The terminal pathway of the complement system is activated in focal penetrating but not in mild diffuse traumatic brain injury

Journal of Neurotrauma

Volumn 30, Issue 23, 2013, Pages 1954-1965

  Rostami, Elham ^a   Davidsson, Johan ^b   Gyorgy, Andrea ^c   Agoston, Denes V ^c   Risling, Mårten ^a   Bellander, Bo Michael ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

C1q; C3; C5b 9; complement; synaptic stripping; TBI

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT MEMBRANE ATTACK COMPLEX; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CONTUSION; COMPLEMENT ACTIVATION; COMPLEMENT BLOOD LEVEL; COMPLEMENT SYSTEM; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICROGLIA; NONHUMAN; PROTEIN MICROARRAY; RAT; RAT MODEL; SURVIVAL TIME; TRAUMATIC BRAIN INJURY;

ACCELERATION; ANIMALS; ANTIGENS, NUCLEAR; BLOTTING, WESTERN; BRAIN INJURIES; C-REACTIVE PROTEIN; COMPLEMENT ACTIVATION; COMPLEMENT C1Q; COMPLEMENT C3; COMPLEMENT PATHWAY, CLASSICAL; DIFFUSE AXONAL INJURY; HEAD INJURIES, PENETRATING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICROARRAY ANALYSIS; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; ROTATION;

EID: 84888084730     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2583     Document Type: Article

References (47)

