Neuronal precursor cell proliferation in the hippocampus after transient cerebral ischemia: a comparative study of two rat strains using stereological tools

Experimental and Translational Stroke Medicine

Volumn 2, Issue 1, 2010, Pages

  Kelsen, Jesper ^a,b,c   Larsen, Marianne H ^d   Sørensen, Jens C ^b   Møller, Arne ^b   Frøkiær, Jørgen ^a,b   Nielsen, Søren ^a   Nyengaard, Jens R ^b   Mikkelsen, Jens D ^c   Rønn, Lars C B ^e  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c Rigshospitalet   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e NEUROSEARCH A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CEREBRAL ARTERY; ANTERIOR CHOROID ARTERY; ARTERY CLAMP; ARTICLE; BRAIN ARTERY; BRAIN CORTEX; BRAIN DAMAGE; BRAIN INFARCTION SIZE; BRAIN SIZE; CAROTID ARTERY BIFURCATION; CELL PROLIFERATION; COMMON CAROTID ARTERY; COMPUTER PROGRAM; CONTROLLED STUDY; CORPUS STRIATUM; DEVICE; DISEASE MODEL; HEMISPHERE; HIPPOCAMPUS; HYPOTHALAMIC ARTERY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NEOCORTEX; NEURAL STEM CELL; NONHUMAN; OCCLUDING FILAMENT; OPTICAL FRACTIONATOR; PRIORITY JOURNAL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; SPRAGUE DAWLEY RAT; STEREOMETRY; STRAIN DIFFERENCE; TRANSIENT ISCHEMIC ATTACK; TWO DIMENSIONAL NUCLEATOR;

EID: 77953275520     PISSN: None     EISSN: 20407378     Source Type: Journal    
DOI: 10.1186/2040-7378-2-8     Document Type: Article

References (64)

1. Barone FC, Feuerstein GZ. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999, 19:819-834. 10.1097/00004647-199908000-00001, 10458589.
2. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001, 2:734-744. 10.1038/35094583, 11584311.
3. Allan SM, Tyrrell PJ, Rothwell NJ. Interleukin-1 and neuronal injury. Nat Rev Immunol 2005, 5:629-640. 10.1038/nri1664, 16034365.
4. Feuerstein G. Inflammation and stroke: therapeutic effects of adenoviral expression of secretory Leukocyte Protease Inhibitor. Front Biosci 2006, 11:1750-1757. 10.2741/1920, 16368553.
5. Candelario-Jalil E. Injury and repair mechanisms in ischemic stroke: considerations for the development of novel neurotherapeutics. Curr Opin Investig Drugs 2009, 10:644-654.
6. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002, 8:963-970. 10.1038/nm747, 12161747.
7. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci USA 2004, 101:11839-11844. 10.1073/pnas.0404474101, 511061, 15280535.
8. Coyle P. Outcomes to middle cerebral artery occlusion in hypertensive and normotensive rats. Hypertension 1984, 6:I69-I74.
9. Brint S, Jacewicz M, Kiessling M, Tanabe J, Pulsinelli W. Focal Brain Ischemia in the Rat - Methods for Reproducible Neocortical Infarction Using Tandem Occlusion of the Distal Middle Cerebral and Ipsilateral Common Carotid Arteries. Journal of Cerebral Blood Flow and Metabolism 1988, 8:474-485.
10. Barone FC, Price WJ, White RF, Willette RN, Feuerstein GZ. Genetic hypertension and increased susceptibility to cerebral ischemia. Neurosci Biobehav Rev 1992, 16:219-233. 10.1016/S0149-7634(05)80182-4, 1630732.
11. Coyle P. Different susceptibilities to cerebral infarction in spontaneously hypertensive (SHR) and normotensive Sprague-Dawley rats. Stroke 1986, 17:520-525.
