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Mcl-1 is vital for neutrophil survival

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Abstract

Upon entry to the systemic circulation, neutrophils exhibit a short mean time to cell death. The viability of most cell types in a steady state is preserved by the interplay of the Bcl-2 family of proteins, wherein the anti-apoptotic members inhibit the action of their pro-apoptotic counterparts. Neutrophils, however, display absent or severely reduced expression of several anti-apoptotic Bcl-2 family proteins. Hence, they rely on the expression of Mcl-1, an anti-apoptotic member of the Bcl-2 family, for survival. This protein is uniquely short-lived relative to related proteins and its loss likely precipitates the induction of apoptosis in neutrophils. This review describes the role of Mcl-1 in the neutrophil in the context of apoptosis and highlights the proteins’ importance to the cell. We also address neutrophil apoptosis in the broader context of the cells’ response to pathogens, focussing particularly on the strategies used by pathogens to manipulate the apoptotic pathway to their own ends.

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References

  1. Butterfield TA, Best TM, Merrick MA. The dual roles of neutrophils and macrophages in inflammation: a critical balance between tissue damage and repair. J Athl Train. 2006;41:457–65.

    PubMed Central  PubMed  Google Scholar 

  2. Summers C, Rankin SM, Condliffe AM, Singh N, Peters AM, Chilvers ER. Neutrophil kinetics in health and disease. Trends Immunol. 2010;31:318–24.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Tak T, Tesselaar K, Pillay J, Borghans JA, Koenderman L. What’s your age again? Determination of human neutrophil half-lives revisited. J Leukoc Biol. 2013;94:595–601.

    Article  CAS  PubMed  Google Scholar 

  4. Dancey JT, Deubelbeiss KA, Harker LA, Finch CA. Neutrophil kinetics in man. J Clin Invest. 1976;58:705–15.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Begley CG, Lopez AF, Nicola NA. Purified colony-stimulating factors enhance the survival of human neutrophils and eosinophils in vitro: a rapid and sensitive microassay for colony-stimulating factors. Blood. 1986;68:162–6.

    CAS  PubMed  Google Scholar 

  6. Lopez AF, Williamson DJ, Gamble JR, Begley CG, Harlan JM, et al. Recombinant human granulocyte-macrophage colony-stimulating factor stimulates in vitro mature human neutrophil and eosinophil function, surface receptor expression, and survival. J Clin Invest. 1986;78:1220–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood. 1992;80:2012–20.

    CAS  PubMed  Google Scholar 

  8. Dunican AL, Leuenroth SJ, Grutkoski P, Ayala A, Simms HH. TNFα-induced suppression of PMN apoptosis is mediated through interleukin-8 production. Shock. 2000;14:284–9.

    Article  CAS  PubMed  Google Scholar 

  9. Klausen P, Bjerregaard MD, Borregaard N, Cowland JB. End-stage differentiation of neutrophil granulocytes in vivo is accompanied by up-regulation of p27kip1 and down-regulation of CDK2, CDK4, and CDK6. J Leukoc Biol. 2004;75:569–78.

    Article  CAS  PubMed  Google Scholar 

  10. Moulding DA, Quayle JA. Anthony Hart C, Edwards SW. Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood. 1998;92:2495–502.

    CAS  PubMed  Google Scholar 

  11. Moulding DA, Giles RV, Spiller DG, White MRH, Tidd DM, Edwards SW. Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood. 2000;96:1756–63.

    CAS  PubMed  Google Scholar 

  12. Moulding DA, Akgul C, Derouet M, White MRH, Edwards SW. BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukocyte Biol. 2001;70:783–92.

    CAS  PubMed  Google Scholar 

  13. Xiao K, Chen P, Chang DC. The VTLISFG motif in the BH1 domain plays a significant role in regulating the degradation of Mcl-1. FEBS Open Bio. 2014;4:147–52.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Rossi AG, Sawatzky DA, Walker A, Ward C, Sheldrake TA, et al. Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat Med. 2006;12:1056–64.

