Front Cell Dev Biol. 2018 Sep 04;6:109. doi: 10.3389/fcell.2018.00109. eCollection 2018.
Autophagy in Neutrophils: From Granulopoiesis to Neutrophil Extracellular Traps.
Frontiers in cell and developmental biology
Panagiotis Skendros, Ioannis Mitroulis, Konstantinos Ritis
Affiliations
Affiliations
- Laboratory of Molecular Hematology, Department of Medicine, Democritus University of Thrace, Alexandroupolis, Greece.
- First Department of Internal Medicine, University Hospital of Alexandroupolis, Democritus University of Thrace, Alexandroupolis, Greece.
- Institute for Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Dresden, Germany.
- National Center for Tumor Diseases, Dresden, Germany.
PMID: 30234114
PMCID: PMC6131573 DOI: 10.3389/fcell.2018.00109
Abstract
Autophagy is an evolutionarily conserved intracellular degradation system aiming to maintain cell homeostasis in response to cellular stress. At physiological states, basal or constitutive level of autophagy activity is usually low; however, it is markedly up-regulated in response to oxidative stress, nutrient starvation, and various immunological stimuli including pathogens. Many studies over the last years have indicated the implication of autophagy in a plethora of cell populations and functions. In this review, we focus on the role of autophagy in the biology of neutrophils. Early studies provided a link between autophagy and neutrophil cell death, a process essential for resolution of inflammation. Since then, several lines of evidence both in the human system and in murine models propose a critical role for autophagy in neutrophil-driven inflammation and defense against pathogens. Autophagy is essential for major neutrophil functions, including degranulation, reactive oxygen species production, and release of neutrophil extracellular traps. Going back to neutrophil generation in the bone marrow, autophagy plays a critical role in myelopoiesis, driving the differentiation of progenitor cells of the myeloid lineage toward neutrophils. Taken together, in this review we discuss the functional role of autophagy in neutrophils throughout their life, from their production in the bone marrow to inflammatory responses and NETotic cell death.
Keywords: autophagy; degranulation; granulopoiesis; inflammation; neutrophil; neutrophil extracellular traps; phagocytosis
References
- Biochem Biophys Res Commun. 2015 Aug 14;464(1):94-9 - PubMed
- Dev Cell. 2018 Mar 12;44(5):542-553 - PubMed
- Cell Host Microbe. 2008 Nov 13;4(5):458-69 - PubMed
- Front Immunol. 2016 Nov 04;7:484 - PubMed
- Nature. 2017 Mar 9;543(7644):205-210 - PubMed
- Annu Rev Genet. 2009;43:67-93 - PubMed
- Autophagy. 2018;14(2):207-215 - PubMed
- J Pathol. 2014 Jul;233(3):294-307 - PubMed
- Immunology. 2017 Nov;152(3):517-525 - PubMed
- Nat Rev Rheumatol. 2016 Sep;12(9):517-31 - PubMed
