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Microglial SMAD4 regulated by microRNA-146a promotes migration of microglia which support tumor progression in a glioma environment

Karthikeyan, Aparna, Gupta, Neelima, Tang, Carol, Mallilankaraman, Karthik, Silambarasan, Maskomani, Shi, Meng, Lu, Lei, Ang, Beng Ti +2 more·2018·Oncotarget
DOI 10.18632/oncotarget.25116PMC PMC5982777
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  • miRNAs targeting several genes regulate microglia behavior and functions in diverse CNS pathologies.

    “Recently, miRNAs targeting several genes are involved in regulating microglia behavior and functions in diverse CNS pathologies including ischemic brain injuries (Selvamani et al., 2012; Zhao et al., 2013; Karthikeyan et al., 2018), multiple sclerosis (Ponomarev et al., 2011) and prion disease (Saba et al., 2012; Slota and Booth, 2019).”

    From miR-142-3p Regulates BDNF Expression in Activated Rodent Microglia Through Its Target CAMK2A (2020) · cites this paper as Karthikeyan et al., 2018

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  1. [1]Shi Y Ping YF Zhang X Bian XW Hostile takeover: glioma stem cells recruit TAMs to support tumor progression Cell Stem Cell 2015 16 219 20 25748928
  2. [2]Erreni M Solinas G Brescia P Osti D Zunino F Colombo P Destro A Roncalli M Mantovani A Draghi R Levi D Rodriguez Y Baena R Gaetani P Human glioblastoma tumours and neural cancer stem cells express the chemokine CX3CL1 and its receptor CX3CR1 Eur J Cancer 2010 46 3383 92 20728344
  3. [3]Svensson A Özen I Genové G Paul G Bengzon J Endogenous brain pericytes are widely activated and contribute to mouse glioma microvasculature PLoS One 2015 10 e0123553 25875288 PMC4395339
  4. [4]Graeber MB Scheithauer BW Kreutzberg GW Microglia in brain tumors Glia 2002 40 252 59 12379912
  5. [5]Roggendorf W Strupp S Paulus W Distribution and characterization of microglia/macrophages in human brain tumors Acta Neuropathol 1996 92 288 93 8870831
  6. [6]Dheen ST Kaur C Ling EA Microglial activation and its implications in the brain diseases Curr Med Chem 2007 14 1189 97 17504139
  7. [7]Francos-Quijorna I Amo-Aparicio J Martinez-Muriana A López-Vales R IL-4 drives microglia and macrophages toward a phenotype conducive for tissue repair and functional recovery after spinal cord injury Glia 2016 64 2079 92 27470986
  8. [10]Tang Y Le W Differential roles of M1 and M2 microglia in neurodegenerative diseases Mol Neurobiol 2016 53 1181 94 25598354
  9. [11]Grimaldi A D’Alessandro G Golia MT Grössinger EM Di Angelantonio S Ragozzino D Santoro A Esposito V Wulff H Catalano M Limatola C KCa3.1 inhibition switches the phenotype of glioma-infiltrating microglia/macrophages Cell Death Dis 2016 7 e2174 27054329 PMC4855657
  10. [12]Prosniak M Harshyne LA Andrews DW Kenyon LC Bedelbaeva K Apanasovich TV Heber-Katz E Curtis MT Cotzia P Hooper DC Glioma grade is associated with the accumulation and activity of cells bearing M2 monocyte markers Clin Cancer Res 2013 19 3776 86 23741072
  11. [13]Szulzewsky F Pelz A Feng X Synowitz M Markovic D Langmann T Holtman IR Wang X Eggen BJ Boddeke HW Hambardzumyan D Wolf SA Kettenmann H Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1 PLoS One 2015 10 e0116644 25658639 PMC4320099
  12. [14]Gabrusiewicz K Rodriguez B Wei J Hashimoto Y Healy LM Maiti SN Thomas G Zhou S Wang Q Elakkad A Liebelt BD Yaghi NK Ezhilarasan R Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype JCI Insight 2016 1 1 PMC4784261 26973881