    Article  CAS  PubMed  Google Scholar 

  15. Leitch AE, Lucas CD, Marwick JA, Duffin R, Haslett C, Rossi AG. Cyclin-dependent kinases 7 and 9 specifically regulate neutrophil transcription and their inhibition drives apoptosis to promote resolution of inflammation. Cell Death Differ. 2012;19:1950–61.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Lucas CD, Dorward DA, Tait MA, Fox S, Marwick JA, et al. Downregulation of Mcl-1 has anti-inflammatory pro-resolution effects and enhances bacterial clearance from the lung. Mucosal Immunol. 2014;7:857–68.

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Gautam S, Kirschnek S, Wiesmeier M, Vier J, Hacker G. Roscovitine-induced apoptosis in neutrophils and neutrophil progenitors is regulated by the Bcl-2-family members Bim, Puma, Noxa and Mcl-1. PLoS ONE. 2013;8:e79352.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Willis SN, Chen L, Dewson G, Wei A, Naik E, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005;19:1294–305.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol. 2006;8:1348–58.

    Article  CAS  PubMed  Google Scholar 

  20. Epling-Burnette PK, Zhong B, Bai F, Jiang K, Bailey RD, et al. Cooperative regulation of Mcl-1 by Janus kinase/stat and phosphatidylinositol 3-kinase contribute to granulocyte-macrophage colony-stimulating factor-delayed apoptosis in human neutrophils. J Immunol. 2001;166:7486–95.

    Article  CAS  PubMed  Google Scholar 

  21. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell. 2005;17:393–403.

    Article  CAS  PubMed  Google Scholar 

  22. Gardai SJ, Hildeman DA, Frankel SK, Whitlock BB, Frasch SC, et al. Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem. 2004;279:21085–95.

    Article  CAS  PubMed  Google Scholar 

  23. El Kebir D, Jozsef L, Khreiss T, Pan W, Petasis NA, et al. Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid A in human neutrophils: a novel mechanism for resolution of inflammation. J Immunol. 2007;179:616–22.

    Article  PubMed  Google Scholar 

  24. Allaeys I, Gymninova I, Canet-Jourdan C, Poubelle PE. IL-32γ delays spontaneous apoptosis of human neutrophils through MCL-1, regulated primarily by the p38 MAPK pathway. PLoS ONE. 2014;9:e109256.

    Article  PubMed Central  PubMed  Google Scholar 

  25. De Mesquita DD, Zhan Q, Crossley L, Badwey JA. p90-RSK and Akt may promote rapid phosphorylation/inactivation of glycogen synthase kinase 3 in chemoattractant-stimulated neutrophils. FEBS Lett. 2001;502:84–8.

    Article  PubMed  Google Scholar 

  26. Yang TT, Chen CL, Lin WC, Lin YS, Tseng PC, et al. Glycogen synthase kinase-3beta inactivation is an intracellular marker and regulator for endotoxemic neutrophilia. J Mol Med (Berl). 2013;91:207–17.

    Article  CAS  PubMed  Google Scholar 

  27. François S, El Benna J, Dang PMC, Pedruzzi E, Gougerot-Pocidalo M-A, Elbim C. Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-κB signaling pathways, leading to increased levels of Mcl-1, A1 and phosphorylated Bad. J Immunol. 2005;174:3633–42.

    Article  PubMed  Google Scholar 

  28. El Kebir DE, Damlaj A, Filep JG. Toll-like receptor 9 signaling delays neutrophil apoptosis by increasing transcription of Mcl-1. PLoS ONE. 2014;9:e87006.

    Article  PubMed Central  PubMed  Google Scholar 

  29. Yum H-K, Arcaroli J, Kupfner J, Shenkar R, Penninger JM, et al. Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. J Immunol. 2001;167:6601–8.

    Article  CAS  PubMed  Google Scholar 

  30. Sabroe I, Jones EC, Usher LR, Whyte MKB, Dower SK. Toll-like receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte lipopolysaccharide responses. J Immunol. 2002;168:4701–10.

