NLRP3 inflammasome couples purinergic signaling with activation of the complement cascade for the optimal release of cells from bone marrow.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
04 2019
04 2019
Historique:
received:
21
01
2019
accepted:
20
02
2019
revised:
17
02
2019
pubmed:
9
3
2019
medline:
10
8
2019
entrez:
9
3
2019
Statut:
ppublish
Résumé
The mechanisms that regulate egress of hematopoietic stem/progenitor cells (HSPCs) into peripheral blood (PB) in response to stress, inflammation, tissue/organ injury, or administration of mobilization-inducing drugs are still not well understood, and because of the importance of stem cell trafficking in maintaining organism homeostasis, several complementary pathways are believed to be involved. Our group proposes that mobilization of HSPCs is mainly a result of sterile inflammation in the bone marrow (BM) microenvironment in response to pro-mobilizing stimuli and that during the initiation phase of the mobilization process BM-residing cells belonging to the innate immunity system, including granulocytes and monocytes, release danger-associated molecular pattern molecules (DAMPs, also known as alarmins), reactive oxygen species (ROS), as well as proteolytic and lipolytic enzymes. These factors together orchestrate the release of HSPCs into PB. One of the most important DAMPs released in the initiation phase of mobilization is extracellular adenosine triphosphate, a potent activator of the inflammasome. As a result of its activation, IL-1β and IL-18 as well as other pro-mobilizing mediators, including DAMPs such as high molecular group box 1 (Hmgb1) and S100 calcium-binding protein A9 (S100a9), are released. These DAMPs are important activators of the complement cascade (ComC) in the mannan-binding lectin (MBL)-dependent pathway. Specifically, Hmgb1 and S100a9 bind to MBL, which leads to activation of MBL-associated proteases, which activate the ComC and in parallel also trigger activation of the coagulation cascade (CoaC). In this review, we will highlight the novel role of the innate immunity cell-expressed NLRP3 inflammasome, which, during the initiation phase of HSPC mobilization, couples purinergic signaling with the MBL-dependent pathway of the ComC and, in parallel, the CoaC for optimal release of HSPCs. These data are important to optimize the pharmacological mobilization of HSPCs.
Identifiants
pubmed: 30846866
doi: 10.1038/s41375-019-0436-6
pii: 10.1038/s41375-019-0436-6
pmc: PMC6477784
mid: NIHMS1024154
doi:
Substances chimiques
Inflammasomes
0
NLR Family, Pyrin Domain-Containing 3 Protein
0
Purines
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Pagination
815-825Subventions
Organisme : NIDDK NIH HHS
ID : R01 DK074720
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL134644
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL112788
Pays : United States
Références
Ratajczak MZ. A novel view of the adult bone marrow stem cell hierarchy and stem cell trafficking. Leukemia. 2015;29:776–82.
doi: 10.1038/leu.2014.346
Hoggatt J, Pelus LM. Many mechanisms mediating mobilization: an alliterative review. Curr Opin Hematol. 2011;18:231–8.
doi: 10.1097/MOH.0b013e3283477962
Schuettpelz LG, Link DC. Regulation of hematopoietic stem cell activity by inflammation. Front Immunol. 2013;4:204.
doi: 10.3389/fimmu.2013.00204
Nguyen TS, Lapidot T, Ruf W. Extravascular coagulation in hematopoietic stem and progenitor cell regulation. Blood. 2018;132:123–31.
doi: 10.1182/blood-2017-12-768986
Tay J, Levesque JP, Winkler IG. Cellular players of hematopoietic stem cell mobilization in the bone marrow niche. Int J Hematol. 2017;105:129–40.
doi: 10.1007/s12185-016-2162-4
Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N, Moseman EA, et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 2007;131:994–1008.
doi: 10.1016/j.cell.2007.09.047
Levesque JP, Helwani FM, Winkler IG. The endosteal ‘osteoblastic’ niche and its role in hematopoietic stem cell homing and mobilization. Leukemia. 2010;24:1979–92.
