Role of Sam68 as an adaptor protein in inflammatory signaling.

Arthritis BCR Cardiovascular disease Inflammation Inflammatory bowel disease Sam68 TCR TLR TNF

Journal

Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402

Informations de publication

Date de publication:
14 Feb 2024
Historique:
received: 18 08 2023
accepted: 25 12 2023
revised: 25 11 2023
medline: 14 2 2024
pubmed: 14 2 2024
entrez: 13 2 2024
Statut: epublish

Résumé

Sam68 is a ubiquitously expressed KH-domain containing RNA-binding protein highly studied for its involvement in regulating multiple steps of RNA metabolism. Sam68 also contains multiple protein-protein interaction regions such as proline-rich regions, tyrosine phosphorylation sites, and arginine methylation sites, all of which facilitate its participation as an adaptor protein in multiple signaling pathways, likely independent of its RNA-binding role. This review focuses on providing a comprehensive report on the adaptor roles of Sam68 in inflammatory signaling and inflammatory diseases. The insights presented here have the potential to open new avenues in inflammation research and justify targeting Sam68 to control aberrant inflammatory responses.

Identifiants

pubmed: 38351330
doi: 10.1007/s00018-023-05108-9
pii: 10.1007/s00018-023-05108-9
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

89

Subventions

Organisme : NIH/NIDDK
ID : R01DK128463
Organisme : NIH/NIAID
ID : R01AI116730
Organisme : NIH/NCI
ID : R21CA246194
Organisme : Juvenile Diabetes Research Foundation United States of America
ID : 3-SRA-2022-1193-S-B

Informations de copyright

© 2024. The Author(s).