  13. [15]Ellert-Miklaszewska A Dabrowski M Lipko M Sliwa M Maleszewska M Kaminska B Molecular definition of the pro-tumorigenic phenotype of glioma-activated microglia Glia 2013 61 1178 90 23650109
  14. [16]Hambardzumyan D Gutmann DH Kettenmann H The role of microglia and macrophages in glioma maintenance and progression Nat Neurosci 2016 19 20 27 26713745 PMC4876023
  15. [17]Attisano L Wrana JL Signal transduction by the TGF-β superfamily Science 2002 296 1646 47 12040180
  16. [18]Chung KS Cho SH Shin JS Kim DH Choi JH Choi SY Rhee YK Hong HD Lee KT Ginsenoside Rh2 induces cell cycle arrest and differentiation in human leukemia cells by upregulating TGF-β expression Carcinogenesis 2013 34 331 40 23125221
  17. [20]Yuan JH Yang F Wang F Ma JZ Guo YJ Tao QF Liu F Pan W Wang TT Zhou CC Wang SB Wang YZ Yang Y A long noncoding RNA activated by TGF-β promotes the invasion-metastasis cascade in hepatocellular carcinoma Cancer Cell 2014 25 666 81 24768205
  18. [21]Juang YL Jeng YM Chen CL Lien HC PRRX2 as a novel TGF-β-induced factor enhances invasion and migration in mammary epithelial cell and correlates with poor prognosis in breast cancer Mol Carcinog 2016 55 2247 59 26824226
  19. [23]Bruna A Darken RS Rojo F Ocaña A Peñuelas S Arias A Paris R Tortosa A Mora J Baselga J Seoane J High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene Cancer Cell 2007 11 147 60 17292826
  20. [24]Eichhorn PJ Rodón L Gonzàlez-Juncà A Dirac A Gili M Martínez-Sáez E Aura C Barba I Peg V Prat A Cuartas I Jimenez J García-Dorado D USP15 stabilizes TGF-β receptor I and promotes oncogenesis through the activation of TGF-β signaling in glioblastoma Nat Med 2012 18 429 35 22344298
  21. [25]Verhaak RG Hoadley KA Purdom E Wang V Qi Y Wilkerson MD Miller CR Ding L Golub T Mesirov JP Alexe G Lawrence M O’Kelly M Cancer Genome Atlas Research Network Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 Cancer Cell 2010 17 98 110 20129251 PMC2818769
  22. [26]Hernanda PY Chen K Das AM Sideras K Wang W Li J Cao W Bots SJ Kodach LL de Man RA Ijzermans JN Janssen HL Stubbs AP SMAD4 exerts a tumor-promoting role in hepatocellular carcinoma Oncogene 2015 34 5055 68 25531314
  23. [27]Fullerton PT Jr Creighton CJ Matzuk MM Insights into SMAD4 loss in pancreatic cancer from inducible restoration of TGF-β signaling Mol Endocrinol 2015 29 1440 53 26284758 PMC4588735
  24. [28]Bardeesy N Cheng KH Berger JH Chu GC Pahler J Olson P Hezel AF Horner J Lauwers GY Hanahan D DePinho RA Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer Genes Dev 2006 20 3130 46 17114584 PMC1635148
  25. [29]Joseph JV Balasubramaniyan V Walenkamp A Kruyt FA TGF-β as a therapeutic target in high grade gliomas - promises and challenges Biochem Pharmacol 2013 85 478 85 23159669
  26. [30]Wesolowska A Kwiatkowska A Slomnicki L Dembinski M Master A Sliwa M Franciszkiewicz K Chouaib S Kaminska B Microglia-derived TGF-beta as an important regulator of glioblastoma invasion—an inhibition of TGF-beta-dependent effects by shrna against human TGF-beta type II receptor Oncogene 2008 27 918 30 17684491
  27. [31]Jadhav SP Kamath SP Choolani M Lu J Dheen ST microRNA-200b modulates microglia-mediated neuroinflammation via the cJun/MAPK pathway J Neurochem 2014 130 388 401 24749688
  28. [32]Patnala R Arumugam TV Gupta N Dheen ST HDAC inhibitor sodium butyrate-mediated epigenetic regulation enhances neuroprotective function of microglia during ischemic stroke Mol Neurobiol 2017 54 6391 6411 27722928