12. Coyle P, Jokelainen PT. Differential outcome to middle cerebral artery occlusion in spontaneously hypertensive stroke-prone rats (SHRSP) and Wistar Kyoto (WKY) rats. Stroke 1983, 14:605-611.
13. Grabowski M, Nordborg C, Brundin P, Johansson BB. Middle cerebral artery occlusion in the hypertensive and normotensive rat: a study of histopathology and behaviour. J Hypertens 1988, 6:405-411. 10.1097/00004872-198805000-00011, 3385206.
14. Perfilieva E, Risedal A, Nyberg J, Johansson BB, Eriksson PS. Gender and strain influence on neurogenesis in dentate gyrus of young rats. J Cereb Blood Flow Metab 2001, 21:211-217. 10.1097/00004647-200103000-00004, 11295875.
15. Marks L, Carswell HV, Peters EE, Graham DI, Patterson J, Dominiczak AF, Macrae IM. Characterization of the microglial response to cerebral ischemia in the stroke-prone spontaneously hypertensive rat. Hypertension 2001, 38:116-122.
16. Kohno K, Back T, Hoehn-Berlage M, Hossmann KA. A modified rat model of middle cerebral artery thread occlusion under electrophysiological control for magnetic resonance investigations. Magn Reson Imaging 1995, 13:65-71. 10.1016/0730-725X(94)00081-D, 7898281.
17. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-91.
18. Zarow GJ, Karibe H, States BA, Graham SH, Weinstein PR. Endovascular suture occlusion of the middle cerebral artery in rats: Effect of suture insertion distance on cerebral blood flow, infarct distribution and infarct volume. Neurological Research 1997, 19:409-416.
19. Hundahl C, Kelsen J, Kjaer K, Ronn LC, Weber RE, Geuens E, Hay-Schmidt A, Nyengaard JR. Does neuroglobin protect neurons from ischemic insult? A quantitative investigation of neuroglobin expression following transient MCAo in spontaneously hypertensive rats. Brain Res 2006, 1085:19-27. 10.1016/j.brainres.2006.02.040, 16647691.
20. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 1988, 96:857-881. 10.1111/j.1699-0463.1988.tb00954.x, 3056461.
21. Gundersen HJ. The nucleator. J Microsc 1988, 151(Pt 1):3-21.
22. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987, 147(Pt 3):229-263.
23. Larsen JO. Stereology of nerve cross sections. J Neurosci Methods 1998, 85:107-118. 10.1016/S0165-0270(98)00129-0, 9874147.
24. Nyengaard JR, Evans SM. Section introduction. Quantitative methods in neuroscience 2004, 185-196. Oxford University Press, Evans SM, Janson AM, Nyengaard JR, 1.
25. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 2001, 204:232-246. 10.1046/j.1365-2818.2001.00958.x, 11903800.
26. 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, 231:482-497. 10.1002/ar.1092310411, 1793176.
27. Dittmar M, Spruss T, Schuierer G, Horn M. External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 2003, 34:2252-2257. 10.1161/01.STR.0000083625.54851.9A, 12893948.
28. Kelsen J, Kjaer K, Chen G, Pedersen M, Rohl L, Frokiaer J, Nielsen S, Nyengaard JR, Ronn LC. Parecoxib is neuroprotective in spontaneously hypertensive rats after transient middle cerebral artery occlusion: a divided treatment response?. J Neuroinflammation 2006, 3:31. 10.1186/1742-2094-3-31, 1764728, 17150094.
29. He Z, Yamawaki T, Yang S, Day AL, Simpkins JW, Naritomi H. Experimental model of small deep infarcts involving the hypothalamus in rats: changes in body temperature and postural reflex. Stroke 1999, 30:2743-2751.
30. He Z, Yang SH, Naritomi H, Yamawaki T, Liu QL, King MA, Day AL, Simpkins JW. Definition of the anterior choroidal artery territory in rats using intraluminal occluding technique. Journal of the Neurological Sciences 2000, 182:16-28. 10.1016/S0022-510X(00)00434-2, 11102635.
