The Minocycline Ameliorated the Synaptic Plasticity Impairment in Vascular Dementia

Document Type : Research article

Authors

1 Imam Reza Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

2 Department of Physiology, The Medical School, Shiraz University of Medical Sciences, Shiraz, Iran.

3 Clinical Neurology Research Centre, Shiraz University of Medical Sciences, Shiraz, Iran.

4 Neuroscience Research Center, Neuropharmacology Institute, Kerman University of Medical Sciences, Kerman, Iran.

Abstract

Chronic cerebral hypoperfusion (CCH) leads to vascular dementia with progressive hippocampal damage and cognitive impairments. In the present study, we compared early and late Minocycline (MINO) treatment on cognitive function, long and short-term synaptic-plasticity following CCH. We used bilateral common carotid arteries occlusion model (2VO) for induction of hypoperfusion. Male Sprague-Dawley rats were divided into 5 following groups (each having 2 subgroups): 2VO + V (vehicle), 2VO+MINO-E (early treatment of MINO on days 0 to 3 after 2VO), 2VO+MINO-L (late-treatment on days 21 to 32 after 2VO), control, and sham. Passive-avoidance (PA) and radial arm maze (RAM) tests were used to investigate learning and memory. Long term and short term synaptic plasticity were assessed by field potential recording, the brains were removed after recording and preserved for histological study to count pyramidal cells in CA1 region. Cerebral hypoperfusion could impair memory performance, synaptic plasticity, and basal synaptic transmission (BST) along with hippocampal cell loss. Thus, we found a significant reduction in step-through latency (STL) of PA test with a higher number of working and reference errors in RAM in CCH rats. However, only late treatment with MINO improved memory performance, synaptic plasticity, hippocampal cell loss, and increased neurotransmitter pool (NP) in CCH rats, but early treatment could not produce long-lasting beneficial effects 32 days after 2VO. MINO may improve synaptic plasticity and memory performance in hypo-perfused rats directly and indirectly by increasing NP and/or suppressing inflammatory factors, respectively.

Graphical Abstract

The Minocycline Ameliorated the Synaptic Plasticity Impairment in Vascular Dementia

