375
Views
12
CrossRef citations to date
0
Altmetric
Sports Medicine and Biomechanics

Inflammatory and apoptotic signalling pathways and concussion severity: a genetic association study

, , , , &
Pages 2226-2234 | Accepted 28 Feb 2018, Published online: 06 Mar 2018

References

  • Abrahams, S., Mc Fie, S., Patricios, J., Posthumus, M., & September, A. V. (2014). Risk factors for sports concussion: An evidence-based systematic review. British Journal of Sports Medicine, 48(2), 91–97.
  • Almolda, B., Villacampa, N., Manders, P., Hidalgo, J., Campbell, I. L., González, B., & Castellano, B. (2014). Effects of astrocyte-targeted production of interleukin-6 in the mouse on the host response to nerve injury. Glia, 62(7), 1142–1161.
  • Basu, A., Krady, J. K., & Levison, S. W. (2004). Interleukin-1: A master regulator of neuroinflammation. Neuroscience Letters, 156, 151–156.
  • Bélanger, M., Allaman, I., & Magistretti, P. J. (2011). Differential effects of pro- and anti-inflammatory cytokines alone or in combinations on the metabolic profile of astrocytes. Journal of Neurochemistry, 116(4), 564–576.
  • Blaylock, R. L., & Maroon, J. (2011). Immunoexcitotoxicity as a central mechanism in chronic traumatic encephalopathy — A unifying hypothesis. Surgical Neurology International, 2(107.10), 4103.
  • Brown, G. C., & Neher, J. J. (2010). Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Molecular Neurobiology, 41(2–3), 242–247.
  • Cancelliere, C., Hincapié, C. A., Keightley, M., Godbolt, A. K., Côté, P., Kristman, V. L., … Cassidy, J. D. (2014). Systematic review of prognosis and return to play after sport concussion: Results of the international collaboration on mild traumatic brain injury prognosis. Archives of Physical Medicine and Rehabilitation, 95(3 Suppl), S210–29.
  • Chao, C. C. C., Hu, S. X., Ehrlich, L., & Peterson, P. K. K. (1995). Interleukin-1 and tumor necrosis factor-alpha synergistically mediate neurotoxicity: Involvement of nitric oxide and of N-methyl-D-aspartate receptors. Brain, Behavior, and Immunity, 9, 355–365.
  • Chen, J.-K., Johnston, K. M., Collie, A., McCrory, P., & Ptito, A. (2007). A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. Journal of Neurology, Neurosurgery, and Psychiatry, 78, 1231–1238.
  • Clausen, F., Hånell, A., Israelsson, C., Hedin, J., Ebendal, T., Mir, A. K., … Marklund, N. (2011). Neutralization of interleukin-1β reduces cerebral edema and tissue loss and improves late cognitive outcome following traumatic brain injury in mice. European Journal of Neuroscience, 34, 110–123.
  • Conti, A. C., Raghupathi, R., Trojanowski, J. Q., & McIntosh, T. K. (1998). Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. The Journal of Neuroscience, 18(15), 5663–5672.
  • Erlanger, D., Kaushik, T., Cantu, R., Barth, J. T., Broshek, D. K., Freeman, J. R., & Webbe, F. M. (2003). Symptom-based assessment of the severity of a concussion. Journal of Neurosurgery, 98(3), 477–484.
  • Erta, M., Quintana, A., & Hidalgo, J. (2012). Interleukin-6, a major cytokine in the central nervous system. International Journal of Biological Sciences, 8(9), 1254–1266.
  • Fishman, D., Faulds, G., Jeffery, R., Mohamed-Ali, V., Yudkin, J. S., Humphries, S., & Woo, P. (1998). The effect of novel polymorphisms in the interleukin-6 (IL-6) gene on IL-6 transcription and plasma IL-6 Levels, and an association with systemic-onset juvenile chronic arthritis. American Society for Clinical Investigation, 102(7), 1369–1376.
  • Frost, B., & Feany, M. B. (2015). Connecting the dots between tau dysfunction and neurodegeneration. Trends in Cell Biology, 25(1), 46–53.