Références

Bielli P, Busà R, Paronetto MP, Sette C (2011) The RNA-binding protein Sam68 is a multifunctional player in human cancer. Endocr Relat Cancer 18(4):R91–R102. https://doi.org/10.1530/erc-11-0041
doi: 10.1530/erc-11-0041 pubmed: 21565971
Frisone P, Pradella D, Di Matteo A, Belloni E, Ghigna C, Paronetto MP (2015) SAM68: signal transduction and RNA metabolism in human cancer. Biomed Res Int 2015:528954. https://doi.org/10.1155/2015/528954
doi: 10.1155/2015/528954 pubmed: 26273626 pmcid: 4529925
Feracci M, Foot JN, Grellscheid SN et al (2016) Structural basis of RNA recognition and dimerization by the STAR proteins T-STAR and Sam68. Nat Commun 7(1):10355. https://doi.org/10.1038/ncomms10355
doi: 10.1038/ncomms10355 pubmed: 26758068 pmcid: 4735526
Li QH, Fan TX, Pang TX, Yuan WS, Han ZC (2006) Effect of proline rich domain of an RNA-binding protein Sam68 in cell growth process, death and B cell signal transduction. Chin Med J 119(18):1536–1542
doi: 10.1097/00029330-200609020-00006 pubmed: 16996007
Sun W, Qin R, Wang R et al (2018) Sam68 promotes invasion, migration, and proliferation of fibroblast-like synoviocytes by enhancing the NF-κB/P65 pathway in rheumatoid arthritis. Inflammation 41(5):1661–1670. https://doi.org/10.1007/s10753-018-0809-4
doi: 10.1007/s10753-018-0809-4 pubmed: 29785588
Ramakrishnan P, Baltimore D (2011) Sam68 is required for both NF-κB activation and apoptosis signaling by the TNF receptor. Mol Cell 43(2):167–179. https://doi.org/10.1016/j.molcel.2011.05.007
doi: 10.1016/j.molcel.2011.05.007 pubmed: 21620750 pmcid: 3142289
Lin C-H, Liao C-C, Wang S-Y et al (2022) Comparative O-GlcNAc proteomic analysis reveals a role of O-GlcNAcylated SAM68 in lung cancer aggressiveness. Cancers 14(1):243
doi: 10.3390/cancers14010243 pubmed: 35008409 pmcid: 8749979
Côté J, Boisvert FM, Boulanger MC, Bedford MT, Richard S (2003) Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol Biol Cell 14(1):274–287. https://doi.org/10.1091/mbc.e02-08-0484
doi: 10.1091/mbc.e02-08-0484 pubmed: 12529443 pmcid: 140244
Babic I, Cherry E, Fujita DJ (2006) SUMO modification of Sam68 enhances its ability to repress cyclin D1 expression and inhibits its ability to induce apoptosis. Oncogene 25(36):4955–4964. https://doi.org/10.1038/sj.onc.1209504
doi: 10.1038/sj.onc.1209504 pubmed: 16568089
Babic I, Jakymiw A, Fujita DJ (2004) The RNA binding protein Sam68 is acetylated in tumor cell lines, and its acetylation correlates with enhanced RNA binding activity. Oncogene 23(21):3781–3789. https://doi.org/10.1038/sj.onc.1207484
doi: 10.1038/sj.onc.1207484 pubmed: 15021911
Rho J, Choi S, Jung CR, Im DS (2007) Arginine methylation of Sam68 and SLM proteins negatively regulates their poly(U) RNA binding activity. Arch Biochem Biophys 466(1):49–57. https://doi.org/10.1016/j.abb.2007.07.017
doi: 10.1016/j.abb.2007.07.017 pubmed: 17764653
Zhao J, Li J, Hassan W, Xu D, Wang X, Huang Z (2020) Sam68 promotes aerobic glycolysis in colorectal cancer by regulating PKM2 alternative splicing. Ann Transl Med 8(7):459
doi: 10.21037/atm.2020.03.108 pubmed: 32395503 pmcid: 7210197
Stockley J, Markert E, Zhou Y et al (2015) The RNA-binding protein Sam68 regulates expression and transcription function of the androgen receptor splice variant AR-V7. Sci Rep 5(1):1–13
doi: 10.1038/srep13426
Najib S, Martín-Romero C, González-Yanes C, Sánchez-Margalet V (2005) Role of Sam68 as an adaptor protein in signal transduction. Cell Mol Life Sci CMLS 62(1):36–43. https://doi.org/10.1007/s00018-004-4309-3
doi: 10.1007/s00018-004-4309-3 pubmed: 15619005
Pérez-Pérez A, Sánchez-Jiménez F, Vilariño-García T, de la Cruz L, Virizuela JA, Sánchez-Margalet V (2016) Sam68 mediates the activation of insulin and leptin signalling in breast cancer cells. PLoS ONE 11(7):e0158218. https://doi.org/10.1371/journal.pone.0158218
