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http://dx.doi.org/10.4196/kjpp.2020.24.1.1

Autophagy in neutrophils  

Shrestha, Sanjeeb (Department of Physiology, School of Medicine, Kyungpook National University)
Lee, Jae Man (Department of Biochemistry and Cell Biology, School of Medicine, Kyungpook National University)
Hong, Chang-Won (Department of Physiology, School of Medicine, Kyungpook National University)
Publication Information
The Korean Journal of Physiology and Pharmacology / v.24, no.1, 2020 , pp. 1-10 More about this Journal
Abstract
Autophagy is a highly conserved intracellular degradation and energy-recycling mechanism that contributes to the maintenance of cellular homeostasis. Extensive researches over the past decades have defined the role of autophagy innate immune cells. In this review, we describe the current state of knowledge regarding the role of autophagy in neutrophil biology and a picture of molecular mechanism underlying autophagy in neutrophils. Neutrophils are professional phagocytes that comprise the first line of defense against pathogen. Autophagy machineries are highly conserved in neutrophils. Autophagy is not only involved in generalized function of neutrophils such as differentiation in bone marrow but also plays crucial role effector functions of neutrophils such as granule formation, degranulation, neutrophil extracellular traps release, cytokine production, bactericidal activity and controlling inflammation. This review outlines the current understanding of autophagy in neutrophils and provides insight towards identification of novel therapeutics targeting autophagy in neutrophils.
Keywords
Autophagy; Bactericidal activity; Neutrophil; Neutrophil extracellular trap;
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1 Parzych KR, Klionsky DJ. An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal. 2014;20:460-473.   DOI
2 Backer JM. The intricate regulation and complex functions of the Class III phosphoinositide 3-kinase Vps34. Biochem J. 2016;473: 2251-2271.   DOI
3 Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y. A protein conjugation system essential for autophagy. Nature. 1998;395:395-398.   DOI
4 Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3-12.   DOI
5 Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408:488-492.   DOI
6 Codogno P, Mehrpour M, Proikas-Cezanne T. Canonical and noncanonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Biol . 2011;13:7-12.   DOI
7 Chargui A, Cesaro A, Mimouna S, Fareh M, Brest P, Naquet P, Darfeuille-Michaud A, Hebuterne X, Mograbi B, Vouret-Craviari V, Hofman P. Subversion of autophagy in adherent invasive Escherichia coli-infected neutrophils induces inflammation and cell death. PLoS One. 2012;7:e51727.   DOI
8 Goldmann O, Medina E. The expanding world of extracellular traps: not only neutrophils but much more. Front Immunol. 2013; 3:420.   DOI
9 Mihalache CC, Yousefi S, Conus S, Villiger PM, Schneider EM, Simon HU. Inflammation-associated autophagy-related programmed necrotic death of human neutrophils characterized by organelle fusion events. J Immunol. 2011;186:6532-6542.   DOI
10 Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, Magalhaes MA, Glogauer M, Grinstein S, Brumell JH. Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci U S A. 2009;106:6226-6231.   DOI
11 Rinchai D, Riyapa D, Buddhisa S, Utispan K, Titball RW, Stevens MP, Stevens JM, Ogawa M, Tanida I, Koike M, Uchiyama Y, Ato M, Lertmemongkolchai G. Macroautophagy is essential for killing of intracellular Burkholderia pseudomallei in human neutrophils. Autophagy. 2015;11:748-755.   DOI
12 Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011; 18:581-588.   DOI
13 Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 2009;5:e1000639.   DOI
14 Boe DM, Curtis BJ, Chen MM, Ippolito JA, Kovacs EJ. Extracellular traps and macrophages: new roles for the versatile phagocyte. J Leukoc Biol. 2015;97:1023-1035.   DOI
15 Kenny EF, Herzig A, Kruger R, Muth A, Mondal S, Thompson PR, Brinkmann V, Bernuth HV, Zychlinsky A. Diverse stimuli engage different neutrophil extracellular trap pathways. Elife. 2017;6:e24437.   DOI
16 Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol. 2012;189:2689-2695.   DOI
17 Cowland JB, Borregaard N. Granulopoiesis and granules of human neutrophils. Immunol Rev. 2016;273:11-28.   DOI
18 Lawrence SM, Corriden R, Nizet V. The ontogeny of a neutrophil: mechanisms of granulopoiesis and homeostasis. Microbiol Mol Biol Rev. 2018;82:e00057-17.
