Neutrophil elastase mediates acute pathogenesis and is a determinant of long-term behavioral recovery after traumatic injury to the immature brain

Neurobiology of Disease

Volumn 74, Issue , 2015, Pages 263-280

  Semple, Bridgette D ^a,b   Trivedi, Alpa ^a   Gimlin, Kayleen ^a   Noble Haeusslein, Linda J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Behavior; Cell death; Neutrophil elastase; Pathology; Pediatric; Traumatic brain injury

Indexed keywords

CASPASE 3; HEME OXYGENASE 1; LEUKOCYTE ELASTASE; CASP3 PROTEIN, MOUSE; GELATINASE B; HMOX1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MMP9 PROTEIN, MOUSE; PROTEINASE INHIBITOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; GENOTYPE; HIPPOCAMPUS; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERINATAL PERIOD; PROTEIN EXPRESSION; SPINAL CORD INJURY; TRAUMATIC BRAIN INJURY; WILD TYPE; ACUTE DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; BRAIN EDEMA; BRAIN INJURY; C57BL MOUSE; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; MOTOR ACTIVITY; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; SPATIAL MEMORY;

ACUTE DISEASE; ANIMALS; BRAIN; BRAIN EDEMA; BRAIN INJURIES; CASPASE 3; CELL DEATH; DISEASE MODELS, ANIMAL; HEME OXYGENASE-1; LEUKOCYTE ELASTASE; MALE; MATRIX METALLOPROTEINASE 9; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEUTROPHILS; OXIDATIVE STRESS; PROTEASE INHIBITORS; RECOVERY OF FUNCTION; SPATIAL MEMORY;

EID: 84919334406     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.12.003     Document Type: Article

References (109)

1. Ahmed S.H., He Y.Y., Nassief A., Xu J., Xu X.M., CYea Hsu Effects of lipopolysaccharide priming on acute ischemic brain injury. Stroke 2000, 31:193-199.
2. Allen C., Thornton P., Denes A., McColl B.W., Pierozynski A., Monestier M., Pinteaux E., Rothwell N., Allan S.M. Neutrophil cerebrovascular transmigration triggers rapid neurotoxicity through release of proteases associated with decondensed DNA. J. Immunol. 2012, 189:381-392.
3. Allport J.R., Lim Y.C., Shipley J.M., Senior R.M., Shapiro S.D., Matsuyoshi N., Vestweber D., Luscinskas F.W. Neutrophils from MMP-9- or neutrophil elastase-deficient mice show no defect in transendothelial migration under flow in vitro. J. Leukoc. Biol. 2002, 71:821-828.
4. Anderson V., Catroppa C., Morse S., Haritou F., Rosenfeld J. Functional plasticity or vulnerability after early brain injury?. Pediatrics 2005, 116:1374-1382.
5. Anderson V., Godfrey C., Rosenfeld J.V., Catroppa C. 10years outcome from childhood traumatic brain injury. Int. J. Dev. Neurosci. 2012, 30:217-224.
6. Anthony D.C., Bolton S.J., Fearn S., Perry V.H. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 1997, 120:435-444.
7. Anthony D., Dempster R., Fearn S., Clements J., Wells G., Perry V.H., Walker K. CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood-brain barrier breakdown. Curr. Biol. 1998, 8:923-926.
8. Aoshiba K., Yasuda K., Yasui S., Tamaoki J., Nagai A. Serine proteases increase oxidative stress in lung cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 281:L556-L564.
9. Bank U., Ansorge S. More than destructive: neutrophil-derived serine proteases in cytokine bioactivity control. J. Leukoc. Biol. 2001, 69:197-206.
10. Bao F., Shultz S.R., Hepburn J.D., Omana V., Weaver L.C., Cain D.P., Brown A. A CD11d monoclonal antibody treatment reduces tissue injury and improves neurological outcome after fluid percussion brain injury in rats. J. Neurotrauma 2012, 29:2375-2392.