31. Evans SM, Janson AM, Nyengaard JR. Quantitative methods in neuroscience 2004, Oxford University Press.
32. Koizumi J, Yoshida Y, Nakazawa T, Ooneda G. Experimental studies of ischemic brain edema: 1. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jpn J Stroke 1986, 8:1-8.
33. Sicard K, Fisher M. Animal models of focal brain ischemia. Experimental & Translational Stroke Medicine 2009, 1:7. 2820445, 20150985, 10.1186/2040-7378-1-7.
34. Laing RJ, Jakubowski J, Laing RW. Middle cerebral artery occlusion without craniectomy in rats. Which method works best?. Stroke 1993, 24:294-297.
35. Oliff HS, Weber E, Eilon G, Marek P. The role of strain/vendor differences on the outcome of focal ischemia induced by intraluminal middle cerebral artery occlusion in the rat. Brain Res 1995, 675:20-26. 10.1016/0006-8993(95)00033-M, 7796130.
36. Takano K, Tatlisumak T, Bergmann AG, Gibson DG, Fisher M. Reproducibility and reliability of middle cerebral artery occlusion using a silicone-coated suture (Koizumi) in rats. J Neurol Sci 1997, 153:8-11. 10.1016/S0022-510X(97)00184-6, 9455971.
37. Schmid-Elsaesser R, Zausinger S, Hungerhuber E, Baethmann A, Reulen HJ. A critical reevaluation of the intraluminal thread model of focal cerebral ischemia: evidence of inadvertent premature reperfusion and subarachnoid hemorrhage in rats by laser-Doppler flowmetry. Stroke 1998, 29:2162-2170.
38. Gerriets T, Stolz E, Walberer M, Muller C, Rottger C, Kluge A, Kaps M, Fisher M, Bachmann G. Complications and pitfalls in rat stroke models for middle cerebral artery occlusion: a comparison between the suture and the macrosphere model using magnetic resonance angiography. Stroke 2004, 35:2372-2377. 10.1161/01.STR.0000142134.37512.a7, 15345802.
39. Braeuninger S, Kleinschnitz C. Rodent models of focal cerebral ischemia: procedural pitfalls and translational problems. Experimental & Translational Stroke Medicine 2009, 1:8. 2820446, 20150986, 10.1186/2040-7378-1-8.
40. Woitzik J, Schilling L. Control of completeness and immediate detection of bleeding by a single laser-Doppler flow probe during intravascular middle cerebral artery occlusion in rats. J Neurosci Methods 2002, 122:75-78. 10.1016/S0165-0270(02)00277-7, 12535766.
41. Prieto R, Carceller F, Roda JM, Avendano C. The intraluminal thread model revisited: rat strain differences in local cerebral blood flow. Neurol Res 2005, 27:47-52. 10.1179/016164105X18214, 15829158.
42. Lehrmann E, Christensen T, Zimmer J, Diemer NH, Finsen B. Microglial and macrophage reactions mark progressive changes and define the penumbra in the rat neocortex and striatum after transient middle cerebral artery occlusion. J Comp Neurol 1997, 386:461-476. 10.1002/(SICI)1096-9861(19970929)386:3<461::AID-CNE9>3.0.CO;2-#, 9303429.
43. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 1999, 30:77-105. 10.1016/S0165-0173(99)00007-7, 10407127.
44. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318. 10.1016/0166-2236(96)10049-7, 8843599.
45. Streit WJ, Mrak RE, Griffin WS. Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 2004, 1:14. 10.1186/1742-2094-1-14, 509427, 15285801.
46. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 1986, 17:1304-1308.
47. Rieke GK, Bowers DE, Penn P. Vascular supply pattern to rat caudatoputamen and globus pallidus: scanning electronmicroscopic study of vascular endocasts of stroke-prone vessels. Stroke 1981, 12:840-847.