doi: 10.1371/journal.pone.0158218 pubmed: 27415018 pmcid: 4944952
Fu K, Sun X, Zheng W et al (2013) Sam68 modulates the promoter specificity of NF-κB and mediates expression of CD25 in activated T cells. Nat Commun 4:1909. https://doi.org/10.1038/ncomms2916
doi: 10.1038/ncomms2916 pubmed: 23715268
Tomalka JA, de Jesus TJ, Ramakrishnan P (2017) Sam68 is a regulator of Toll-like receptor signaling. Cell Mol Immunol 14(1):107–117. https://doi.org/10.1038/cmi.2016.32
doi: 10.1038/cmi.2016.32 pubmed: 27374795
Xiao J, Wang Q, Yang Q et al (2018) Clinical significance and effect of Sam68 expression in gastric cancer. Oncol Lett 15(4):4745–4752. https://doi.org/10.3892/ol.2018.7930
doi: 10.3892/ol.2018.7930 pubmed: 29552114 pmcid: 5840748
Goodman WA, Basavarajappa SC, Liu AR, Rodriguez FDS, Mathes T, Ramakrishnan P (2021) Sam68 contributes to intestinal inflammation in experimental and human colitis. Cell Mol Life Sci CMLS 78(23):7635–7648. https://doi.org/10.1007/s00018-021-03976-7
doi: 10.1007/s00018-021-03976-7 pubmed: 34693458
Xu L, Sun C, Zhang S et al (2015) Sam68 promotes NF-κB activation and apoptosis signaling in articular chondrocytes during osteoarthritis. Inflamm Res 64(11):895–902. https://doi.org/10.1007/s00011-015-0872-3
doi: 10.1007/s00011-015-0872-3 pubmed: 26350037
Han S, Xu S, Zhou J et al (2019) Sam68 impedes the recovery of arterial injury by augmenting inflammatory response. J Mol Cell Cardiol 137:82–92. https://doi.org/10.1016/j.yjmcc.2019.10.003
doi: 10.1016/j.yjmcc.2019.10.003 pubmed: 31639388 pmcid: 6889069
Jordan MS, Singer AL, Koretzky GA (2003) Adaptors as central mediators of signal transduction in immune cells. Nat Immunol 4(2):110–116. https://doi.org/10.1038/ni0203-110
doi: 10.1038/ni0203-110 pubmed: 12555096
Borowicz P, Chan H, Hauge A, Spurkland A (2020) Adaptor proteins: Flexible and dynamic modulators of immune cell signalling. Scand J Immunol 92(5):e12951. https://doi.org/10.1111/sji.12951
doi: 10.1111/sji.12951 pubmed: 32734639
Hwang JR, Byeon Y, Kim D, Park SG (2020) Recent insights of T cell receptor-mediated signaling pathways for T cell activation and development. Exp Mol Med 52(5):750–761. https://doi.org/10.1038/s12276-020-0435-8
doi: 10.1038/s12276-020-0435-8 pubmed: 32439954 pmcid: 7272404
Lang V, Mège D, Semichon M, Gary-Gouy H, Bismuth G (1997) A dual participation of ZAP-70 and scr protein tyrosine kinases is required for TCR-induced tyrosine phosphorylation of Sam68 in Jurkat T cells. Eur J Immunol 27(12):3360–3367. https://doi.org/10.1002/eji.1830271235
doi: 10.1002/eji.1830271235 pubmed: 9464824
Najib S, Sánchez-Margalet V (2002) Sam68 associates with the SH3 domains of Grb2 recruiting GAP to the Grb2-SOS complex in insulin receptor signaling. J Cell Biochem 86(1):99–106. https://doi.org/10.1002/jcb.10198
doi: 10.1002/jcb.10198 pubmed: 12112020
Fusaki N, Iwamatsu A, Iwashima M, Fujisawa J (1997) Interaction between Sam68 and Src family tyrosine kinases, Fyn and Lck, in T cell receptor signaling. J Biol Chem 272(10):6214–6219. https://doi.org/10.1074/jbc.272.10.6214
doi: 10.1074/jbc.272.10.6214 pubmed: 9045636
Salmond RJ, Filby A, Qureshi I, Caserta S, Zamoyska R (2009) T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol Rev 228(1):9–22. https://doi.org/10.1111/j.1600-065X.2008.00745.x
doi: 10.1111/j.1600-065X.2008.00745.x pubmed: 19290918
Asbach B, Ludwig C, Saksela K, Wagner R (2012) Comprehensive analysis of interactions between the Src-associated protein in mitosis of 68 kDa and the human Src-homology 3 proteome. PLoS ONE 7(6):e38540. https://doi.org/10.1371/journal.pone.0038540
doi: 10.1371/journal.pone.0038540 pubmed: 22745667 pmcid: 3379994
Shah K, Al-Haidari A, Sun J, Kazi JU (2021) T cell receptor (TCR) signaling in health and disease. Signal Transduct Target Ther 6(1):412. https://doi.org/10.1038/s41392-021-00823-w