doi: 10.1038/leu.2010.214
Mendez-Ferrer S, Chow A, Merad M, Frenette PS. Circadian rhythms influence hematopoietic stem cells. Curr Opin Hematol. 2009;16:235–42.
doi: 10.1097/MOH.0b013e32832bd0f5
Borkowska S, Suszynska M, Ratajczak J, Ratajczak MZ. Evidence of a pivotal role for the distal part of the complement cascade in the diurnal release of hematopoietic stem cells into peripheral blood. Cell Transplant. 2016;2:275–82.
doi: 10.3727/096368915X688489
Itkin T, Kumari A, Schneider E, Gur-Cohen S, Ludwig C, Brooks R, et al. MicroRNA-155 promotes G-CSF-induced mobilization of murine hematopoietic stem and progenitor cells via propagation of CXCL12 signaling. Leukemia. 2017;31:1247–50.
doi: 10.1038/leu.2017.50
Ratajczak MZ, Adamiak M. Membrane lipid rafts, master regulators of hematopoietic stem cell retention in bone marrow and their trafficking. Leukemia. 2015;7:1452–7.
doi: 10.1038/leu.2015.66
Borkowska S, Suszynska M, Mierzejewska K, Ismail A, Budkowska M, Salata D, et al. Novel evidence that crosstalk between the complement, coagulation and fibrinolysis proteolytic cascades is involved in mobilization of hematopoietic stem/progenitor cells (HSPCs). Leukemia. 2014;28:2148–54.
doi: 10.1038/leu.2014.115
Ratajczak MZ, Kim CH, Wojakowski W, Janowska-Wieczorek A, Kucia M, Ratajczak J. Innate immunity as orchestrator of stem cell mobilization. Leukemia. 2010;24:1667–75.
doi: 10.1038/leu.2010.162
Ratajczak MZ, Adamiak M, Plonka M, Abdel-Latif A, Ratajczak J. Mobilization of hematopoietic stem cells as a result of innate immunity-mediated sterile inflammation in the bone marrow microenvironment-the involvement of extracellular nucleotides and purinergic signaling. Leukemia. 2018;32:1116–23.
doi: 10.1038/s41375-018-0087-z
Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10:826–37.
doi: 10.1038/nri2873
Winkler IG, Pettit AR, Raggatt LJ, Jacobsen RN, Forristal CE, Barbier V, et al. Hematopoietic stem cell mobilizing agents G-CSF, cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation. Leukemia. 2012;26:1594–601.
doi: 10.1038/leu.2012.17
Golan K, Vagima Y, Ludin A, Itkin T, Cohen-Gur S, Kalinkovich A, et al. S1P promotes murine progenitor cell egress and mobilization via S1P1-mediated ROS signaling and SDF-1 release. Blood. 2012;119:2478–88.
doi: 10.1182/blood-2011-06-358614
Adamiak M, Poniewierska-Baran A, Borkowska S, Schneider G, Abdelbaset-Ismail A, Suszynska M, et al. Evidence that a lipolytic enzyme—hematopoietic-specific phospholipase C-β2—promotes mobilization of hematopoietic stem cells by decreasing their lipid raft-mediated bone marrow retention and increasing the promobilizing effects of granulocytes. Leukemia. 2016;30:919–28.
doi: 10.1038/leu.2015.315
Adamiak M, Bujko K, Cymer M, Plonka M, Glaser T, Kucia M, et al. Novel evidence that extracellular nucleotides and purinergic signaling induce innate immunity-mediated mobilization of hematopoietic stem/progenitor cells. Leukemia. 2018;32:1920–31.
doi: 10.1038/s41375-018-0122-0
Lemoli RM, Ferrari D, Fogli M, Rossi L, Pizzirani C, Forchap S, et al. Extracellular nucleotides are potent stimulators of human hematopoietic stem cells in vitro and in vivo. Blood. 2004;104:1662–70.
doi: 10.1182/blood-2004-03-0834
Groslambert M, Py BF. Spotlight on the NLRP3 inflammasome pathway. J Inflamm Res. 2018;11:359–74.