    Article  CAS  PubMed  Google Scholar 

  31. Sabroe I, Prince LR, Jones EC, Horsburgh MJ, Foster SJ, et al. Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol. 2003;170:5268–75.

    Article  CAS  PubMed  Google Scholar 

  32. Cappon A, Babolin C, Segat D, Cancian L, Amedei A, et al. Helicobacter pylori-derived neutrophil-activating protein increases the lifespan of monocytes and neutrophils. Cell Microbiol. 2010;12:754–64.

    Article  CAS  PubMed  Google Scholar 

  33. Chao J-R, Wang J-M, Lee S-F, Peng H-W, Lin Y-H, et al. Mcl-1 is an immediate-early gene activated by the granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol. 1998;18:4883–98.

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Cowburn AS, Cadwallader KA, Reed BJ, Farahi N, Chilvers ER. Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood. 2002;100:2607–16.

    Article  CAS  PubMed  Google Scholar 

  35. Wang J-M, Chao J-R, Chen W, Kuo M-L. Yen JJ-Y, Yang-Yen H-F. The antiapoptotic gene Mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signalling pathway through a transcription factor complex containing CREB. Mol Cell Biol. 1999;19:6195–206.

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Derouet M, Thomas L, Cross A, Moots RJ, Edwards SW. Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J Biol Chem. 2004;279:26915–21.

    Article  CAS  PubMed  Google Scholar 

  37. Domina AM, Vrana JA, Gregory MA, Hann SR, Craig RW. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene. 2004;23:5301–15.

    Article  CAS  PubMed  Google Scholar 

  38. van den Berg JM, Weyer S, Weening JJ, Roos D, Kuijpers TW. Divergent effects of tumor necrosis factor alpha on apoptosis of human neutrophils. J Leukocyte Biol. 2001;69:467–73.

    PubMed  Google Scholar 

  39. Moldoveanu T, Follis AV, Kriwacki RW, Green DR. Many players in BCL-2 family affairs. Trends Biochem Sci. 2014;39:101–11.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Fiore S, Serhan CN. Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils. J Exp Med. 1990;172:1451–7.

    Article  CAS  PubMed  Google Scholar 

  41. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N, Brady HR. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol. 2000;164:1663–7.

    Article  CAS  PubMed  Google Scholar 

  42. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025–37.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Mitchell S, Thomas G, Harvey K, Cottell D, Reville K, et al. Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. J Am Soc Nephrol. 2002;13:2497–507.

    Article  CAS  PubMed  Google Scholar 

  44. Bannenberg GL, Chiang N, Ariel A, Arita M, Tjonahen E, et al. Molecular circuits of resolution: formation and actions of resolvins and protectins. J Immunol. 2005;174:4345–55.

    Article  CAS  PubMed  Google Scholar 

  45. Campbell EL, Louis NA, Tomassetti SE, Canny GO, Arita M, et al. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J. 2007;21:3162–70.

    Article  CAS  PubMed  Google Scholar 

  46. Perskvist N, Long M, Stendahl O, Zheng L. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol. 2002;168:6358–65.

    Article  CAS  PubMed  Google Scholar 

  47. Watson G, Redmond RW, Wang HP, Huai J, Bouchier-Hayes D. Bacterial ingestion, tumor necrosis factor-α, and heat induce programmed cell death in activated neutrophils. Shock. 1996;5:47–51.

    Article  CAS  PubMed  Google Scholar 

  48. Coxon A, Rieu P, Barkalow FJ, Askari S, Sharpe AH, et al. A Novel Role for the β2 Integrin CD11b/CD18 in Neutrophil Apoptosis: a Homeostatic Mechanism in Inflammation. Immunity. 1996;5:653–66.

