Characterization of recovery, repair, and inflammatory processes following contusion spinal cord injury in old female rats: Is age a limitation?

Immunity and Ageing

Volumn 11, Issue 1, 2014, Pages

  Hooshmand, Mitra J ^a   Galvan, Manuel D ^a   Partida, Elizabeth ^a   Anderson, Aileen J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Complement; Inflammation; Locomotor function; Spinal cord injury

Indexed keywords

COMPLEMENT;

ADULT; AGED; AGING; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; COMPLEMENT ACTIVATION; COMPLEMENT BLOOD LEVEL; CONTROLLED STUDY; CONVALESCENCE; CYTOARCHITECTURE; EXPERIMENTAL SPINAL CORD CONTUSION; FEMALE; GAIT; GROUPS BY AGE; HUMORAL IMMUNITY; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LAMINECTOMY; LOCOMOTION; MACROPHAGE; MICROGLIA; MYELITIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; RAT; SPINAL CORD REGENERATION; STEREOMETRY; SURVIVAL; WHITE MATTER; YOUNG ADULT;

EID: 84927515666     PISSN: None     EISSN: 17424933     Source Type: Journal    
DOI: 10.1186/1742-4933-11-15     Document Type: Article

References (56)

1. Cifu DX, Seel RT, Kreutzer JS, Marwitz J, McKinley WO, Wisor D: Age, outcome, and rehabilitation costs after tetraplegia spinal cord injury. Neurorehabilitation 1999,12(3):177-185.
2. Dai LY: Acute central cervical cord injury: the effect of age upon prognosis. Inj Int J Care Inj 2001,32(3):195-199. 10.1016/S0020-1383(00)00176-5
3. Furlan JC, Bracken MB, Fehlings MG: Is age a key determinant of mortality and neurological outcome after acute traumatic spinal cord injury? Neurobiol Aging 2010,31(3):434-446. 10.1016/j.neurobiolaging.2008.05.003
4. Fehlings MG, Furlan JC: Effect of age on spinal cord injury. J Neurosurg Spine 2007,7(3):275-276. discussion 276 10.3171/SPI-07/09/275
5. Gwak YS, Hains BC, Johnson KM, Hulsebosch CE: Effect of age at time of spinal cord injury on behavioral outcomes in rat. J Neurotrauma 2004,21(8):983-993. 10.1089/0897715041650999
6. Genovese T, Genovese T, Mazzon E, Di Paola R, Crisafulli C, Muia C, Bramanti P, Cuzzocrea S: Increased oxidative-related mechanisms in the spinal cord injury in old rats. Neurosci Lett 2006,393(2-3):141-146.
7. Siegenthaler MM, Berchtold NC, Cotman CW, Keirstead HS: Voluntary running attenuates age-related deficits following SCI. Exp Neurol 2008,210(1):207-216. 10.1016/j.expneurol.2007.10.019
8. CDRF: Spinal Cord Injury Information Network. Birmingham: University of Alabama; 2008.
9. Chaovipoch P, Jelks KA, Gerhold LM, West EJ, Chongthammakun S, Floyd CL: 17beta-estradiol is protective in spinal cord injury in post- and pre-menopausal rats. J Neurotrauma 2006,23(6):830-852. 10.1089/neu.2006.23.830
10. Siegenthaler MM, Ammon DL, Keirstead HS: Myelin pathogenesis and functional deficits following SCI are age-associated. Exp Neurol 2008,213(2):363-371. 10.1016/j.expneurol.2008.06.015
11. Jaerve A, Kruse F, Malik K, Hartung HP, Muller HW: Age-dependent modulation of cortical transcriptomes in spinal cord injury and repair. PLoS ONE 2012,7(12):e49812. 10.1371/journal.pone.0049812
12. Kumamaru H, Saiwai H, Ohkawa Y, Yamada H, Iwamoto Y, Okada S: Age-related differences in cellular and molecular profiles of inflammatory responses after spinal cord injury. J Cell Physiol 2012,227(4):1335-1346. 10.1002/jcp.22845
13. Long JM, Mouton PR, Jucker M, Ingram DK: What counts in brain aging? Design-based stereological analysis of cell number. J Gerontol A Biol Sci Med Sci 1999,54(10):B407-B417. 10.1093/gerona/54.10.B407
14. Laing AC, Cox R, Tetzlaff W, Oxland T: Effects of advanced age on the morphometry and degenerative state of the cervical spine in a rat model. Anat Rec (Hoboken) 2011,294(8):1326-1336. 10.1002/ar.21436
15. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE Jr: Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 2003,20(2):179-193. 10.1089/08977150360547099
