Skip to main content
Top
Published in: Journal of Inflammation 1/2014

Open Access 01-12-2014 | Research

Upregulation of ICAM-1 in diabetic rats after transient forebrain ischemia and reperfusion injury

Authors: Li Jing, Jian-Gang Wang, Jian-Zhong Zhang, Cai-Xia Cao, Yue Chang, Jian-Da Dong, Feng-Ying Guo, P Andy Li

Published in: Journal of Inflammation | Issue 1/2014

Login to get access

Abstract

Background

Hyperglycemia exacerbates brain damage caused by cerebral ischemia. Neuroinflammation may play a role in mediating such enhanced damage. The objectives of this study were to examine the mRNA and protein levels and cell type distribution of ICAM-1 after cerebral ischemia in normo-and diabetic hyperglycemic rats.

Results

Compared to normoglycemic ischemia animals, diabetes aggravated neuronal death, decreased Nissl body staining, and increased ICAM-1 mRNA and protein levels in the frontal cortex. The increased ICAM-1 was located not only in vascular endothelial cells but also in cortical neurons.

Conclusions

Our results suggest that exacerbated neuro-inflammation in the brain may mediate the detrimental effects of diabetes on the ischemic brain.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mehta SL, Lin Y, Chen W, Yu F, Cao L, Li PA: Manganese superoxide dismutase deficiency exacerbates ischemic brain damage under hyperglycemic conditions by altering autophagy. Transl Stroke Res. 2011, 2: 42-50. 10.1007/s12975-010-0027-3.PubMedPubMedCentralCrossRef Mehta SL, Lin Y, Chen W, Yu F, Cao L, Li PA: Manganese superoxide dismutase deficiency exacerbates ischemic brain damage under hyperglycemic conditions by altering autophagy. Transl Stroke Res. 2011, 2: 42-50. 10.1007/s12975-010-0027-3.PubMedPubMedCentralCrossRef
2.
go back to reference Supanc V, Biloglav Z, Kes VB, Demarin V: Role of cell adhesion molecules in acute ischemic stroke. Ann Saudi Med. 2011, 31: 365-370. 10.4103/0256-4947.83217.PubMedPubMedCentralCrossRef Supanc V, Biloglav Z, Kes VB, Demarin V: Role of cell adhesion molecules in acute ischemic stroke. Ann Saudi Med. 2011, 31: 365-370. 10.4103/0256-4947.83217.PubMedPubMedCentralCrossRef
3.
go back to reference Krause GS, White BC, Aust SD, Nayini NR, Kumar K: Brain cell death following ischemia and reperfusion: a proposed biochemical sequence. Crit Care Med. 1998, 16: 714-726. 10.1097/00003246-198807000-00015.CrossRef Krause GS, White BC, Aust SD, Nayini NR, Kumar K: Brain cell death following ischemia and reperfusion: a proposed biochemical sequence. Crit Care Med. 1998, 16: 714-726. 10.1097/00003246-198807000-00015.CrossRef
4.
go back to reference Wang X, Sirén AL, Liu Y, Yue TL, Barone FC, Feuerstein GZ: Upregulation of intercellular adhesion molecule 1 (ICAM-1) on brain microvascular endothelial cells in rat ischemic cortex. Brain Res Mol Brain Res. 1994, 26: 61-68. 10.1016/0169-328X(94)90074-4.PubMedCrossRef Wang X, Sirén AL, Liu Y, Yue TL, Barone FC, Feuerstein GZ: Upregulation of intercellular adhesion molecule 1 (ICAM-1) on brain microvascular endothelial cells in rat ischemic cortex. Brain Res Mol Brain Res. 1994, 26: 61-68. 10.1016/0169-328X(94)90074-4.PubMedCrossRef
5.
go back to reference Enzmann G, Mysiorek C, Gorina R, Cheng YJ, Ghavampour S, Hannocks MJ, Prinz V, Dirnagl U, Endres M, Prinz M, Beschorner R, Harter PN, Mittelbronn M, Engelhardt B, Sorokin L: The neurovascular unit as a selective barrier to polymorphonuclear granulocyte (PMN) infiltration into the brain after ischemic injury. Acta Neuropathol. 2013, 125: 395-412. 10.1007/s00401-012-1076-3.PubMedPubMedCentralCrossRef Enzmann G, Mysiorek C, Gorina R, Cheng YJ, Ghavampour S, Hannocks MJ, Prinz V, Dirnagl U, Endres M, Prinz M, Beschorner R, Harter PN, Mittelbronn M, Engelhardt B, Sorokin L: The neurovascular unit as a selective barrier to polymorphonuclear granulocyte (PMN) infiltration into the brain after ischemic injury. Acta Neuropathol. 2013, 125: 395-412. 10.1007/s00401-012-1076-3.PubMedPubMedCentralCrossRef