doi: 10.1038/s41392-021-00823-w pubmed: 34897277 pmcid: 8666445
Volpe E, Cesari E, Mercatelli N et al (2019) The RNA binding protein Sam68 controls T helper 1 differentiation and anti-mycobacterial response through modulation of miR-29. Cell Death Differ 26(6):1169–1180. https://doi.org/10.1038/s41418-018-0201-9
doi: 10.1038/s41418-018-0201-9 pubmed: 30258098
Treanor B (2012) B-cell receptor: from resting state to activate. Immunology 136(1):21–27. https://doi.org/10.1111/j.1365-2567.2012.03564.x
doi: 10.1111/j.1365-2567.2012.03564.x pubmed: 22269039 pmcid: 3372753
Tokunaga R, Naseem M, Lo JH et al (2019) B cell and B cell-related pathways for novel cancer treatments. Cancer Treat Rev 73:10–19. https://doi.org/10.1016/j.ctrv.2018.12.001
doi: 10.1016/j.ctrv.2018.12.001 pubmed: 30551036
Finan PM, Hall A, Kellie S (1996) Sam68 from an immortalised B-cell line associates with a subset of SH3 domains. FEBS Lett 389(2):141–144. https://doi.org/10.1016/0014-5793(96)00552-2
doi: 10.1016/0014-5793(96)00552-2 pubmed: 8766817
Sánchez-Margalet V, Najib S (2001) Sam68 is a docking protein linking GAP and PI3K in insulin receptor signaling. Mol Cell Endocrinol 183(1–2):113–121. https://doi.org/10.1016/s0303-7207(01)00587-1
doi: 10.1016/s0303-7207(01)00587-1 pubmed: 11604231
Guinamard R, Fougereau M, Seckinger P (1997) The SH3 domain of Bruton’s tyrosine kinase interacts with Vav, Sam68 and EWS. Scand J Immunol 45(6):587–595. https://doi.org/10.1046/j.1365-3083.1997.d01-447.x
doi: 10.1046/j.1365-3083.1997.d01-447.x pubmed: 9201297
de Jesus AA, Chen G, Yang D et al (2023) Constitutively active Lyn kinase causes a cutaneous small vessel vasculitis and liver fibrosis syndrome. Nat Commun 14(1):1502. https://doi.org/10.1038/s41467-023-36941-y
doi: 10.1038/s41467-023-36941-y pubmed: 36932076 pmcid: 10022554
Sanderson MP, Wex E, Kono T, Uto K, Schnapp A (2010) Syk and Lyn mediate distinct Syk phosphorylation events in FcɛRI-signal transduction: implications for regulation of IgE-mediated degranulation. Mol Immunol 48(1):171–178. https://doi.org/10.1016/j.molimm.2010.08.012
doi: 10.1016/j.molimm.2010.08.012 pubmed: 20828828
Kurosaki T, Kurosaki M (1997) Transphosphorylation of Bruton’s tyrosine kinase on tyrosine 551 is critical for B cell antigen receptor function. J Biol Chem 272(25):15595–15598. https://doi.org/10.1074/jbc.272.25.15595
doi: 10.1074/jbc.272.25.15595 pubmed: 9188445
Baba Y, Hashimoto S, Matsushita M et al (2001) BLNK mediates Syk-dependent Btk activation. Proc Natl Acad Sci USA 98(5):2582–2586. https://doi.org/10.1073/pnas.051626198
doi: 10.1073/pnas.051626198 pubmed: 11226282 pmcid: 30181
Desaulniers P, Fernandes M, Gilbert C, Bourgoin SG, Naccache PH (2001) Crystal-induced neutrophil activation. VII. Involvement of Syk in the responses to monosodium urate crystals. J Leukocyte Biol 70(4):659–668
doi: 10.1189/jlb.70.4.659 pubmed: 11590204
Guitard E, Barlat I, Maurier F, Schweighoffer F, Tocque B (1998) Sam68 is a Ras-GAP-associated protein in mitosis. Biochem Biophys Res Commun 245(2):562–566. https://doi.org/10.1006/bbrc.1998.8374
doi: 10.1006/bbrc.1998.8374 pubmed: 9571195
Neumann K, Oellerich T, Urlaub H, Wienands J (2009) The B-lymphoid Grb2 interaction code. Immunol Rev 232(1):135–149. https://doi.org/10.1111/j.1600-065X.2009.00845.x
doi: 10.1111/j.1600-065X.2009.00845.x pubmed: 19909361
Boucher J, Kleinridders A, Kahn CR (2014) Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harbor Perspect Biol. https://doi.org/10.1101/cshperspect.a009191
doi: 10.1101/cshperspect.a009191
Sánchez-Margalet V, Najib S (1999) p68 Sam is a substrate of the insulin receptor and associates with the SH2 domains of p85 PI3K. FEBS Lett 455(3):307–310. https://doi.org/10.1016/S0014-5793(99)00887-X
doi: 10.1016/S0014-5793(99)00887-X pubmed: 10437794
