Activation of AMPK enhances neutrophil chemotaxis and bacterial killing

Molecular Medicine

Volumn 19, Issue 1, 2013, Pages 387-398

  Park, Dae Won ^a,b   Jiang, Shaoning ^a   Tadie, Jean Marc ^a,c   Stigler, William S ^a   Gao, Yong ^a   Deshane, Jessy ^a   Abraham, Edward ^d   Zmijewski, Jaroslaw W ^a  

^a and Clinical Center   (United States)

^b Korea University College of Medicine   (South Korea)

^c RENNES UNIVERSITY HOSPITAL   (France)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; 6 CHLORO 8 NICOTINAMIDO BETA CARBOLINE; ACTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; I KAPPA B ALPHA; LIPOPOLYSACCHARIDE; METFORMIN; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERICIDAL ACTIVITY; CELL ISOLATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PERITONITIS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SEPSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTINS; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BACTEREMIA; CHEMOTAXIS, LEUKOCYTE; ENZYME ACTIVATION; HETEROCYCLIC COMPOUNDS, 3-RING; HL-60 CELLS; HUMANS; MALE; METFORMIN; MICE; MICE, INBRED C57BL; NEUTROPHILS; PERITONITIS; PHAGOCYTOSIS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PYRIDINES; RIBONUCLEOTIDES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 84889639030     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2013.00065     Document Type: Article

References (71)

