Preservation of the blood brain barrier and cortical neuronal tissue by Liraglutide, a long acting glucagon-like-1 analogue, after experimental traumatic brain injury

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Hakon, Jakob ^a,b   Ruscher, Karsten ^a   Romner, Bertil ^b,c   Tomasevic, Gregor ^a,c  

^a LUND UNIVERSITY   (Sweden)

^b Department of Neurosurgery Copenhagen University Hospital Risgshospitalet ^*  (Denmark)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EVANS BLUE; GLUCAGON LIKE PEPTIDE 1; LIRAGLUTIDE; PHOSPHATE BUFFERED SALINE; GLUCOSE BLOOD LEVEL; NEUROPROTECTIVE AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CONTUSION; BRAIN CORTEX; BRAIN EDEMA; BRAIN WATER; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG TARGETING; EXTRAVASATION; INJURY SEVERITY; MALE; NERVE CELL NECROSIS; NERVE INJURY; NEUROPROTECTION; NONHUMAN; RAT; SENSORIMOTOR FUNCTION; SIGNAL TRANSDUCTION; THALAMUS; TRAUMATIC BRAIN INJURY; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN INJURIES; CELL DEATH; DISEASE MODEL; DRUG EFFECTS; GLUCOSE BLOOD LEVEL; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SENSORIMOTOR CORTEX; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; BLOOD GLUCOSE; BLOOD-BRAIN BARRIER; BRAIN EDEMA; BRAIN INJURIES; CELL DEATH; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; GLUCAGON-LIKE PEPTIDE 1; LIRAGLUTIDE; MALE; NEURONS; NEUROPROTECTIVE AGENTS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; SENSORIMOTOR CORTEX;

EID: 84926512824     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120074     Document Type: Article

References (76)

1. Xiong Y, Mahmood A, Chopp M. Emerging treatments for traumatic brain injury. Expert Opin Emerg Drugs. 2009; 14: 67-84. doi: 10.1517/14728210902769601 PMID: 19249984
2. Narotam PK, Morrison JF, Nathoo N. Brain tissue oxygen monitoring in traumatic brain injury and major trauma: outcome analysis of a brain tissue oxygen-directed therapy. J Neurosurg. 2009; 111: 672-82. doi: 10.3171/2009.4.JNS081150 PMID: 19463048
3. Unterberg AW, Stover J, Kress B, Kiening KL. Edema and brain trauma. Neuroscience. 2004; 129: 1021-1029. PMID: 15561417
4. Chodobski A, Zink BJ, Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res. 2011; 2: 492-516. doi: 10.1007/s12975-011-0125-x PMID: 22299022
5. Holst JJ, Burcelin R, Nathanson E. Neuroprotective properties of GLP-1: theoretical and practical applications. Curr Med Res Opin. 2011; 27: 547-58. doi: 10.1185/03007995.2010.549466 PMID: 21222567
6. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007; 87: 1409-39. PMID: 17928588
7. Hunter K, Hölscher C. Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis. BMC neurosci. BioMed Central Ltd; 2012; 13: 33.
8. Hou J, Manaenko A, Hakon J, Hansen-Schwartz J, Tang J, Zhang JH. Liraglutide, a long-acting GLP-1 mimetic, and its metabolite attenuate inflammation after intracerebral hemorrhage. J cereb Blood Flow Metab. Nature Publishing Group; 2012; 1-10. doi: 10.1038/jcbfm.2012.144 PMID: 23072746
9. Iwai T, Ito S, Tanimitsu K, Udagawa S, Oka J-I. Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes. Neurosci Res. 2006; 55: 352-60. PMID: 16720054
10. Darsalia V, Mansouri S, Ortsäter H, Olverling A, Nozadze N, Kappe C, et al. Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats. Clin Sci (Lond). 2012; 122: 473-83. doi: 10.1042/CS20110374 PMID: 22150224
11. Lee CH, Yan B, Yoo K-Y, Choi JH, Kwon S-H, Her S, et al. Ischemia-induced changes in glucagon-like peptide-1 receptor and neuroprotective effect of its agonist, exendin-4, in experimental transient cerebral ischemia. J Neurosci Res. 2011; 89: 1103-13. doi: 10.1002/jnr.22596 PMID: 21472764
12. Briyal S, Gulati K, Gulati A. Repeated administration of exendin-4 reduces focal cerebral ischemia-induced infarction in rats. Brain res. Elsevier B.V.; 2012; 1427: 23-34. doi: 10.1016/j.brainres.2011.10.026 PMID: 22055454