    Article  PubMed  Google Scholar 

  49. Blomgran R, Zheng L, Stendahl O. Uropathogenic Escherichia coli triggers oxygen-dependent apoptosis in human neutrophils through the cooperative effect of type 1 fimbriae and lipopolysaccharide. Infect Immun. 2004;72:4570–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Zhang B, Hirahashi J, Cullere X, Mayadas TN. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem. 2003;278:28443–54.

    Article  CAS  PubMed  Google Scholar 

  51. Renshaw SA, Timmons SJ, Eaton V, Usher LR, Akil M, et al. Inflammatory neutrophils retain susceptibility to apoptosis mediated via the Fas death receptor. J Leukocyte Biol. 2000;67:662–8.

    CAS  PubMed  Google Scholar 

  52. O’Donnell JA, Kennedy CL, Pellegrini M, Nowell CJ, Zhang JG, et al. Fas regulates neutrophil lifespan during viral and bacterial infection. J Leukoc Biol. 2015;97:321–6.

    Article  PubMed  Google Scholar 

  53. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 1995;14:5579–88.

    PubMed Central  CAS  PubMed  Google Scholar 

  54. Watson RW, O’Neill A, Brannigan AE, Coffey R, Marshall JC, et al. Regulation of Fas antibody induced neutrophil apoptosis is both caspase and mitochondrial dependent. FEBS Lett. 1999;453:67–71.

    Article  CAS  PubMed  Google Scholar 

  55. Croker BA, O’Donnell JA, Nowell CJ, Metcalf D, Dewson G, et al. Fas-mediated neutrophil apoptosis is accelerated by Bid, Bak, and Bax and inhibited by Bcl-2 and Mcl-1. Proc Natl Acad Sci USA. 2011;108:13135–40.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Matsuda T, Saito H, Inoue T, Fukatsu K, Lin MT et al. Ratio of bacteria to polymorphonuclear neutrophils (PMNs) determines PMN fate. Shock (Augusta, Ga). 1999;12:365–72.

  57. Blomgran R, Zheng L, Stendahl O. Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J Leukocyte Biol. 2007;81:1213–23.

    Article  CAS  PubMed  Google Scholar 

  58. Conus S, Pop C, Snipas SJ, Salvesen GS, Simon HU. Cathepsin D primes caspase-8 activation by multiple intra-chain proteolysis. J Biol Chem. 2012;287:21142–51.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Gross A, Yin XM, Wang K, Wei MC, Jockel J, et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem. 1999;274:1156–63.

    Article  CAS  PubMed  Google Scholar 

  60. Werneburg NW, Bronk SF, Guicciardi ME, Thomas L, Dikeakos JD, et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) protein-induced lysosomal translocation of proapoptotic effectors is mediated by phosphofurin acidic cluster sorting protein-2 (PACS-2). J Biol Chem. 2012;287:24427–37.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Zhao K, Zhou H, Zhao X, Wolff DW, Tu Y, et al. Phosphatidic acid mediates the targeting of tBid to induce lysosomal membrane permeabilization and apoptosis. J Lipid Res. 2012;53:2102–14.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, et al. BAX activation is initiated at a novel interaction site. Nature. 2008;455:1076–81.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, et al. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell. 2008;135:1074–84.

    Article  CAS  PubMed  Google Scholar 

  64. Altznauer F, Conus S, Cavalli A, Folkers G, Simon HU. Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem. 2004;279:5947–57.

    Article  CAS  PubMed  Google Scholar 

  65. Herrant M, Jacquel A, Marchetti S, Belhacene N, Colosetti P, et al. Cleavage of Mcl-1 by caspases impaired its ability to counteract Bim-induced apoptosis. Oncogene. 2004;23:7863–73.