Keywords


(1)        Duncombe J, Kitamura A, Hase Y, Ihara M, Kalaria RN and Horsburgh K. Chronic cerebral hypoperfusion: a key mechanism leading to vascular cognitive impairment and dementia. Closing the translational gap between rodent models and human vascular cognitive impairment and dementia. Clin. Sci. (Lond.) (2017) 131: 2451-68.
(2)        Sweeney MD, Montagne A, Sagare AP, Nation DA, Schneider LS, Chui HC, Harrington MG, Pa J, Law M, Wang DJJ, Jacobs RE, Doubal FN, Ramirez J, Black SE, Nedergaard M, Benveniste H, Dichgans M, Iadecola C, Love S, Bath PM, Markus HS, Salman RA, Allan SM, Quinn TJ, Kalaria RN, Werring DJ, Carare RO, Touyz RM, Williams SCR, Moskowitz MA, Katusic ZS, Lutz SE, Lazarov O, Minshall RD, Rehman J, Davis TP, Wellington CL, González HM, Yuan C, Lockhart SN, Hughes TM, Chen CLH, Sachdev P, O'Brien JT, Skoog I, Pantoni L, Gustafson DR, Biessels GJ, Wallin A, Smith EE, Mok V, Wong A, Passmore P, Barkof F, Muller M, Breteler MMB, Román GC, Hamel E, Seshadri S, Gottesman RF, van Buchem MA, Arvanitakis Z, Schneider JA, Drewes LR, Hachinski V, Finch CE, Toga AW, Wardlaw JM and Zlokovic BV. Vascular dysfunction-The disregarded partner of Alzheimer's disease. Alzheimers Dement. (2019) 15: 158-67.
(3)        Kynast J, Lampe L, Luck T, Frisch S, Arelin K, Hoffmann KT, Loeffler M, Riedel-Heller SG, Villringer A and Schroeter ML. White matter hyperintensities associated with small vessel disease impair social cognition beside attention and memory. J. Cereb. Blood Flow Metab. (2018) 38: 996-1009.
(4)        Bliss TV and Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature (1993) 361: 31-9.
(5)        Shabani M, Ebrahimpoor F, Firouzjaei MA, Kamali L, Shid Moosavi SM, Noorafshan A and Haghani M. Modulation of sphingosine-1-phosphate receptor by FTY720 contributes in improvement of hepatic encephalopathy induced by bile duct ligation. Brain Res. Bull. (2019) 146: 253-69.
(6)        Karimi N, Haghani M, Noorafshan A and Moosavi SMS. Structural and functional disorders of hippocampus following ischemia/reperfusion in lower limbs and kidneys. Neurosci. (2017) 358: 238-48.
(7)        Lenart N, Brough D and Denes A. Inflammasomes link vascular disease with neuroinflammation and brain disorders. J. Cereb. Blood Flow Metab. (2016) 36: 1668-85.
(8)        Kielian T, Esen N, Liu S, Phulwani NK, Syed MM, Phillips N, Nishina K, Cheung AL, Schwartzman JD and Ruhe J. Minocycline modulates neuroinflammation independently of its antimicrobial activity in staphylococcus aureus-induced brain abscess. Am. J. Pathol. (2007) 171: 1199-214.
(9)        Kraus RL, Pasieczny R, Lariosa-Willingham K, Turner MS, Jiang A and Trauger JW. Antioxidant properties of minocycline: neuroprotection in an oxidative stress assay and direct radical-scavenging activity. J. Neurochem. (2005) 94: 819-27.
(10)      Lu Y, Huang Z, Hua Y and Xiao G. Minocycline promotes BDNF expression of N2a cells via inhibition of mir-155-mediated repression after oxygen-glucose deprivation and reoxygenation. Cell Mol. Neurobiol. (2018) 38: 1305-13.
(11)      Yong VW, Wells J, Giuliani F, Casha S, Power C and Metz LM. The promise of minocycline in neurology. Lancet Neurol. (2004) 3: 744-51.
(12)      Venkat P, Shen Y, Chopp M and Chen J. Cell-based and pharmacological neurorestorative therapies for ischemic stroke. Neuropharmacol. (2018) 134: 310-22.
(13)      Mohammadian F, Firouzjaei MA, Haghani M, Shabani M, Shid Moosavi SM and Mohammadi F. Inhibition of inflammation is not enough for recovery of cognitive impairment in hepatic encephalopathy: Effects of minocycline and ibuprofen. Brain Res. Bull. (2019) 149: 96-105.
(14)      Kloppenburg M, Breedveld FC, Terwiel JP, Mallee C and Dijkmans BA. Minocycline in active rheumatoid arthritis. A double-blind, placebo-controlled trial. Arthritis Rheum. (1994) 37: 629-36.