13. Sato K, Kameda M, Yasuhara T, Agari T, Baba T, Wang F, et al. Neuroprotective effects of liraglutide for stroke model of rats. Int J Mol Sci. 2013; 14: 21513-24. doi: 10.3390/ijms141121513 PMID: 24177570
14. Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, Holloway HW, et al. GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism. Proc Natl Acad Sci U S A. 2009; 106: 1285-90. doi: 10.1073/pnas.0806720106 PMID: 19164583
15. McClean PL, Hölscher C. Liraglutide can reverse memory impairment, synaptic loss and reduce plaque load in aged APP/PS1 mice, a model of Alzheimer's disease. Neuropharmacology. Elsevier; 2014; 76 Pt A: 57-67. doi: 10.1016/j.neuropharm.2013.08.005 PMID: 23973293
16. Bertilsson G, Patrone C, Zachrisson O, Andersson A, Dannaeus K, Heidrich J, et al. Peptide hormone exendin-4 stimulates subventricular zone neurogenesis in the adult rodent brain and induces recovery in an animal model of Parkinson's disease. J Neurosci Res. 2008; 86: 326-38. PMID: 17803225
17. Albert-Weissenberger C, Sirén A-L. Experimental traumatic brain injury. Exp Transl Stroke Med. 2010; 2: 16. doi: 10.1186/2040-7378-2-16 PMID: 20707892
18. Schwarzkopf TM, Horn T, Lang D, Klein J. Blood gases and energy metabolites in mouse blood before and after cerebral ischemia: the effects of anesthetics. Exp Biol Med. 2013; 238: 84-9. doi: 10.1258/ebm.2012.012261 PMID: 23479767
19. Dixon CE, Clifton GL, Lighthall JW, Yaghmai a a, Hayes RL. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods. 1991; 39: 253-62. PMID: 1787745
20. Hamm RJ, Dixon CE, Gbadebo DM, Singha a K, Jenkins LW, Lyeth BG, et al. Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J Neurotrauma. 1992; 9: 11-20. PMID: 1619672
21. Hunter AJ, Hatcher J, Virley D, Nelson P, Irving E, Hadingham SJ, et al. Functional assessments in mice and rats after focal stroke. Neuropharmacology. 2000; 39: 806-16. PMID: 10699446
22. Yrjänheikki J, Koistinaho J, Kettunen M, Kauppinen R a, Appel K, Hüll M, et al. Long-term protective effect of atorvastatin in permanent focal cerebral ischemia. Brain Res. 2005; 1052: 174-9. PMID: 16023089
23. De Ryck M, Van Reempts J, Duytschaever H, Van Deuren B, Clincke G. Neocortical localization of tactile/proprioceptive limb placing reactions in the rat. Brain Res. 1992; 573: 44-60. PMID: 1576535
24. Madinier A, Quattromani MJ, Sjölund C, Ruscher K, Wieloch T. Enriched housing enhances recovery of limb placement ability and reduces aggrecan-containing perineuronal nets in the rat somatosensory cortex after experimental stroke. PLoS One. 2014; 9: e93121. doi: 10.1371/journal.pone.0093121 PMID: 24664200
25. Başkaya MK, Doʇan A, Temiz C, Dempsey RJ. Application of 2,3,5-triphenyltetrazolium chloride staining to evaluate injury volume after controlled cortical impact brain injury: role of brain edema in evolution of injury volume. J Neurotrauma. 2000; 17: 93-9. PMID: 10674761
26. Fukui S, Fazzina G, Amorini AM, Dunbar JG, Marmarou A. Differential effects of atrial natriuretic peptide on the brain water and sodium after experimental cortical contusion in the rat. J cereb Blood Flow Metab. 2003; 23: 1212-8. PMID: 14526231
27. Hall ED, Bryant YD, Cho W, Sullivan PG. Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. J Neurotrauma. 2008; 25: 235-47. doi: 10.1089/neu.2007.0383 PMID: 18352837
28. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab. 1990; 10: 290-293. PMID: 1689322
29. Zhang Y-B, Li S-X, Chen X-P, Yang L, Zhang Y-G, Liu R, et al. Autophagy is activated and might protect neurons from degeneration after traumatic brain injury. Neurosci Bull. 2008; 24: 143-9. doi: 10.1007/s12264-008-1108-0 PMID: 18500386
30. Kenne E, Erlandsson A, Lindbom L, Hillered L, Clausen F. Neutrophil depletion reduces edema formation and tissue loss following traumatic brain injury in mice. J Neuroinflammation. BioMed Central Ltd; 2012; 9: 17.