Quintana-Portillo R, Canfrán-Duque A, Issad T, Sánchez-Margalet V, González-Yanes C (2012) Sam68 interacts with IRS1. Biochem Pharmacol 83(1):78–87. https://doi.org/10.1016/j.bcp.2011.09.030
doi: 10.1016/j.bcp.2011.09.030 pubmed: 22005517
Wu W, Liu Y, Wang Y (2016) Sam68 promotes Schwann cell proliferation by enhancing the PI3K/Akt pathway and acts on regeneration after sciatic nerve crush. Biochem Biophys Res Commun 473(4):1045–1051. https://doi.org/10.1016/j.bbrc.2016.04.013
doi: 10.1016/j.bbrc.2016.04.013 pubmed: 27059137
Chen L, Chen R, Wang H, Liang F (2015) Mechanisms linking inflammation to insulin resistance. Int J Endocrinol 2015:508409. https://doi.org/10.1155/2015/508409
doi: 10.1155/2015/508409 pubmed: 26136779 pmcid: 4468292
Rehman K, Akash MS (2016) Mechanisms of inflammatory responses and development of insulin resistance: how are they interlinked? J Biomed Sci 23(1):87. https://doi.org/10.1186/s12929-016-0303-y
doi: 10.1186/s12929-016-0303-y pubmed: 27912756 pmcid: 5135788
Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM (1994) Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci USA 91(11):4854–4858. https://doi.org/10.1073/pnas.91.11.4854
doi: 10.1073/pnas.91.11.4854 pubmed: 8197147 pmcid: 43887
Maroni P, Citterio L, Piccoletti R, Bendinelli P (2009) Sam68 and ERKs regulate leptin-induced expression of OB-Rb mRNA in C2C12 myotubes. Mol Cell Endocrinol 309(1–2):26–31. https://doi.org/10.1016/j.mce.2009.05.021
doi: 10.1016/j.mce.2009.05.021 pubmed: 19524014
Villanueva EC, Myers MG Jr (2008) Leptin receptor signaling and the regulation of mammalian physiology. Int J Obesity 32(Suppl 7):S8-12. https://doi.org/10.1038/ijo.2008.232
doi: 10.1038/ijo.2008.232
La Cava A (2017) Leptin in inflammation and autoimmunity. Cytokine 98:51–58. https://doi.org/10.1016/j.cyto.2016.10.011
doi: 10.1016/j.cyto.2016.10.011 pubmed: 27916613 pmcid: 5453851
Procaccini C, Lourenco EV, Matarese G, La Cava A (2009) Leptin signaling: a key pathway in immune responses. Curr Signal Transduct Ther 4(1):22–30. https://doi.org/10.2174/157436209787048711
doi: 10.2174/157436209787048711 pubmed: 19774101 pmcid: 2747760
Li C, Friedman JM (1999) Leptin receptor activation of SH2 domain containing protein tyrosine phosphatase 2 modulates Ob receptor signal transduction. Proc Natl Acad Sci USA 96(17):9677–9682. https://doi.org/10.1073/pnas.96.17.9677
doi: 10.1073/pnas.96.17.9677 pubmed: 10449753 pmcid: 22269
Aggarwal BB, Gupta SC, Kim JH (2012) Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood 119(3):651–665. https://doi.org/10.1182/blood-2011-04-325225
doi: 10.1182/blood-2011-04-325225 pubmed: 22053109 pmcid: 3265196
Hildt E, Oess S (1999) Identification of Grb2 as a novel binding partner of tumor necrosis factor (TNF) receptor I. J Exp Med 189(11):1707–1714. https://doi.org/10.1084/jem.189.11.1707
doi: 10.1084/jem.189.11.1707 pubmed: 10359574 pmcid: 2193078
Lu Y, Li X, Liu S, Zhang Y, Zhang D (2018) Toll-like receptors and inflammatory bowel disease. Front Immunol 9:72. https://doi.org/10.3389/fimmu.2018.00072
doi: 10.3389/fimmu.2018.00072 pubmed: 29441063 pmcid: 5797585
Lai CY, Su YW, Lin KI, Hsu LC, Chuang TH (2017) Natural modulators of endosomal toll-like receptor-mediated psoriatic skin inflammation. J Immunol Res 2017:7807313. https://doi.org/10.1155/2017/7807313
doi: 10.1155/2017/7807313 pubmed: 28894754 pmcid: 5574364
Huang QQ, Pope RM (2009) The role of toll-like receptors in rheumatoid arthritis. Curr Rheumatol Rep 11(5):357–364. https://doi.org/10.1007/s11926-009-0051-z
doi: 10.1007/s11926-009-0051-z pubmed: 19772831 pmcid: 2913446
Green NM, Marshak-Rothstein A (2011) Toll-like receptor driven B cell activation in the induction of systemic autoimmunity. Semin Immunol 23(2):106–112. https://doi.org/10.1016/j.smim.2011.01.016