doi: 10.2147/JIR.S141220
He Y, Hara H, Núñez G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem Sci. 2016;41:1012–21.
doi: 10.1016/j.tibs.2016.09.002
Place DE, Kanneganti TD. Recent advances in inflammasome biology. Curr Opin Immunol. 2018;50:32–38.
doi: 10.1016/j.coi.2017.10.011
Malik A, Kanneganti TD. Function and regulation of IL-1α in inflammatory diseases and cancer. Immunol Rev. 2018;281:124–37.
doi: 10.1111/imr.12615
Fibbe WE, Hamilton MS, Laterveer LL, Kibbelaar RE, Falkenburg JH, Visser JW, et al. Sustained engraftment of mice transplanted with IL-1-primed blood-derived stem cells. J Immunol. 1992;148:417–21.
pubmed: 1345921
Adamiak M, Abdelbaset-Ismail A, Suszynska M, Abdel-Latif A, Ratajczak J, Ratajczak MZ. Novel evidence that the mannan-binding lectin pathway of complement activation plays a pivotal role in triggering mobilization of hematopoietic stem/progenitor cells by activation of both the complement and coagulation cascades. Leukemia. 2017;31:262–5.
doi: 10.1038/leu.2016.278
Masters SL, Gerlic M, Metcalf D, Preston S, Pellegrini M, O’Donnell JA, et al. NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity. 2012;37:1009–23.
doi: 10.1016/j.immuni.2012.08.027
Tuncer S, Fiorillo MT, Sorrentino R. The multifaceted nature of NLRP12. J Leukoc Biol. 2014;96:991–1000.
doi: 10.1189/jlb.3RU0514-265RR
Denes A, Coutts G, Lénárt N, Cruickshank SM, Pelegrin P, Skinner J, et al. AIM2 and NLRC4 inflammasomes contribute with ASC to acute brain injury independently of NLRP3. Proc Natl Acad Sci USA. 2015;112:4050–5.
doi: 10.1073/pnas.1419090112
Marquez-Curtis LA, Turner AR, Sridharan S, Ratajczak MZ, Janowska-Wieczorek A. The ins and outs of hematopoietic stem cells: studies to improve transplantation outcomes. Stem Cell Rev. 2011;3:590–607.
doi: 10.1007/s12015-010-9212-8
Di A, Xiong S, Ye Z, Malireddi RKS, Kometani S, Zhong M, et al. The TWIK2 potassium efflux channel in macrophages mediates NLRP3 inflammasome-Induced inflammation. Immunity. 2018;49:56–65.e4.
doi: 10.1016/j.immuni.2018.04.032
Velders GA, van Os R, Hagoort H, Verzaal P, Guiot HF, Lindley IJ, et al. Reduced stem cell mobilization in mice receiving antibiotic modulation of the intestinal flora: involvement of endotoxins as cofactors in mobilization. Blood. 2004;103:340–6.
doi: 10.1182/blood-2002-07-2270
Schuettpelz LG, Borgerding JN, Christopher MJ, Gopalan PK, Romine MP, Herman AC, et al. G-CSF regulates hematopoietic stem cell activity, in part, through activation of Toll-like receptor signaling. Leukemia. 2014;28:1851–60.
doi: 10.1038/leu.2014.68
Gonzalez-Nieto D, Li L, Kohler A, Ghiaur G, Ishikawa E, Sengupta A, et al. Connexin-43 in the osteogenic BM niche regulates its cellular composition and the bidirectional traffic of hematopoietic stem cells and progenitors. Blood. 2012;119:5144–54.
doi: 10.1182/blood-2011-07-368506
Burnstock G. An introduction to the roles of purinergic signalling in neurodegeneration, neuroprotection and neuroregeneration. Neuropharmacology. 2016;104:4–17.
doi: 10.1016/j.neuropharm.2015.05.031
Koldej R, Collins J, Ritchie D. P2X7 polymorphisms and stem cell mobilisation. Leukemia. 2018;32:2724–6.
doi: 10.1038/s41375-018-0232-8
Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol. 2011;11:201–12.