(15)      Garcez ML, Mina F, Bellettini-Santos T, Carneiro FG, Luz AP, Schiavo GL, Andrighetti MS, Scheid MG, Bolfe RP and Budni J. Minocycline reduces inflammatory parameters in the brain structures and serum and reverses memory impairment caused by the administration of amyloid beta (1-42) in mice. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. (2017) 77: 23-31.
(16)      Cronin A and Grealy M. Neuroprotective and Neuro-restorative Effects of Minocycline and Rasagiline in a Zebrafish 6-Hydroxydopamine Model of Parkinson's Disease. Neurosci. (2017) 367: 34-46.
(17)      Squair JW, Ruiz I, Phillips AA, Zheng MMZ, Sarafis ZK, Sachdeva R, Gopaul R, Liu J,Tetzlaff W, West CR and Krassioukov AV. Minocycline reduces the severity of autonomic dysreflexia after experimental spinal cord injury. J. Neurotrauma. (2018) 35: 2861-71.
(18)      Jiang Y, Liu Y, Zhu C, Ma X, Ma L, Zhou L, Huang Q, Cen L, Pi R and Chen X. Minocycline enhances hippocampal memory, neuroplasticity and synapse-associated proteins in aged C57 BL/6 mice. Neurobiol. Learn Mem. (2015) 121: 20-9.
(19)      Cho KO, La HO, Cho YJ, Sung KW and Kim SY. Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion. J. Neurosci. Res. (2006) 83: 285-91.
(20)      Cai ZY, Yan Y, Sun SQ, Zhang J, Huang LG, Yan N, Wu F and Li JY. Minocycline attenuates cognitive impairment and restrains oxidative stress in the hippocampus of rats with chronic cerebral hypoperfusion. Neurosci. Bull. (2008) 24: 305-13.
(21)      Ma J, Zhang J, Hou WW, Wu XH, Liao RJ, Chen Y, Wang Z, Zhang XN, ZhangLS, Zhou YD, Chen Z and Hu WW. Early treatment of minocycline alleviates white matter and cognitive impairments after chronic cerebral hypoperfusion. Sci. Rep. (2015) 5: 12079.
(22)      Manso Y, Holland PR, Kitamura A, Szymkowiak S, Duncombe J, Hennessy E, Searcy JL, Marangoni M, Randall AD, Brown JT, McColl BW and Horsburgh K. Minocycline reduces microgliosis and improves subcortical white matter function in a model of cerebral vascular disease. Glia. (2018) 66: 34-46.
(23)      Bayat M, Sharifi MD, Haghani M and Shabani M. Enriched environment improves synaptic plasticity and cognitive deficiency in chronic cerebral hypoperfused rats. Brain Res. Bull. (2015) 119: 34-40.
(24)      Shabani M, Haghani M, Tazangi PE, Bayat M, Shid Moosavi SM and Ranjbar H. Netrin-1 improves the amyloid-beta-mediated suppression of memory and synaptic plasticity. Brain Res. Bull. (2017) 131: 107-16.
(25)      Aghaei I, Hajali V, Dehpour A, Haghani M, Sheibani V and Shabani M. Alterations in the intrinsic electrophysiological properties of Purkinje neurons in a rat model of hepatic encephalopathy: Relative preventing effect of PPARgamma agonist. Brain Res. Bull. (2016) 121: 16-25.
(26)      Haghani M, Keshavarz S, Nazari M and Rafati A. Electrophysiology of cerebral ischemia and reperfusion: First evidence for the role of synapse in ischemic tolerance. Synapse. (2016) 70: 351-60.
(27)      Esmaeili Tazangi P, Moosavi SM, Shabani M and Haghani M. Erythropoietin improves synaptic plasticity and memory deficits by decrease of the neurotransmitter release probability in the rat model of Alzheimer's disease. Pharmacol. Biochem. Behav. (2015) 130: 15-21.
(28)      Kuang X, Scofield VL, Yan M, Stoica G, Liu N and Wong PK. Attenuation of oxidative stress, inflammation and apoptosis by minocycline prevents retrovirus-induced neurodegeneration in mice. Brain Res. (2009) 1286: 174-84.
(29)      Feng L, Gao J, Wang Y, Cheong YK, Ren G and Yang Z. Etidronate-zinc complex ameliorated cognitive and synaptic plasticity impairments in 2-vessel occlusion model rats by reducing neuroinflammation. Neurosci. (2018) 390: 206-17.
(30)      Hei Y, Chen R, Yi X, Long Q, Gao D and Liu W. HMGB1 neutralization attenuates hippocampal neuronal death and cognitive impairment in rats with chronic cerebral hypoperfusion via suppressing inflammatory responses and oxidative stress. Neurosci. (2018) 383: 150-9.