doi: 10.1016/j.smim.2011.01.016 pubmed: 21306913 pmcid: 3070769
Covacu R, Arvidsson L, Andersson A et al (2009) TLR activation induces TNF-alpha production from adult neural stem/progenitor cells. J Immunol (Baltimore, Md). 182(11):6889–6895. https://doi.org/10.4049/jimmunol.0802907
doi: 10.4049/jimmunol.0802907
Berenbaum F, Walker C (2020) Osteoarthritis and inflammation: a serious disease with overlapping phenotypic patterns. Postgrad Med 132(4):377–384. https://doi.org/10.1080/00325481.2020.1730669
doi: 10.1080/00325481.2020.1730669 pubmed: 32100608
Cho Y, Jeong S, Kim H et al (2021) Disease-modifying therapeutic strategies in osteoarthritis: current status and future directions. Exp Mol Med 53(11):1689–1696. https://doi.org/10.1038/s12276-021-00710-y
doi: 10.1038/s12276-021-00710-y pubmed: 34848838 pmcid: 8640059
Molnar V, Matišić V, Kodvanj I et al (2021) Cytokines and chemokines involved in osteoarthritis pathogenesis. Int J Mol Sci 22(17):9208
doi: 10.3390/ijms22179208 pubmed: 34502117 pmcid: 8431625
Herrero-Beaumont G, Pérez-Baos S, Sánchez-Pernaute O, Roman-Blas JA, Lamuedra A, Largo R (2019) Targeting chronic innate inflammatory pathways, the main road to prevention of osteoarthritis progression. Biochem Pharmacol 165:24–32. https://doi.org/10.1016/j.bcp.2019.02.030
doi: 10.1016/j.bcp.2019.02.030 pubmed: 30825432
Yang J, Hu S, Bian Y et al (2022) Targeting cell death: pyroptosis, ferroptosis, apoptosis and necroptosis in osteoarthritis. Front Cell Develop Biol. https://doi.org/10.3389/fcell.2021.789948
doi: 10.3389/fcell.2021.789948
Guo Q, Wang Y, Xu D, Nossent J, Pavlos NJ, Xu J (2018) Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone research 6:15. https://doi.org/10.1038/s41413-018-0016-9
doi: 10.1038/s41413-018-0016-9 pubmed: 29736302 pmcid: 5920070
Ibáñez-Costa A, Perez-Sanchez C, Patiño-Trives AM et al (2022) Splicing machinery is impaired in rheumatoid arthritis, associated with disease activity and modulated by anti-TNF therapy. Ann Rheum Dis 81(1):56–67. https://doi.org/10.1136/annrheumdis-2021-220308
doi: 10.1136/annrheumdis-2021-220308 pubmed: 34625402
Ilchovska D, Barrow DM (2021) An Overview of the NF-kB mechanism of pathophysiology in rheumatoid arthritis, investigation of the NF-kB ligand RANKL and related nutritional interventions. Autoimmun Rev 20(2):102741. https://doi.org/10.1016/j.autrev.2020.102741
doi: 10.1016/j.autrev.2020.102741 pubmed: 33340772
Fu K, Sun X, Wier EM, Hodgson A, Hobbs RP, Wan F (2016) Sam68/KHDRBS1-dependent NF-κB activation confers radioprotection to the colon epithelium in γ-irradiated mice. Elife. https://doi.org/10.7554/eLife.21957
doi: 10.7554/eLife.21957 pubmed: 27996939 pmcid: 5214542
Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448(7152):427–434. https://doi.org/10.1038/nature06005
doi: 10.1038/nature06005 pubmed: 17653185
Silverberg MS, Satsangi J, Ahmad T et al (2005) Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 19(Suppl A):5A-36A
doi: 10.1155/2005/269076 pubmed: 16151544
Artis D (2008) Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8(6):411–420
doi: 10.1038/nri2316 pubmed: 18469830
Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10(3):159–169
doi: 10.1038/nri2710 pubmed: 20182457
Iwamoto M, Koji T, Makiyama K, Kobayashi N, Nakane PK (1996) Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol 180(2):152–159. https://doi.org/10.1002/(sici)1096-9896(199610)180:2%3c152::Aid-path649%3e3.0.Co;2-y
doi: 10.1002/(sici)1096-9896(199610)180:2<152::Aid-path649>3.0.Co;2-y pubmed: 8976873
Hagiwara C, Tanaka M, Kudo H (2002) Increase in colorectal epithelial apoptotic cells in patients with ulcerative colitis ultimately requiring surgery. J Gastroenterol Hepatol 17(7):758–764. https://doi.org/10.1046/j.1440-1746.2002.02791.x
doi: 10.1046/j.1440-1746.2002.02791.x pubmed: 12121505