  29. [33]Karthikeyan A Patnala R Jadhav SP Eng-Ang L Dheen ST Micrornas: key players in microglia and astrocyte mediated inflammation in cns pathologies Curr Med Chem 2016 23 3528 46 27528056
  30. [34]Taganov KD Boldin MP Chang KJ Baltimore D NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses Proc Natl Acad Sci USA 2006 103 12481 86 16885212 PMC1567904
  31. [36]Saba R Sorensen DL Booth SA MicroRNA-146a: a dominant, negative regulator of the innate immune response Front Immunol 2014 5 578 25484882 PMC4240164
  32. [37]Mei J Bachoo R Zhang CL MicroRNA-146a inhibits glioma development by targeting Notch1 Mol Cell Biol 2011 31 3584 92 21730286 PMC3165557
  33. [38]Massagué J Seoane J Wotton D Smad transcription factors Genes Dev 2005 19 2783 810 16322555
  34. [39]Rhodes DR Yu J Shanker K Deshpande N Varambally R Ghosh D Barrette T Pandey A Chinnaiyan AM ONCOMINE: a cancer microarray database and integrated data-mining platform Neoplasia 2004 6 1 6 15068665 PMC1635162
  35. [40]Lukiw WJ Zhao Y Cui JG An NF-kappaB-sensitive micro RNA-146a-mediated inflammatory circuit in Alzheimer disease and in stressed human brain cells J Biol Chem 2008 283 31315 22 18801740 PMC2581572
  36. [42]Parkhurst CN Yang G Ninan I Savas JN Yates JR 3rd Lafaille JJ Hempstead BL Littman DR Gan WB Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor Cell 2013 155 1596 609 24360280 PMC4033691
  37. [44]Paolicelli RC Bolasco G Pagani F Maggi L Scianni M Panzanelli P Giustetto M Ferreira TA Guiducci E Dumas L Ragozzino D Gross CT Synaptic pruning by microglia is necessary for normal brain development Science 2011 333 1456 58 21778362
  38. [45]Kaur C Rathnasamy G Ling EA Biology of microglia in the developing brain J Neuropathol Exp Neurol 2017 76 736 53 28859332
  39. [46]Zhai H Heppner FL Tsirka SE Microglia/macrophages promote glioma progression Glia 2011 59 472 85 21264953 PMC3080032
  40. [47]Resende FF Bai X Del Bel EA Kirchhoff F Scheller A Titze-de-Almeida R Evaluation of TgH(CX3CR1-EGFP) mice implanted with mCherry-GL261 cells as an in vivo model for morphometrical analysis of glioma-microglia interaction BMC Cancer 2016 16 72 26856327 PMC4746826
  41. [48]Richter N Wendt S Georgieva PB Hambardzumyan D Nolte C Kettenmann H Glioma-associated microglia and macrophages/monocytes display distinct electrophysiological properties and do not communicate via gap junctions Neurosci Lett 2014 583 130 35 25261595 PMC4274622
  42. [49]Zheng Y Yang W Aldape K He J Lu Z Epidermal growth factor (EGF)-enhanced vascular cell adhesion molecule-1 (VCAM-1) expression promotes macrophage and glioblastoma cell interaction and tumor cell invasion J Biol Chem 2013 288 31488 95 24045955 PMC3814745
  43. [50]Nolte C Kirchhoff F Kettenmann H Epidermal growth factor is a motility factor for microglial cells in vitro: evidence for EGF receptor expression Eur J Neurosci 1997 9 1690 98 9283823
  44. [51]De Simone R Ambrosini E Carnevale D Ajmone-Cat MA Minghetti L NGF promotes microglial migration through the activation of its high affinity receptor: modulation by TGF-β J Neuroimmunol 2007 190 53 60 17868907
  45. [52]Suzumura A Sawada M Yamamoto H Marunouchi T Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro J Immunol 1993 151 2150 58 8345199
  46. [54]Spittau B Wullkopf L Zhou X Rilka J Pfeifer D Krieglstein K Endogenous transforming growth factor-beta promotes quiescence of primary microglia in vitro Glia 2013 61 287 300 23065670