11. Becker K.J. Anti-leukocyte antibodies: LeukArrest (Hu23F2G) and Enlimomab (R6.5) in acute stroke. Curr. Med. Res. Opin. 2002, 19:s18-s22.
12. Belaaouaj A., McCarthy R., Baumann M., Gao Z., Ley T.J., Abraham S.N., Shapiro S.D. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat. Med. 1998, 4:615-618.
13. Beray-Berthat V., Croci N., Plotkine M., Margaill I. Polymorphonuclear neutrophils contribute to infarction and oxidative stress in the cortex but not in the striatum after ischemia-reperfusion in rats. Brain Res. 2003, 987:32-38.
14. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:14515-14520.
15. Chang E.F., Claus C.P., Vreman H.J., Wong R.J., Noble-Haeusslein L.J. Heme regulation in traumatic brain injury: relevance to the adult and developing brain. J. Cereb. Blood Flow Metab. 2005, 25:1401-1417.
16. Clark R.S., Schiding J.K., Kaczorowski S.L., Marion D.W., Kochanek P.M. Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J. Neurotrauma 1994, 11:499-506.
17. Clark R.S., Kochanek P.M., Watkins S.C., Chen M., Dixon C.E., Seidberg N.A., Melick J., Loeffert J.E., Nathaniel P.D., Jin K.L., Graham S.H. Caspase-3 mediated neuronal death after traumatic brain injury in rats. J. Neurochem. 2000, 74:740-753.
18. Claus C.P., Tsuru-Aoyagi K., Adwanikar H., Walker B., Whetstone W., Noble-Haeusslein L.J. Age is a determinant of the inflammatory response and loss of cortical volume after traumatic brain injury. Dev. Neurosci. 2010, 32:454-465.
19. Cojocaru I.M., Cojocaru M., Burcin C. Evaluation of granulocyte elastase as a sensitive diagnostic parameter of inflammation in first ischemic stroke. Rom. J. Intern. Med. 2006, 44:317-321.
20. Cousar J.L., Lai Y., Marco C.D., Bayir H., Adelson P.D., Janesko-Feldman K.L., Kochanek P.M., Clark R.S. Heme oxygenase 1 in cerebrospinal fluid from infants and children after severe traumatic brain injury. Dev. Neurosci. 2006, 28:342-347.
21. Cuartero M.I., Ballesteros I., Moraga A., Nombela F., Vivancos J., Hamilton J.A., Corbí A.L., Lizasoain I., Moro M.A. N2 neutrophils, novel players in brain inflammation after stroke. Stroke 2013, 44:3498-3508.
22. Davis M.J., Haley T., Duvoisin R.M., Raber J. Measures of anxiety, sensorimotor function, and memory in male and female mGluR4-/- mice. Behav. Brain Res. 2012, 229:21-28.
23. Delclaux C., Delacourt C., D'Ortho M.P., Boyer V., Lafuma C., Harf A. Role of gelatinase B and elastase in human polymorphonuclear neutrophil migration across basement membrane. Am. J. Respir. Cell Mol. Biol. 1996, 14:288-295.
24. Dinkel K., Dhabhar F.S., Sapolsky R.M. Neurotoxic effects of polymorphonuclear granulocytes on hippocampal primary cultures. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:331-336.
25. Dixon C.E., Markgraf C.G., Angileri F., Pike B.R., Wolfson B., Newcomb J.K., Bismar M.M., Blanco A.J., Clifton G.L., Hayes R.L. Protective effects of moderate hypothermia on behavioral deficits but not necrotic cavitation following cortical impact injury in the rat. J. Neurotrauma 1998, 15:95-103.
26. Dredge B.K., Jensen K.B. NeuN/Rbfox3 Nuclear and Cytoplasmic Isoforms Differentially Regulate Alternative Splicing and Nonsense-Mediated Decay of Rbfox2. PLoS One 2011, 6:e21585.
27. Easton A.S. Neutrophils and stroke - can neutrophils mitigate disease in the central nervous system?. Int. Immunopharmacol. 2013, 17:1218-1225.
