Enhancement of neurogenesis and memory by a neurotrophic peptide in mild to moderate traumatic brain injury

Neurosurgery

Volumn 76, Issue 2, 2015, Pages 201-214

  Chohan, Muhammad Omar ^a   Bragina, Olga ^a   Kazim, Syed Faraz ^b,c   Statom, Gloria ^a   Baazaoui, Narjes ^b   Bragin, Denis ^a   Iqbal, Khalid ^b   Nemoto, Edwin ^a   Yonas, Howard ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Ciliary neurotrophic factor; Dentate gyrus; Memory; Neural stem cells; Neurogenesis; Therapeutics; Traumatic brain injury

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BIOLOGICAL MARKER; CENTRAL NERVOUS SYSTEM AGENTS; CILIARY NEUROTROPHIC FACTOR; EARLY GROWTH RESPONSE FACTOR 1; MICROTUBULE ASSOCIATED PROTEIN 2; PEPTIDE 6; SYNAPTOPHYSIN; TAU PROTEIN; UNCLASSIFIED DRUG; PEPTIDE;

ADULT; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN FUNCTION; CELL COUNT; CELL DENSITY; CELL LOSS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CONTUSION; DENTATE GYRUS; DISEASE SEVERITY; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; LONG TERM CARE; MEMORY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; SYNAPSE; TRAUMATIC BRAIN INJURY; TREATMENT OUTCOME; ANIMAL; BRAIN INJURY; C57BL MOUSE; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; DISEASE MODEL; DRUG EFFECTS; HIPPOCAMPUS; MALE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN INJURIES; CELL DIFFERENTIATION; CILIARY NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEURAL STEM CELLS; NEUROGENESIS; PEPTIDES;

EID: 84926089927     PISSN: 0148396X     EISSN: 15244040     Source Type: Journal    
DOI: 10.1227/NEU.0000000000000577     Document Type: Article

References (88)