16. Nishi RA, Liu H, Chu Y, Hamamura M, Su MY, Nalcioglu O, Anderson AJ: Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J Neurotrauma 2007,24(4):674-689. 10.1089/neu.2006.0204
17. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH: Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 2001,18(2):187-201. 10.1089/08977150150502613
18. Vrinten DH, Hamers FF: 'CatWalk' automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; a comparison with von Frey testing. Pain 2003,102(1-2):203-209.
19. Bresnahan JC, Beattie MS, Todd FD 3rd, Noyes DH: A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp Neurol 1987,95(3):548-570. 10.1016/0014-4886(87)90299-8
20. Guth L, Zhang Z, Steward O: The unique histopathological responses of the injured spinal cord. Implications for neuroprotective therapy. Ann N Y Acad Sci 1999, 890:366-384. 10.1111/j.1749-6632.1999.tb08017.x
21. Jaerve A, Schiwy N, Schmitz C, Mueller HW: Differential effect of aging on axon sprouting and regenerative growth in spinal cord injury. Exp Neurol 2011,231(2):284-294. 10.1016/j.expneurol.2011.07.002
22. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW: Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997,17(14):5395-5406.
23. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT: Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 1999,158(2):351-365. 10.1006/exnr.1999.7118
24. Sroga JM, Jones TB, Kigerl KA, McGaughy VM, Popovich PG: Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 2003,462(2):223-240. 10.1002/cne.10736
25. Gris D, Marsh DR, Oatway MA, Chen Y, Hamilton EF, Dekaban GA, Weaver LC: Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J Neurosci 2004,24(16):4043-4051. 10.1523/JNEUROSCI.5343-03.2004
26. Fleming JC, Norenberg MD, Ramsay DA, Dekaban GA, Marcillo AE, Saenz AD, Pasquale-Styles M, Dietrich WD, Weaver LC: The cellular inflammatory response in human spinal cords after injury. Brain 2006,129(Pt 12):3249-3269.
27. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ: Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 2010,133(Pt 2):433-447.
28. Anderson AJ, Robert S, Huang W, Young W, Cotman CW: Activation of complement pathways after contusion-induced spinal cord injury. J Neurotrauma 2004,21(12):1831-1846. 10.1089/neu.2004.21.1831
29. Cole DS, Hughes TR, Gasque P, Morgan BP: Complement regulator loss on apoptotic neuronal cells causes increased complement activation and promotes both phagocytosis and cell lysis. Mol Immunol 2006,43(12):1953-1964. 10.1016/j.molimm.2005.11.015
30. Ziporen L, Donin N, Shmushkovich T, Gross A, Fishelson Z: Programmed necrotic cell death induced by complement involves a Bid-dependent pathway. J Immunol 2009,182(1):515-521. 10.4049/jimmunol.182.1.515
31. Rodakowski J, Skidmore ER, Anderson SJ, Begley A, Jensen MP, Buhule OD, Boninger ML: Additive effect of Age on disability for individuals with spinal cord injuries. Arch Phys Med Rehabil 2014,95(6):1076-1082. 10.1016/j.apmr.2014.01.022
32. Selvarajah S, Hammond ER, Haider AH, Abularrage CJ, Becker D, Dhiman N, Hyder O, Gupta D, Black JH 3rd, Schneider EB: The burden of acute traumatic spinal cord injury among adults in the united states: an update. J Neurotrauma 2014,31(3):228-238. 10.1089/neu.2013.3098
33. Carlson SL, Parrish ME, Springer JE, Doty K, Dossett L: Acute inflammatory response in spinal cord following impact injury. Exp Neurol 1998,151(1):77-88. 10.1006/exnr.1998.6785
34. Popovich PG, Wei P, Stokes BT: Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 1997,377(3):443-464. 10.1002/(SICI)1096-9861(19970120)377:3<443::AID-CNE10>3.0.CO;2-S
35. Rebhun J, Madorsky JG, Glovsky MM: Proteins of the complement system and acute phase reactants in sera of patients with spinal cord injury. Ann Allergy 1991,66(4):335-338.
36. Duce JA, Hollander W, Jaffe R, Abraham CR: Activation of early components of complement targets myelin and oligodendrocytes in the aged rhesus monkey brain. Neurobiol Aging 2006,27(4):633-644. 10.1016/j.neurobiolaging.2005.03.027