28. Eisener-Dorman A.F., Lawrence D.A., Bolivar V.J. Cautionary insights on knockout mouse studies: the gene or not the gene?. Brain Behav. Immun. 2009, 23:318-324.
29. Elliott M.B., Jallo J.J., Tuma R.F. An investigation of cerebral edema and injury volume assessments for controlled cortical impact injury. J. Neurosci. Methods 2008, 168:320-324.
30. Emerich D.F., RLr Dean, Bartus R.T. The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct?. Exp. Neurol. 2002, 173:168-181.
31. Fan P., Yamauchi T., Noble L., Ferriero D. Age-dependent differences in glutathione peroxidase activity after traumatic brain injury. J. Neurotrauma 2003, 20:437-445.
32. Faul M., Xu L., Wald M.M., Coronado V.G. Traumatic brain injury in the United States: Emergency department visits, hospitalizations and deaths 2002-2006 2010, Centers for Disease Control and Prevention, National Center for Injury Prevention and Control Atlanta, GA.
33. Fischer B.M., Voynow J.A. Neutrophil elastase induces MUC5AC gene expression in airway epithelium via a pathway involving reactive oxygen species. Am. J. Respir. Cell Mol. Biol. 2002, 26:447-452.
34. Fitrolaki D.M., Dimitriou H., Kalmanti M., Briassoulis G. CD64-neutrophil expression and stress metabolic patterns in early sepsis and severe traumatic brain injury in children. BMC Pediatr. 2013, 13:31.
35. Frankowski H., Gu Y.H., Heo J.H., Milner R., del Zoppo G.J. Use of gel zymography to examine matrix metalloproteinases (gelatinase) expression in brain tissue or in primary glial cultures. Methods Mol. Biol. 2012, 814:221-233.
36. Fridlender Z.G., Sun J., Kim S., Kapoor V., Cheng G., Lea Ling Polarization of tumor-associated neutrophil phenotype by TGF-beta: 'N1' versus 'N2' TAN. Cancer Cell 2009, 16:183-194.
37. Fukuda K., Panter S.S., Sharp F.R., Noble L.J. Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci. Lett. 1995, 199:127-130.
38. Fukuda K., Richmon J.D., Sato M., Sharp F.R., Panter S.S., Noble L.J. Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury. Brain Res. 1996, 736:68-75.
39. Gould T.D., Dao D.T., Kovacsics C.E. The Open Field Test. Neuromethods 2009, 42:1-20.
40. Grenda D.S., Johnson S.E., Mayer J.R., McLemore M.L., Benson K.F., Horwitz M., Link D.C. Mice expressing a neutrophil elastase mutation derived from patients with severe congenital neutropenia have normal granulopoiesis. Blood 2002, 100:3221-3228.
41. Hadass O., Tomlinson B.N., Gooyit M., Chen S., Purdy J.J., Walker J.M., Zhang C., Giritharan A.B., Purnell W., CRn Robinson, Shin D., Schroeder V.A., Suckow M.A., Simonyi A.Y., Sun G., Mobashery S., Cui J., Chang M., Gu Z. Selective inhibition of matrix metalloproteinase-9 attenuates secondary damage resulting from severe traumatic brain injury. PLoS One 2013, 8:e76904.
42. Hausmann R., Kaiser A., Lang C., Bohnert M., Betz P. A quantitative immunohistochemical study on the time-dependent course of acute inflammatory cellular response to human brain injury. Int. J. Legal Med. 1999, 112:227-232.
43. Hirche T.O., Atkinson J.J., Bahr S., Belaaouaj A. Deficiency in neutrophil elastase does not impair neutrophil recruitment to inflamed sites. Am. J. Respir. Cell Mol. Biol. 2004, 30:576-584.
44. Holmin S., Mathiesen T., Shetye J., Biberfeld P. Intracerebral inflammatory response to experimental brain contusion. Acta Neurochir. (Wien) 1995, 132:110-119.