19 Gullberg U, Andersson E, Garwicz D, Lindmark A, Olsson I. Biosynthesis, processing and sorting of neutrophil proteins: insight into neutrophil granule development. Eur J Haematol. 1997;58:137-153.   DOI
20 Peng HH, Liu YJ, Ojcius DM, Lee CM, Chen RH, Huang PR, Martel J, Young JD. Mineral particles stimulate innate immunity through neutrophil extracellular traps containing HMGB1. Sci Rep. 2017;7:16628.   DOI
21 Neumann A, Papareddy P, Westman J, Hyldegaard O, Snall J, Norrby-Teglund A, Herwald H. Immunoregulation of neutrophil extracellular trap formation by endothelial-derived p33 (gC1q receptor). J Innate Immun. 2018;10:30-43.   DOI
22 Lacy P. Mechanisms of degranulation in neutrophils. Allergy Asthma Clin Immunol. 2006;2:98-108.   DOI
23 Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol . 2011;11:519-531.   DOI
24 Tecchio C, Cassatella MA. Neutrophil-derived cytokines involved in physiological and pathological angiogenesis. Chem Immunol Allergy. 2014;99:123-137.   DOI
25 Tecchio C, Micheletti A, Cassatella MA. Neutrophil-derived cytokines: facts beyond expression. Front Immunol. 2014;5:508.
26 Naegelen I, Beaume N, Plançon S, Schenten V, Tschirhart EJ, Brechard S. Regulation of neutrophil degranulation and cytokine secretion: a novel model approach based on linear fitting. J Immunol Res. 2015;2015:817038.   DOI
27 Angelidou I, Chrysanthopoulou A, Mitsios A, Arelaki S, Arampatzioglou A, Kambas K, Ritis D, Tsironidou V, Moschos I, Dalla V, Stakos D, Kouklakis G, Mitroulis I, Ritis K, Skendros P. REDD1/ autophagy pathway is associated with Neutrophil-Driven IL-1${\beta}$ inflammatory response in active ulcerative colitis. J Immunol. 2018; 200:3950-3961.   DOI
28 Lv XX, Liu SS, Li K, Cui B, Liu C, Hu ZW. Cigarette smoke promotes COPD by activating platelet-activating factor receptor and inducing neutrophil autophagic death in mice. Oncotarget. 2017;8:74720-74735.   DOI
29 Sharma A, Simonson TJ, Jondle CN, Mishra BB, Sharma J. Minclemediated neutrophil extracellular trap formation by regulation of autophagy. J Infect Dis. 2017;215:1040-1048.   DOI
30 Zhao M, Klionsky DJ. AMPK-dependent phosphorylation of ULK1 induces autophagy. Cell Metab. 2011;13:119-120.   DOI
31 Xu F, Zhang C, Zou Z, Fan EKY, Chen L, Li Y, Billiar TR, Wilson MA, Shi X, Fan J. Aging-related Atg5 defect impairs neutrophil extracellular traps formation. Immunology. 2017;151:417-432.   DOI
32 Bhattacharya A, Wei Q, Shin JN, Abdel Fattah E, Bonilla DL, Xiang Q, Eissa NT. Autophagy Is required for neutrophil-mediated inflammation. Cell Rep. 2015;12:1731-1739.   DOI
33 Park SY, Shrestha S, Youn YJ, Kim JK, Kim SY, Kim HJ, Park SH, Ahn WG, Kim S, Lee MG, Jung KS, Park YB, Mo EK, Ko Y, Lee SY, Koh Y, Park MJ, Song DK, Hong CW. Autophagy primes neutrophils for neutrophil extracellular trap formation during sepsis. Am J Respir Crit Care Med. 2017;196:577-589.   DOI
34 Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, Agarwal R, Aghi MK, Agnello M, Agostinis P, Aguilar PV, Aguirre-Ghiso J, Airoldi EM, et al . Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1-222.   DOI
35 Rozman S, Yousefi S, Oberson K, Kaufmann T, Benarafa C, Simon HU. The generation of neutrophils in the bone marrow is controlled by autophagy. Cell Death Differ. 2015;22:445-456.   DOI