6.
go back to reference Choi JS, Park J, Suk K, Moon C, Park YK, Han HS: Mild hypothermia attenuates intercellular adhesion molecule-1 induction via activation of extracellular signal-regulated kinase-1/2 in a focal cerebral ischemia model. Stroke Res Treat. 2011, 2011: 846716-PubMedPubMedCentral Choi JS, Park J, Suk K, Moon C, Park YK, Han HS: Mild hypothermia attenuates intercellular adhesion molecule-1 induction via activation of extracellular signal-regulated kinase-1/2 in a focal cerebral ischemia model. Stroke Res Treat. 2011, 2011: 846716-PubMedPubMedCentral
7.
go back to reference Fotis L, Agrogiannis G, Vlachos IS, Pantopoulou A, Margoni A, Kostaki M, Verikokos C, Tzivras D, Mikhailidis DP, Perrea D: Intercellular adhesion molecule (ICAM)-1 and vascular cell adhesion molecule (VCAM)-1 at the early stages of atherosclerosis in a rat model. In Vivo. 2012, 26: 243-250.PubMed Fotis L, Agrogiannis G, Vlachos IS, Pantopoulou A, Margoni A, Kostaki M, Verikokos C, Tzivras D, Mikhailidis DP, Perrea D: Intercellular adhesion molecule (ICAM)-1 and vascular cell adhesion molecule (VCAM)-1 at the early stages of atherosclerosis in a rat model. In Vivo. 2012, 26: 243-250.PubMed
8.
go back to reference Zhu YP, Shen T, Lin YJ, Chen BD, Ruan Y, Cao Y, Qiao Y, Man Y, Wang S, Li J: Astragalus polysaccharides suppress ICAM-1 and VCAM-1 expression in TNF-α-treated human vascular endothelial cells by blocking NF-κB activation. Acta Pharmacol Sin. 2013, 34: 1036-1042. 10.1038/aps.2013.46.PubMedPubMedCentralCrossRef Zhu YP, Shen T, Lin YJ, Chen BD, Ruan Y, Cao Y, Qiao Y, Man Y, Wang S, Li J: Astragalus polysaccharides suppress ICAM-1 and VCAM-1 expression in TNF-α-treated human vascular endothelial cells by blocking NF-κB activation. Acta Pharmacol Sin. 2013, 34: 1036-1042. 10.1038/aps.2013.46.PubMedPubMedCentralCrossRef
9.
go back to reference Li M, Qu YZ, Zhao ZW, Wu SX, Liu YY, Wei XY, Gao L, Gao GD: Astragaloside IV protects against focal cerebral ischemia/reperfusion injury correlating to suppression of neutrophils adhesion-related molecules. Neurochem Int. 2012, 60: 458-465. 10.1016/j.neuint.2012.01.026.PubMedCrossRef Li M, Qu YZ, Zhao ZW, Wu SX, Liu YY, Wei XY, Gao L, Gao GD: Astragaloside IV protects against focal cerebral ischemia/reperfusion injury correlating to suppression of neutrophils adhesion-related molecules. Neurochem Int. 2012, 60: 458-465. 10.1016/j.neuint.2012.01.026.PubMedCrossRef
10.
go back to reference Su Y, Mao N, Li M, Dong X, Lin FZ, Xu Y, Li YB: Sarpogrelate inhibits the expression of ICAM-1 and monocyte-endothelial adhesion induced by high glucose in human endothelial cells. Mol Cell Biochem. 2013, 373: 195-199. 10.1007/s11010-012-1490-9.PubMedCrossRef Su Y, Mao N, Li M, Dong X, Lin FZ, Xu Y, Li YB: Sarpogrelate inhibits the expression of ICAM-1 and monocyte-endothelial adhesion induced by high glucose in human endothelial cells. Mol Cell Biochem. 2013, 373: 195-199. 10.1007/s11010-012-1490-9.PubMedCrossRef
11.
go back to reference Guan T, Liu Q, Qian Y, Yang H, Kong J, Kou J, Yu B: Ruscogenin reduces cerebral ischemic injury via NF-κB-mediated inflammatory pathway in the mouse model of experimental stroke. Eur J Pharmacol. 2013, 714: 303-311. 10.1016/j.ejphar.2013.07.036.PubMedCrossRef Guan T, Liu Q, Qian Y, Yang H, Kong J, Kou J, Yu B: Ruscogenin reduces cerebral ischemic injury via NF-κB-mediated inflammatory pathway in the mouse model of experimental stroke. Eur J Pharmacol. 2013, 714: 303-311. 10.1016/j.ejphar.2013.07.036.PubMedCrossRef