45. Ikegame Y., Yamashita K., Hayashi S., Yoshimura S., Nakashima S., Iwama T. Neutrophil elastase inhibitor prevents ischemic brain damage via reduction of vasogenic edema. Hypertens. Res. 2010, 33:704-707.
46. Inoue N., Oka N., Kitamura T., Shibata K., Itatani K., Tomoyasu T., Miyaji K. Neutrophil elastase inhibitor sivelestat attenuates perioperative inflammatory response in pediatric heart surgery with cardiopulmonary bypass. Int. Heart J. 2013, 54:149-153.
47. Iwamoto S., Higashi A., Ueno T., Goto M., Iguro Y., Sakata R. Protective effect of sivelestat sodium hydrate (ONO-5046) on ischemic spinal cord injury. Interact. Cardiovasc. Thorac. Surg. 2009, 8:606-609.
48. Iwatsuki K., Kumura E., Yoshimine T., Yamamoto K., Sato M., Hayakawa T. Increase in jugular levels of polymorphonuclear neutrophil elastase in patients with acute cerebral infarction. Neurol. Res. 1998, 20:397-402.
49. Jackson P.L., Xu X., Wilson L., Weathington N.M., Clancy J.P., Blalock J.E., Gaggar A. Human neutrophil elastase-mediated cleavage sites of MMP-9 and TIMP-1: implications to cystic fibrosis proteolytic dysfunction. Mol. Med. 2010, 16:159-166.
50. Junger W.G., Rhind S.G., Rizoli S.B., Cuschieri J., Baker A.J., Shek P.N., Hoyt D.B., Bulger E.M. Prehospital hypertonic saline resuscitation attenuates the activation and promotes apoptosis of neutrophils in patients with severe traumatic brain injury. Shock 2013, 40:366-374.
51. Kawabata K., Hagio T., Matsuoka S. The role of neutrophil elastase in acute lung injury. Eur. J. Pharmacol. 2002, 451:1-10.
52. Kenne E., Erlandsson A., Lindbom L., Hillered L., Clausen F. Neutrophil depletion reduces edema formation and tissue loss following traumatic brain injury in mice. J. Neuroinflammation 2012, 9. 10.1186/1742-2094-1189-1117.
53. Kikuchi T., Kugimiya T., Katashima S. Usefulness of sivelestat sodium administration in patients with aspiration pneumonia. J. Anesth. 2006, 20.
54. Knoblach S.M., Faden A.I. Administration of either anti-intercellular adhesion molecule-1 or a nonspecific control antibody improves recovery after traumatic brain injury in the rat. J. Neurotrauma 2002, 19:1039-1050.
55. Kohira S., Oka N., Inoue N., Itatani K., Hanayama N., Kitamura T., Fujii M., Takeda A., Oshima H., Tojo K., Yoshitake S., Miyaji K. Effect of the Neutrophil Elastase Inhibitor Sivelestat on Perioperative Inflammatory Response After Pediatric Heart Surgery with Cardiopulmonary Bypass: A Prospective Randomized Study. Artif. Organs 2013, 37:1027-1033.
56. Korkmaz B., Moreau T., Gauthier F. Neutrophil elastase, proteinase 3 and cathepsin G: Physicochemical properties, activity and physiopathological functions. Biochimie 2008, 90:227-242.
57. Krams M., Lees K.R., Hacke W., Grieve A.P., Orgogozo J.M., Ford G.A., Investigators A.S. Acute Stroke Therapy by Inhibition of Neutrophils (ASTIN): an adaptive dose-response study of UK-279,276 in acute ischemic stroke. Stroke 2003, 34:2543-2548.
58. Kraupp B.G., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., Schulte-Hermann R. In situ detection of fragmented DNA (tunel assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note. Hepatology 1995, 21:1465-1468.
59. Langlois J.A. Traumatic brain injury in the United States: Assessing outcomes in children: Summary and recommendations from the Expert Working Group, October 26-27 2000, Division of Acute Care, Rehabilitation Research and Disability Prevention, National Center for Injury Prevention and Control, Centers for Disease Control and Prevention, Department of Health and Human Services Atlanta, GA.