31. Draper K, Ponsford J. Long-term outcome following traumatic brain injury: a comparison of subjective reports by those injured and their relatives. Neuropsychol Rehabil. 2009; 19: 645-61. doi: 10.1080/17405620802613935 PMID: 19629849
32. Tweedie D, Rachmany L, Rubovitch V, Lehrmann E, Zhang Y, Becker KG, et al. Exendin-4, a glucagon-like peptide-1 receptor agonist prevents mTBI-induced changes in hippocampus gene expression and memory deficits in mice. Exp Neurol. Elsevier Inc.; 2013; 239: 170-82. doi: 10.1016/j.expneurol.2012.10.001 PMID: 23059457
33. Rachmany L, Tweedie D, Li Y, Rubovitch V, Holloway HW, Miller J, et al. Exendin-4 induced glucagon-like peptide-1 receptor activation reverses behavioral impairments of mild traumatic brain injury in mice. Age. 2012;
34. Tweedie D, Rachmany L, Rubovitch V, Zhang Y, Becker KG, Perez E, et al. Changes in mouse cognition and hippocampal gene expression observed in a mild physical- and blast-traumatic brain injury. Neurobiol Dis. Elsevier Inc.; 2013; 54: 1-11. doi: 10.1016/j.nbd.2013.02.006 PMID: 23454194
35. Eakin K, Li Y, Chiang Y-H, Hoffer BJ, Rosenheim H, Greig NH, et al. Exendin-4 ameliorates traumatic brain injury-induced cognitive impairment in rats. PLoS One. 2013; 8: e82016. doi: 10.1371/journal.pone.0082016 PMID: 24312624
36. Nishibe M, Barbay S, Guggenmos D, Nudo RJ. Reorganization of motor cortex after controlled cortical impact in rats and implications for functional recovery. J Neurotrauma. 2010; 27: 2221-32. doi: 10.1089/neu.2010.1456 PMID: 20873958
37. Feickert HJ, Drommer S, Heyer R. Severe head injury in children: impact of risk factors on outcome. J Trauma. 1999; 47: 33-8. PMID: 10421183
38. Sztriha L, Joó F, Szerdahelyi P. Time-course of changes in water, sodium, potassium and calcium contents of various brain regions in rats after systemic kainic acid administration. Acta Neuropathol. 1986; 70: 169-76. PMID: 3739624
39. Forbes ML, Hendrich KS, Kochanek PM, Williams DS, Schiding JK, Wisniewski SR, et al. Assessment of cerebral blood flow and CO2 reactivity after controlled cortical impact by perfusion magnetic resonance imaging using arterial spin-labeling in rats. J cereb Blood Flow Metab. 1997; 17: 865-74. PMID: 9290584
40. Knoblach SM, Faden AI. Administration of either anti-intercellular adhesion molecule-1 or a nonspecific control antibody improves recovery after traumatic brain injury in the rat. J Neurotrauma. 2002; 19: 1039-50. PMID: 12482117
41. Whalen MJ, Carlos TM, Dixon CE, Robichaud P, Clark RS, Marion DW, et al. Reduced brain edema after traumatic brain injury in mice deficient in P-selectin and intercellular adhesion molecule-1. J Leukoc Biol. 2000; 67: 160-8. PMID: 10670575
42. Schoettle RJ, Kochanek PM, Magargee MJ, Uhl MW, Nemoto EM. Early polymorphonuclear leukocyte accumulation correlates with the development of posttraumatic cerebral edema in rats. J Neurotrauma. 1990; 7: 207-17. PMID: 2127947
43. Collard CD, Park K a, Montalto MC, Alapati S, Buras J a, Stahl GL, et al. Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem. 2002; 277: 14801-11. PMID: 11847215
44. Fischer S, Wiesnet M, Renz D, Schaper W. H2O2 induces paracellular permeability of porcine brain-derived microvascular endothelial cells by activation of the p44/42 MAP kinase pathway. Eur J Cell Biol. 2005; 84: 687-97. PMID: 16106912
45. Shigemori Y, Katayama Y, Mori T, Maeda T, Kawamata T. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir Suppl. 2006; 96: 130-3. PMID: 16671440
46. Ceriello A, Novials A, Ortega E, Canivell S, La Sala L, Pujadas G, et al. Glucagon-Like Peptide 1 Reduces Endothelial Dysfunction, Inflammation, and Oxidative Stress Induced by Both Hyperglycemia and Hypoglycemia in Type 1 Diabetes. Diabetes Care. 2013; 1-5. PMID: 23390628
47. Shiraki A, Oyama J, Komoda H, Asaka M, Komatsu A, Sakuma M, et al. The glucagon-like peptide 1 analog liraglutide reduces TNF-α-induced oxidative stress and inflammation in endothelial cells. Atherosclerosis. Elsevier Ireland Ltd; 2012; 221: 375-82.