  47. [55]Le Y Iribarren P Gong W Cui Y Zhang X Wang JM TGF-β1 disrupts endotoxin signaling in microglial cells through Smad3 and MAPK pathways J Immunol 2004 173 962 68 15240683
  48. [56]Tichauer JE von Bernhardi R Transforming growth factor-β stimulates β amyloid uptake by microglia through Smad3-dependent mechanisms J Neurosci Res 2012 90 1970 80 22715062
  49. [57]Liu X Qin Y Dai A Zhang Y Xue H Ni H Han L Zhu L Yuan D Tao T Cao M SMAD4 is involved in the development of endotoxin tolerance in microglia Cell Mol Neurobiol 2016 36 777 88 26758028 PMC11482473
  50. [58]Costello I Biondi CA Taylor JM Bikoff EK Robertson EJ Smad4-dependent pathways control basement membrane deposition and endodermal cell migration at early stages of mouse development BMC Dev Biol 2009 9 54 19849841 PMC2773778
  51. [59]Levy L Hill CS Smad4 dependency defines two classes of transforming growth factor {β} (TGF-{β}) target genes and distinguishes TGF-{β}-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses Mol Cell Biol 2005 25 8108 25 16135802 PMC1234333
  52. [60]Kong H Omran A Ashhab MU Gan N Peng J He F Wu L Deng X Yin F Changes in microglial inflammation-related and brain-enriched MicroRNAs expressions in response to in vitro oxygen-glucose deprivation Neurochem Res 2014 39 233 43 24338221
  53. [61]Alexandrov PN Dua P Lukiw WJ Up-regulation of miRNA-146a in progressive, age-related inflammatory neurodegenerative disorders of the human CNS Front Neurol 2014 5 181 25324823 PMC4179622
  54. [62]Deng M Du G Zhao J Du X miR-146a negatively regulates the induction of proinflammatory cytokines in response to Japanese encephalitis virus infection in microglial cells Arch Virol 2017 162 1495 505 28190197
  55. [63]Katakowski M Buller B Zheng X Lu Y Rogers T Osobamiro O Shu W Jiang F Chopp M Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth Cancer Lett 2013 335 201 04 23419525 PMC3665755
  56. [64]Kim YJ Hwang SY Hwang JS Lee JW Oh ES Han IO C6 glioma cell insoluble matrix components enhance interferon-γ-stimulated inducible nitric-oxide synthase/nitric oxide production in BV2 microglial cells J Biol Chem 2008 283 2526 33 17981810
  57. [65]Shen X Burguillos MA Osman AM Frijhoff J Carrillo-Jiménez A Kanatani S Augsten M Saidi D Rodhe J Kavanagh E Rongvaux A Rraklli V Nyman U Glioma-induced inhibition of caspase-3 in microglia promotes a tumor-supportive phenotype Nat Immunol 2016 17 1282 90 27618552
  58. [66]Mallilankaraman K Cárdenas C Doonan PJ Chandramoorthy HC Irrinki KM Golenár T Csordás G Madireddi P Yang J Müller M Miller R Kolesar JE Molgó J MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism Nat Cell Biol 2012 14 1336 43 23178883 PMC3511605
  59. [67]Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ ΔC(T)) Method Methods 2001 25 402 08 11846609

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Authors
Karthikeyan, A., Gupta, N., Tang, C., Mallilankaraman, K., Silambarasan, M., Shi, M., Lu, L., Ang, B. T., Ling, E.-A., & Dheen, S. T.
Affiliations
  • Department of Anatomy, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
  • Department of Research, National Neuroscience Institute, Singapore
  • Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
  • School of Biological Sciences, Nanyang Technological University, Singapore
Venue
Oncotarget
Publisher
Impact Journals, LLC
Published
2018-05-18
Volume
9
Issue
38
Pages
24950-24969
ISSN
1949-2553
DOI
10.18632/oncotarget.25116
PMC
PMC5982777
Cited by
22
References
6
Language
en

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