1. Stuart LM, Ezekowitz RA. (2008) Phagocytosis and comparative innate immunity: learning on the fly. Nat. Rev. Immunol. 8:131-41.
2. Phillipson M, Kubes P. (2011) The neutrophil in vascular inflammation. Nat. Med. 17:1381-90.
3. Foxman EF, Campbell JJ, Butcher EC. (1997) Multistep navigation and the combinatorial control of leukocyte chemotaxis. J. Cell Biol. 139:1349-60.
4. Williams MR, Azcutia V, Newton G, Alcaide P, Luscinskas FW. (2011) Emerging mechanisms of neutrophil recruitment across endothelium. Trends Immunol. 32:461-9.
5. Lambeth JD. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4:181-9.
6. Hampton MB, Kettle AJ, Winterbourn CC. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood. 92:3007-17.
7. Brinkmann V, et al. (2004) Neutrophil extracellular traps kill bacteria. Science. 303:1532-5.
8. Papayannopoulos V, Zychlinsky A. (2009) NETs: a new strategy for using old weapons. Trends Immunol. 30:513-21.
9. Brown KA, et al. (2006) Neutrophils in development of multiple organ failure in sepsis. Lancet. 368:157-69.
10. Vincent JL, Abraham E. (2006) The last 100 years of sepsis. Am. J. Respir. Crit. Care Med. 173:256-63.
11. van der Poll T, Opal SM. (2008) Host-pathogen interactions in sepsis. Lancet Infect. Dis. 8:32-43.
12. Muller LM, et al. (2005) Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin. Infect. Dis. 41:281-8.
13. Abraham E. (2003) Neutrophils and acute lung injury. Crit. Care Med. 31: S195-9.
14. Chaudry IH, Ayala A. (1993) Mechanism of increased susceptibility to infection following hemorrhage. Am. J. Surg. 165:59S-67S.
15. Stephan RN, Kupper TS, Geha AS, Baue AE, Chaudry IH. (1987) Hemorrhage without tissue trauma produces immunosuppression and enhances susceptibility to sepsis. Arch. Surg. 122:62-8.
16. Alves-Filho JC, de Freitas A, Russo M, Cunha FQ. (2006) Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit. Care Med. 34:461-70.
17. Arraes SM, et al. (2006) Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood. 108:2906-13.
18. Tavares-Murta BM, et al. (2002) Failure of neutrophil chemotactic function in septic patients. Crit. Care Med. 30:1056-61.
19. Alves-Filho JC, de Freitas A, Spiller F, Souto FO, Cunha FQ. (2008) The role of neutrophils in severe sepsis. Shock. 30 Suppl 1:3-9.
20. Rios-Santos F, et al. (2007) Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am. J. Respir. Crit. Care Med. 175:490-7.
21. Benjamim CF, et al. (2002) Inhibition of leukocyte rolling by nitric oxide during sepsis leads to reduced migration of active microbicidal neutrophils. Infect. Immun. 70:3602-10.
22. Bailey CJ, Turner RC. (1996) Metformin. N. Engl. J. Med. 334:574-9.
23. Saenz A, et al. (2005) Metformin monotherapy for type 2 diabetes mellitus. Cochrane Database Syst. Rev. 3:CD002966.
24. Wulffele MG, Kooy A, de Zeeuw D, Stehouwer CD, Gansevoort RT. (2004) The effect of metformin on blood pressure, plasma cholesterol and triglycerides in type 2 diabetes mellitus: a systematic review. J. Intern. Med. 256:1-14.
25. El-Mir MY, et al. (2000) Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 275:223-8.
26. Hawley SA, Gadalla AE, Olsen GS, Hardie DG. (2002) The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-independent mechanism. Diabetes. 51:2420-5.
27. Hardie DG, Ross FA, Hawley SA. (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13:251-62.
28. O'Neill LA, Hardie DG. (2013) Metabolism of inflammation limited by AMPK and pseudostarvation. Nature. 493:346-55.
29. Zhao X, et al. (2008) Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 295:L497-504.
30. Bergheim I, et al. (2006) Metformin prevents endotoxin-induced liver injury after partial hepatectomy. J. Pharmacol. Exp. Ther. 316:1053-61.
31. Zmijewski JW, et al. (2008) Mitochondrial respiratory complex I regulates neutrophil activation and severity of lung injury. Am. J. Respir. Crit. Care Med. 178:168-79.
32. Hattori Y, Suzuki K, Hattori S, Kasai K. (2006) Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension. 47:1183-8.
33. Sag D, Carling D, Stout RD, Suttles J. (2008) Adenosine 5′-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J. Immunol. 181:8633-41.
34. Xing J, et al. (2013) Inhibition of AMP-activated protein kinase accentuates lipopolysaccharide-induced lung endothelial barrier dysfunction and lung injury in vivo. Am. J. Pathol. 182:1021-30.
35. Jeong HW, et al. (2009) Berberine suppresses proinflammatory responses through AMPK activation in macrophages. Am. J. Physiol. Endocrinol. Metab. 296:E955-64.
36. Tsoyi K, et al. (2011) Metformin inhibits HMGB1 release in LPS-treated RAW 264.7 cells and increases survival rate of endotoxaemic mice. Br. J. Pharmacol. 162:1498-508.
37. Pearce EL, et al. (2009) Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature. 460:103-7.
38. Chan O, Burke JD, Gao DF, Fish EN. (2012) The chemokine CCL5 regulates glucose uptake and AMP kinase signaling in activated T cells to facilitate chemotaxis. J. Biol. Chem. 287:29406-16.