Edelblum KL, Yan F, Yamaoka T, Polk DB (2006) Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. Inflamm Bowel Dis 12(5):413–424. https://doi.org/10.1097/01.MIB.0000217334.30689.3e
doi: 10.1097/01.MIB.0000217334.30689.3e pubmed: 16670531
Bradford EM, Ryu SH, Singh AP et al (2017) Epithelial TNF receptor signaling promotes mucosal repair in inflammatory bowel disease. J Immunol (Baltimore, Md). 199(5):1886–1897. https://doi.org/10.4049/jimmunol.1601066
doi: 10.4049/jimmunol.1601066
Gareb B, Otten AT, Frijlink HW, Dijkstra G, Kosterink JGW (2020) Review: local tumor necrosis factor-α inhibition in inflammatory bowel disease. Pharmaceutics. https://doi.org/10.3390/pharmaceutics12060539
doi: 10.3390/pharmaceutics12060539 pubmed: 32545207 pmcid: 7356880
Dubé PE, Punit S, Polk DB (2015) Redeeming an old foe: protective as well as pathophysiological roles for tumor necrosis factor in inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 308(3):161–170
doi: 10.1152/ajpgi.00142.2014
Qian J, Zhao W, Miao X, Li L, Zhang D (2016) Sam68 modulates apoptosis of intestinal epithelial cells via mediating NF-κB activation in ulcerative colitis. Mol Immunol 75:48–59. https://doi.org/10.1016/j.molimm.2016.05.011
doi: 10.1016/j.molimm.2016.05.011 pubmed: 27235792
Mabrouk ME, Diep QN, Benkirane K, Touyz RM, Schiffrin EL (2004) SAM68: a downstream target of angiotensin II signaling in vascular smooth muscle cells in genetic hypertension. Am J Physiol Heart Circ Physiol 286(5):H1954–H1962. https://doi.org/10.1152/ajpheart.00134.2003
doi: 10.1152/ajpheart.00134.2003 pubmed: 14693677
Lukong KE, Richard S (2003) Sam68, the KH domain-containing superSTAR. Biochem Biophys Acta 1653(2):73–86. https://doi.org/10.1016/j.bbcan.2003.09.001
doi: 10.1016/j.bbcan.2003.09.001 pubmed: 14643926
Locatelli A, Lange CA (2011) Met receptors induce Sam68-dependent cell migration by activation of alternate extracellular signal-regulated kinase family members. J Biol Chem 286(24):21062–21072. https://doi.org/10.1074/jbc.M110.211409
doi: 10.1074/jbc.M110.211409 pubmed: 21489997 pmcid: 3122167
Lukong KE, Larocque D, Tyner AL, Richard S (2005) Tyrosine phosphorylation of Sam68 by breast tumor kinase regulates intranuclear localization and cell cycle progression*. J Biol Chem 280(46):38639–38647. https://doi.org/10.1074/jbc.M505802200
doi: 10.1074/jbc.M505802200 pubmed: 16179349
Vogel G, Richard S (2012) Emerging roles for Sam68 in adipogenesis and neuronal development. RNA Biol 9(9):1129–1133. https://doi.org/10.4161/rna.21409
doi: 10.4161/rna.21409 pubmed: 23018781 pmcid: 3579877
Benoit YD, Mitchell RR, Risueño RM et al (2017) Sam68 allows selective targeting of human cancer stem cells. Cell Chem Biol 24(7):833–44.e9. https://doi.org/10.1016/j.chembiol.2017.05.026
doi: 10.1016/j.chembiol.2017.05.026 pubmed: 28648376
Benoit YD, Guezguez B, Boyd AL, Bhatia M (2014) Molecular pathways: epigenetic modulation of Wnt-glycogen synthase kinase-3 signaling to target human cancer stem cells. Clin Cancer Res 20(21):5372–5378. https://doi.org/10.1158/1078-0432.Ccr-13-2491
doi: 10.1158/1078-0432.Ccr-13-2491 pubmed: 25006223
Masibag AN, Bergin CJ, Haebe JR et al (2021) Pharmacological targeting of Sam68 functions in colorectal cancer stem cells. iScience 24(12):103442. https://doi.org/10.1016/j.isci.2021.103442
doi: 10.1016/j.isci.2021.103442 pubmed: 34877499 pmcid: 8633986
Wu Z, Peng Y, Xiong L et al (2022) Role of Sam68 in sunitinib induced renal cell carcinoma apoptosis. Cancer Med 11(19):3674–3686. https://doi.org/10.1002/cam4.4743
doi: 10.1002/cam4.4743 pubmed: 35476809 pmcid: 9554455
Boisvert FM, Chénard CA, Richard S (2005) Protein interfaces in signaling regulated by arginine methylation. Sci STKE 2005(271):re2. https://doi.org/10.1126/stke.2712005re2
doi: 10.1126/stke.2712005re2 pubmed: 15713950