36 van der Linden M, Westerlaken GHA, van der Vlist M, van Montfrans J, Meyaard L. Differential signalling and kinetics of neutrophil extracellular trap release revealed by quantitative live imaging. Sci Rep. 2017;7:6529.   DOI
37 Maugeri N, Campana L, Gavina M, Covino C, De Metrio M, Panciroli C, Maiuri L, Maseri A, D'Angelo A, Bianchi ME, Rovere- Querini P, Manfredi AA. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J Thromb Haemost. 2014;12:2074-2088.   DOI
38 Chatfield SM, Grebe K, Whitehead LW, Rogers KL, Nebl T, Murphy JM, Wicks IP. Monosodium urate crystals generate nuclease resistant neutrophil extracellular traps via a distinct molecular pathway. J Immunol. 2018;200:1802-1816.   DOI
39 Remijsen Q, Vanden Berghe T, Wirawan E, Asselbergh B, Parthoens E, De Rycke R, Noppen S, Delforge M, Willems J, Vandenabeele P. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res. 2011;21:290-304.   DOI
40 Douda DN, Khan MA, Grasemann H, Palaniyar N. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc Natl Acad Sci U S A. 2015;112:2817-2822.   DOI
41 Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol. 2010;185:7413-7425.   DOI
42 Chow OA, von Kockritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS, Cogen AL, Gallo RL, Monestier M, Wang Y, Glass CK, Nizet V. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe. 2010;8:445-454.   DOI
43 Apostolidou E, Skendros P, Kambas K, Mitroulis I, Konstantinidis T, Chrysanthopoulou A, Nakos K, Tsironidou V, Koffa M, Boumpas DT, Ritis K. Neutrophil extracellular traps regulate IL-1${\beta}$-mediated inflammation in familial Mediterranean fever. Ann Rheum Dis. 2016;75:269-277.   DOI
44 Iula L, Keitelman IA, Sabbione F, Fuentes F, Guzman M, Galletti JG, Gerber PP, Ostrowski M, Geffner JR, Jancic CC, Trevani AS. Autophagy mediates interleukin-1${\beta}$ secretion in human neutrophils. Front Immunol. 2018;9:269.   DOI
45 Harris J. Autophagy and cytokines. Cytokine. 2011;56:140-144.   DOI
46 Harris J, Hartman M, Roche C, Zeng SG, O'Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem. 2011; 286:9587-9597.   DOI
47 Netea-Maier RT, Plantinga TS, van de Veerdonk FL, Smit JW, Netea MG. Modulation of inflammation by autophagy: consequences for human disease. Autophagy. 2016;12:245-260.   DOI
48 Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011;469:323-335.   DOI
49 Zhang F, Liu AL, Gao S, Ma S, Guo SB. Neutrophil dysfunction in sepsis. Chin Med J (Engl). 2016;129:2741-2744.   DOI
50 Segal AW, Loewi G. Neutrophil dysfunction in Crohn's disease. Lancet . 1976;2:219-221.   DOI
51 Davis WC, Douglas SD, Fudenberg HH. A selective neutrophil dysfunction syndrome: impaired killing of staphylococci. Ann Intern Med. 1968;69:1237-1243.   DOI
52 Jin L, Batra S, Jeyaseelan S. Deletion of Nlrp3 augments survival during polymicrobial sepsis by decreasing autophagy and enhancing phagocytosis. J Immunol. 2017;198:1253-1262.   DOI
53 Kimmey JM, Huynh JP, Weiss LA, Park S, Kambal A, Debnath J, Virgin HW, Stallings CL. Unique role for ATG5 in neutrophilmediated immunopathology during M. tuberculosis infection. Nature. 2015;528:565-569.   DOI