37. Nagra RM, Becher B, Tourtellotte WW, Antel JP, Gold D, Paladino T, Smith RA, Nelson JR, Reynolds WF: Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis. J Neuroimmunol 1997,78(1-2):97-107.
38. Reynolds WF, Rhees J, Maciejewski D, Paladino T, Sieburg H, Maki RA, Masliah E: Myeloperoxidase polymorphism is associated with gender specific risk for Alzheimer's disease. Exp Neurol 1999,155(1):31-41. 10.1006/exnr.1998.6977
39. Kyrkanides S, O'Banion MK, Whiteley PE, Daeschner JC, Olschowka JA: Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury. J Neuroimmunol 2001,119(2):269-277. 10.1016/S0165-5728(01)00404-0
40. Sutherland GR, Dix GA, Auer RN: Effect of age in rodent models of focal and forebrain ischemia. Stroke 1996,27(9):1663-1667. discussion 1668 10.1161/01.STR.27.9.1663
41. Hurley SD, Coleman PD: Facial nerve axotomy in aged and young adult rats: analysis of the glial response. Neurobiol Aging 2003,24(3):511-518. 10.1016/S0197-4580(02)00097-0
42. Saville LR, Pospisil CH, Mawhinney LA, Bao F, Simedrea FC, Peters AA, O'Connell PJ, Weaver LC, Dekaban GA: A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: a potential neuroprotective treatment. J Neuroimmunol 2004,156(1-2):42-57.
43. Fleming JC, Bao F, Chen Y, Hamilton EF, Relton JK, Weaver LC: Alpha4beta1 integrin blockade after spinal cord injury decreases damage and improves neurological function. Exp Neurol 2008,214(2):147-159. 10.1016/j.expneurol.2008.04.024
44. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M: Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 1998,4(7):814-821. 10.1038/nm0798-814
45. Shechter R, Raposo C, London A, Sagi I, Schwartz M: The glial scar-monocyte interplay: a pivotal resolution phase in spinal cord repair. PLoS One 2011,6(12):e27969. 10.1371/journal.pone.0027969
46. Popovich PG, van Rooijen N, Hickey WF, Preidis G, McGaughy V: Hematogenous macrophages express CD8 and distribute to regions of lesion cavitation after spinal cord injury. Exp Neurol 2003,182(2):275-287. 10.1016/S0014-4886(03)00120-1
47. Batchelor PE, Tan S, Wills TE, Porritt MJ, Howells DW: Comparison of inflammation in the brain and spinal cord following mechanical injury. J Neurotrauma 2008,25(10):1217-1225. 10.1089/neu.2007.0308
48. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG: Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009,29(43):13435-13444. 10.1523/JNEUROSCI.3257-09.2009
49. Ondarza AB, Ye Z, Hulsebosch CE: Direct evidence of primary afferent sprouting in distant segments following spinal cord injury in the rat: colocalization of GAP-43 and CGRP. Exp Neurol 2003,184(1):373-380. 10.1016/j.expneurol.2003.07.002
50. Mills CD, Grady JJ, Hulsebosch CE: Changes in exploratory behavior as a measure of chronic central pain following spinal cord injury. J Neurotrauma 2001,18(10):1091-1105. 10.1089/08977150152693773
51. Hulsebosch CE, Hains BC, Crown ED, Carlton SM: Mechanisms of chronic central neuropathic pain after spinal cord injury. Brain Res Rev 2009,60(1):202-213. 10.1016/j.brainresrev.2008.12.010
52. Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, Fulga V, Yoles E: Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J Neuroimmunol 2003,142(1-2):10-16.
53. Swartz KR, Fee DB, Joy KM, Roberts KN, Sun S, Scheff NN, Wilson ME, Scheff SW: Gender differences in spinal cord injury are not estrogen-dependent. J Neurotrauma 2007,24(3):473-480. 10.1089/neu.2006.0167
54. Yune TY, Kim SJ, Lee SM, Lee YK, Oh YJ, Kim YC, Markelonis GJ, Oh TH: Systemic administration of 17beta-estradiol reduces apoptotic cell death and improves functional recovery following traumatic spinal cord injury in rats. J Neurotrauma 2004,21(3):293-306. 10.1089/089771504322972086
55. Schmitz C, Hof PR: Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 2000,20(1):93-114. 10.1016/S0891-0618(00)00066-1
56. Dodds AW, Sim RB: Complement: A Practical Approach. Oxford; New York: IRL Press at Oxford University Press; 1997:274.