12.
go back to reference Ge H, Wen Y, Yang G, Betz AL: Increased expression of intercellular adhesion molecule-1 in mouse focal cerebral ischemia model. Chin Med J (Engl). 2000, 113: 75-79. Ge H, Wen Y, Yang G, Betz AL: Increased expression of intercellular adhesion molecule-1 in mouse focal cerebral ischemia model. Chin Med J (Engl). 2000, 113: 75-79.
13.
go back to reference Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS: A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001, 107: 1255-1262. 10.1172/JCI11871.PubMedPubMedCentralCrossRef Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS: A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001, 107: 1255-1262. 10.1172/JCI11871.PubMedPubMedCentralCrossRef
14.
go back to reference Navarro JF, Mora C: Role of inflammation in diabetic complications. Nephrol Dial Transplant. 2005, 20: 2601-2604. 10.1093/ndt/gfi155.PubMedCrossRef Navarro JF, Mora C: Role of inflammation in diabetic complications. Nephrol Dial Transplant. 2005, 20: 2601-2604. 10.1093/ndt/gfi155.PubMedCrossRef
15.
go back to reference Ding C, He Q, Li PA: Diabetes increases expression of ICAM after a brief period of cerebral ischemia. J Neuroimmunol. 2005, 161: 61-67. 10.1016/j.jneuroim.2004.12.011.PubMedCrossRef Ding C, He Q, Li PA: Diabetes increases expression of ICAM after a brief period of cerebral ischemia. J Neuroimmunol. 2005, 161: 61-67. 10.1016/j.jneuroim.2004.12.011.PubMedCrossRef
16.
go back to reference Smolock AR, Mishra G, Eguchi K, Equchi S, Scalia R: Protein kinase C upregulates intercellular adhesion molecule-1 and leukocyte-endothelium interactions in hyperglycemia via activation of endothelial expressed calpain. Arterioscler Thromb Vasc Biol. 2011, 31: 289-296. 10.1161/ATVBAHA.110.217901.PubMedPubMedCentralCrossRef Smolock AR, Mishra G, Eguchi K, Equchi S, Scalia R: Protein kinase C upregulates intercellular adhesion molecule-1 and leukocyte-endothelium interactions in hyperglycemia via activation of endothelial expressed calpain. Arterioscler Thromb Vasc Biol. 2011, 31: 289-296. 10.1161/ATVBAHA.110.217901.PubMedPubMedCentralCrossRef
17.
go back to reference Li PA, Shamloo M, Katsura K, Smith ML, Siesjo BK: Critical values for plasma glucose in aggravating ischaemic brain damage: correlation to extracellular pH. Neurobiol Dis. 1995, 2: 97-108. 10.1006/nbdi.1995.0010.PubMedCrossRef Li PA, Shamloo M, Katsura K, Smith ML, Siesjo BK: Critical values for plasma glucose in aggravating ischaemic brain damage: correlation to extracellular pH. Neurobiol Dis. 1995, 2: 97-108. 10.1006/nbdi.1995.0010.PubMedCrossRef
18.
go back to reference Jing L, Zhang JZ, Zhao L, Wang YL, Guo FY: High-expression of transforming growth factor β1 and phosphorylation of extracellular signal-regulated protein kinase in vascular smooth muscle cells from aorta and renal arterioles of spontaneous hypertension rats. Clin Exp Hypertens. 2007, 29: 107-117. 10.1080/10641960701195447.PubMedCrossRef Jing L, Zhang JZ, Zhao L, Wang YL, Guo FY: High-expression of transforming growth factor β1 and phosphorylation of extracellular signal-regulated protein kinase in vascular smooth muscle cells from aorta and renal arterioles of spontaneous hypertension rats. Clin Exp Hypertens. 2007, 29: 107-117. 10.1080/10641960701195447.PubMedCrossRef
19.
go back to reference Jing L, Zhang JZ, Sun JP, Guo FY, An X, Yang K, Li PA: Inhibition of extracellular sinal-regulated kinases amerliorates hypertension-induced renal vascular remodeling in rat models. Int J Mol Sci. 2011, 12: 8333-8346. 10.3390/ijms12128333.PubMedPubMedCentralCrossRef Jing L, Zhang JZ, Sun JP, Guo FY, An X, Yang K, Li PA: Inhibition of extracellular sinal-regulated kinases amerliorates hypertension-induced renal vascular remodeling in rat models. Int J Mol Sci. 2011, 12: 8333-8346. 10.3390/ijms12128333.PubMedPubMedCentralCrossRef