1. Graham, D., and Lantos, PI. (2002). Greenfield's Neuropathology. Oxford University Press, New York.
2. Holbourn, A. (1943). Mechanics of head injuries. Lancet 2, 438-441.
3. Morganti-Kossmann, M.C., Rancan, M., Otto, V.I., Stahel, P.F., and Kossmann, T. (2001). Role of cerebral inflammation after traumatic brain injury: a revisited concept. Shock 16, 165-177.
4. Rogers, J., Cooper, N.R., Webster, S., Schultz, J., McGeer, P.L., Styren, S.D., Civin, W.H., Brachova, L., Bradt, B., Ward, P., et al. (1992). Complement activation by beta-amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 89, 10, 016-10, 020.
5. Webster, S., Bonnell, B., and Rogers, J. (1997). Charge-based binding of complement component C1q to the Alzheimer amyloid beta-peptide. Am. J. Pathol. 150, 1531-1536.
6. Yasojima, K., Schwab, C., McGeer, E.G., and McGeer, P.L. (1999). Up-regulated production and activation of the complement system in Alzheimer's disease brain. Am. J. Pathol. 154, 927-936.
7. Anderson, A.J., Robert, S., Huang, W., Young, W., and Cotman, C.W. (2004). Activation of complement pathways after contusion-induced spinal cord injury. J. Neurotrauma 21, 1831-1846.
8. Qiao, F., Atkinson, C., Kindy, M.S., Shunmugavel, A., Morgan, B.P., Song, H., and Tomlinson, S. (2010). The alternative and terminal pathways of complement mediate post-traumatic spinal cord inflammation and injury. Am. J. Pathol. 177, 3061-3070.
9. Svensson, M., Liu, L., Mattsson, P., Morgan, B.P., and Aldskogius, H. (1995). Evidence for activation of the terminal pathway of complement and upregulation of sulfated glycoprotein (SGP)-2 in the hypoglossal nucleus following peripheral nerve injury. Mol. Chem. Neuropathol. 24, 53-68.
10. Bellander, B.M., Singhrao, S.K., Ohlsson, M., Mattsson, P., and Svensson, M. (2001). Complement activation in the human brain after traumatic head injury. J. Neurotrauma 18, 1295-1311.
11. Stahel, P.F., Kossmann, T., Morganti-Kossmann, M.C., Hans, V.H., and Barnum, S.R. (1997). Experimental diffuse axonal injury induces enhanced neuronal C5a receptor mRNA expression in rats. Brain Res. Mol. Brain Res. 50, 205-212.
12. Huber-Lang, M., Sarma, J.V., Zetoune, F.S., Rittirsch, D., Neff, T.A., McGuire, S.R., Lambris, J.D., Warner, R.L., Flierl, M.A., Hoesel, L.M., Gebhard, F., Younger, J.G., Drouin, S.M., Wetsel, R.A., and Ward, P.A. (2006). Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med 12, 682-687.
13. Gasque, P., Fontaine, M., and Morgan, B.P. (1995). Complement expression in human brain. Biosynthesis of terminal pathway components and regulators in human glial cells and cell lines. J. Immunol. 154, 4726-4733.
14. Morgan, B.P. and Gasque, P. (1997). Extrahepatic complement biosynthesis: where: when and why? Clin Exp Immunol 107, 1-7.
15. Bellander, B.M., Bendel, O., Von Euler, G., Ohlsson, M., and Svensson, M. (2004). Activation of microglial cells and complement following traumatic injury in rat entorhinal-hippocampal slice cultures. J. Neurotrauma 21, 605-615.
16. Trouw, L.A., Blom, A.M., and Gasque, P. (2008). Role of complement and complement regulators in the removal of apoptotic cells. Mol. Immunol. 45, 1199-1207.
17. Gasque, P. (2004). Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 41, 1089-1098.
18. Bellander, B.M., von Holst, H., Fredman, P., and Svensson, M. (1996). Activation of the complement cascade and increase of clusterin in the brain following a cortical contusion in the adult rat. J. Neurosurg. 85, 468-475.
19. Dalle Lucca, J.J., Chavko, M., Dubick, M.A., Adeeb, S., Falabella, M.J., Slack, J.L., McCarron, R., and Li, Y. (2012). Blast-induced moderate neurotrauma (BINT) elicits early complement activation and tumor necrosis factor alpha (TNFalpha) release in a rat brain. J. Neurol. Sci. 318, 146-154.
20. Stahel, P.F., Morganti-Kossmann, M.C., Perez, D., Redaelli, C., Gloor, B., Trentz, O., and Kossmann, T. (2001). Intrathecal levels of complement-derived soluble membrane attack complex (sC5b-9) correlate with blood-brain barrier dysfunction in patients with traumatic brain injury. J. Neurotrauma 18, 773-781.
21. Bellander, B.M., Olafsson, I.H., Ghatan, P.H., Bro Skejo, H.P., Hansson, L.O., Wanecek, M., and Svensson, M.A. (2011). Secondary insults following traumatic brain injury enhance complement activation in the human brain and release of the tissue damage marker S100B. Acta Neurochir. (Wien) 153, 90-100.
22. Stahel, P.F., Flierl, M.A., Morgan, B.P., Persigehl, I., Stoll, C., Conrad, C., Touban, B.M., Smith, W.R., Beauchamp, K., Schmidt, O.I., Ertel, W., and Leinhase, I. (2009). Absence of the complement regulatory molecule CD59a leads to exacerbated neuropathology after traumatic brain injury in mice. J. Neuroinflammation 6, 2.