  • Gaudino, M., Andreotti, F., Zamparelli, R., Di Castelnuovo, A., Nasso, G., Burzotta, F., & Iacoviello, L. (2003). The −174G/C interleukin-6 polymorphism influences postoperative interleukin-6 levels and postoperative atrial fibrillation. Is atrial fibrillation an inflammatory complication? Circulation, 108, 195–199.
  • González, J. R., Armengol, L., Solé, X., Guinó, E., Mercader, J. M., Estivill, X., & Moreno, V. (2007). SNPassoc: An R package to perform whole genome association studies. Bioinformatics, 23(5), 644–645.
  • Guskiewicz, K. M., Register-Mihalik, J., McCrory, P., McCrea, M., Johnston, K., Makdissi, M., … Meeuwisse, W. (2013). Evidence-based approach to revising the SCAT2: Introducing the SCAT3. British Journal of Sports Medicine, 47(5), 289–293.
  • Harrison, J. L., Rowe, R. K., O’Hara, B. F., Adelson, P. D., & Lifshitz, J. (2014). Acute over-the-counter pharmacological intervention does not adversely affect behavioral outcome following diffuse traumatic brain injury in the mouse. Experimental Brain Research, 232(9), 2709–2719.
  • Heise, V., Filippini, N., Ebmeier, K. P., & Mackay, C. E. (2011). The APOE ɛ4 allele modulates brain white matter integrity in healthy adults. Molecular Psychiatry, 16(9), 908–916.
  • Hopkins, S. J., & Rothwell, N. J. (1995). Cytokines and the nervous system I : Expression and recognition. Trends in Neurosciences, 18, 83–88.
  • Hulkkonen, J., Pertovaara, M., Antonen, J., Pasternack, A., & Hurme, M. (2001). Elevated interleukin-6 plasma levels are regulated by the promoter region polymorphism of the IL6 gene in primary Sjogren’s syndrome and correlate with the clinical manifestations of the disease. Clinical and Experimental Immunology, 6, 656–661.
  • Jeter, C. B., Hergenroeder, G. W., Hylin, M. J., Redell, J. B., Moore, A. N., & Dash, P. K. (2013). Biomarkers for the diagnosis and prognosis of mild traumatic brain injury/concussion. Journal of Neurotrauma, 30(8), 657–670.
  • Kerr, Z. Y., Marshall, S. W., & Guskiewicz, K. M. (2012). Reliability of concussion history in former professional football players. Medicine and Science in Sports and Exercise, 44(3), 377–382.
  • Kerr, Z. Y., Mihalik, J. P., Guskiewicz, K. M., Rosamond, W. D., Evenson, K. R., & Marshall, S. W. (2015). Agreement between athlete-recalled and clinically documented concussion histories in former collegiate athletes. The American Journal of Sports Medicine, 43(3), 606–613.
  • Kinnaman, K. A., Mannix, R. C., Dawn Comstock, R., & Meehan, W. P. (2013). Management strategies and medication use for treating paediatric patients with concussions. Acta Paediatrica, International Journal of Paediatrics, 102(9), 424–428.
  • Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: A diffusion tensor imaging study. Brain, 130(10), 2508–2519.
  • Lai, A. Y., & Todd, K. G. (2008). Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia, 56, 259–270.
  • Lee, S. C., Dickson, D. W., Liu, W., & Brosnan, C. F. (1993). Induction of nitric oxide synthase activity in human astrocytes by interleukin-1β and interferon-γ. Journal of Neuroimmunology, 46(1), 19–24.
  • Lenzlinger, P. M., Morganti-Kossmann, M. C., Laurer, H. L., & McIntosh, T. K. (2001). The duality of the inflammatory response to traumatic brain injury. Molecular Neurobiology, 24(1–3), 169–181.
  • Little, J., Higgins, J. P. T., Ioannidis, J. P. A., Moher, D., Gagnon, F., Von Elm, E., … Birkett, N. (2009). STrengthening the REporting of genetic association studies (STREGA)- An extension of the STROBE statement. European Journal of Clinical Investigation, 39(4), 247–266.
