Chloride Co-transporter NKCC1 Inhibitor Bumetanide Enhances Neurogenesis and Behavioral Recovery in Rats After Experimental Stroke

Molecular Neurobiology

Volumn 54, Issue 4, 2017, Pages 2406-2414

  Xu, Wangshu ^a,b   Mu, Xiaopeng ^a   Wang, Huibin ^a   Song, Chengguang ^c   Ma, Wenping ^d   Jolkkonen, Jukka ^e   Zhao, Chuansheng ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c Benxi Central Hospital of China Medical University   (China)

^d PEKING UNIVERSITY   (China)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Behavioral recovery; Neurogenesis; Neuronal survival; NKCC1 inhibitor; Stroke

Indexed keywords

BROXURIDINE; BUMETANIDE; CELL PROTEIN; DCX PROTEIN; ENDOTHELIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; IBA 1 PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; NERVE PROTEIN; NEUN PROTEIN, RAT;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEAM WALKING TEST; BEHAVIORAL RECOVERY; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; EXPERIMENTAL STROKE; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; RAT; SENSORIMOTOR FUNCTION; SUBVENTRICULAR ZONE; WALK TEST; ANIMAL; BRAIN INFARCTION; CELL MOTION; COMPLICATION; DRUG EFFECTS; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; STROKE; WISTAR RAT;

ANIMALS; ANTIGENS, NUCLEAR; BEHAVIOR, ANIMAL; BRAIN INFARCTION; BROMODEOXYURIDINE; BUMETANIDE; CELL MOVEMENT; CELL PROLIFERATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; RATS, WISTAR; SOLUTE CARRIER FAMILY 12, MEMBER 2; STROKE;

EID: 84960109021     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-9819-0     Document Type: Article

References (43)

1. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8(9):963–970
2. Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26(50):13007–13016
3. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z et al (2006) Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24(3):739–747
4. Young SZ, Taylor MM, Bordey A (2011) Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur J Neurosci 33(6):1123–1132
5. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439(7076):589–593
6. Cancedda L, Fiumelli H, Chen K, Poo MM (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27(19):5224–5235
7. Jaenisch N, Witte OW, Frahm C (2010) Downregulation of potassium chloride cotransporter KCC2 after transient focal cerebral ischemia. Stroke 41(3):e151–e159
8. Wang G, Huang H, He Y, Ruan L, Huang J (2014) Bumetanide protects focal cerebral ischemia-reperfusion injury in rat. Int J Clin Exp Pathol 7(4):1487–1494
9. Begum G, Yuan H, Kahle KT, Li L, Wang S, Shi Y, Shmukler BE, Yang SS et al (2015) Inhibition of WNK3 kinase signaling reduces brain damage and accelerates neurological recovery after stroke. Stroke 46(7):1956–1965
10. −-cotransporter in choroid plexus attenuates traumatic brain injury-induced brain edema and neuronal damage. Eur J Pharmacol 548(1–3):99–105
11. O’Donnell ME, Lam TI, Tran L, Anderson SE (2004) The role of the blood–brain barrier Na-K-2Cl cotransporter in stroke. Adv Exp Med Biol 559:67–75
12. Yan Y, Dempsey RJ, Flemmer A, Forbush B, Sun D (2003) Inhibition of Na(+)-K(+)-Cl(−) cotransporter during focal cerebral ischemia decreases edema and neuronal damage. Brain Res 961(1):22–31
13. Soleman S, Yip P, Leasure JL, Moon L (2010) Sustained sensorimotor impairments after endothelin-1 induced focal cerebral ischemia (stroke) in aged rats. Exp Neurol 222(1):13–24
14. Cleary RT, Sun H, Huynh T, Manning SM, Li Y, Rotenberg A, Talos DM, Kahle KT et al (2013) Bumetanide enhances phenobarbital efficacy in a rat model of hypoxic neonatal seizures. PLoS One 8(3), e57148
15. Puskarjov M, Kahle KT, Ruusuvuori E, Kaila K (2014) Pharmacotherapeutic targeting of cation-chloride cotransporters in neonatal seizures. Epilepsia 55(6):806–818
16. Loscher W, Puskarjov M, Kaila K (2013) Cation-chloride cotransporters NKCC1 and KCC2 as potential targets for novel antiepileptic and antiepileptogenic treatments. Neuropharmacology 69:62–74
17. Topfer M, Tollner K, Brandt C, Twele F, Broer S, Loscher W (2014) Consequences of inhibition of bumetanide metabolism in rodents on brain penetration and effects of bumetanide in chronic models of epilepsy. Eur J Neurosci 39(4):673–687
18. Brandt C, Nozadze M, Heuchert N, Rattka M, Loscher W (2010) Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. J Neurosci 30(25):8602–8612
19. Mazarati A, Shin D, Sankar R (2009) Bumetanide inhibits rapid kindling in neonatal rats. Epilepsia 50(9):2117–2122
20. Zhao CS, Puurunen K, Schallert T, Sivenius J, Jolkkonen J (2005) Effect of cholinergic medication, before and after focal photothrombotic ischemic cortical injury, on histological and functional outcome in aged and young adult rats. Behav Brain Res 156(1):85–94
21. Zhao S, Zhao M, Xiao T, Jolkkonen J, Zhao C (2013) Constraint-induced movement therapy overcomes the intrinsic axonal growth-inhibitory signals in stroke rats. Stroke 44(6):1698–1705
22. Kong S, Cheng Z, Liu J, Wang Y (2014) Downregulated GABA and BDNF-TrkB pathway in chronic cyclothiazide seizure model. Neural Plast 2014:310146
23. Jessberger S, Zhao C, Toni N, Clemenson GD Jr, Li Y, Gage FH (2007) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27(35):9400–9407
24. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C et al (2004) Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24(4):441–448
25. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T et al (2006) Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26(24):6627–6636
26. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47(6):803–815
27. Ge S, Pradhan DA, G-l M, Song H (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30(1):1–8
28. Nabekura J, Ueno T, Okabe A, Furuta A, Iwaki T, Shimizu-Okabe C, Fukuda A, Akaike N (2002) Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury. J Neurosci 22(11):4412–4417
29. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61(6):820–838
30. Ben-Ari Y (2014) The GABA excitatory/inhibitory developmental sequence: a personal journey. Neuroscience 279:187–219
31. Mennerick S, Zorumski CF (2000) Neural activity and survival in the developing nervous system. Mol Neurobiol 22(1–3):41–54
32. Di Filippo M, Tozzi A, Costa C, Belcastro V, Tantucci M, Picconi B, Calabresi P (2008) Plasticity and repair in the post-ischemic brain. Neuropharmacology 55(3):353–362
33. Rossini PM, Calautti C, Pauri F, Baron JC (2003) Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2(8):493–502
34. Leinekugel X, Medina I, Khalilov I, Ben-Ari Y, Khazipov R (1997) Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18(2):243–255
35. Shulga A, Magalhaes AC, Autio H, Plantman S, di Lieto A, Nykjaer A, Carlstedt T, Risling M et al (2012) The loop diuretic bumetanide blocks posttraumatic p75NTR upregulation and rescues injured neurons. J Neurosci 32(5):1757–1770
36. Jantzie LL, Hu MY, Park HK, Jackson MC, Yu J, Maxwell JR, Jensen FE (2015) Chloride cotransporter NKCC1 inhibitor bumetanide protects against white matter injury in a rodent model of periventricular leukomalacia. Pediatr Res 77(4):554–562
37. Chen H, Luo J, Kintner DB, Shull GE, Sun D (2005) Na(+)-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J Cereb Blood Flow Metab 25(1):54–66
38. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56(2):149–171
39. Badan I, Buchhold B, Hamm A, Gratz M, Walker LC, Platt D, Kessler C, Popa-Wagner A (2003) Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J Cereb Blood Flow Metab 23(7):845–854
40. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468(7321):305–309
41. Lake EM, Chaudhuri J, Thomason L, Janik R, Ganguly M, Brown M, McLaurin J, Corbett D et al (2015) The effects of delayed reduction of tonic inhibition on ischemic lesion and sensorimotor function. J Cereb Blood Flow Metab 35(10):1601–1609
42. Sugiura S, Kitagawa K, Tanaka S, Todo K, Omura-Matsuoka E, Sasaki T, Mabuchi T, Matsushita K et al (2005) Adenovirus-mediated gene transfer of heparin-binding epidermal growth factor-like growth factor enhances neurogenesis and angiogenesis after focal cerebral ischemia in rats. Stroke 36(4):859–864
43. Minnerup J, Kim JB, Schmidt A, Diederich K, Bauer H, Schilling M, Strecker JK, Ringelstein EB et al (2011) Effects of neural progenitor cells on sensorimotor recovery and endogenous repair mechanisms after photothrombotic stroke. Stroke 42(6):1757–1763