60. Lee T.W., Tsang V.W., Birch N.P. Synaptic plasticity-associated proteases and protease inhibitors in the brain linked to the processing of extracellular matrix and cell adhesion molecules. Neuron Glia Biol. 2008, 4:223-234.
61. Liu S., Levine S.R., Winn H.R. Targeting ischemic penumbra Part 1: from physiology to therapeutic strategy. J Exp Stroke Transl Med 2010, 3:47-55.
62. Matayoshi H., Hirata T., Yamashita S., Ishida K., Mizukami Y., Gondo T., Matsumoto M., Sakabe T. Neutrophil elastase inhibitor attenuates hippocampal neuronal damage after transient forebrain ischemia in rats. Brain Res. 2009, 1259:98-106.
63. Matsumoto S., Hidaka S., Goto K., Hagiwara S., Shingu C., Iwasaka H., Noguchi T. Sivelestat treatment for acute respiratory distress syndrome in an infant. J. Anesth. 2009, 23:288-291.
64. Mehta J.L., Nichols W.W., Nicolini F.A., Hendricks J., Donnelly W.H., Saldeen T.G. Neutrophil elastase inhibitor ICI 200,880 protects against attenuation of coronary flow reserve and myocardial dysfunction following temporary coronary artery occlusion in the dog. Cardiovasc. Res. 1994, 28:947-956.
65. Meyer-Hoffert U., Wiedow O. Neutrophil serine proteases: mediators of innate immune responses. Curr. Opin. Hematol. 2011, 18:19-24.
66. Mussack T., Biberthaler P., Gippner-Steppert C., Kanz K.G., Wiedemann E., Mutschler W., Jochum M. Early cellular brain damage and systemic inflammatory response after cardiopulmonary resuscitation or isolated severe head trauma: a comparative pilot study on common pathomechanisms. Resuscitation 2001, 49:193-199.
67. Nagy Z., Kolev K., Csonka E., Vastag M., Machovich R. Perturbation of the integrity of the blood-brain barrier by fibrinolytic enzymes. Blood Coagul. Fibrinolysis 1998, 9:471-478.
68. Natale J.E., Joseph J.G., Pretzlaff R.K., Silber T.J., Guerguerian A.M. Clinical trials in pediatric traumatic brain injury: unique challenges and potential responses. Dev. Neurosci. 2006, 28:276-290.
69. Newcombe V.F., Williams G.B., Outtrim J.G., Chatfield D., Gulia Abate M., Geeraerts T., Manktelow A., Room H., Mariappen L., Hutchinson P.J., Coles J.P., Menon D.K. Microstructural basis of contusion expansion in traumatic brain injury: insights from diffusion tensor imaging. J. Cereb. Blood Flow Metab. 2013, 33:855-862.
70. Nguyen H.X., O'Barr T.J., Anderson A.J. Polymorphonuclear leukocytes promote neurotoxicity through release of matrix metalloproteinases, reactive oxygen species, and TNF-α. J. Neurochem. 2007, 102:900-912.
71. Noble L.J., Donovan F., Igarashi T., Goussev S., Werb Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 2002, 22:7526-7535.
72. Phan S.H., Gannon D.E., Ward P.A., Karmiol S. Mechanism of neutrophil-induced xanthine dehydrogenase to xanthine oxidase conversion in endothelial cells: evidence of a role for elastase. Am. J. Respir. Cell Mol. Biol. 1992, 6:270-278.
73. Piccard H., Muschel R.J., Opdenakker G. On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit. Rev. Oncol. Hematol. 2012, 82:296-309.
74. Pinheiro J., Bates D., DebRoy S., Sarkar D., Team R.D.C. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3:1-104 2012.
75. Potts M., Koh S.-E., Whetstone W., Walker B., Yoneyama T., Claus C., Manvelyan H., Noble-Haeusslein L. Traumatic injury to the immature brain: inflammation, oxidative injury, and iron-mediated damage as potential therapeutic targets. Neuroreport 2006, 3:143-153.