1. Faul M, Xu L, Wald MM, Coronado VG. Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Atlanta, GA: US Department of Health And Human Services, Centers for Disease Control and Prevention National Center for Injury Prevention and Control; 2010. Available at www.cdc.gov/TraumaticBrainInjury. Accessed on March 26, 2014.
2. Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21(5):375-378.
3. Finkelstein EA, Corso PS, Miller T. The Incidence and Economic Burden of Injuries in the United States. New York, NY: Oxford University Press; 2006.
4. Jain KK. Neuroprotection in traumatic brain injury. Drug Discov Today. 2008;13 (23-24):1082-1089.
5. Margulies S, Hicks R. Combination therapies for traumatic brain injury: prospective considerations. J Neurotrauma. 2009;26(6):925-939.
6. Kotapka MJ, Graham DI, Adams JH, Gennarelli TA. Hippocampal pathology in fatal human head injury without high intracranial pressure. J Neurotrauma. 1994; 11(3):317-324.
7. Williams S, Raghupathi R, MacKinnon MA, McIntosh TK, Saatman KE, Graham DI. In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathol. 2001;102(6):581-590.
8. Chirumamilla S, Sun D, Bullock MR, Colello RJ. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J Neurotrauma. 2002;19(6):693-703.
9. Dash PK, Mach SA, Moore AN. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res. 2001;63(4):313-319.
10. Yoshimura S, Takagi Y, Harada J, et al. FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci U S A. 2001;98(10): 5874-5879.
11. Yoshimura S, Teramoto T, Whalen MJ, et al. FGF-2 regulates neurogenesis and degeneration in the dentate gyrus after traumatic brain injury in mice. J Clin Invest. 2003;112(8):1202-1210.
12. Sun D, Bullock MR, McGinn MJ, et al. Basic fibroblast growth factor-enhanced neurogenesis contributes to cognitive recovery in rats following traumatic brain injury. Exp Neurol. 2009;216(1):56-65.
13. Kleindienst A, Harvey HB, Rice AC, et al. Intraventricular infusion of the neurotrophic protein S100B improves cognitive recovery after fluid percussion injury in the rat. J Neurotrauma. 2004;21(5):541-547.
14. Kleindienst A, McGinn MJ, Harvey HB, Colello RJ, Hamm RJ, Bullock MR. Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J Neurotrauma. 2005;22(6):645-655.
15. Lu D, Mahmood A, Qu C, Goussev A, Schallert T, Chopp M. Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J Neurotrauma. 2005;22(9):1011-1017.
16. Miller RG, Moore DH, Jackson CE; WALS Study Group. Western ALS Study Group. Amyotroph Lateral Scler Other Motor Neuron Disord. 2004;5(suppl 1):121-124.
17. Emerich DF, Thanos CG. Intracompartmental delivery of CNTF as therapy for Huntington's disease and retinitis pigmentosa. Curr Gene Ther. 2006;6(1): 147-159.
18. Price RD, Milne SA, Sharkey J, Matsuoka N. Advances in small molecules promoting neurotrophic function. Pharmacol Ther. 2007;115(2):292-306.
19. Chohan MO, Li B, Blanchard J, et al. Enhancement of dentate gyrus neurogenesis, dendritic and synaptic plasticity and memory by a neurotrophic peptide. Neurobiol Aging. 2011;32(8):1420-1434.
20. Blanchard J, Wanka L, Tung YC, et al. Pharmacologic reversal of neurogenic and neuroplastic abnormalities and cognitive impairments without affecting Abeta and tau pathologies in 3xTg-AD mice. Acta Neuropathol. 2010;120(5):605-621.
21. Blanchard J, Bolognin S, Chohan MO, Rabe A, Iqbal K, Grundke-Iqbal I. Rescue of synaptic failure and alleviation of learning and memory impairments in a trisomic mouse model of down syndrome. J Neuropathol Exp Neurol. 2011;70 (12):1070-1079.
22. Hicks RR, Numan S, Dhillon HS, Prasad MR, Seroogy KB. Alterations in BDNF and NT-3 mRNAs in rat hippocampus after experimental brain trauma. Brain Res Mol Brain Res. 1997;48(2):401-406.
23. Oyesiku NM, Evans CO, Houston S, et al. Regional changes in the expression of neurotrophic factors and their receptors following acute traumatic brain injury in the adult rat brain. Brain Res. 1999;833(2):161-172.
24. Yang K, Perez-Polo JR, Mu XS, et al. Increased expression of brain-derived neurotrophic factor but not neurotrophin-3 mRNA in rat brain after cortical impact injury. J Neurosci Res. 1996;44(2):157-164.
25. Tatebayashi Y, Lee MH, Li L, Iqbal K, Grundke-Iqbal I. The dentate gyrus neurogenesis: a therapeutic target for Alzheimer's disease. Acta Neuropathol. 2003; 105(3):225-232.
26. Chen H, Tung YC, Li B, Iqbal K, Grundke-Iqbal I. Trophic factors counteract elevated FGF-2-induced inhibition of adult neurogenesis. Neurobiol Aging. 2007; 28(8):1148-1162.
27. Exo JL, Shellington DK, Bayir H, et al. Resuscitation of traumatic brain injury and hemorrhagic shock with polynitroxylated albumin, hextend, hypertonic saline, and lactated Ringer's: effects on acute hemodynamics, survival, and neuronal death in mice. J Neurotrauma. 2009;26(12):2403-2408.
28. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991;231(4):482-497.
29. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297(5868):681-683.
30. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci. 2010; 11(5):339-350.
31. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development. 2003;130(2):391-399.
32. Emsley JG, Hagg T. Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice. Exp Neurol. 2003;183(2): 298-310.
33. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol. 2006;495(1):70-83.
34. Duan X, Chang JH, Ge S, et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell. 2007;130(6):1146-1158.
35. Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol. 2005;15(5):599-606.
36. Snyder JS, Choe JS, Clifford MA, et al. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci. 2009;29(46):14484-14495.
37. Jessberger S, Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci. 2003;18(10):2707-2712.
38. Omalu BI, DeKosky ST, Hamilton RL, et al. Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery. 2006;59(5):1086-1092; discussion 1092-1093.
39. Lye TC, Shores EA. Traumatic brain injury as a risk factor for Alzheimer's disease: a review. Neuropsychol Rev. 2000;10(2):115-129.
40. Jiang T, Yu JT, Tian Y, Tan L. Epidemiology and etiology of Alzheimer's disease: from genetic to non-genetic factors. Curr Alzheimer Res. 2013;10(8):852-867.
41. Jellinger KA. Traumatic brain injury as a risk factor for Alzheimer's disease. J Neurol Neurosurg Psychiatry. 2004;75(3):511-512.
42. Sivanandam TM, Thakur MK. Traumatic brain injury: a risk factor for Alzheimer's disease. Neurosci Biobehav Rev. 2012;36(5):1376-1381.
43. Zhou H, Chen L, Gao X, Luo B, Chen J. Moderate traumatic brain injury triggers rapid necrotic death of immature neurons in the hippocampus. J Neuropathol Exp Neurol. 2012;71(4):348-359.
44. Saatman KE, Feeko KJ, Pape RL, Raghupathi R. Differential behavioral and histopathological responses to graded cortical impact injury in mice. J Neurotrauma. 2006;23(8):1241-1253.
45. Rola R, Mizumatsu S, Otsuka S, et al. Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp Neurol. 2006;202(1):189-199.
46. Gao X, Deng P, Xu ZC, Chen J. Moderate traumatic brain injury causes acute dendritic and synaptic degeneration in the hippocampal dentate gyrus. PLoS One. 2011;6(9):e24566.
47. Liu F, You Y, Li X, et al. Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J Neurosci. 2009;29(16):5075-5087.
48. Gao X, Enikolopov G, Chen J. Moderate traumatic brain injury promotes proliferation of quiescent neural progenitors in the adult hippocampus. Exp Neurol. 2009;219(2):516-523.
49. Hill-Felberg SJ, McIntosh TK, Oliver DL, Raghupathi R, Barbarese E. Concurrent loss and proliferation of astrocytes following lateral fluid percussion brain injury in the adult rat. J Neurosci Res. 1999;57(2):271-279.
50. Gao X, Chen J. Moderate traumatic brain injury promotes neural precursor proliferation without increasing neurogenesis in the adult hippocampus. Exp Neurol. 2013;239:38-48.
51. Acosta SA, Tajiri N, Shinozuka K, et al. Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PloS One. 2013;8(1):e53376.
52. Chiaretti A, Piastra M, Polidori G, et al. Correlation between neurotrophic factor expression and outcome of children with severe traumatic brain injury. Intensive Care Med. 2003;29(8):1329-1338.
53. Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL, Wecht CH. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery. 2005;57(1):128-134; discussion 128-134.
54. Small GW, Kepe V, Siddarth P, et al. PET scanning of brain tau in retired national football league players: preliminary findings. Am J Geriatr Psychiatry. 2013;21(2):138-144.
55. Fakhran S, Yaeger K, Alhilali L. Symptomatic white matter changes in mild traumatic brain injury resemble pathologic features of early Alzheimer dementia. Radiology. 2013;269(1):249-257.
56. Chauhan NB. Chronic neurodegenerative consequences of traumatic brain injury. Restor Neurol Neurosci. 2014;32(2):337-365.
57. Stopa EG, Gonzalez AM, Chorsky R, et al. Basic fibroblast growth factor in Alzheimer's disease. Biochem Biophys Res Commun. 1990;171(2):690-696.
58. Hock C, Heese K, Hulette C, Rosenberg C, Otten U. Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol. 2000;57(6):846-851.
59. Fahnestock M, Michalski B, Xu B, Coughlin MD. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci. 2001;18(2):210-220.
60. Hicks RR, Baldwin SA, Scheff SW. Serum extravasation and cytoskeletal alterations following traumatic brain injury in rats. Comparison of lateral fluid percussion and cortical impact models. Mol Chem Neuropathol. 1997;32(1-3):1-16.
