Attenuated traumatic axonal injury and improved functional outcome after traumatic brain injury in mice lacking Sarm1

Brain

Volumn 139, Issue 4, 2016, Pages 1094-1105

  Henninger, Nils ^a   Bouley, James ^a   Sikoglu, Elif M ^a   An, Jiyan ^b   Moore, Constance M ^a   King, Jean A ^a   Bowser, Robert ^b   Freeman, Marc R ^a   Brown, Robert H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

axon; knockout; traumatic axonal injury; traumatic brain injury; Wallerian degeneration

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CHOLINE; N ACETYLASPARTIC ACID; PROTEIN; PROTEIN AGGREGATE; STERILE ALPHA ARMADILLO TOLL INTERLEUKIN RECEPTOR HOMOLOGY DOMAIN PROTEIN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; ARMADILLO DOMAIN PROTEIN; CYTOSKELETON PROTEIN; SARM1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXON; AXONAL INJURY; BRAIN BLOOD FLOW; BRAIN PERFUSION; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; FUNCTIONAL STATUS; MALE; MOTOR PERFORMANCE; MOUSE; NEUROFILAMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PHENOTYPE; PRECLINICAL STUDY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRAUMATIC BRAIN INJURY; WALLERIAN DEGENERATION; WILD TYPE; ANIMAL; BRAIN INJURY; C57BL MOUSE; CONVALESCENCE; DEFICIENCY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

AMYLOID BETA-PEPTIDES; ANIMALS; ARMADILLO DOMAIN PROTEINS; AXONS; BRAIN INJURIES; CORPUS CALLOSUM; CYTOSKELETAL PROTEINS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOVERY OF FUNCTION; WALLERIAN DEGENERATION;

EID: 84964005136     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww001     Document Type: Article

References (58)

