian H, Xu W. Tumor-derived exosomes induce N2 polarization of neutrophils to promote gastric cancer cell migration. Mol Cancer. 2018;17:146.
pubmed: 30292233
pmcid: 6174070
doi: 10.1186/s12943-018-0898-6
Barichello T, Generoso JS, Simões LR, Elias SG, Quevedo J. Role of oxidative stress in the pathophysiology of pneumococcal meningitis. Oxid Med Cell Longev. 2013;2013:371465.
pubmed: 23766853
pmcid: 3665263
doi: 10.1155/2013/371465
Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol. 2008;9:361–8.
pubmed: 18297073
pmcid: 4112825
doi: 10.1038/ni1569
Kuzmich NN, Sivak KV, Chubarev VN, Porozov YB, Savateeva-Lyubimova TN, Peri F. TLR4 Signaling pathway modulators as potential therapeutics in inflammation and sepsis. Vaccines. 2017;5:34.
pmcid: 5748601
doi: 10.3390/vaccines5040034
Li P, Wu YH, Zhu YT, Li MX, Pei HH. Requirement of Rab21 in LPS-induced TLR4 signaling and pro-inflammatory responses in macrophages and monocytes. Biochem Biophys Res Commun. 2019;508:169–76.
pubmed: 30471852
doi: 10.1016/j.bbrc.2018.11.074
Marongiu L, Gornati L, Artuso I, Zanoni I, Granucci F. Below the surface: the inner lives of TLR4 and TLR9. J Leukoc Biol. 2019;106:147–60.
pubmed: 30900780
doi: 10.1002/JLB.3MIR1218-483RR
Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature. 2009;458:1191–5.
pubmed: 19252480
doi: 10.1038/nature07830
Rosadini CV, Kagan JC. Early innate immune responses to bacterial LPS. Curr Opin Immunol. 2017;44:14–19.
pubmed: 27842237
doi: 10.1016/j.coi.2016.10.005
Khaled AR, Butfiloski EJ, Sobel ES, Schiffenbauer J. Functional consequences of the SHP-1 defect in motheaten viable mice: role of NF-kappa B. Cell Immunol. 1998;185:49–58.
pubmed: 9636682
doi: 10.1006/cimm.1998.1272
Massa PT, Wu C. Increased inducible activation of NF-kappaB and responsive genes in astrocytes deficient in the protein tyrosine phosphatase SHP-1. J Interferon Cytokine Res. 1998;18:499–507.
pubmed: 9712366
doi: 10.1089/jir.1998.18.499
Fujioka Y, Matozaki T, Noguchi T, Iwamatsu A, Yamao T, Takahashi N, et al. A novel membrane glycoprotein, SHPS-1, that binds the SH2-domain-containing protein tyrosine phosphatase SHP-2 in response to mitogens and cell adhesion. Mol Cell Biol. 1996;16:6887–99.
pubmed: 8943344
pmcid: 231692
doi: 10.1128/MCB.16.12.6887
Oshima K, Ruhul Amin AR, Suzuki A, Hamaguchi M, Matsuda S. SHPS-1, a multifunctional transmembrane glycoprotein. FEBS Lett. 2002;519:1–7.
pubmed: 12023008
doi: 10.1016/S0014-5793(02)02703-5
Timms JF, Carlberg K, Gu H, Chen H, Kamatkar S, Nadler MJ, et al. Identification of major binding proteins and substrates for the SH2-containing protein tyrosine phosphatase SHP-1 in macrophages. Mol Cell Biol. 1998;18:3838–50.
pubmed: 9632768
pmcid: 108968
doi: 10.1128/MCB.18.7.3838
Miyake A, Murata Y, Okazawa H, Ikeda H, Niwayama Y, Ohnishi H, et al. Negative regulation by SHPS-1 of Toll-like receptor-dependent proinflammatory cytokine production in macrophages. Genes Cells. 2008;13:209–19.
pubmed: 18233962
doi: 10.1111/j.1365-2443.2007.01161.x
Lu R, Pan H, Shively JE. CEACAM1 negatively regulates IL-1β production in LPS activated neutrophils by recruiting SHP-1 to a SYK-TLR4-CEACAM1 complex. PLoS Pathog. 2012;8:e1002597.
pubmed: 22496641
pmcid: 3320586
doi: 10.1371/journal.ppat.1002597
Ramachandran IR, Song W, Lapteva N, Seethammagari M, Slawin KM, Spencer DM, et al. The phosphatase SRC homology region 2 domain-containing phosphatase-1 is an intrinsic central regulator of dendritic cell function. J Immunol. 2011;186:3934–45.
pubmed: 21357539
doi: 10.4049/jimmunol.1001675
You M, Flick LM, Yu D, Feng GS. Modulation of the nuclear factor kappa B pathway by Shp-2 tyrosine phosphatase in mediating the induction of interleukin (IL)-6 by IL-1 or tumor necrosis factor. J Exp Med. 2001;193:101–10.