48. Krasner NM, Ido Y, Ruderman NB, Cacicedo JM. Glucagon-like peptide-1 (GLP-1) analog liraglutide inhibits endothelial cell inflammation through a calcium and AMPK dependent mechanism. PLoS One. 2014; 9: e97554. doi: 10.1371/journal.pone.0097554 PMID: 24835252
49. Wang G, Jiang X, Pu H, Zhang W, An C, Hu X, et al. Scriptaid, a novel histone deacetylase inhibitor, protects against traumatic brain injury via modulation of PTEN and AKT pathway: scriptaid protects against TBI via AKT. Neurotherapeutics. 2013; 10: 124-42. doi: 10.1007/s13311-012-0157-2 PMID: 23132328
50. Shein NA, Grigoriadis N, Alexandrovich AG, Simeonidou C, Lourbopoulos A, Polyzoidou E, et al. Histone deacetylase inhibitor ITF2357 is neuroprotective, improves functional recovery, and induces glial apoptosis following experimental traumatic brain injury. FASEB J. 2009; 23: 4266-75. doi: 10.1096/fj.09-134700 PMID: 19723705
51. Dellavalle B, Hempel C, Johansen FF, Anders J, Kurtzhals L. GLP-1 improves neuropathology after murine cold lesion brain trauma. Ann Clin Transl Neurol. 2014; 1: 721-732. doi: 10.1002/acn3.99 PMID: 25493285
52. Heile AMB, Wallrapp C, Klinge PM, Samii A, Kassem M, Silverberg G, et al. Cerebral transplantation of encapsulated mesenchymal stem cells improves cellular pathology after experimental traumatic brain injury. Neurosci Lett. 2009; 463: 176-81. doi: 10.1016/j.neulet.2009.07.071 PMID: 19638295
53. Teramoto S, Miyamoto N, Yatomi K, Tanaka Y, Oishi H, Arai H, et al. Exendin-4, a glucagon-like peptide-1 receptor agonist, provides neuroprotection in mice transient focal cerebral ischemia. J cereb Blood Flow Metab. Nature Publishing Group; 2011; 31: 1696-705. doi: 10.1038/jcbfm.2011.51 PMID: 21487412
54. Li Y, Tweedie D, Mattson MP, Holloway HW, Greig NH. Enhancing the GLP-1 receptor signaling pathway leads to proliferation and neuroprotection in human neuroblastoma cells. J Neurochem. 2010; 113: 1621-31. doi: 10.1111/j.1471-4159.2010.06731.x PMID: 20374430
55. Perry T, Haughey NJ, Mattson MP, Egan JM, Greig NH. Protection and reversal of excitotoxic neuronal damage by glucagon-like peptide-1 and exendin-4. J Pharmacol Exp Ther. 2002; 302: 881-8. PMID: 12183643
56. Kochanek PM, Marion DW, Zhang W, Schiding JK, White M, Palmer AM, et al. Severe controlled cortical impact in rats: assessment of cerebral edema, blood flow, and contusion volume. J Neurotrauma. 1995; 12: 1015-25. PMID: 8742130
57. Conti AC, Raghupathi R, Trojanowski JQ, McIntosh TK. Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J Neurosci. 1998; 18: 5663-72. PMID: 9671657
58. Jeremitsky E, Omert LA, Dunham CM, Wilberger J, Rodriguez A. The impact of hyperglycemia on patients with severe brain injury. J Trauma. 2005; 58: 47-50. PMID: 15674149
59. Eakins J. Blood glucose control in the trauma patient. J Diabetes Sci Technol. 2009; 3: 1373-6. PMID: 20144391
60. McCowen KC, Malhotra A, Bistrian BR. Stress-induced hyperglycemia. Crit Care Clin. 2001; 17: 107-24. PMID: 11219223
61. Laird AM, Miller PR, Kilgo PD, Meredith JW, Chang MC. Relationship of Early Hyperglycemia to Mortality in Trauma Patients. J Trauma. 2004; 56: 1058-1062. PMID: 15179246
62. Tomlinson DR, Gardiner NJ. Glucose neurotoxicity. Nat Rev Neurosci. 2008; 9: 36-45. PMID: 18094705
63. Li P, Shuaib A, Miyashita H, He Q-P, Siesjo BK, Warner DS. Hyperglycemia Enhances Extracellular Glutamate Accumulation in Rats Subjected to Forebrain Ischemia Editorial Comment. Stroke. 2000; 31: 183-192. PMID: 10625736
