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The goal of NeuroMac

The main goal of the second funding period is to better understand the molecular mechanisms of myeloid cell diversity in the CNS and the interactions of microglia with neurons and other glial cells during development, health and perturbation. In detail, we want to:

  • explore the molecular mechanisms determining myeloid cell identity in the healthy and diseased CNS (Area A)
  • examine the spatial distribution of brain myeloid cells (Area A)
  • identify the cellular mechanisms for the establishment context-associated microglia states and for the interactions of myeloid cells with other cells in the affected CNS (Areas A, B)
  • use myeloid cells therapeutically in preclinical models of CNS diseases (Area B)
Research Program

News

Publications

Wogram E, Prinz M: APOE set the microglia free. Nat Immunol 24(11):1790-1791; doi: 10.1038/s41590-023-01651-6 (2023).

Faust TE, Feinberg PA, O’Connor C, Kawaguchi R, Chan A, Strasburger H, Frosch M, Boyle MA, Masuda T, Amann L, Knobeloch K-P, Prinz M, Schaefer A, Schafer DP: A comparative analysis of microglial inducible Cre lines. Cell Rep 42(9):113031; doi: 10.1016/j.celrep.2023.113031 (2023).

Lauer EM, Riegler E, Mutter JA, Alig SK, Bleul S, Kuehn J, Ranganathan L, Klingler C, Demerath T, Würtemberger U, Rau A, Weiß J, Eisenblaetter M, Bamberg F, Prinz M, Finke J, Duyster J, Illerhaus G, Diehn M, Alizadeh AA, Schorb E, Reinacher PC, and Scherer F: Improved early outcome prediction by MRI-based 3D tumor volume assessment in patients with CNS lymphomas. Neuro Oncol noad177; doi: 10.1093/neuonc/noad177 (2023).

Forde AJ, Kolter J, Zwicky P, Baasch S, Lohrmann F, Eckert M, Gres V, Lagies S, Gorka O, Rambold AS, Buescher JM, Kammerer B, Lachmann N, Prinz M, Groß O, Pearce EJ, Becher B, Henneke P: Metabolic rewiring tunes dermal macrophages in staphylococcal skin infection. Sci Immunol 8(86):eadg3517; doi: 10.1126/sciimmunol.adg3517 (2023).

Macpherson AJ, Pachnis V, Prinz M: Boundaries and integration between microbiota, the nervous system, and immunity. Immunity 56(8):1712-1726; doi: 10.1016/j.immuni.2023.07.011 (2023).

Apostolova P, Kreutmair S, Toffalori C, Punta M, Unger S, Burk A-C, Wehr C, Maas-Bauer K, Melchinger W, Haring E, Hoefflin R, Shoumariyeh K, Hupfer V, Lauer EM, Duquesne S, Lowinus T, Núñez NG, Alberti C, da Costa Pereira S, Merten CH, […], Boerries M, […], Zeiser R: Phase II trial of hypomethylating agent combined with nivolumab for acute myeloid leukaemia relapse after allogeneic haematopoietic cell transplantation—Immune signature correlates with response. Br J Haematol; doi: 10.1111/bjh.19007 (2023).

Gulen MF, Samson N, Keller A, Schwabenland M, Liu C, Glück S, Thacker VV, Favre L, Mangeat B, Kroese LJ, Krimpenfort P, Prinz M, Ablasser A: cGAS-STING drives ageing-related inflammation and neurodegeneration . Nature 620(7973):374-380; doi: 10.1038/s41586-023-06373-1 (2023).

Langenbach M, Giesler S, Richtsfeld S, Costa-Pereira S, Rindlisbacher L, Wertheimer T, Braun LM, Andrieux G, Duquesne S, Pfeifer D, Woessner NM, Menssen HD, Taromi S, Duyster J, Börries M, Brummer T, Blazar BR, Minguet S, Turko P, Levesque MP, Becher B, Zeiser R: MDM2 Inhibition Enhances Immune Checkpoint Inhibitor Efficacy by Increasing IL15 and MHC Class II Production. Mol Cancer Res 21(8):849-864; doi: 10.1158/1541-7786.MCR-22-0898 (2023).

Frumer GR, Shin S-H, Jung S, Kim J-S: Not just Glia-Dissecting brain macrophages in the mouse. Glia, doi: 10.1002/glia.24445 (2023).

Lenz M, Eichler A, Kruse P, Galanis C, Kleidonas D, Andrieux G, Boerries M, Jedlicka P, Müller U, Deller T, Vlachos A: The Amyloid Precursor Protein Regulates Synaptic Transmission at Medial Perforant Path Synapses. J Neurosci 43(29):5290-5304; doi: 10.1523/JNEUROSCI.1824-22.2023 (2023).