76. Prestigiacomo C.J., Kim S.C., Connolly J.E.S., Liao H., Yan S.F., Pinsky D.J. CD18-mediated neutrophil recruitment contributes to the pathogenesis of reperfused by not nonreperfused stroke. Stroke 1999, 30:1110-1117.
77. Pullela R., Raber J., Pfankuch T., Ferriero D.M., Claus C.P., Koh S.-E., Yamauchi T., Rola R., Fike J.R., Noble-Haeusslein L.J. Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Dev. Neurosci. 2006, 28:396-409.
78. Rhind S.G., Crnko N.T., Baker A.J., Morrison L.J., Shek P.N., Scarpelini S., Rizoli S.B. Prehospital resuscitation with hypertonic saline-dextran modulates inflammatory, coagulation and endothelial activation marker profiles in severe traumatic brain injured patients. J. Neuroinflammation 2010, 18:5.
79. Rhodes J. Peripheral immune cells in the pathology of traumatic brain injury?. Curr. Opin. Crit. Care 2011, 17:122-130.
80. Roberts D.J., Jenne C.N., Léger C., Kramer A.H., Gallagher C.N., Todd S., Parney I.F., Doig C.J., Yong V.W., Kubes P., Zygun D.A. A prospective evaluation of the temporal matrix metalloproteinase response after severe traumatic brain injury in humans. J. Neurotrauma 2013, 30:1717-1726.
81. Ryter S.W., Tyrrell R.M. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 2000, 15:289-309.
82. Schmitz C., Hof P.R. Design-based stereology in neuroscience. Neuroscience 2005, 130:813-831.
83. Semple B.D., Bye N., Ziebell J.M., Morganti-Kossmann M.C. Deficiency of the chemokine receptor CXCR2 attenuates neutrophil infiltration and cortical damage following closed head injury. Neurobiol. Dis. 2010, 40:394-403.
84. Semple B.D., Bye N., Rancan M., Ziebell J.M., Morganti-Kossmann M.C. Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL2-/- mice. J. Cereb. Blood Flow Metab. 2010, 30:769-782.
85. Semple B.D., Canchola S.A., Noble-Haeusslein L. Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. J. Neurotrauma 2012, 29:2672-2683.
86. Semple B.D., Blomgren K., Gimlin K., Ferriero D.M., Noble-Haeusslein L.J. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog. Neurobiol. 2013, 106-107:1-16.
87. Shapiro S.D. Neutrophil Elastase: Path Clearer, Pathogen Killer, or Just Pathologic?. Am. J. Respir. Cell Mol. Biol. 2002, 26:266-268.
88. Shimakura A., Kamanaka Y., Ikeda Y., Kondo K., Suzuki Y., Umenura K. Neutrophil elastase inhibition reduces cerebral ischemic damage in the middle cerebral artery occlusion. Brain Res. 2000, 858:55-60.
89. Sommerhoff C.P., Krell R.D., Williams J.L., Gomes B.C., Strimpler A.M., Nadel J.A. Inhibition of human neutrophil elastase by ICI 200,355. Eur. J. Pharmacol. 1991, 193:153-158.
90. Starcher B., O'neal P., Granstein R.D., Beissert S. Inhibition of neutrophil elastase suppresses the development of skin tumors in hairless mice. J Invest Dermatol 1996, 107:159-163.
91. Stirling D.P., Liu S., Kubes P., Yong V.W. Depletion of Ly6G/Gr-1 Leukocytes after Spinal Cord Injury in Mice Alters Wound Healing and Worsens Neurological Outcome. J. Neurosci. Methods 2009, 29:753-764.
92. Stowe A.M., Adair-Kirk T.L., Gonzales E.R., Perez R.S., Shah A.R., Park T.S., Gidday J.M. Neutrophil elastase and neurovascular injury following focal stroke and reperfusion. Neurobiol. Dis. 2009, 35:82-90.
93. Team R.C. R: A language and environment for statistical computing. R Foundation for Statistical Computing 2012, (pp http://www.R-project.org/. Vienna.).