20.
go back to reference Carlson M, Nakamura Y, Payson R, O’Connell , Leppert M, Lathrop GM, Lalouel JM, White R: Isolation and mapping of a polymorphic DNA sequence (pMCT108. 2) on chromosome 18 [D18S24]. Nucleic Acids Res. 1988, 16: 4188-10.1093/nar/16.9.4188.PubMedPubMedCentralCrossRef Carlson M, Nakamura Y, Payson R, O’Connell , Leppert M, Lathrop GM, Lalouel JM, White R: Isolation and mapping of a polymorphic DNA sequence (pMCT108. 2) on chromosome 18 [D18S24]. Nucleic Acids Res. 1988, 16: 4188-10.1093/nar/16.9.4188.PubMedPubMedCentralCrossRef
21.
go back to reference Katz FE, Parkar M, Stanley K, Murray LJ, Clark EA, Greaves MF: Chromosome mapping of cell membrane antigens expressed on activated B cells. Eur J Immunol. 1985, 15: 103-106. 10.1002/eji.1830150121.PubMedCrossRef Katz FE, Parkar M, Stanley K, Murray LJ, Clark EA, Greaves MF: Chromosome mapping of cell membrane antigens expressed on activated B cells. Eur J Immunol. 1985, 15: 103-106. 10.1002/eji.1830150121.PubMedCrossRef
22.
go back to reference Nie Z, Fryer AD, Jacoby DB: β2-Agonists inhibit TNF-α-induced ICAM-1 expression in human airway parasympathetic neurons. PLoS One. 2012, 7: e44780-10.1371/journal.pone.0044780.PubMedPubMedCentralCrossRef Nie Z, Fryer AD, Jacoby DB: β2-Agonists inhibit TNF-α-induced ICAM-1 expression in human airway parasympathetic neurons. PLoS One. 2012, 7: e44780-10.1371/journal.pone.0044780.PubMedPubMedCentralCrossRef
23.
go back to reference Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW: ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular endothelium under flow. Blood. 2005, 106: 584-592. 10.1182/blood-2004-12-4942.PubMedPubMedCentralCrossRef Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW: ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular endothelium under flow. Blood. 2005, 106: 584-592. 10.1182/blood-2004-12-4942.PubMedPubMedCentralCrossRef
25.
go back to reference Cao J, Shi X, Li W, Liu J, Miao X, Xiu J: Protective effect of anti-intercellular adhesion molecule-1 antibody on global cerebral ischemia/reperfusion injury in the rat. Biosci Trends. 2009, 3: 48-52.PubMed Cao J, Shi X, Li W, Liu J, Miao X, Xiu J: Protective effect of anti-intercellular adhesion molecule-1 antibody on global cerebral ischemia/reperfusion injury in the rat. Biosci Trends. 2009, 3: 48-52.PubMed
26.
go back to reference Liu L, Wang Z, Wang X, Song L, Chen H, Bémeur C, Ste-Marie L, Montgomery J: Comparison of two rat models of cerebral ischemia under hyperglycemic conditions. Microsurgery. 2007, 27: 258-262. 10.1002/micr.20351.PubMedCrossRef Liu L, Wang Z, Wang X, Song L, Chen H, Bémeur C, Ste-Marie L, Montgomery J: Comparison of two rat models of cerebral ischemia under hyperglycemic conditions. Microsurgery. 2007, 27: 258-262. 10.1002/micr.20351.PubMedCrossRef
27.
go back to reference Bačun T, Glavaš-Obrovac L, Belovari T, Mihaljević I, Hanich T, Belaj VF, Vcev A: Insulin administration in the mild hyperglycaemia changes expression of proinflammatory adhesion molecules on human aortic endothelial cells. Coll Antropol. 2010, 34: 911-915.PubMed Bačun T, Glavaš-Obrovac L, Belovari T, Mihaljević I, Hanich T, Belaj VF, Vcev A: Insulin administration in the mild hyperglycaemia changes expression of proinflammatory adhesion molecules on human aortic endothelial cells. Coll Antropol. 2010, 34: 911-915.PubMed
28.
go back to reference Kern TS: Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res. 2007, 2007: 95103-10.1155/2007/95103.PubMedPubMedCentralCrossRef Kern TS: Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res. 2007, 2007: 95103-10.1155/2007/95103.PubMedPubMedCentralCrossRef