Kopp MA, Meisel C, Liebscher T, Watzlawick R, Cinelli P, Schweizerhof O, Blex C, Lübstorf T, Prilipp E, Niedeggen A, Druschel C, Schaser K-D, Wanner GA, Curt A, Lindemann G, Nugeva N, Fehlings MG, Vajkoczy P, Cabraja M, Dengler J, Ertel W, Ekkernkamp A, Rehahn K, Martus P, Volk H-D, Unterwalder N, Kölsch U, Brommer B, Hellmann RC, Baumgartner E, Hirt J, Geurtz L-C, Ossami Saidy RR, Prüss H, Laginha I, Failli V, Grittner U, Dirnagl U, Schwab JM: The spinal cord injury-induced immune deficiency syndrome: results of the SCIentinel study. Brain 146(8):3500-3512; doi: 10.1093/brain/awad092 (2023).

Frosch M, Amann L, Prinz M: CNS-associated macrophages shape the inflammatory response in a mouse model of Parkinson’s disease. Nat Commun 14(1), 3753. doi: 10.1038/s41467-023-39061-9 (2023).

Zeiser R, Prinz M: Immune checkpoint inhibitor induced neurocognitive deficits in patients. Brain Commun 5(3), fcad186; doi: 10.1093/braincomms/fcad186 (2023).

Kleidonas D, Kirsch M, Andrieux G, Pfeifer D, Boerries M, Vlachos A: Microglia modulate TNFα-mediated synaptic plasticity. Glia (Online ahead of print). Open access. doi: 10.1002/glia.24383 (2023).

Schwabenland M, Mossad O, Sievert A, Peres AG, Ringel E, Baasch S, Kolter J, Cascone G, Dokalis N, Vlachos A, Ruzsics Z, Henneke P, Prinz M, Blank T: Neonatal immune challenge poses a sex-specific risk for epigenetic microglial reprogramming and behavioral impairment. Nat Commun 14(1):2721; doi: 10.1038/s41467-023-38373-0 (2023).

Kragesteen BK, Giladi A, David E, Halevi S, Geirsdóttir L, Lempke OM, Li B, Bapst AM, Xie K, Katzenelenbogen Y, Dahl S, Sheban F, Gurevich-Shapiro A, Zada M, Phan TS, Avellino R, Wang S-Y, Barboy O, Shlomi-Loubaton S, Winning S, Markwerth PP, Dekalo S, Keren-Shaul H, Kedmi M, […] Amit I: The transcriptional and regulatory identity of erythropoietin producing cells. Nature Medicine 29, 1191–1200 (2023).

Eichler A, Kleidonas D, Turi Z, Fliegauf M, Kirsch M, Pfeifer D, Masuda T, Prinz M, Lenz M, Vlachos A: Microglial Cytokines Mediate Plasticity Induced by 10 Hz Repetitive Magnetic Stimulation. J Neurosci 43(17), 3042–3060; doi: 10.1523/JNEUROSCI.2226-22.2023 (2023).

Banerjee P, Mehta AR, Nirujogi RS, Cooper J, James OG, Nanda J, Longden J, Burr K, McDade K, Salzinger A, Paza E, Newton J, Story D, Pal S, Smith C, Alessi DR, Selvaraj BT, Priller J, Chandran S: Cell-autonomous immune dysfunction driven by disrupted autophagy in C9orf72-ALS iPSC-derived microglia contributes to neurodegeneration. Sci Adv 9(16), eabq0651; doi: 10.1126/sciadv.abq0651 (2023).

Petry P, Oschwald A, Kierdorf K: Microglial tissue surveillance: The never-resting gardener in the developing and adult CNS. Eur J Immunol e2250232; doi: 10.1002/eji.202250232 (2023).

Lenz M, Eichler A, Kruse P, Stöhr P, Kleidonas D, Galanis C, Lu H, Vlachos A: Denervated mouse CA1 pyramidal neurons express homeostatic synaptic plasticity following entorhinal cortex lesion. Front Mol Neurosci 16, 1148219. Open access. doi: 10.3389/fnmol.2023.1148219 (2023).

Rigat L, Ouk K, Kramer A, Priller J: Dysfunction of circadian and sleep rhythms in the early stages of Alzheimer’s disease. Acta Physiol (Oxf);e13970; doi: 10.1111/apha.13970 (2023).

Topczewska PM, Rompe ZA, Jakob MO, Stamm A, Leclère PS, Preußer A, Duerr CU, Thole LML, Kotsch K, Artis D, Klose CSN: ILC2 require cell-intrinsic ST2 signals to promote type 2 immune responses. Front Immunol 14:1130933; doi: 10.3389/fimmu.2023.1130933 (2023).

Eichler A, Kleidonas D, Turi Z, Fliegauf M, Kirsch M, Pfeifer D, Masuda T, Prinz M, Lenz M, Vlachos A: Microglial Cytokines Mediate Plasticity Induced by 10 Hz Repetitive Magnetic Stimulation. J Neurosci JN-RM-2226-22; doi: 10.1523/JNEUROSCI.2226-22.2023 (2023).