48. Reglodi D, Somogyvari-Vigh A, Maderdrut JL, Vigh S, Arimura A. Postischemic spontaneous hyperthermia and its effects in middle cerebral artery occlusion in the rat. Exp Neurol 2000, 163:399-407. 10.1006/exnr.2000.7367, 10833314.
49. Abraham H, Somogyvari-Vigh A, Maderdrut JL, Vigh S, Arimura A. Filament size influences temperature changes and brain damage following middle cerebral artery occlusion in rats. Exp Brain Res 2002, 142:131-138. 10.1007/s00221-001-0909-4, 11797090.
50. Zhao Q, Memezawa H, Smith ML, Siesjo BK. Hyperthermia complicates middle cerebral artery occlusion induced by an intraluminal filament. Brain Res 1994, 649:253-259. 10.1016/0006-8993(94)91071-5, 7953639.
51. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 2001, 98:4710-4715. 10.1073/pnas.081011098, 31899, 11296300.
52. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa K, Miyata T, Okano H, Hori M, Matsumoto M. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 2001, 32:1890-1896.
53. Ernst C, Christie BR. Temporally specific proliferation events are induced in the hippocampus following acute focal injury. J Neurosci Res 2006, 83:349-361. 10.1002/jnr.20724, 16342206.
54. Liu J, Solway K, Messing RO, Sharp FR. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 1998, 18:7768-7778.
55. Sasaki T, Kitagawa K, Yamagata K, Takemiya T, Tanaka S, Omura-Matsuoka E, Sugiura S, Matsumoto M, Hori M. Amelioration of hippocampal neuronal damage after transient forebrain ischemia in cyclooxygenase-2-deficient mice. J Cereb Blood Flow Metab 2004, 24:107-113. 10.1097/01.WCB.0000100065.36077.4A, 14688622.
56. Madsen TM, Treschow A, Bengzon J, Bolwig TG, Lindvall O, Tingstrom A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000, 47:1043-1049. 10.1016/S0006-3223(00)00228-6, 10862803.
57. Kluska MM, Witte OW, Bolz J, Redecker C. Neurogenesis in the adult dentate gyrus after cortical infarcts: effects of infarct location, N-methyl-D-aspartate receptor blockade and anti-inflammatory treatment. Neuroscience 2005, 135:723-735. 10.1016/j.neuroscience.2005.06.082, 16154293.
58. Arvidsson A, Kokaia Z, Lindvall O. N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 2001, 14:10-18. 10.1046/j.0953-816x.2001.01611.x, 11488944.
59. Takasawa K, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, Matsushita K, Ohstuki T, Miyata T, Okano H, Hori M, et al. Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2002, 22:299-307. 10.1097/00004647-200203000-00007, 11891435.
60. Dempsey RJ, Sailor KA, Bowen KK, Tureyen K, Vemuganti R. Stroke-induced progenitor cell proliferation in adult spontaneously hypertensive rat brain: effect of exogenous IGF-1 and GDNF. J Neurochem 2003, 87:586-597. 10.1046/j.1471-4159.2003.02022.x, 14535942.
61. Darsalia V, Heldmann U, Lindvall O, Kokaia Z. Stroke-induced neurogenesis in aged brain. Stroke 2005, 36:1790-1795. 10.1161/01.STR.0000173151.36031.be, 16002766.
62. Sabbatini M, Strocchi P, Vitaioli L, Amenta F. The hippocampus in spontaneously hypertensive rats: a quantitative microanatomical study. Neuroscience 2000, 100:251-258. 10.1016/S0306-4522(00)00297-9, 11008165.
63. Sabbatini M, Catalani A, Consoli C, Marletta N, Tomassoni D, Avola R. The hippocampus in spontaneously hypertensive rats: an animal model of vascular dementia?. Mech Ageing Dev 2002, 123:547-559. 10.1016/S0047-6374(01)00362-1, 11796140.
64. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000, 425:479-494. 10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3, 10975875.