    Article  CAS  PubMed  Google Scholar 

  66. Wardle DJ, Burgon J, Sabroe I, Bingle CD, Whyte MK, Renshaw SA. Effective caspase inhibition blocks neutrophil apoptosis and reveals Mcl-1 as both a regulator and a target of neutrophil caspase activation. PLoS ONE. 2011;6:e15768.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Weber K, Harper N, Schwabe J, Cohen GM. BIM-mediated membrane insertion of the BAK pore domain is an essential requirement for apoptosis. Cell Reports. 2013;5:409–20.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Sarosiek K, Chi X, Bachman J, Sims J, Montero J, et al. BID preferentially activates BAK while BIM preferentially activates BAX, affecting chemotherapy response. Mol Cell. 2013;51:751–65.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Murphy BM, O’Neill AJ, Adrain C, Watson RW, Martin SJ. The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. J Exp Med. 2003;197:625–32.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  70. Widlak P, Garrard WT. Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J Cell Biochem. 2005;94:1078–87.

    Article  CAS  PubMed  Google Scholar 

  71. Pederzoli M, Kantari C, Gausson V, Moriceau S, Witko-Sarsat V. Proteinase-3 induces procaspase-3 activation in the absence of apoptosis: potential role of this compartmentalized activation of membrane-associated procaspase-3 in neutrophils. J Immunol. 2005;174:6381–90.

    Article  CAS  PubMed  Google Scholar 

  72. Loison F, Zhu H, Karatepe K, Kasorn A, Liu P, et al. Proteinase 3-dependent caspase-3 cleavage modulates neutrophil death and inflammation. J Clin Invest. 2014;124:4445–58.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288:1053–8.

    Article  CAS  PubMed  Google Scholar 

  74. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science. 2007;315:856–9.

    Article  CAS  PubMed  Google Scholar 

  75. Tonino SH, van Laar J, van Oers MH, Wang JY, Eldering E, Kater AP. ROS-mediated upregulation of Noxa overcomes chemoresistance in chronic lymphocytic leukemia. Oncogene. 2011;30:701–13.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Eno CO, Zhao G, Venkatanarayan A, Wang B, Flores ER, Li C. Noxa couples lysosomal membrane permeabilization and apoptosis during oxidative stress. Free Radical Bio Med. 2013;65:26–37.

    Article  CAS  Google Scholar 

  77. Madenspacher JH, Azzam KM, Gowdy KM, Malcolm KC, Nick JA, et al. p53 Integrates host defense and cell fate during bacterial pneumonia. J Exp Med. 2013;210:891–904.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Bianchi SM, Prince LR, McPhillips K, Allen L, Marriott HM, et al. Impairment of apoptotic cell engulfment by pyocyanin, a toxic metabolite of Pseudomonas aeruginosa. Am J Resp Crit Care Med. 2008;177:35–43.

    Article  CAS  PubMed  Google Scholar 

  79. Prince LR, Bianchi SM, Vaughan KM, Bewley MA, Marriott HM, et al. Subversion of a lysosomal pathway regulating neutrophil apoptosis by a major bacterial toxin, pyocyanin. J Immunol. 2008;180:3502–11.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. Jensen PO, Bjarnsholt T, Phipps R, Rasmussen TB, Calum H, et al. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology. 2007;153:1329–38.

    Article  CAS  PubMed  Google Scholar 

  81. van Gennip M, Christensen LD, Alhede M, Phipps R, Jensen PO, et al. Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS. 2009;117:537–46.

    Article  PubMed  Google Scholar 

  82. van Gennip M, Christensen LD, Alhede M, Qvortrup K, Jensen PO, et al. Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo. Infect Immun. 2012;80:2601–7.

    Article  PubMed Central  PubMed  Google Scholar 

  83. Genestier A-L, Michallet M-C, Prévost G, Bellot G, Chalabreysse L, et al. Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest. 2005;115:3117–27.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Zysk G, Bejo L, Schneider-Wald BK, Nau R, Heinz HP. Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae. Clin Exp Immunol. 2000;122:61–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Alemán M, Schierloh P, de la Barrera SS, Musella RM, Saab MA, et al. Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving Toll-like receptor 2 and p38 mitogen protein kinase in Tuberculosis patients. Infect Immun. 2004;72:5150–8.