Zeiser R, Chen Y-B, Youssef NN, Ayuk F: Pathophysiology of gastrointestinal acute graft-versus-host disease and the potential role of glucagon-like peptide 2. Br J Haematol 201(4), 620-627; doi: 10.1111/bjh.18778 (2023).

Jakob MO, Spari D, Sànchez Taltavull D, Salm L, Yilmaz B, Doucet Ladevèze R, MooserC, Pereyra D, Ouyang Y, Schmidt T, Mattiola I, Starlinger P, Stroka D, Tschan F, Candinas D, Gasteiger G, Klose CSN, Diefenbach A, Gomez de Agüero M, Beldi G: ILC3s restrict the dissemination of intestinal bacteria to safeguard liver regeneration after surgery. Cell Rep 42(3):112269; doi: 10.1016/j.celrep.2023.112269 (2023).

Mass E, Nimmerjahn F, Kierdorf K and Schlitzer A.Tissue-specific macrophages: how they develop and choreograph tissue biology. Nat Rev Immunol 1–17; doi: 10.1038/s41577-023-00848-y (2023).

Amann L, Masuda T, Prinz M: Mechanisms of myeloid cell entry to the healthy and diseased central nervous system. Nat Immunol 24(3):393-407; doi: 10.1038/s41590-022-01415-8 (2023).

De Schepper S, Ge JZ, Crowley G, Ferreira LSS, Garceau D, Toomey CE, Sokolova D, Rueda-Carrasco J, Shin S-H, Kim J-S, Childs T, Lashley T, Burden JJ, Sasner M, Frigerio CS, Jung S, Hong S: Perivascular cells induce microglial phagocytic states and synaptic engulfment via SPP1 in mouse models of Alzheimer’s disease. Nat Neurosci 26(3): 406–415; doi: 10.1038/s41593-023-01257-z (2023).

Griewahn L, Müller-Foxworth M, Peintner L, Wissler M, Weiss M, Brauns-Schubert P, Massoumi R, Borner C, Groß O, Yabal M, Charvet C, Maurer U: SPATA2 restricts OTULIN-dependent LUBAC activity independently of CYLD. Cell Rep 42(1):111961; doi: 10.1016/j.celrep.2022.111961 (2023).

Thelen B, Schipperges V, Knörlein P, Hummel JF, Arnold F, Kupferschmid L, Klose CSN, Arnold SJ, Boerries M, Tanriver Y: Eomes is sufficient to regulate IL-10 expression and cytotoxic effector molecules in murine CD4+ T cells. Front Immunol 14:1058267; doi: 10.3389/fimmu.2023.1058267 (2023).

Neuwirt E, Magnani G, Ćiković T, Wöhrle S, Fischer L, Kostina A, Flemming S, Fischenich NJ, Saller BS, Gorka O, Renner S, Agarinis C, Parker CN, Boettcher A, Farady CJ, Kesselring R, Berlin C, Backofen R, Rodriguez-Franco M, Kreutz C, Prinz M, Tholen M, Reinheckel T, Ott T, Groß CJ, Jost PJ, Groß O: Tyrosine kinase inhibitors can activate the NLRP3 inflammasome in myeloid cells through lysosomal damage and cell lysis. Sci Signal 16(768):eabh1083; doi: 10.1126/scisignal.abh1083 (2023).

Giacomello G, Otto C, Priller J, Ruprecht K, Böttcher C, Parr MK: 1,2-13C2-Glucose Tracing Approach to Assess Metabolic Alterations of Human Monocytes under Neuroinflammatory Conditions. Curr Issues Mol Biol 45(1):765-781; doi: 10.3390/cimb45010051 (2023).

Wallach T, Raden M, Hinkelmann L, Brehm M, Rabsch D, Weidling H, Krüger C, Kettenmann H, Backofen R, Lehnardt S: Distinct SARS-CoV-2 RNA fragments activate Toll-like receptors 7 and 8 and induce cytokine release from human macrophages and microglia. Front Immunol, 13; doi.org/10.3389/fimmu.2022.1066456 (2023).

Faust TE, Feinberg PA, O’Connor C, Kawaguchi R, Chan A, Strasburger H, Masuda T, Amann L, Knobeloch KP, Prinz M, Schaefer A and Schafer DP: A comparative analysis of microglial inducible Cre lines. bioRxiv; doi: 10.1101/2023.01.09.523268 (2023).

Rapp J, Jung M, Klar RFU, Wolf J, Arnold J, Gorka O, Groß O, Lange C, Agostini H, Schlunck G, Bucher F: STAT3 signaling induced by the IL-6 family of cytokines modulates angiogenesis. J Cell Sci 136(1):jcs260182; doi: 10.1242/jcs.260182 (2023).

Voss M, Pinkert S, Kespohl M, Gimber N, Klingel K, Schmoranzer J, Laue M, Gaida M, Kloetzel P-M, Beling A: A Conserved Cysteine Residue in Coxsackievirus B3 Protein 3A with Implication for Elevated Virulence. Viruses 14(4), 769, doi: 10.3390/v14040769 (2022).