  • Loddick, S. A., & Rothwell, N. J. (1996). Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. Journal of Cerebral Blood Flow and Metabolism : Official Journal of the International Society of Cerebral Blood Flow and Metabolism, 16(5), 932–940.
  • Lovell, M. R., & Collins, M. W. (1998). Neuropsychological assessment of the college football player. The Journal of Head Trauma Rehabilitation, 13(2), 9–26.
  • Madura, S. A., McDevitt, J. K., Tierney, R. T., Mansell, J. L., Hayes, D. J., Gaughan, J. P., & Krynetskiy, E. (2016). Genetic variation in SLC17A7 promoter associated with response to sport-related concussions. Brain Injury, 30(7), 908–913.
  • Makdissi, M., Darby, D., Maruff, P., Ugoni, A., Brukner, P., & McCrory, P. R. (2010). Natural history of concussion in sport markers of severity and implications for management. American Journal of Sports Medicine, 38(3), 464–471.
  • Mccrea, M., Guskiewicz, K. M., Marshall, S. W., Barr, W., Randolph, C., Cantu, R. C., … Page, P. (2014). Acute effects and recovery time following concussion in collegiate football players. Jama, 290(19), 2556–2563.
  • McCrory, P., Meeuwisse, W., Dvorak, J., Aubry, M., Bailes, J., Broglio, S., … Vos, P. E. (2017). Consensus statement on concussion in sport—The 5th international conference on concussion in sport held in Berlin, October 2016. British Journal of Sports Medicine. doi:10.1136/bjsports-2017-097699
  • McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R., … Turner, M. (2013). Consensus statement on concussion in sport: The 4th international conference on concussion in sport held in Zurich, November 2012. British Journal of Sports Medicine, 47(2), 250–258.
  • McDevitt, J. K., Tierney, R. T., Mansell, J. L., Driban, J. B., Higgins, M., Toone, N., … Krynetskiy, E. (2011). Neuronal structural protein polymorphism and concussion in college athletes. Brain Injury, 25(11), 1108–1113.
  • McDevitt, J. K., Tierney, R. T., Phillips, J., Gaughan, J. P., Torg, J. S., & Krynetskiy, E. (2015). Association between GRIN2A promoter polymorphism and recovery from concussion. Brain Injury, 29(13–14), 1674–1681.
  • Merritt, V., & Arnett, P. (2016). Apolipoprotein E (APOE) ϵ4 allele Is associated with increased symptom reporting following sports concussion. Journal of the International Neuropsychological Society, 21(1), 89–94.
  • Merritt, V., Rabinowitz, A., & Arnett, P. (2016). The e4 allele of the APOE gene influences neurocognitive performance variability following sports-related concussion. Archives of Clinical Neuropsychology, 31(6), 628.
  • Mietelska-Porowska, A., Wasik, U., Goras, M., Filipek, A., & Niewiadomska, G. (2014). Tau protein modifications and interactions: Their role in function and dysfunction. International Journal of Molecular Sciences, 15, 4671–4713.
  • Miñambres, E., Cemborain, A., Sánchez-Velasco, P., Gandarillas, M., Díaz-Regañón, G., Sánchez-González, U., & Leyva-Cobián, F. (2003). Correlation between transcranial interleukin-6 gradient and outcome in patients with acute brain injury. Critical Care Medicine, 31(3), 933–938.
  • Morganti-Kossmann, M. C., Rancan, M., Stahel, P. F., & Kossmann, T. (2002). Inflammatory response in acute traumatic brain injury: A double-edged sword. Current Opinion in Critical Care, 8(2), 101–105.
  • Nathoo, N., Chetty, R., Van Dellen, J. R., & Barnett, G. H. (2003). Genetic vulnerability following traumatic brain injury: The role of apolipoprotein E. Molecular Pathology, 56(3), 132–136.