54 Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, Cowland JB, Borregaard N. The transcriptional program of terminal granulocytic differentiation. Blood . 2005;105:1785-1796.   DOI
55 Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, Zhang J, Haug J, Li L. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood. 2003101:383-389.   DOI
56 Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006;6:173-182.   DOI
57 Furze RC, Rankin SM. Neutrophil mobilization and clearance in the bone marrow. Immunology. 2008;125:281-288.   DOI
58 Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood . 1998;92:3007-3017.   DOI
59 Segal AW. How neutrophils kill microbes. Annu Rev Immunol. 2005;23:197-223.   DOI
60 Huang Y, Tan P, Wang X, Yi Y, Hu Y, Wang D, Wang F. Transcriptomic insights into temporal expression pattern of autophagy genes during monocytic and granulocytic differentiation. Autophagy. 2018;14:558-559.   DOI
61 Koschade SE, Brandts CH. Selective autophagy in normal and malignant hematopoiesis. J Mol Biol. 2019. doi: 10.1016/j.jmb. 2019.06.025. [Epub ahead of print]
62 Orsini M, Chateauvieux S, Rhim J, Gaigneaux A, Cheillan D, Christov C, Dicato M, Morceau F, Diederich M. Sphingolipidmediated inflammatory signaling leading to autophagy inhibition converts erythropoiesis to myelopoiesis in human hematopoietic stem/progenitor cells. Cell Death Differ. 2019;26:1796-1812.   DOI
63 da Silva FM, Massart-Leen AM, Burvenich C. Development and maturation of neutrophils. Vet Q. 1994;16:220-225.   DOI
64 Riffelmacher T, Clarke A, Richter FC, Stranks A, Pandey S, Danielli S, Hublitz P, Yu Z, Johnson E, Schwerd T, McCullagh J, Uhlig H, Jacobsen SEW, Simon AK. Autophagy-dependent generation of free fatty acids is critical for normal neutrophil differentiation. Immunity. 2017;47:466-480.e5.   DOI
65 Byrd AS, O'Brien XM, Johnson CM, Lavigne LM, Reichner JS. An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J Immunol. 2013;190:4136-4148.   DOI
66 Stranks AJ, Hansen AL, Panse I, Mortensen M, Ferguson DJ, Puleston DJ, Shenderov K, Watson AS, Veldhoen M, Phadwal K, Cerundolo V, Simon AK. Autophagy controls acquisition of aging features in macrophages. J Innate Immun. 2015;7:375-391.   DOI
67 Ma R, Li T, Cao M, Si Y, Wu X, Zhao L, Yao Z, Zhang Y, Fang S, Deng R, Novakovic VA, Bi Y, Kou J, Yu B, Yang S, Wang J, Zhou J, Shi J. Extracellular DNA traps released by acute promyelocytic leukemia cells through autophagy. Cell Death Dis. 2016;7:e2283.   DOI
68 Germic N, Stojkov D, Oberson K, Yousefi S, Simon HU. Neither eosinophils nor neutrophils require ATG5-dependent autophagy for extracellular DNA trap formation. Immunology. 2017;152:517-525.   DOI
69 Rorvig S, Ostergaard O, Heegaard NH, Borregaard N. Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: correlation with transcriptome profiling of neutrophil precursors. J Leukoc Biol. 2013;94:711-721.   DOI
70 Masson PL, Heremans JF, Schonne E. Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J Exp Med. 1969;130:643-658.   DOI
71 Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles ininflammation. Microbes Infect. 2003;5:1317-1327.   DOI
72 Patel JM, Sapey E, Parekh D, Scott A, Dosanjh D, Gao F, Thickett DR. Sepsis Induces a Dysregulated neutrophil phenotype that is associated with increased mortality. Mediators Inflamm. 2018; 2018:4065362.