Auteurs

Vemana Gowd (V)

Department of Pathology, School of Medicine, Case Western Reserve University and University Hospitals Cleveland Medical Center, 6526, Wolstein Research Building, 2103 Cornell Road, Cleveland, OH, 44106, USA.

Joseph D'Amato Kass (JD)

Department of Pathology, School of Medicine, Case Western Reserve University and University Hospitals Cleveland Medical Center, 6526, Wolstein Research Building, 2103 Cornell Road, Cleveland, OH, 44106, USA.

Nandini Sarkar (N)

Department of Pathology, School of Medicine, Case Western Reserve University and University Hospitals Cleveland Medical Center, 6526, Wolstein Research Building, 2103 Cornell Road, Cleveland, OH, 44106, USA.

Parameswaran Ramakrishnan (P)

Department of Pathology, School of Medicine, Case Western Reserve University and University Hospitals Cleveland Medical Center, 6526, Wolstein Research Building, 2103 Cornell Road, Cleveland, OH, 44106, USA. pxr150@case.edu.
The Case Comprehensive Cancer Center, School of Medicine, Case Western Reserve University, Cleveland, OH, 44106, USA. pxr150@case.edu.
Department of Biochemistry, School of Medicine, Case Western Reserve University, Cleveland, OH, 44106, USA. pxr150@case.edu.

Classifications MeSH