Francisella tularensis Modulates a Distinct Subset of Regulatory Factors and Sustains Mitochondrial Integrity to Impair Human Neutrophil Apoptosis

Journal of Innate Immunity

Volumn 8, Issue 3, 2016, Pages 299-313

  McCracken, Jenna M ^a,b   Kinkead, Lauren C ^a,b   McCaffrey, Ramona L ^a,b   Allen, Lee Ann H ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Apoptosis; Mitochondria; Neutrophils; Proliferating cell nuclear antigen; R roscovitine; X linked inhibitor of apoptosis protein

Indexed keywords

CALPAIN; CALPASTATIN; CASPASE 3; CASPASE 9; CYCLINE; PROTEIN BAX; PROTEIN BID; ROSCOVITINE; X LINKED INHIBITOR OF APOPTOSIS; BAX PROTEIN, HUMAN; CALCIUM BINDING PROTEIN; PROTEIN BINDING; XIAP PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; GENE TRANSLOCATION; HUMAN; HUMAN CELL; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL INTEGRITY; MITOCHONDRION; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; TULAREMIA; UPREGULATION; CELL CULTURE; FRANCISELLA TULARENSIS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PROTEIN TRANSPORT;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CALCIUM-BINDING PROTEINS; CASPASE 3; CASPASE 9; CELLS, CULTURED; FRANCISELLA TULARENSIS; HUMANS; MITOCHONDRIA; NEUTROPHILS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN TRANSPORT; TULAREMIA; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84959213466     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000443882     Document Type: Article

References (45)