73 Meng W, Paunel-Gorgulu A, Flohe S, Hoffmann A, Witte I, MacKenzie C, Baldus SE, Windolf J, Logters TT. Depletion of neutrophil extracellular traps in vivo results in hypersusceptibility to polymicrobial sepsis in mice. Crit Care. 2012;16:R137.   DOI
74 Haimovici A, Brigger D, Torbett BE, Fey MF, Tschan MP. Induction of the autophagy-associated gene MAP1S via PU.1 supports APL differentiation. Leuk Res. 2014;38:1041-1047.   DOI
75 Schlafli AM, Shan-Krauer D, Garattini E, Tschan MP. Regulation and function of autophagy in retinoic acid mediated therapy of myeloid leukemia and breast cancer. Ital J Anat Embryol. 2015;120:9-10.
76 Britschgi A, Yousefi S, Laedrach J, Shan D, Simon H-U, Tobler A, Fey MF, Tschan MP. Blocking the autophagy gene 5 (ATG5) impairs ATRA-induced myeloid differentiation, and ATG5 is downregulated in AML. Blood. 2008;112:309.   DOI
77 Abdel Fattah E, Bhattacharya A, Herron A, Safdar Z, Eissa NT. Critical role for IL-18 in spontaneous lung inflammation caused by autophagy deficiency. J Immunol. 2015;194:5407-5416.   DOI
78 Skendros P, Chrysanthopoulou A, Rousset F, Kambas K, Arampatzioglou A, Mitsios A, Bocly V, Konstantinidis T, Pellet P, Angelidou I, Apostolidou E, Ritis D, Tsironidou V, Galtsidis S, Papagoras C, Stakos D, Kouklakis G, Dalla V, Koffa M, Mitroulis I, et al . Regulated in development and DNA damage responses 1 (REDD1) links stress with IL-1${\beta}$-mediated familial Mediterranean fever attack through autophagy-driven neutrophil extracellular traps. J Allergy Clin Immunol. 2017;140:1378-1387.e13.   DOI
79 Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532-1535.   DOI
80 Naegele M, Tillack K, Reinhardt S, Schippling S, Martin R, Sospedra M. Neutrophils in multiple sclerosis are characterized by a primed phenotype. J Neuroimmunol. 2012;242:60-71.   DOI
81 Borregaard N. Neutrophils, from marrow to microbes. Immunity. 2010;33:657-670.   DOI
82 Ryter SW, Cloonan SM, Choi AM. Autophagy: a critical regulator of cellular metabolism and homeostasis. Mol Cells. 2013;36:7-16.   DOI
83 Nezis IP, Vaccaro MI, Devenish RJ, Juhasz G. Autophagy in development, cell differentiation, and homeodynamics: from molecular mechanisms to diseases and pathophysiology. Biomed Res Int. 2014;2014:349623.   DOI
84 Mitroulis I, Kourtzelis I, Kambas K, Rafail S, Chrysanthopoulou A, Speletas M, Ritis K. Regulation of the autophagic machinery in human neutrophils. Eur J Immunol. 2010;40:1461-1472.   DOI
85 Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol. 2009;335:1-32.   DOI
86 Das G, Shravage BV, Baehrecke EH. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb Perspect Biol. 2012;4:a008813.   DOI
87 Kantari C, Pederzoli-Ribeil M, Witko-Sarsat V. The role of neutrophils and monocytes in innate immunity. Contrib Microbiol. 2008;15:118-146.   DOI
88 Cuervo AM. Autophagy: many paths to the same end. Mol Cell Biochem. 2004;263:55-72.   DOI
89 Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med . 2003;9:65-76.   DOI
90 Mizushima N. Autophagy: process and function. Genes Dev. 2007; 21:2861-2873.   DOI
91 Itakura A, McCarty OJ. Pivotal role for the mTOR pathway in the formation of neutrophil extracellular traps via regulation of autophagy. Am J Physiol Cell Physiol. 2013;30:C348-C354.   DOI