doi: 10.1038/nri2938
Pruijt JF, Verzaal P, Van Os R, de Kruijf EJ, van Schie ML, Mantovani A, et al. Neutrophils are indispensable for hematopoietic stem cell mobilization induced by interleukin-8 in mice. Proc Natl Acad Sci USA. 2002;99:6228–33.
doi: 10.1073/pnas.092112999
Levesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ. Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol. 2002;30:440–9.
doi: 10.1016/S0301-472X(02)00788-9
Wysoczynski M, Ratajczak J, Pedziwiatr D, Rokosh G, Bolli R, Ratajczak MZ. Identification of heme oxygenase 1 (HO-1) as a novel negative regulator of mobilization of hematopoietic stem/progenitor cells. Stem Cell Rev. 2015;11:110–8.
doi: 10.1007/s12015-014-9547-7
Adamiak M, Abdelbaset-Ismail A, Moore JB 4th, Zhao J, Abdel-Latif A, Wysoczynski M, et al. Inducible nitric oxide synthase (iNOS) is a novel negative regulator of hematopoietic stem/progenitor cell trafficking. Stem Cell Rev. 2017;13:92–103.
doi: 10.1007/s12015-016-9693-1
Nurmi K, Kareinen I, Virkanen J, Rajamäki K, Kouri VP, Vaali K, et al. Hemin and Cobalt protoporphyrin inhibit NLRP3 inflammasome activation by enhancing autophagy: a novel mechanism of inflammasome regulation. J Innate Immun. 2017;9:65–82.
doi: 10.1159/000448894
Hernandez-Cuellar E, Tsuchiya K, Hara H, Fang R, Sakai S, Kawamura I, et al. Cutting edge: nitric oxide inhibits the NLRP3 inflammasome. J Immunol. 2012;189:5113–7.
doi: 10.4049/jimmunol.1202479
Abdelbaset-Ismail A, Borkowska-Rzeszotek S, Kubis E, Bujko K, Brzeźniakiewicz-Janus K, Bolkun L, et al. Activation of the complement cascade enhances motility of leukemic cells by downregulating expression of HO-1. Leukemia. 2017;31:446–58.
doi: 10.1038/leu.2016.198
Adamiak M, Bujko K, Lenkiewicz A, Kucia M, Ratajczak J, Ratajczak MZ. Novel evidence that the ectonucleotidases CD39 and CD73, which are expressed on hematopoietic stem/progenitor cells (HSPCs), regulate mobilization and homing - studies in CD39-/- and CD73-/- mice and with small-molecule CD39 and CD73 inhibitors. Blood. 2018;132:2060.
Hoggatt J, Singh P, Tate TA, Chou BK, Datari SR, Fukuda S, et al. Rapid mobilization reveals a highly engraftable hematopoietic stem cell. Cell. 2018;172:191–204.e10.
doi: 10.1016/j.cell.2017.11.003
Ratajczak MZ, Bartke A, Darzynkiewicz Z. Prolonged growth hormone/insulin/insulin-like growth factor nutrient response signaling pathway as a silent killer of stem cells and a culprit in aging. Stem Cell Rev. 2017;13:443–53.
doi: 10.1007/s12015-017-9728-2
Bhartiya D. Pluripotent stem cells in adult tissues: struggling to be acknowledged over two decades. Stem Cell Rev. 2017;13:713–24.
doi: 10.1007/s12015-017-9756-y
Smadja DM. Bone marrow very small embryonic-like stem cells: new generation of autologous cell therapy soon ready for prime time? Stem Cell Rev. 2017;13:198–201.
doi: 10.1007/s12015-017-9718-4
Lee HM, Wysoczynski M, Liu R, Shin DM, Kucia M, Botto M, et al. Mobilization studies in complement-deficient mice reveal that optimal AMD3100 mobilization of hematopoietic stem cells depends on complement cascade activation by AMD3100-stimulated granulocytes. Leukemia. 2010;24:573–82.