    Article  PubMed Central  PubMed  Google Scholar 

  86. Corleis B, Korbel D, Wilson R, Bylund J, Chee R, Schaible UE. Escape of Mycobacterium tuberculosis from oxidative killing by neutrophils. Cell Microbiol. 2012;14:1109–21.

    Article  CAS  PubMed  Google Scholar 

  87. Aguilo JI, Alonso H, Uranga S, Marinova D, Arbués A, et al. ESX-1-induced apoptosis is involved in cell-to-cell spread of Mycobacterium tuberculosis. Cell Microbiol. 2013;15:1994–2005.

    Article  CAS  PubMed  Google Scholar 

  88. Greenlee-Wacker MC, Rigby KM, Kobayashi SD, Porter AR, DeLeo FR, Nauseef WM. Phagocytosis of Staphylococcus aureus by human neutrophils prevents macrophage efferocytosis and induces programmed necrosis. J Immunol. 2014;192:4709–17.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Kobayashi SD, Braughton KR, Palazzolo-Ballance AM, Kennedy AD, Sampaio E, et al. Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus. J Innate Immun. 2010;2:560–75.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  90. Goebel S, Gross U, Lüder CGK. Inhibition of host cell apoptosis by Toxoplasma gondii is accompanied by reduced activation of the caspase cascade and alterations of poly(ADP-ribose) polymerase expression. J Cell Sci. 2001;114:3495–505.

    CAS  PubMed  Google Scholar 

  91. Choi KS, Park JT, Dumler JS. Anaplasma phagocytophilum delay of neutrophil apoptosis through the p38 mitogen-activated protein kinase signal pathway. Infect Immun. 2005;73:8209–18.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  92. Sarkar A, Hellberg L, Bhattacharyya A, Behnen M, Wang K, et al. Infection with Anaplasma phagocytophilum activates the phosphatidylinositol 3-Kinase/Akt and NF-kappaB survival pathways in neutrophil granulocytes. Infect Immun. 2012;80:1615–23.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  93. Chen A, Seifert HS. Neisseria gonorrhoeae-mediated inhibition of apoptotic signalling in polymorphonuclear leukocytes. Infect Immun. 2011;79:4447–58.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. Simons MP, Nauseef WM, Griffith TS, Apicella MA. Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell Microbiol. 2006;8:1780–90.

    Article  CAS  PubMed  Google Scholar 

  95. Smirnov A, Daily KP, Criss AK. Assembly of NADPH oxidase in human neutrophils is modulated by the opacity-associated protein expression State of Neisseria gonorrhoeae. Infect Immun. 2014;82:1036–44.

    Article  PubMed Central  PubMed  Google Scholar 

  96. Gunderson CW, Seifert HS. Neisseria gonorrhoeae elicits extracellular traps in primary neutrophil culture while suppressing the oxidative burst. mBio. 2015;6:e02452–14.

  97. McCaffrey RL, Allen LA. Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukocyte Biol. 2006;80:1224–30.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  98. Schwartz JT, Barker JH, Kaufman J, Fayram DC, McCracken JM, Allen LA. Francisella tularensis inhibits the intrinsic and extrinsic pathways to delay constitutive apoptosis and prolong human neutrophil lifespan. J Immunol. 2013;188:3351–63.

    Article  Google Scholar 

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Acknowledgments

This work was supported in part from a grant provided by Science Foundation Ireland (No. RFP2816).

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The authors declare that they have no conflict of interest.

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  1. Centre for Microbial-Host Interactions, Institute of Technology Tallaght, Old Blessington Road, Tallaght, Dublin 24, Ireland

    Mark P. Murphy & Emma Caraher

  2. Centre of Applied Science for Health, Institute of Technology Tallaght, Dublin, Ireland

    Mark P. Murphy & Emma Caraher

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Correspondence to Mark P. Murphy.

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Murphy, M.P., Caraher, E. Mcl-1 is vital for neutrophil survival. Immunol Res 62, 225–233 (2015). https://doi.org/10.1007/s12026-015-8655-z

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