61. Truettner J, Schmidt-Kastner R, Busto R, et al. Expression of brain-derived neurotrophic factor, nerve growth factor, and heat shock protein HSP70 following fluid percussion brain injury in rats. J Neurotrauma. 1999;16(6):471-486.
62. Posmantur RM, Kampfl A, Taft WC, et al. Diminished microtubule-associated protein 2 (MAP2) immunoreactivity following cortical impact brain injury. J Neurotrauma. 1996;13(3):125-137.
63. Chohan MO, Haque N, Alonso A, et al. Hyperphosphorylation-induced self assembly of murine tau: a comparison with human tau. J Neural Transm. 2005; 112(8):1035-1047.
64. Dodart JC, Mathis C, Bales KR, Paul SM. Does my mouse have Alzheimer's disease? Genes Brain Behav. 2002;1(3):142-155.
65. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D. Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F betaamyloid precursor protein and Alzheimer's disease. J Neurosci. 1996;16(18): 5795-5811.
66. Tatebayashi Y, Miyasaka T, Chui DH, et al. Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci U S A. 2002;99(21):13896-13901.
67. Lewis J, McGowan E, Rockwood J, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet. 2000;25(4):402-405.
68. Hsiao K, Chapman P, Nilsen S, et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science. 1996;274(5284):99-102.
69. Oddo S, Caccamo A, Shepherd JD, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron. 2003;39(3):409-421.
70. Chen LJ, Wang YJ, Tseng GF. Compression alters kinase and phosphatase activity and tau and MAP2 phosphorylation transiently while inducing the fast adaptive dendritic remodeling of underlying cortical neurons. J Neurotrauma. 2010;27(9): 1657-1669.
71. Riedel G, Micheau J, Lam AG, et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci. 1999;2(10): 898-905.
72. Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience. 1991;40(3):599-636.
73. Aitken PG, Schiff SJ. Selective neuronal vulnerability to hypoxia in vitro. Neurosci Lett. 1986;67(1):92-96.
74. Crepel V, Krnjevic K, Ben-Ari Y. Developmental and regional differences in the vulnerability of rat hippocampal slices to lack of glucose. Neuroscience. 1992;47(3): 579-587.
75. Kass IS, Lipton P. Calcium and long-term transmission damage following anoxia in dentate gyrus and CA1 regions of the rat hippocampal slice. J Physiol. 1986;378: 313-334.
76. Kreisman NR, Soliman S, Gozal D. Regional differences in hypoxic depolarization and swelling in hippocampal slices. J Neurophysiol. 2000;83(2):1031-1038.
77. Laeremans A, Sabanov V, Ahmed T, et al. Distinct and simultaneously active plasticity mechanisms in mouse hippocampus during different phases of Morris water maze training. Brain Struct Funct. 2014 Feb 23 [Epub ahead of print].
78. Florian C, Roullet P. Hippocampal CA3-region is crucial for acquisition and memory consolidation in Morris water maze task in mice. Behav Brain Res. 2004; 154(2):365-374.
79. Acosta SA, Tajiki N, Shinozuka K, et al. Combination therapy of human umbilical cord blood cells and granulocyte colony stimulating factor reduces histopathological and motor impairments in an experimental model of chronic traumatic brain injury. PLoS One. 2014;9(3):e90953.
80. Magen I, Gozes I. Davunetide: peptide therapeutic in neurological disorders. Curr Med Chem. 2014;21(23):2591-2598.
81. Lu XC, Chen RW, Yao C, et al. NNZ-2566, a glypromate analog, improves functional recovery and attenuates apoptosis and inflammation in a rat model of penetrating ballistic-type brain injury. J Neurotrauma. 2009;26(1):141-154.
82. Yang P, Arnold SA, Habas A, Hetman M, Hagg T. Ciliary neurotrophic factor mediates dopamine D2 receptor-induced CNS neurogenesis in adult mice. J Neurosci. 2008;28(9):2231-2241.
83. Chen ZY, Cao L, Wang LM, et al. Development of neurotrophic molecules for treatment of neurodegeneration. Curr Protein Pept Sci. 2001;2(3):261-276.
84. Kazim SF, Blanchard J, Dai CL, et al. Disease modifying effect of chronic oral treatment with a neurotrophic peptidergic compound in a triple transgenic mouse model of Alzheimer's disease. Neurobiol Dis. 2014;71C:110.
85. Inoue M, Nakayama C, Kikuchi K, et al. D1 cap region involved in the receptor recognition and neural cell survival activity of human ciliary neurotrophic factor. Proc Natl Acad Sci U S A. 1995;92(19):8579-8583.
86. Shimazaki T, Shingo T, Weiss S. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci. 2001;21(19):7642-7653.
87. Bauer S, Patterson PH. Leukemia inhibitory factor promotes neural stem cell selfrenewal in the adult brain. J Neurosci. 2006;26(46):12089-12099.
88. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development. 2005;132(24):5503-5514.