doi: 10.1038/leu.2009.271
Lee HM, Wu W, Wysoczynski M, Liu R, Zuba-Surma EK, Kucia M, et al. Impaired mobilization of hematopoietic stem/progenitor cells in C5-deficient mice supports the pivotal involvement of innate immunity in this process and reveals novel promobilization effects of granulocytes. Leukemia. 2009;23:2052–62.
doi: 10.1038/leu.2009.158
Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med. 2006;12:682–7.
doi: 10.1038/nm1419
Ratajczak MZ, Lee H, Wysoczynski M, Wan W, Marlicz W, Laughlin MJ, et al. Novel insight into stem cell mobilization-plasma sphingosine-1-phosphate is a major chemoattractant that directs the egress of hematopoietic stem progenitor cells from the bone marrow and its level in peripheral blood increases during mobilization due to activation of complement cascade/membrane attack complex. Leukemia. 2010;24:976–85.
doi: 10.1038/leu.2010.53
Juarez JG, Harun N, Thien M, Welschinger R, Baraz R, Pena AD, et al. Sphingosine-1-phosphate facilitates trafficking of hematopoietic stem cells and their mobilization by CXCR4 antagonists in mice. Blood. 2012;119:707–16.
doi: 10.1182/blood-2011-04-348904
Adamiak M, Chelvarajan L, Lynch KR, Santos WL, Abdel-Latif A, Ratajczak MZ. Mobilization studies in m ice deficient in sphingosine kinase 2 support a crucial role of the plasma level of sphingosine-1-phosphate in the egress of hematopoietic stem progenitor cells. Oncotarget. 2017;39:65588–600.
Mierzejewska K, Klyachkin YM, Ratajczak J, Abdel-Latif A, Kucia M, Ratajczak MZ. Sphingosine-1-phosphate-mediated mobilization of hematopoietic stem/progenitor cells during intravascular hemolysis requires attenuation of SDF-1-CXCR4 retention signaling in bone marrow. Biomed Res Int. 2013;2013:814549.
doi: 10.1155/2013/814549
Kim CH, Wu W, Wysoczynski M, Abdel-Latif A, Sunkara M, Morris A, et al. Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: a novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia. 2012;26:106–16.
doi: 10.1038/leu.2011.185
Adamiak M, Borkowska S, Wysoczynski M, Suszynska M, Kucia M, Rokosh G, et al. Evidence for the involvement of sphingosine-1-phosphate in the homing and engraftment of hematopoietic stem cells to bone marrow. Oncotarget. 2015;6:18819–28.
doi: 10.18632/oncotarget.4710
Cypryk W, Nyman TA, Matikainen S. From inflammasome to exosome-does extracellular vesicle secretion constitute an inflammasome-dependent immune response? Front Immunol. 2018;9:2188.
doi: 10.3389/fimmu.2018.02188
Frame JM, Long T, Schuster-Kubaczka C, Esain V, Lim SE, Daley GQ, et al. Inflammasome-mediated regulation of hematopoiesis in the vertebrate embryo. Blood. 2018;132:330.
Baryawno N, Severe N, Scadden DT. Hematopoiesis: reconciling historic controversies about the niche. Cell Stem Cell. 2017;5:590–2.
doi: 10.1016/j.stem.2017.03.025
Mendelson A, Frenette PS. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat Med. 2014;8:833–46.
doi: 10.1038/nm.3647
Sallman DA, Cluzeau T, Basiorka AA, List A. Unraveling the pathogenesis of MDS: the NLRP3 inflammasome and pyroptosis drive the MDS phenotype. Front Oncol. 2016;6:151.
doi: 10.3389/fonc.2016.00151
Kovtonyuk LV, Fritsch K, Feng X, Manz MG, Takizawa H. Inflamm-aging of hematopoiesis, hematopoietic stem cells, and the bone marrow microenvironment. Front Immunol. 2016;7:502.
doi: 10.3389/fimmu.2016.00502
Linz BM, Neely CJ, Kartchner LB, Mendoza AE, Khoury AL, Truax A, et al. Innate immune cell recovery is positively regulated by NLRP12 during emergency hematopoiesis. J Immunol. 2017;198:2426–33.
doi: 10.4049/jimmunol.1601048