92 Wong CO, Gregory S, Hu H, Chao Y, Sepulveda VE, He Y, Li- Kroeger D, Goldman WE, Bellen HJ, Venkatachalam K. Lysosomal degradation is required for sustained phagocytosis of bacteria by macrophages. Cell Host Microbe. 2017;21:719-730.e6.   DOI
93 Lee WL, Harrison RE, Grinstein S. Phagocytosis by neutrophils. Microbes Infect . 2003;5:1299-1306.   DOI
94 Chargui A, El May MV. Autophagy mediates neutrophil responses to bacterial infection. APMIS. 2014;122:1047-1058.   DOI
95 Gong L, Cullinane M, Treerat P, Ramm G, Prescott M, Adler B, Boyce JD, Devenish RJ. The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis. PLoS One. 2011;6:e17852.   DOI
96 Ramachandran G, Gade P, Tsai P, Lu W, Kalvakolanu DV, Rosen GM, Cross AS. Potential role of autophagy in the bactericidal activity of human PMNs for Bacillus anthracis. Pathog Dis. 2015;73: ftv080.   DOI
97 Itoh H, Matsuo H, Kitamura N, Yamamoto S, Higuchi T, Takematsu H, Kamikubo Y, Kondo T, Yamashita K, Sasada M, Takaori-Kondo A, Adachi S. Enhancement of neutrophil autophagy by an IVIG preparation against multidrug-resistant bacteria as well as drug-sensitive strains. J Leukoc Biol. 2015;98:107-117.   DOI
98 Ullah I, Ritchie ND, Evans TJ. The interrelationship between phagocytosis, autophagy and formation of neutrophil extracellular traps following infection of human neutrophils by Streptococcus pneumoniae. Innate Immun. 2017;23:413-423.   DOI
99 Wang C, Mendonsa GR, Symington JW, Zhang Q, Cadwell K, Virgin HW, Mysorekar IU. Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo. Proc Natl Acad Sci U S A. 2012;109:11008-11013.   DOI
100 Konstantinidis T, Kambas K, Mitsios A, Panopoulou M, Tsironidou V, Dellaporta E, Kouklakis G, Arampatzioglou A, Angelidou I, Mitroulis I, Skendros P, Ritis K. Immunomodulatory role of clarithromycin in acinetobacter baumannii infection via formation of neutrophil extracellular traps. Antimicrob Agents Chemother. 2015;60:1040-1048.
101 Sharma A, Steichen AL, Jondle CN, Mishra BB, Sharma J. Protective role of Mincle in bacterial pneumonia by regulation of neutrophil mediated phagocytosis and extracellular trap formation. J Infect Dis. 2014;209:1837-1846.   DOI
102 Li XF, Chen DP, Ouyang FZ, Chen MM, Wu Y, Kuang DM, Zheng L. Increased autophagy sustains the survival and pro-tumourigenic effects of neutrophils in human hepatocellular carcinoma. J Hepatol. 2015;62:131-139.   DOI
103 Park J, Wysocki RW, Amoozgar Z, Maiorino L, Fein MR, Jorns J, Schott AF, Kinugasa-Katayama Y, Lee Y, Won NH, Nakasone ES, Hearn SA, Kuttner V, Qiu J, Almeida AS, Perurena N, Kessenbrock K, Goldberg MS, Egeblad M. Cancer cells induce metastasissupporting neutrophil extracellular DNA traps. Sci Transl Med. 2016;8:361ra138.   DOI
104 Tohme S, Yazdani HO, Al-Khafaji AB, Chidi AP, Loughran P, Mowen K, Wang Y, Simmons RL, Huang H, Tsung A. Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Cancer Res. 2016;76:1367-1380.   DOI
105 Najmeh S, Cools-Lartigue J, Rayes RF, Gowing S, Vourtzoumis P, Bourdeau F, Giannias B, Berube J, Rousseau S, Ferri LE, Spicer JD. Neutrophil extracellular traps sequester circulating tumor cells via ${\beta}$1-integrin mediated interactions. Int J Cancer. 2017;140:2321-2330.   DOI
106 Leach J, Morton JP, Sansom OJ. Neutrophils: Homing in on the myeloid mechanisms of metastasis. Mol Immunol. 2019;110:69-76.   DOI
107 Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood. 1997;89:3503-3521.   DOI