pubmed: 11136824
pmcid: 2195877
doi: 10.1084/jem.193.1.101
Feng J, He L, Li Y, Xiao F, Hu G. Modeling of PH domains and phosphoinositides interactions and beyond. Adv Exp Med Biol. 2019;1111:19–32.
pubmed: 30069854
doi: 10.1007/5584_2018_236
Niogret C, Birchmeier W, Guarda G. SHP-2 in lymphocytes’ cytokine and inhibitory receptor signaling. Front Immunol. 2019;10:2468.
pubmed: 31708921
pmcid: 6823243
doi: 10.3389/fimmu.2019.02468
van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis. 2008;11:91–99.
pubmed: 18264787
doi: 10.1007/s10456-008-9093-5
Buwitt-Beckmann U, Heine H, Wiesmüller KH, Jung G, Brock R, Akira S, et al. Toll-like receptor 6-independent signaling by diacylated lipopeptides. Eur J Immunol. 2005;35:282–9.
pubmed: 15580661
doi: 10.1002/eji.200424955
Pashenkov MV, Murugina NE, Budikhina AS, Pinegin BV. Synergistic interactions between NOD receptors and TLRs: Mechanisms and clinical implications. J Leukoc Biol. 2019;105:669–80.
pubmed: 30517768
doi: 10.1002/JLB.2RU0718-290R
Jakopin Ž, Corsini E. THP-1 Cells and pro-inflammatory cytokine production: an in vitro tool for functional characterization of NOD1/NOD2 antagonists. Int J Mol Sci. 2019;20:4265.
pmcid: 6747088
doi: 10.3390/ijms20174265
van Heel DA, Ghosh S, Butler M, Hunt KA, Lundberg AM, Ahmad T, et al. Muramyl dipeptide and toll-like receptor sensitivity in NOD2-associated Crohn’s disease. Lancet. 2005;365:1794–6.
pubmed: 15910952
doi: 10.1016/S0140-6736(05)66582-8
Bretz NP, Ridinger J, Rupp AK, Rimbach K, Keller S, Rupp C, et al. Body fluid exosomes promote secretion of inflammatory cytokines in monocytic cells via Toll-like receptor signaling. J Biol Chem. 2013;288:36691–702.
pubmed: 24225954
pmcid: 3868779
doi: 10.1074/jbc.M113.512806
Chow A, Zhou W, Liu L, Fong MY, Champer J, Van Haute D, et al. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB. Sci Rep. 2014;4:5750.
pubmed: 25034888
pmcid: 4102923
doi: 10.1038/srep05750
Kim EJ, Suk K, Lee WH. SHPS-1 and a synthetic peptide representing its ITIM inhibit the MyD88, but not TRIF, pathway of TLR signaling through activation of SHP and PI3K in THP-1 cells. Inflamm Res. 2013;62:377–86.
pubmed: 23314616
doi: 10.1007/s00011-013-0589-0
Medvedev AE, Piao W, Shoenfelt J, Rhee SH, Chen H, Basu S, et al. Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J Biol Chem. 2007;282:16042–53.
pubmed: 17392283
doi: 10.1074/jbc.M606781200
Chaudhary A, Fresquez TM, Naranjo MJ. Tyrosine kinase Syk associates with toll-like receptor 4 and regulates signaling in human monocytic cells. Immunol Cell Biol. 2007;85:249–56.
pubmed: 17228323
doi: 10.1038/sj.icb7100030
An H, Zhao W, Hou J, Zhang Y, Xie Y, Zheng Y, et al. SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity. 2006;25:919–28.
pubmed: 17157040
doi: 10.1016/j.immuni.2006.10.014
Shimamura S, Sasaki K, Tanaka M. The Src substrate SKAP2 regulates actin assembly by interacting with WAVE2 and cortactin proteins. J Biol Chem. 2013;288:1171–83.
pubmed: 23161539
doi: 10.1074/jbc.M112.386722
Fløyel T, Meyerovich K, Prause MC, Kaur S, Frørup C, Mortensen HB, et al. SKAP2, a candidate gene for type 1 diabetes, regulates β-cell apoptosis and glycemic control in newly diagnosed patients. Diabetes. 2021;70:464–76.
pubmed: 33203694
doi: 10.2337/db20-0092
Bui TM, Wiesolek HL, Sumagin R. ICAM-1: A master regulator of cellular responses in inflammation, injury resolution, and tumorigenesis. J Leukoc Biol. 2020;108:787–99.
pubmed: 32182390
doi: 10.1002/JLB.2MR0220-549R
Chen R. Isolation and culture of mouse bone marrow-derived macrophages (BMM’phi'). Bio-protocol. 2012;2:e68.
doi: 10.21769/BioProtoc.68