94. Tiefenbacher C.P., Ebert M., Niroomand F., Batkai S., Tillmanns H., Zimmermann R., Kübler W. Inhibition of elastase improves myocardial function after repetitive ischaemia and myocardial infarction in the rat heart. Pflugers Arch. 1997, 433:563-570.
95. Tkalcevic J., Novelli M., Phylactides M., Iredale J.P., Segal A.W., Roes J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 2000, 12:201-210.
96. Tonai T., Shiba K., Taketani Y., Ohmoto Y., Murata K., Muraguchi M., Ohsaki H., Takeda E., Nishisho T. A neutrophil elastase inhibitor (ONO-5046) reduces neurologic damage after spinal cord injury in rats. J. Neurochem. 2001, 78:1064-1072.
97. Tong W., Igarashi T., Ferriero D.M., Noble L.J. Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability. Exp. Neurol. 2002, 176:105-116.
98. Tsuru-Aoyagi K., Potts M., Trivedi A., Pfankuch T., Raber J., Wendland M., Claus C., Koh S.-E., Ferriero D., Noble-Haeusslein L. Glutathione peroxidase activity modulates recovery in the injured immature brain. Ann. Neurol. 2009, 65:540-549.
99. Weinzierl M., Mautes A.E., Whetstone W., Lin Y., Noble-Haeusslein L.J. Endothelin-mediated induction of heme oxygenase-1 in the spinal cord is attenuated in transgenic mice overexpressing superoxide dismutase. Brain Res. 2004, 1030:125-132.
100. Weiss S.J. Tissue destruction by neutrophils. N. Engl. J. Med. 1989, 329:365-376.
101. Whalen M.J., Clark R.S., Dixon C.E., Robichaud P., Marion D.W., Vagni V., Graham S.H., Virag L., Hasko G., Stachlewitz R., Szabo C., Kochanek P.M. Reduction of cognitive and motor deficits after traumatic brain injury in mice deficient in poly(ADP-ribose). J. Cereb. Blood Flow Metab. 1999, 19:835-842.
102. Williams J.C., Falcone R.C., Knee C., Stein R.L., Strimpler A.M., Reaves B., Giles R.E., Krell R.D. Biologic characterization of ICI 200,880 and ICI 200,355, novel inhibitors of human neutrophil elastase. Am. Rev. Respir. Dis. 1991, 144:875-883.
103. Woodman R.C., Reinhardt P.H., Kanwar S., Johnston F.L., Kubes P. Effects of human neutrophil elastase (HNE) on neutrophil function in vitro and in inflamed microvessels. Blood 1993, 82:2188-2195.
104. Yang M., Silverman J.L., Crawley J.N. Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci. 2011, (Chapter 8, Unit 8.26.1-8.26.16).
105. Young R.E., Thompson R.D., Larbi K.Y., La M., Roberts C.E., Shapiro S.D., Perritti M., Nourshargh S. Neutrophil elastase (NE)-deficient mice demonstrate a nonredundant role for NE in neutrophil migration, generation of proinflammatory mediators, and phagocytosis in response to zymosan particles in vivo. J. Immunol. 2004, 172:4493-4502.
106. 4-induced neutrophil transmigration in vivo assessed with a specific inhibitor and neutrophil elastase deficient mice. Br. J. Pharmacol. 2007, 151:628-637.
107. Young M.E., Clark M.H., Goffus A., Hoane M.R. Mixed effects modeling of Morris water maze data: Advantages and cautionary notes. Learn. Motiv. 2009, 40:160-177.
108. Zeiher B.G., Matsuoka S., Kawabata K., Repine J.E. Neutrophil elastase and acute lung injury: Prospects for sivelestat and other neutrophil elastase inhibitors as therapeutics. Crit. Care Med. 2002, 30:S281-S287.
109. Zhou X., Dai Q., Huang X. Neutrophils in acute lung injury. Front Biosci (Landmark Ed) 2012, 17:2278-2283.