(31)      Sa Santos S, Santos SM, Pinto AR, Ramu VG, Heras M, Bardaji E, Tavares I and Castanho MARB. Amidated and Ibuprofen-Conjugated Kyotorphins Promote Neuronal Rescue and Memory Recovery in Cerebral Hypoperfusion Dementia Model. Front. Aging Neurosci. (2016) 8: 1.
(32)      Wang DP, Yin H, Lin Q, Fang SP, Shen JH, Wu YF, Su SH and Hai J. Andrographolide enhances hippocampal BDNF signaling and suppresses neuronal apoptosis, astroglial activation, neuroinflammation, and spatial memory deficits in a rat model of chronic cerebral hypoperfusion. Naunyn Schmiedebergs Arch Pharmacol. (2019) 392: 1277-84.
(33)      Su SH, Wu YF, Lin Q and Hai J. Cannabinoid receptor agonist WIN55,212-2 and fatty acid amide hydrolase inhibitor URB597 ameliorate neuroinflammatory responses in chronic cerebral hypoperfusion model by blocking NF-kappaB pathways. Naunyn Schmiedebergs Arch Pharmacol. (2017) 390: 1189-200.
(34)      McGeer PL, Guo JP, Lee M, Kennedy K and McGeer EG. Alzheimer's Disease Can Be Spared by Nonsteroidal Anti-Inflammatory Drugs. J. Alzheimers Dis. (2018) 62: 1219-22.
(35)      McGeer PL, Rogers J and McGeer EG. Inflammation, Antiinflammatory Agents, and Alzheimer's Disease: The Last 22 Years. J. Alzheimers Dis. (2016) 54: 853-7.
(36)      Karimi N, Bayat M, Haghani M, Saadi HF and Ghazipour GR. 2.45 GHz microwave radiation impairs learning, memory, and hippocampal synaptic plasticity in the rat. Toxicology and industrial health. (2018) 34: 873-83.
(37)      Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA and Pittman QJ. Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation. Proc. Natl. Acad. Sci. U.S.A. (2008) 105: 17151-6.
(38)      Fogal B and Hewett SJ. Interleukin-1beta: a bridge between inflammation and excitotoxicity? J. Neurochem. (2008) 106: 1-23.
(39)      Lana D, Melani A, Pugliese AM, Cipriani S, Nosi D, Pedata F and Giovannini MG . The neuron-astrocyte-microglia triad in a rat model of chronic cerebral hypoperfusion: protective effect of dipyridamole. Front. Aging Neurosci. (2014) 6: 322.
(40)      Barres BA. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron. (2008) 60: 430-40.
(41)      Jalini S, Ye H, Tonkikh AA, Charlton MP and Carlen PL. Raised intracellular calcium contributes to ischemia-induced depression of evoked synaptic transmission. PLoS One. (2016) 11: e0148110.
(42)      Li Y, Lei Z and Xu ZC. Enhancement of inhibitory synaptic transmission in large aspiny neurons after transient cerebral ischemia. Neurosci. (2009) 159: 670-81.
(43)      Wang Z, Fan J, Wang J, Li Y, Duan D, Du G and Wang Q. Chronic cerebral hypoperfusion induces long-lasting cognitive deficits accompanied by long-term hippocampal silent synapses increase in rats. Behav. Brain Res. (2016) 301: 243-52.
(44)      Tahamtan M, Aghaei I, Pooladvand V, Sheibani V, Khaksari M and Shabani M. Characterization of the CA1 pyramidal neurons in rat model of hepatic cirrhosis: insights into their electrophysiological properties. Metab. Brain Dis. (2017) 32: 881-9.
(45)      Dobrunz LE and Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron. (1997) 18: 995-1008.
(46)      Li CJ, Zhou M, Li HG, Lv Q, Xu XL and Guo LJ. Clonidine suppresses the induction of long-term potentiation by inhibiting HCN channels at the Schaffer collateral-CA1 synapse in anesthetized adult rats. Cell Mol. Neurobiol. (2013) 33: 1075-86.
(47)      Griffin R, Nally R, Nolan Y, McCartney Y, Linden J and Lynch MA. The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem. (2006) 99: 1263-72.
(48)      Clare R, King VG, Wirenfeldt M and Vinters HV. Synapse loss in dementias. J. Neurosci. Res. (2010) 88: 2083-90.
(49)      Yao ZH, Yao XL, Zhang Y, Zhang SF and Hu JC. Luteolin Could Improve Cognitive Dysfunction by Inhibiting Neuroinflammation. Neurochem. Res. (2018) 43: 806-20.
(50)      Pickering M and O'Connor JJ. Pro-inflammatory cytokines and their effects in the dentate gyrus. Prog. Brain Res. (2007) 163: 339-54.