29.
go back to reference Kim SW, Kim CE, Kim MH: Flavonoids inhibit high glucose-induced up-regulation of ICAM-1 via the p38 MAPK pathway in human vein endothelial cells. Biochem Biophys Res Commun. 2011, 415: 602-607. 10.1016/j.bbrc.2011.10.115.PubMedCrossRef Kim SW, Kim CE, Kim MH: Flavonoids inhibit high glucose-induced up-regulation of ICAM-1 via the p38 MAPK pathway in human vein endothelial cells. Biochem Biophys Res Commun. 2011, 415: 602-607. 10.1016/j.bbrc.2011.10.115.PubMedCrossRef
30.
go back to reference Tsuruta R, Fujita M, Ono T, Koda Y, Koga Y, Yamamoto T, Nanba M, Shitara M, Kasaoka S, Maruyama I, Yuasa M, Maekawa T: Hyperglycemia enhances excessive superoxide anion radical generation, oxidative stress, early inflammation, and endothelial injury in forebrain ischemia/reperfusion rats. Brain Res. 2010, 1309: 155-163. 10.1016/j.brainres.2009.10.065.PubMedCrossRef Tsuruta R, Fujita M, Ono T, Koda Y, Koga Y, Yamamoto T, Nanba M, Shitara M, Kasaoka S, Maruyama I, Yuasa M, Maekawa T: Hyperglycemia enhances excessive superoxide anion radical generation, oxidative stress, early inflammation, and endothelial injury in forebrain ischemia/reperfusion rats. Brain Res. 2010, 1309: 155-163. 10.1016/j.brainres.2009.10.065.PubMedCrossRef
31.
go back to reference Wolburg K, Gerhardt H, Schulz M, Wolburg H, Engelhardt B: Ultrastructural localization of adhesion molecules in the healthy and inflamed choroid plexus of the mouse. Cell Tissue Res. 1999, 296: 259-269. 10.1007/s004410051287.PubMedCrossRef Wolburg K, Gerhardt H, Schulz M, Wolburg H, Engelhardt B: Ultrastructural localization of adhesion molecules in the healthy and inflamed choroid plexus of the mouse. Cell Tissue Res. 1999, 296: 259-269. 10.1007/s004410051287.PubMedCrossRef
32.
go back to reference Yang J, Gu Y, Huang X, Shen A, Cheng C: Dynamic changes of ICAM-1 expression in peripheral nervous system following sciatic nerve injury. Neurol Res. 2011, 33: 75-83. 10.1179/016164110X12714125204353.PubMedCrossRef Yang J, Gu Y, Huang X, Shen A, Cheng C: Dynamic changes of ICAM-1 expression in peripheral nervous system following sciatic nerve injury. Neurol Res. 2011, 33: 75-83. 10.1179/016164110X12714125204353.PubMedCrossRef
33.
go back to reference Sandireddy R, Yerra VG, Areti A, Komirshetty P, Kumar A: Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014, 2014: 674987-10.1155/2014/674987. doi: 10.1155/2014/674987PubMedPubMedCentralCrossRef Sandireddy R, Yerra VG, Areti A, Komirshetty P, Kumar A: Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014, 2014: 674987-10.1155/2014/674987. doi: 10.1155/2014/674987PubMedPubMedCentralCrossRef
34.
go back to reference Meng X-F, Wang X-L, Tian X-J, Yang Z-H, Chu G-P, Zhang J, Li M, Shi J, Zhang C: Nod-like receptor protein 1 inflammasome mediates neuron injury under high glucose. Mol Neurobiol. 2014, 49: 673-684. 10.1007/s12035-013-8551-2.PubMedCrossRef Meng X-F, Wang X-L, Tian X-J, Yang Z-H, Chu G-P, Zhang J, Li M, Shi J, Zhang C: Nod-like receptor protein 1 inflammasome mediates neuron injury under high glucose. Mol Neurobiol. 2014, 49: 673-684. 10.1007/s12035-013-8551-2.PubMedCrossRef
Metadata
Title
Upregulation of ICAM-1 in diabetic rats after transient forebrain ischemia and reperfusion injury
Authors
Li Jing
Jian-Gang Wang
Jian-Zhong Zhang
Cai-Xia Cao
Yue Chang
Jian-Da Dong
Feng-Ying Guo
P Andy Li
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Inflammation / Issue 1/2014
Electronic ISSN: 1476-9255
DOI
https://doi.org/10.1186/s12950-014-0035-2

Other articles of this Issue 1/2014

Journal of Inflammation 1/2014 Go to the issue