23. Stahel, P.F., Morganti-Kossmann, M.C., and Kossmann, T. (1998). The role of the complement system in traumatic brain injury. Brain Res. Brain Res. Rev. 27, 243-256.
24. Rahpeymai, Y., Hietala, M.A., Wilhelmsson, U., Fotheringham, A., Davies, I., Nilsson, A.K., Zwirner, J., Wetsel, R.A., Gerard, C., Pekny, M., and Pekna, M. (2006). Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J 25, 1364-1374.
25. Pekny, M., Wilhelmsson, U., Bogestal, Y.R., and Pekna, M. (2007). The role of astrocytes and complement system in neural plasticity. Int. Rev. Neurobiol. 82, 95-111.
26. Stevens, B., Allen, N.J., Vazquez, L.E., Howell, G.R., Christopherson, K.S., Nouri, N., Micheva, K.D., Mehalow, A.K., Huberman, A.D., Stafford, B., Sher, A., Litke, A.M., Lambris, J.D., Smith, S.J., John, S.W., and Barres, B.A. (2007). The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178.
27. Berg, A., Zelano, J., Stephan, A., Thams, S., Barres, B.A., Pekny, M., Pekna, M., and Cullheim, S. (2012). Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3. Exp. Neurol. 237, 8-17.
28. Diaz Padilla, N., Bleeker, W.K., Lubbers, Y., Rigter, G.M., Van Mierlo, G.J., Daha, M.R., and Hack, C.E. (2003). Rat C-reactive protein activates the autologous complement system. Immunology 109, 564-571.
29. Burger, W., Schade, R., and Hirschelmann, R. (1987). The rat Creactive protein-isolation and response to experimental inflammation and tissue damage. Agents Actions 21, 93-97.
30. Davidsson, J., and Risling, M. (2011). A new model to produce sagittal plane rotational induced diffuse axonal injuries. Front. Neurol. 2, 41.
31. Davidsson, J.A., and Risling, M. (2009). Injury threshhold for sagittal plane rotational induced diffuse axonal injuries. International IRCOBI conference on the biomechanics of injury. 43-56.
32. Risling, M., Plantman, S., Angeria, M., Rostami, E., Bellander, B.M., Kirkegaard, M., Arborelius, U., and Davidsson, J. (2011). Mechanisms of blast induced brain injuries, experimental studies in rats. Neuroimage 54, Suppl. 1, S89-97.
33. Plantman, S., Ng, K.C., Lu, J., Davidsson, J., and Risling, M. (2012). Characterization of a novel rat model of penetrating traumatic brain injury. J Neurotrauma 29, 1219-1232.
34. Rostami, E., Davidsson, J., Ng, K.C., Lu, J., Gyorgy, A., Walker, J., Wingo, D., Plantman, S., Bellander, B.M., Agoston, D.V., and Risling, M. (2012). A model for mild traumatic brain injury that induces limited transient memory impairment and increased levels of axon related serum biomarkers. Front. Neurol. 3, 115.
35. Gyorgy, A.B., Walker, J., Wingo, D., Eidelman, O., Pollard, H.B., Molnar, A., and Agoston, D.V. (2010). Reverse phase protein microarray technology in traumatic brain injury. J. Neurosci. Methods 192, 96-101.
36. Bruck, W. (1997). The role of macrophages in Wallerian degeneration. Brain Pathol. 7, 741-752.
37. Koski, C.L., Vanguri, P., and Shin, M.L. (1985). Activation of the alternative pathway of complement by human peripheral nerve myelin. J. Immunol. 134, 1810-1814.
38. Koski, C.L., Estep, A.E., Sawant-Mane, S., Shin, M.L., Highbarger, L., and Hansch, G.M. (1996). Complement regulatory molecules on human myelin and glial cells: differential expression affects the deposition of activated complement proteins. J. Neurochem. 66, 303-312.
39. Shitaka, Y., Tran, H.T., Bennett, R.E., Sanchez, L., Levy, M.A., Dikranian, K., and Brody, D.L. (2011). Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J. Neuropathol. Exp. Neurol. 70, 551-567.
40. Buki, A., and Povlishock, J.T. (2006). All roads lead to disconnection?-Traumatic axonal injury revisited. Acta. Neurochir (Wien) 148, 181-193.
41. Singleton, R.H., Zhu, J., Stone, J.R., and Povlishock, J.T. (2002). Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. J. Neurosci. 22, 791-802.
42. Vargas, M.E., and Barres, B.A. (2007). Why is Wallerian degeneration in the CNS so slow? Annu. Rev. Neurosci. 30, 153-179.
43. Fork, M., Bartels, C., Ebert, A.D., Grubich, C., Synowitz, H., and Wallesch, C.W. (2005). Neuropsychological sequelae of diffuse traumatic brain injury. Brain Inj. 19, 101-108.
44. Koenigs, M., Huey, E.D., Raymont, V., Cheon, B., Solomon, J., Wassermann, E.M., and Grafman, J. (2008). Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nat. Neurosci. 11, 232-237.
45. van Beek, J., Elward, K., and Gasque, P. (2003). Activation of complement in the central nervous system: roles in neurodegeneration and neuroprotection. Ann. N. Y. Acad. Sci. 992, 56-71.
46. Bonifati, D.M., and Kishore, U. (2007). Role of complement in neurodegeneration and neuroinflammation. Mol. Immunol. 44, 999-1010.
47. Selkoe, D.J. (2002). Alzheimer's disease is a synaptic failure. Science 298, 789-791.