1. Nauseef WM: How human neutrophils kill and degrade microbes: An integrated view. Immunol Rev 2007; 219: 88-102.
2. Kennedy A, DeLeo F: Neutrophil apoptosis and the resolution of infection. Immunol Res 2009; 43: 25-61.
3. Gabelloni M, Trevani A, Sabatte J, Geffner J: Mechanisms regulating neutrophil survival and cell death. Semin Immunopathol 2013; 35: 423-437.
4. McCracken JM, Allen L-AH: Regulation of human neutrophil apoptosis and lifespan in health and disease. J Cell Death 2014; 7: 15-23.
5. Kobayashi SD, DeLeo FR: Role of neutrophils in innate immunity: A systems biology-level approach. Wiley Interdiscip Rev Syst Biol Med 2009; 1: 309-333.
6. Nathan C: Points of control in inflammation. Nature 2002; 420: 846-852.
7. McLendon MK, Apicella M, Allen L-AH: Francisella tularensis : Taxomony, genetics and immunopathogenesis of a potenial agent of biowarfare. Annu Rev Microbiol 2006; 60: 167-185.
8. Schricker RL, Eigelsbach HT, Mitten JO, Hall WC: Pathogenesis of tularemia in monkeys aerogenically exposed to Francisella tularensis 425. Infect Immun 1972; 5: 734-744.
9. Hall WC, Kovatch RM, Schricker RL: Tularemic pneumonia: pathogenesis of the aerosolinduced disease in monkeys. J Pathol 1973; 110: 193-201.
10. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, Frelinger JA, Kawula TH: Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun 2008; 76: 5843-5852.
11. Bosio CM, Elkins KL: Susceptibility to secondary Francisella tularensis live vaccine strain infection in B-cell-deficient mice is associated with neutrophilia but not with defects in specific T-cell-mediated immunity. Infect Immun 2001; 69: 194-203.
12. Malik M, Bakshi CS, McCabe K, Catlett SV, Shah A, Singh R, Jackson PL, Gaggar A, Metzger DW, Melendez JA, Blalock JE, Sellati TJ: Matrix metalloproteinase 9 activity enhances host susceptibility to pulmonary infection with type A and B strains of Francisella tularensis. J Immunol 2007; 178: 1013-1020.
13. Allen L-AH: Editorial: Leukocytes in tularemia-so many cells, so little time. J Leukoc Biol 2013; 93: 641-644.
14. Allen L-AH: Neutrophils: potential therapeutic targets in tularemia Front Cell Infect Microbiol 2013; 3: 109.
15. McCaffrey RL, Allen L-AH: Pivotal advance: Francisella tularensis evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukoc Biol 2006; 80: 1224-1230.
16. McCaffrey RL, Schwartz JT, Lindemann SR, Moreland JG, Buchan BW, Jones BD, Allen L-AH: Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J Leukoc Biol 2010; 88: 791-805.
17. Schwartz JT, Barker JH, Kaufman J, Fayram DC, McCracken JM, Allen L-AH: Francisella tularensis inhibits the intrinsic and extrinsic pathways to delay constitutive apoptosis and prolong human neutrophil lifespan. J Immunol 2012; 188: 3351-3363.
18. Witko-Sarsat V, Pederzoli-Ribeil M, Hirsh E, Sozzani S, Cassatella MA: Regulating neutrophil apoptosis: new players enter the game. Trends Immunol 2011; 32: 117-124.
19. Geering B, Simon HU: Peculiarities of cell death mechanisms in neutrophils. Cell Death Differ 2011; 18: 1457-1469.
20. Schwartz JT, Bandyopadhyay S, Kobayashi SD, McCracken J, Whitney AR, DeLeo FR, Allen L-AH: Francisella tualrensis alters human neutrophil gene expression: insights into the molecular basis of delayed neutrophil apoptosis. J Innate Immun 2013; 5: 5124-5136.
21. Rossi AG, Sawatzky DA, Walker A, Ward C, Sheldrake TA, Riley NA, Caldicott A, Martinez-Losa M, Walker TR, Duffin R, Gray M, Crescenzi E, Martin MC, Brady HJ, Savill JS, Dransfield I, Haslett C: Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat Med 2006; 12: 1056-1064.
22. Leitch AE, Haslett C, Rossi AG: Cyclin-dependent kinase inhibitor drugs as potenital novel anti-inflammatory and pro-resolution agents. Br J Pharmacol 2009; 158: 1004-1016.
23. Bandyopadhyay S, Long ME, Allen L-AH: Differential expression of microRNAs in Francisella tularensis-infected human macrophages: miR-155-dependent downregulation of Myd88 inhibits the inflammatory response. PLoS One 2014; 9:e109525.
24. Nauseef WM: Isolation of human neutrophils from venous blood. Methods Mol Biol 2007; 412: 15-20.
25. Rosser BG, Gores GJ: Cellular in vivo assay of calpain activity using a fluorescent substrate. Application to study of anoxic liver injury. Methods Mol Biol 2000; 144: 245-259.
26. Waterhouse NJ, Steel R, Kluck R, Trapani JA: Assaying cytochrome c translocation during apoptosis. Methods Mol Biol 2004; 284: 307-313.
27. Allen L-AH: Immunofluorescence and confocal microscopy of neutrophils. Methods Mol Biol 2007; 412: 273-287.
28. Maianski NA, Geissler J, Srinivasula SM, Alnemri ES, Roos D, Kuijpers TW: Functional characterization of mitochondria in neutrophils: A role restricted to apoptosis. Cell Death Differ 2004; 11: 143-153.
29. Maianski NA, Roos D, Kuijpers TW: Bid truncation, Bid/Bax targeting to the mitochondria, and caspase activation associated with neutrophil apoptosis are inhibited by granulocyte colony-stimulating factor. J Immunol 2004; 172: 7024-7030.
30. Esposti MD: Mitochondria in apoptosis: past, present and future. Biochem Soc Trans 2004; 32: 493-495.
31. O'Connor CL, Anguissola S, Huber HJ, Dussmann H, Prehn JH, Rehm M: Intracellular signaling dynamics during apoptosis execution in the presence or absence of X-linkedinhibitor-of-apoptosis-protein. Biochim Biophys Acta 2008; 1783: 1903-1913.
32. van Raam BJ, Drewniak A, Groenewold V, van den Berg TK, Kuijpers TW: Granulocyte colony-stimulating factor delays neutrophil apoptosis by inhibition of calpains upstream of caspase-3. Blood 2008; 112: 2046-2054.
33. Altznauer F, Conus S, Cavalli A, Folkers G, Simon H-U: Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem 2004; 279: 5947-5957.
34. Kobayashi S, Yamashita K, Takeoka T, Ohtsuki T, Suzuki Y, Takahashi R, Yamamoto K, Kaufmann SH, Uchiyama T, Sasada M, Takahashi A: Calpain-mediated X-linked inhibitor of apoptosis degradation in neutrophil apoptosis and its impairment in chronic neutrophilic leukemia. J Biol Chem 2002; 277: 33968-33977.
35. Witko-Sarsat V, Mocek J, Bouayad D, Tamassia N, Ribeil J-A, Candalh C, Davezac N, Reuter N, Mouthon L, Hermine O, Pederzoli-Ribeil M, Cassatella MA: Proliferating cell nuclear antigen acts as a cytoplasmic platform controlling human neutrophil survival. J Exp Med 2010; 207: 2631-2645.
36. Milot E, Filep JG: Regulation of neutrophil survival/apoptosis by Mcl-1. Sci World J 2011; 11: 1948-1962.
37. Maianski NA, Mul FPJ, van Buul JD, Roos D, Kuijpers TW: Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood 2002; 99: 672-679.
38. Gardai SJ, Hildeman DA, Frankel SK, Whitlock BB, Frasch SC, Borregaard N, Marrack P, Bratton DL, Henson PM: Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem 2004; 279: 21085-21095.
39. Simmons MJ, Fan G, Zong W-X, Degenhardt K, White E, Gelinas C: Bfl-1/A1 functions, similar to Mcl-1, as a selective tBid and Bax antagonist. Oncogene 2008; 27: 1421-1428.
40. Renault TT, Chipuk JE: Death upon a kiss: mitochondrial outer membrane composition and organelle communication govern sensitivity to Bak/Bax-dependent apoptosis. Chem Biol 2014; 21: 114-123.
41. Momeni HR: Role of calpain in apoptosis. Cell J 2011; 13: 65-72.
42. Srinivasa SM, Gupta S, Datta P, Zhang Z, Hegde R, Cheong N, Fernandes-Alnemri T, Alnemri ES: Inhibitor of apoptosis proteins are substrates for the mitochondrial serine protease Omi/Htra2. J Biol Chem 2003; 278: 3146-31472.
43. Koedel U, Frankenberg T, Kirschnek S, Obermaier B, Hacker H, Paul R, Hacker G: Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog 2009; 5:e1000461.
44. Wang K, Hampson P, Hazeldine J, Krystof V, Strnad M, Pechan P, M J: Cyclin-dependent kinase 9 activity regulates neutrophil spontaneous apoptosis. PLoS One 2012; 7:e30128.
45. 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: 1950-1961.