64. Vespa P, Boonyaputthikul R, McArthur DL, Miller C, Etchepare M, Bergsneider M, et al. Intensive insulin therapy reduces microdialysis glucose values without altering glucose utilization or improving the lactate/pyruvate ratio after traumatic brain injury. Crit Care Med. 2006; 34: 850-6. PMID: 16505665
65. Godoy DA, Di Napoli M, Rabinstein AA. Treating hyperglycemia in neurocritical patients: benefits and perils. Neurocrit Care. 2010; 13: 425-38. doi: 10.1007/s12028-010-9404-8 PMID: 20652767
66. Gejl M, Egefjord L, Lerche S, Vang K, Bibby BM, Holst JJ, et al. Glucagon-like peptide-1 decreases intracerebral glucose content by activating hexokinase and changing glucose clearance during hyperglycemia. J cereb Blood Flow Metab. 2012; 32: 2146-52. doi: 10.1038/jcbfm.2012.118 PMID: 22929437
67. Gejl M, Lerche S, Egefjord L, Brock B, Møller N, Vang K, et al. Glucagon-like peptide-1 (GLP-1) raises blood-brain glucose transfer capacity and hexokinase activity in human brain. Front Neuroenergetics. 2013; 5: 2. doi: 10.3389/fnene.2013.00002 PMID: 23543638
68. Nauck MA, Heimesaat MM, Behle K, Holst JJ, Nauck MS, Ritzel R, et al. Effects of glucagon-like peptide 1 on counterregulatory hormone responses, cognitive functions, and insulin secretion during hyper-insulinemic, stepped hypoglycemic clamp experiments in healthy volunteers. J Clin Endocrinol Metab. 2002; 87: 1239-46. PMID: 11889194
69. Greig NH, Tweedie D, Rachmany L, Li Y, Rubovitch V, Schreiber S, et al. Incretin mimetics as pharmacologic tools to elucidate and as a new drug strategy to treat traumatic brain injury. Alzheimers Dement. Elsevier; 2014; 10: S62-75. doi: 10.1016/j.jalz.2013.12.011 PMID: 24529527
70. Sturis J, Gotfredsen CF, Rømer J, Rolin B, Ribel U, Brand CL, et al. GLP-1 derivative liraglutide in rats with beta-cell deficiencies: influence of metabolic state on beta-cell mass dynamics. Br J Pharmacol. 2003; 140: 123-32. PMID: 12967942
71. Services USDoHaH, Administration FaD. Guidance for Industry Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. [Internet]. 2005.
72. Raun K, von Voss P, Gotfredsen CF, Golozoubova V, Rolin B, Knudsen LB. Liraglutide, a long-acting glucagon-like peptide-1 analog, reduces body weight and food intake in obese candy-fed rats, whereas a dipeptidyl peptidase-IV inhibitor, vildagliptin, does not. Diabetes. 2007; 56: 8-15. PMID: 17192459
73. Secher A, Jelsing J, Baquero AF, Hecksher-Sørensen J, Cowley MA, Dalbøge LS, et al. The arcuate nucleus mediates GLP-1 receptor agonist liraglutide-dependent weight loss. J Clin Invest. 2014; 124: 4473-88. doi: 10.1172/JCI75276 PMID: 25202980
74. Cummings BP, Stanhope KL, Graham JL, Baskin DG, Griffen SC, Nilsson C, et al. Chronic administration of the glucagon-like peptide-1 analog, liraglutide, delays the onset of diabetes and lowers triglycerides in UCD-T2DM rats. Diabetes. 2010; 59: 2653-61. doi: 10.2337/db09-1564 PMID: 20622169
75. Astrup A, Rössner S, Van Gaal L, Rissanen A, Niskanen L, Al Hakim M, et al. Effects of liraglutide in the treatment of obesity: a randomised, double-blind, placebo-controlled study. Lancet. Elsevier Ltd; 2009; 374: 1606-16.
76. DeFronzo R, Bergenstal R, Bode B, Kushner R, Lewin A, Skjøth T, et al. Effects of Liraglutide 3.0 Mg and 1.8 Mg on Body Weight and Cardiometabolic Risk Factors in Overweight and Obese Adults with Type 2 Diabetes Mellitus (T2DM): The Scale Diabetes Randomized, Double-Blind, Placebo-Controlled, 56-Week Trial. Int Congr Endocrinol Endocr Soc Chicago, IL. 2014;