  • Norris, J. G., Tang, L. P., Sparacio, S. M., & Benveniste, E. N. (1994). Signal transduction pathways mediating astrocyte IL-6 induction by IL-1 beta and tumor necrosis factor-alpha. Journal of Immunology (Baltimore, Md. : 1950), 152(2), 841–850. Retrieved from http://www.jimmunol.org/content/152/2/841.abstract
  • Panenka, W., Gardner, A., Dretsch, M., Crynen, G., Crawford, F. C., & Iverson, G. L. (2017). Systematic review of genetic risk factors for sustaining a mild traumatic brain injury. Journal of Neurotrauma, 34, 2093–2099. neu.2016.4833.
  • Papa, L., Ramia, M. M., Edwards, D., Johnson, B. D., & Slobounov, S. M. (2014). Systematic review of clinical studies examining biomarkers of brain injury in athletes after sports-related concussion. Journal of Neurotrauma, 32, 661–673.
  • Patterson, Z. R., & Holahan, M. R. (2012). Understanding the neuroinflammatory response following concussion to develop treatment strategies. Frontiers in Cellular Neuroscience, 6(December), 58.
  • Persson, J., Lind, J., Larsson, A., Ingvar, M., Cruts, M., van Broeckhoven, C., … Nyberg, L. (2006). Altered brain white matter integrity in healthy carriers of the APOE epsilon 4 allele: A risk for AD? Neurology, 66(7), 1029–1033.
  • R Core Team, R. (2013). R: A language and environment for statistical computing. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  • Raghupathi, R., Conti, A. C., Graham, D. I., Krajewski, S., Reed, J. C., Grady, M. S., … Mcintosh, T. K. (2002). Mild traumatic brain injury induces apoptotic cell death in the cortex that is preceded by decreases in cellular bcl-2 immunoreactivity. Science, 110(4), 605–616.
  • Rathbone, A. T. L., Surejini, S., Jiang, S., Rathbone, M. P., & Kumbhare, D. A. (2015). A review of the neuro- and systemic inflammatory responses in post concussion symptoms: Introduction of the “post-inflammatory brain syndrome” PIBS. Brain, Behavior, and Immunity, 46, 1–16.
  • Relton, J. K., Martin, D., Thompson, R. C., & Russell, D. A. (1996). Peripheral administration of Interleukin-1 Receptor antagonist inhibits brain damage after focal cerebral ischemia in the rat. Experimental Neurology, 138(2), 206–213.
  • Rink, A., Fung, K. M., Trojanowski, J. Q., Lee, V. M., Neugebauer, E., & McIntosh, T. K. (1995). Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. The American Journal of Pathology, 147(6), 1575–1583. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1869937&tool=pmcentrez&rendertype=abstract
  • Rothwell, N. (2003). Interleukin-1 and neuronal injury: Mechanisms, modification, and therapeutic potential. Brain, Behavior and Immunity, 17, 152–157.
  • Santtila, S., Savinainen, K., & Hurme, M. (1998). Presence of the IL-1RA allele 2 (IL1RN*2) is associated with enhanced IL-1b production in vitro. Scandinavian Journal of Immunology, 47, 195–198.
  • Schaid, D. J., Rowland, C. M., Tines, D. E., Jacobson, R. M., & Poland, G. A. (2002). Score tests for association between traits and haplotypes when linkage phase is ambiguous. American Journal of Human Genetics, 70(2), 425–434.
  • Schlosberg, D., Benifla, M., Kaufer, D., & Friedman, A. (2010). Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nature Reviews Neurology, 6, 393–403.
  • Schneider, K. J., Iverson, G. L., Emery, C. A., Mccrory, P., Herring, S. A., & Meeuwisse, W. H. (2013). The effects of rest and treatment following sport-related concussion: A systematic review of the literature. British Journal of Sports Medicine, 47, 304–307.
  • September, A. V., Nell, E.-M., O’Connell, K., Cook, J., Handley, C. J., van der Merwe, L., … Collins, M. (2011). A pathway-based approach investigating the genes encoding interleukin-1, interleukin-6 and the interleukin-1 receptor antagonist provides new insight into the genetic susceptibility of Achilles tendinopathy. British Journal of Sports Medicine, 45, 1040–1047.