39. Bae HB, et al. (2011) AMP-activated protein kinase enhances the phagocytic ability of macro-phages and neutrophils. Faseb. J. 25:4358-68.
40. Zmijewski JW, et al. (2009) Antiinflammatory effects of hydrogen peroxide in neutrophil activation and acute lung injury. Am. J. Respir. Crit. Care Med. 179:694-704.
41. Millius A, Weiner OD. (2009) Chemotaxis in neutrophil-like HL-60 cells. Methods Mol. Biol. 571:167-77.
42. Renckens R, et al. (2006) Endogenous tissue-type plasminogen activator is protective during Escherichia coli-induced abdominal sepsis in mice. J. Immunol. 177:1189-96.
43. Tadie JM, Bae HB, Banerjee S, Zmijewski JW, Abraham E. (2012) Differential activation of RAGE by HMGB1 modulates neutrophil-associated NADPH oxidase activity and bacterial killing. Am. J. Physiol. Cell Physiol. 302:C249-56.
44. Zmijewski JW, et al. (2010) Exposure to hydrogen peroxide induces oxidation and activation of AMPactivated protein kinase. J Biol. Chem. 285:33154-64.
45. Tadie JM, et al. (2012) Toll-like receptor 4 engagement inhibits adenosine 5′-monophosphateactivated protein kinase activation through a high mobility group box 1 protein-dependent mechanism. Mol. Med. 18:659-68.
46. Sullivan JE, et al. (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMPactivated protein kinase. FEBS Lett. 353:33-36.
47. Elferink JG, de Koster BM. (2000) Inhibition of interleukin-8-activated human neutrophil chemotaxis by thapsigargin in a calcium-and cyclic AMP-dependent way. Biochem. Pharmacol. 59:369-75.
48. Elferink JG, de Koster BM, Boonen GJ, de Priester W. (1992) Inhibition of neutrophil chemotaxis by purinoceptor agonists. Arch. Int. Pharmacodyn. Ther. 317:93-106.
49. Hayashi F, Means TK, Luster AD. (2003) Toll-like receptors stimulate human neutrophil function. Blood. 102:2660-9.
50. Nakano A, et al. (2010) AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat. Cell Biol. 12:583-90.
51. Taneja R, Sharma AP, Hallett MB, Findlay GP, Morris MR. (2008) Immature circulating neutrophils in sepsis have impaired phagocytosis and calcium signaling. Shock. 30:618-22.
52. Duignan JP, Collins PB, Johnson AH, Bouchier-Hayes D. (1986) The association of impaired neutrophil chemotaxis with postoperative surgical sepsis. Br. J. Surg. 73:238-40.
53. Yemelyanov A, et al. (2006) Effects of IKK inhibitor PS1145 on NF-kappaB function, proliferation, apoptosis and invasion activity in prostate carcinoma cells. Oncogene. 25:387-98.
54. Cilloni D, et al. (2006) The NF-kappaB pathway blockade by the IKK inhibitor PS1145 can overcome imatinib resistance. Leukemia. 20:61-7.
55. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. (2002) AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol. Chem. 277:23977-80.
56. Inoki K, Kim J, Guan KL. (2012) AMPK and mTOR in cellular energy homeostasis and drug targets. Annu. Rev. Pharmacol. Toxicol. 52:381-400.
57. Gentile LF, et al. (2012) Persistent inflammation and immunosuppression: a common syndrome and new horizon for surgical intensive care. J. Trauma Acute Care Surg. 72:1491-501.
58. Tsaknis G, et al. (2012) Metformin attenuates ventilator-induced lung injury. Crit. Care. 16:R134.
59. Labuzek K, Liber S, Gabryel B, Adamczyk J, Okopien B. (2010) Metformin increases phagocytosis and acidifies lysosomal/endosomal compartments in AMPK-dependent manner in rat primary microglia. Naunyn Schmiedebergs Arch. Pharmacol. 381:171-86.
60. Jiang S, et al. (2013) Mitochondria and AMPactivated protein kinase-dependent mechanism of efferocytosis. J Biol. Chem. 288:26013-26.
61. Park CS, et al. (2012) Metformin reduces airway inflammation and remodeling via activation of AMP-activated protein kinase. Biochem. Pharmacol. 84:1660-70.
62. Li FY, et al. (2012) Endothelium-selective activation of AMP-activated protein kinase prevents diabetes mellitus-induced impairment in vascular function and reendothelialization via induction of heme oxygenase-1 in mice. Circulation. 126:1267-77.
63. Yang Z, Kahn BB, Shi H, Xue BZ. Macrophage alpha1 AMP-activated protein kinase (alpha1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J. Biol. Chem. 285:19051-9.
64. Ji G, et al. (2012) Genistein suppresses LPSinduced inflammatory response through inhibiting NF-kappaB following AMP kinase activation in RAW 264.7 macrophages. PLoS ONE. 7:e53101.
65. Wen H, et al. (2011) Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12:408-15.
66. Zhang Q, et al. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 464:104-7.
67. Pugin J. (2008) Dear SIRS, the concept of "alarmins" makes a lot of sense! Intensive Care Med. 34:218-21.
68. Wang H, et al. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science. 285:248-51.
69. Scaffidi P, Misteli T, Bianchi ME. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 418:191-5.
70. Qin S, et al. (2006) Role of HMGB1 in apoptosismediated sepsis lethality. J. Exp. Med. 203:1637-42.
71. Xu J, et al. (2009) Extracellular histones are major mediators of death in sepsis. Nat. Med. 15:1318-21.