1. Anderson KJ, Scheff SW, Miller KM, Roberts KN, Gilmer LK, Yang C, et al. The phosphorylated axonal form of the neurofilament subunit NF-H (pNF-H) as a blood biomarker of traumatic brain injury. J Neurotrauma 2008; 25: 1079-85.
2. Brown MC, Perry VH, Hunt SP, Lapper SR. Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration. Eur J Neurosci 1994; 6: 420-8.
3. Chuang CF, Bargmann CI. A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev 2005; 19: 270-81.
4. Coleman MP, Freeman MR. Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 2010; 33: 245-67.
5. Conforti L, Gilley J, Coleman MP. Wallerian degeneration: an emerging axon death pathway linking injury and disease. Nat Rev Neurosci 2014; 15: 394-409.
6. DeWitt DS, Prough DS. Traumatic cerebral vascular injury: the effects of concussive brain injury on the cerebral vasculature. J Neurotrauma 2003; 20: 795-825.
7. Duarte JM, Lei H, Mlynarik V, Gruetter R. The neurochemical profile quantified by in vivo 1H NMR spectroscopy. Neuroimage 2012; 61: 342-62.
8. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G∗Power 3.1: tests for correlation and regression analyses. Behav Res Methods 2009; 41: 1149-60.
9. Faul F, Erdfelder E, Lang AG, Buchner A. G∗Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007; 39: 175-91.
10. Faul MD, Xu L, Wald MM, Coronado VG. Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010.
11. Fleminger S, Ponsford J. Long term outcome after traumatic brain injury. BMJ 2005; 331: 1419-20.
12. Flierl MA, Stahel PF, Beauchamp KM, Morgan SJ, Smith WR, Shohami E. Mouse closed head injury model induced by a weightdrop device. Nat Protoc 2009; 4: 1328-37.
13. Freeman MR. Signaling mechanisms regulating Wallerian degeneration. Curr Opin Neurobiol 2014; 27: 224-31.
14. Gardner A, Iverson GL, Stanwell P. A systematic review of proton magnetic resonance spectroscopy findings in sport-related concussion. J Neurotrauma 2014; 31: 1-18.
15. Gatson JW, Barillas J, Hynan LS, Diaz-Arrastia R, Wolf SE, Minei JP. Detection of neurofilament-H in serum as a diagnostic tool to predict injury severity in patients who have suffered mild traumatic brain injury. J Neurosurg 2014; 121: 1232-8.
16. Gerdts J, Brace EJ, Sasaki Y, DiAntonio A, Milbrandt J. Neurobiology. SARM1 activation triggers axon degeneration locally via NAD( + ) destruction. Science 2015; 348: 453-7.
17. Gerdts J, Summers DW, Sasaki Y, DiAntonio A, Milbrandt J. Sarm1-mediated axon degeneration requires both SAM and TIR interactions. J Neurosci 2013; 33: 13569-80.
18. Gilley J, Coleman MP. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 2010; 8: e1000300.
19. Godzik K, Coleman MP. The axon-protective WLD(S) protein partially rescues mitochondrial respiration and glycolysis after axonal injury. J Mol Neurosci 2015; 55: 865-71.
20. Greer JE, McGinn MJ, Povlishock JT. Diffuse traumatic axonal injury in the mouse induces atrophy, c-Jun activation, and axonal outgrowth in the axotomized neuronal population. J Neurosci 2011; 31: 5089-105.
21. Harris JL, Yeh HW, Choi IY, Lee P, Berman NE, Swerdlow RH, et al. Altered neurochemical profile after traumatic brain injury: (1)HMRS biomarkers of pathological mechanisms. J Cereb Blood Flow Metab 2012; 32: 2122-34.
22. Henninger N, Bouley J, Bratane BT, Bastan B, Shea M, Fisher M. Laser Doppler flowmetry predicts occlusion but not tPA-mediated reperfusion success after rat embolic stroke. Exp Neurol 2009; 215: 290-7.
23. Henninger N, Dutzmann S, Sicard KM, Kollmar R, Bardutzky J, Schwab S. Impaired spatial learning in a novel rat model of mild cerebral concussion injury. Exp Neurol 2005; 195: 447-57.
24. Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Exp Neurol 2013; 246: 35-43.
25. Kelley BJ, Farkas O, Lifshitz J, Povlishock JT. Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Exp Neurol 2006; 198: 350-60.
26. Kilinc D, Gallo G, Barbee KA. Mechanical membrane injury induces axonal beading through localized activation of calpain. Exp Neurol 2009; 219: 553-61.
27. Kim Y, Zhou P, Qian L, Chuang JZ, Lee J, Li C, et al. MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. J Exp Med 2007; 204: 2063-74.
28. Kirov, II, Tal A, Babb JS, Reaume J, Bushnik T, Ashman TA, et al. Proton MR spectroscopy correlates diffuse axonal abnormalities with post-concussive symptoms in mild traumatic brain injury. J Neurotrauma 2013; 30: 1200-4.
29. Knoferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, et al. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci USA 2010; 107: 6064-9.
30. Lamprecht MR, Sabatini DM, Carpenter AE. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques 2007; 42: 71-5.