  • Singhal, A., Baker, A. J., Hare, G. M. T., Reinders, F. X., Schlichter, L. C., & Moulton, R. J. (2002). Association between cerebrospinal fluid interleukin-6 concentrations and outcome after severe human traumatic brain injury. Journal of Neurotrauma, 19(8), 929–937.
  • Smith, C., Gentleman, S. M., Leclercq, P. D., Murray, L. S., Griffin, W. S. T., Graham, D. I., & Nicoll, J. A. R. (2013). The neuroinflammatory response in humans after traumatic brain injury. Neuropathology and Applied Neurobiology, 39(6), 654–666.
  • Stivala, F., Mazzarino, M. C., & Malaponte, G. (2006). Analysis of G(−174)C IL-6 polymorphism and plasma concentrations of inflammatory markers in patients with type 2 diabetes and peripheral arterial disease. Journal of Clinical Pathology, 59, 211–216.
  • Su, S.-H., Xu, W., Li, M., Zhang, L., Wu, Y.-F., Yu, F., & Hai, J. (2014). Elevated C-reactive protein levels may be a predictor of persistent unfavourable symptoms in patients with mild traumatic brain injury: A preliminary study. Brain, Behavior, and Immunity, 38, 111–117.
  • Sun, T., Gao, Y., Tan, W., Ma, S., Shi, Y., Yao, J., … Lin, D. (2007). A six-nucleotide insertion-deletion polymorphism in the CASP8 promoter is associated with susceptibility to multiple cancers. Nature Genetics, 39(5), 605–613.
  • Terrell, T. R., Bostick, R. M., Barth, J. T., Mckeag, D., Cantu, R. C., Sloane, R., … Bielak, K. (2013). Genetic polymorphisms, concussion risk, and post concussion neurocognitive deficits in college and high school athletes. British Journal of Sports Medicine, 47(e1), 12–13.
  • Thomas, D. C., & Witte, J. S. (2001). Population Stratification: A problem for case-control studies of candidage-gene associations? Cancer Epidemiology, Biomarkers & Prevention, 11, 505–512.
  • Toulmond, S., & Rothwell, N. J. (1995). Interleukin-1 receptor antagonist inhibits neuronal damage caused by fluid percussion injury in the rat. Brain Research, 671(2), 261–266.
  • Uzan, M., Tanriverdi, T., Baykara, O., Kafadar, A., Sanus, G. Z., Tureci, E., … Buyra, N. (2005). Association between interleukin-1 beta (IL-1β) gene polymorphism and outcome after head injury: An early report. Acta Neurochirurgica, 147(7), 715–720.
  • Warnes, G., & Leisch, F. (2006). Genetics: Population genetics. R Package, version 1.2. 1. The Comprehensive R Archive Network.
  • Winter, C. D., Pringle, A. K., Clough, G. F., & Church, M. K. (2004). Raised parenchymal interleukin-6 levels correlate with improved outcome after traumatic brain injury. Brain, 127(2), 6–11.
  • Woodroofe, M. N., Sarna, G. S., Wadhwa, M., Hayes, G. M., Loughlin, A. J., Tinker, A., & Cuzner, M. L. (1991). Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: Evidence of a role for microglia in cytokine production. Journal of Neuroimmunology, 33(3), 227–236.
  • Yang, S., Gangidine, M., Pritts, T., Goodman, M., & Lentsch, A. (2013). Interleukin 6 mediates neuroinflammation and motor coordination deficits after mild traumatic brain injury and brief hypoxia in mice. Shock, 27(6), 417–428.
  • Zhai, P. P., Xu, L. H., Yang, J. J., Jiang, Z. L., Zhao, G. W., Sun, L., … Li, X. (2015). Reduction of inflammatory responses by l-serine treatment leads to neuroprotection in mice after traumatic brain injury. Neuropharmacology, 95, 1–11.
  • Zhang, X., Graham, S. H., Kochanek, P. M., & Clark, R. S. B. (2003). Caspase-8 expression and proteolysis in human brain after severe head injury 1. The FASEB Journal, 17, 1367–1369.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.