- Cell Death Dis. 2016 Jun 30;7(6):e2283 - PubMed
- Nature. 2015 Dec 24;528(7583):565-9 - PubMed
- Cancer Gene Ther. 2015 Jun;22(6):326-34 - PubMed
- Nat Immunol. 2018 Jan;19(1):29-40 - PubMed
- Clin Exp Immunol. 2015 Jun;180(3):408-18 - PubMed
- PLoS One. 2012;7(12):e51727 - PubMed
- Cell Stem Cell. 2017 May 4;20(5):593-608 - PubMed
- J Immunol. 2013 Sep 1;191(5):2647-56 - PubMed
- Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6226-31 - PubMed
- Curr Opin Immunol. 2018 Feb;50:21-31 - PubMed
- Blood. 2011 Jan 20;117(3):953-9 - PubMed
- Ann Rheum Dis. 2016 Apr;75(4):644-51 - PubMed
- J Thromb Thrombolysis. 2017 Oct;44(3):377-385 - PubMed
- J Allergy Clin Immunol. 2017 Nov;140(5):1378-1387.e13 - PubMed
- Biochem J. 2016 Aug 1;473(15):2251-71 - PubMed
- J Infect Dis. 2017 Apr 1;215(7):1040-1048 - PubMed
- Cell Rep. 2015 Sep 22;12(11):1731-9 - PubMed
- Curr Opin Cell Biol. 2016 Apr;39:61-8 - PubMed
- Cell Tissue Res. 2018 Mar;371(3):455-471 - PubMed
- N Engl J Med. 2011 Aug 25;365(8):758-60 - PubMed
- Front Microbiol. 2016 Jun 08;7:879 - PubMed
- Mol Biol Cell. 2008 Dec;19(12):5360-72 - PubMed
- Annu Rev Pathol. 2014;9:181-218 - PubMed
- Cell. 2014 Sep 11;158(6):1309-1323 - PubMed
- Autophagy. 2013 Nov 1;9(11):1737-49 - PubMed
- J Exp Med. 2012 Apr 9;209(4):819-35 - PubMed
- Immunol Rev. 2016 Sep;273(1):48-60 - PubMed
- Hum Immunol. 2011 Feb;72(2):135-8 - PubMed
- Nature. 1998 Sep 24;395(6700):395-8 - PubMed
- Nat Cell Biol. 2015 Jul;17(7):893-906 - PubMed
- FEBS Lett. 1993 Oct 25;333(1-2):169-74 - PubMed
- Clin Exp Allergy. 2017 Jan;47(1):57-70 - PubMed
- Cell. 2018 Jan 11;172(1-2):147-161.e12 - PubMed
- Blood. 2016 May 5;127(18):2173-81 - PubMed
- PLoS One. 2011;6(12):e29318 - PubMed
- Immunology. 2017 Aug;151(4):417-432 - PubMed
- Cell Stem Cell. 2013 Jan 3;12(1):49-61 - PubMed
- J Immunol. 2010 Dec 15;185(12):7413-25 - PubMed
- Sci Transl Med. 2011 Mar 9;3(73):73ra19 - PubMed
- Nat Commun. 2015 Apr 28;6:7014 - PubMed
- Am J Respir Crit Care Med. 2017 Sep 1;196(5):577-589 - PubMed
- J Leukoc Biol. 2017 Sep;102(3):685-688 - PubMed
- Cell Rep. 2014 Aug 7;8(3):883-96 - PubMed
- Anat Rec. 1984 Mar;208(3):319-27 - PubMed
- Immunol Rev. 2016 Sep;273(1):11-28 - PubMed
- Cell Death Differ. 2015 Mar;22(3):445-56 - PubMed
- J Pathol. 2017 Sep;243(1):111-122 - PubMed
- Cell Stem Cell. 2011 Oct 4;9(4):298-310 - PubMed
- Immunol Rev. 2011 Mar;240(1):92-104 - PubMed
- Nature. 2013 Feb 21;494(7437):323-7 - PubMed
- Genes Dev. 2008 Jan 15;22(2):239-51 - PubMed
- Nature. 2000 Nov 23;408(6811):488-92 - PubMed
- Clin Exp Rheumatol. 2017 Nov-Dec;35 Suppl 108(6):133-134 - PubMed
- Autophagy. 2018;14(3):558-559 - PubMed
- Innate Immun. 2017 Jul;23(5):413-423 - PubMed
- Nat Cell Biol. 2011 Feb;13(2):132-41 - PubMed
- J Clin Invest. 2015 Jan;125(1):25-32 - PubMed
- Sci Rep. 2017 Aug 1;7(1):7023 - PubMed