31. Len TK, Neary JP. Cerebrovascular pathophysiology following mild traumatic brain injury. Clin Physiol Funct Imaging 2011; 31: 85-93.
32. Lin CW, Liu HY, Chen CY, Hsueh YP. Neuronally-expressed Sarm1 regulates expression of inflammatory and antiviral cytokines in brains. Innate Immun 2014; 20: 161-72.
33. Longhi L, Gesuete R, Perego C, Ortolano F, Sacchi N, Villa P, et al. Long-lasting protection in brain trauma by endotoxin preconditioning. J Cereb Blood Flow Metab 2011; 31: 1919-29.
34. Ma M, Ferguson TA, Schoch KM, Li J, Qian Y, Shofer FS, et al. Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration. Neurobiol Dis 2013; 56: 34-46.
35. Martin SM, O'Brien GS, Portera-Cailliau C, Sagasti A. Wallerian degeneration of zebrafish trigeminal axons in the skin is required for regeneration and developmental pruning. Development 2010; 137: 3985-94.
36. Maxwell WL, Bartlett E, Morgan H. Wallerian degeneration in the optic nerve stretch-injury model of traumatic brain injury: a stereological analysis. J Neurotrauma 2015; 32: 780-90.
37. Maxwell WL, Domleo A, McColl G, Jafari SS, Graham DI. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J Neurotrauma 2003; 20: 151-68.
38. McCrea M, Guskiewicz KM, Marshall SW, Barr W, Randolph C, Cantu RC, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003; 290: 2556-63.
39. O'Neill LA, Fitzgerald KA, Bowie AG. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol 2003; 24: 286-90.
40. Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 2012; 337: 481-4.
41. Penkowa M, Camats J, Giralt M, Molinero A, Hernandez J, Carrasco J, et al. Metallothionein-I overexpression alters brain inflammation and stimulates brain repair in transgenic mice with astrocytetargeted interleukin-6 expression. Glia 2003; 42: 287-306.
42. Philip S, Udomphorn Y, Kirkham FJ, Vavilala MS. Cerebrovascular pathophysiology in pediatric traumatic brain injury. J Trauma 2009; 67: S128-34.
43. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 1993; 30: 672-9.
44. Provencher SW. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 2001; 14: 260-4.
45. Samoriski GM, Applegate CD. Repeated generalized seizures induce time-dependent changes in the behavioral seizure response independent of continued seizure induction. J Neurosci 1997; 17: 5581-90.
46. Schuhmann MU, Stiller D, Skardelly M, Bernarding J, Klinge PM, Samii A, et al. Metabolic changes in the vicinity of brain contusions: a proton magnetic resonance spectroscopy and histology study. J Neurotrauma 2003; 20: 725-43.
47. Siman R, Toraskar N, Dang A, McNeil E, McGarvey M, Plaum J, et al. A panel of neuron-enriched proteins as markers for traumatic brain injury in humans. J Neurotrauma 2009; 26: 1867-77.
48. Smith DH, Hicks R, Povlishock JT. Therapy development for diffuse axonal injury. J Neurotrauma 2013; 30: 307-23.
49. Staal JA, Dickson TC, Gasperini R, Liu Y, Foa L, Vickers JC. Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J Neurochem 2010; 112: 1147-55.
50. Vagnozzi R, Signoretti S, Cristofori L, Alessandrini F, Floris R, Isgro E, et al. Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain 2010; 133: 3232-42.
51. Walker PA, Harting MT, Jimenez F, Shah SK, Pati S, Dash PK, et al. Direct intrathecal implantation of mesenchymal stromal cells leads to enhanced neuroprotection via an NFkappaBmediated increase in interleukin-6 production. Stem Cells Dev 2010; 19: 867-76.
52. Waller AV. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond 1850; 140: 423-9.
53. Wang J, Hamm RJ, Povlishock JT. Traumatic axonal injury in the optic nerve: evidence for axonal swelling, disconnection, dieback, and reorganization. J Neurotrauma 2011; 28: 1185-98.
54. Wang JT, Medress ZA, Barres BA. Axon degeneration: molecular mechanisms of a self-destruction pathway. J Cell Biol 2012; 196: 7-18.
55. Warner MA, Marquez de la Plata C, Spence J, Wang JY, Harper C, Moore C, et al. Assessing spatial relationships between axonal integrity, regional brain volumes, and neuropsychological outcomes after traumatic axonal injury. J Neurotrauma 2010; 27: 2121-30.
56. Wolf JA, Stys PK, Lusardi T, Meaney D, Smith DH. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J Neurosci 2001; 21: 1923-30.
57. Yang J, Weimer RM, Kallop D, Olsen O, Wu Z, Renier N, et al. Regulation of axon degeneration after injury and in development by the endogenous calpain inhibitor calpastatin. Neuron 2013; 80: 1175-89.
58. Yin TC, Britt JK, De Jesus-Cortes H, Lu Y, Genova RM, Khan MZ, et al. P7C3 neuroprotective chemicals block axonal degeneration and preserve function after traumatic brain injury. Cell Rep 2014; 8: 1731-40.