- J Cell Sci. 2014 Jan 1;127(Pt 1):3-9 - PubMed
- Nat Rev Neurosci. 2015 Jun;16(6):345-57 - PubMed
- Science. 2004 Mar 5;303(5663):1532-5 - PubMed
- Nat Cell Biol. 2008 Jul;10(7):776-87 - PubMed
- Clin Dev Immunol. 2012;2012:910525 - PubMed
- Front Immunol. 2017 Jan 11;7:678 - PubMed
- Immunity. 2017 Sep 19;47(3):466-480.e5 - PubMed
- Sci Transl Med. 2013 Mar 27;5(178):178ra40 - PubMed
- Annu Rev Biochem. 2017 Jun 20;86:225-244 - PubMed
- Nature. 2016 May 5;533(7601):115-9 - PubMed
- Nat Commun. 2015 Jul 29;6:7901 - PubMed
- Nat Med. 2012 Sep;18(9):1350-8 - PubMed
- Cell Res. 2011 Feb;21(2):290-304 - PubMed
- Pharmacol Res. 2017 Sep;123:146-156 - PubMed
- Ann Rheum Dis. 2014 Oct;73(10):1854-63 - PubMed
- Trends Cell Biol. 2014 Aug;24(8):479-87 - PubMed
- Nat Rev Immunol. 2014 May;14(5):302-14 - PubMed
- Cell Death Differ. 2018 Mar;25(3):486-541 - PubMed
- J Thromb Haemost. 2014 Dec;12(12):2074-88 - PubMed
- Cell. 2012 Apr 13;149(2):274-93 - PubMed
- PLoS One. 2011 Mar 11;6(3):e17852 - PubMed
- Eur Heart J. 2015 Jun 7;36(22):1405-14 - PubMed
- Eur J Immunol. 2010 May;40(5):1461-72 - PubMed
- J Clin Invest. 2015 Jan;125(1):75-84 - PubMed
- Ann Rheum Dis. 2016 Jan;75(1):269-77 - PubMed
- Antimicrob Agents Chemother. 2015 Dec 07;60(2):1040-8 - PubMed
- Cell Death Differ. 2011 Apr;18(4):581-8 - PubMed
- Mol Immunol. 2015 Aug;66(2):319-24 - PubMed
- Science. 2011 Jan 28;331(6016):456-61 - PubMed
- Nat Rev Immunol. 2018 Feb;18(2):134-147 - PubMed
- Proc Natl Acad Sci U S A. 2017 Jan 10;114(2):201-205 - PubMed
- Cell Death Differ. 2015 Mar;22(3):377-88 - PubMed
- EMBO J. 2015 Apr 1;34(7):856-80 - PubMed
- J Immunol. 2016 Dec 1;197(11):4403-4412 - PubMed
- Pathog Dis. 2015 Dec;73(9):ftv080 - PubMed
- J Immunol. 2018 Jun 15;200(12):3950-3961 - PubMed
- J Leukoc Biol. 2015 Jul;98(1):107-17 - PubMed
- PLoS One. 2015 Jun 05;10(6):e0128341 - PubMed
- EMBO Rep. 2013 Dec;14(12):1039-42 - PubMed
- PLoS One. 2012;7(9):e45427 - PubMed
- Nature. 2007 Dec 20;450(7173):1253-7 - PubMed
- J Innate Immun. 2018 Jun 6;:1-8 - PubMed
- J Cell Biol. 1992 Oct;119(2):301-11 - PubMed
- Am J Physiol Cell Physiol. 2013 Aug 1;305(3):C348-54 - PubMed
- J Cell Biol. 2010 Nov 1;191(3):677-91 - PubMed
- Innate Immun. 2016 Nov;22(8):658-665 - PubMed
- Proc Natl Acad Sci U S A. 2010 May 25;107(21):9813-8 - PubMed
- Eur J Clin Invest. 2018 May 17;:e12952 - PubMed
- J Exp Med. 2011 Mar 14;208(3):455-67 - PubMed
- Nat Med. 2017 Mar 7;23(3):279-287 - PubMed
- Nature. 2011 Jan 20;469(7330):323-35 - PubMed
- Semin Immunol. 2016 Dec;28(6):561-569 - PubMed
- Aging Cell. 2014 Aug;13(4):690-8 - PubMed
- Front Immunol. 2018 Feb 19;9:269 - PubMed
- Nat Med. 2016 Feb;22(2):146-53 - PubMed
- Front Immunol. 2012 Dec 18;3:385 - PubMed
- Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17396-401 - PubMed
- Autophagy. 2015;11(5):748-55 - PubMed
Publication Types