Estrogen replacement therapy in diabetic ovariectomized female rats potentiates postischemic leukocyte adhesion in cerebral venules via a RAGE-related process

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 6, 2009, Pages

  Xu, Hao Liang ^a   Vetri, Francesco ^a   Lee, Hae Kyung ^a   Ye, Shuhua ^a   Paisansathan, Chanannait ^a   Mao, Lizhen ^a   Tan, Fulong ^a   Pelligrino, Dale A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Diabetes mellitus; Inflammation; Neutrophil; Transient forebrain ischemia

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ANTISENSE OLIGONUCLEOTIDE; ESTRADIOL; ESTROGEN; LIGAND; MESSENGER RNA; OLIGODEOXYNUCLEOTIDE; RHODAMINE 6G; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN ISCHEMIA; CELL INFILTRATION; COMPARATIVE STUDY; CONTROLLED STUDY; ESTROGEN THERAPY; FEMALE; IMMUNOREACTIVITY; IN VIVO STUDY; INJECTION; LEUKOCYTE; LEUKOCYTE ADHERENCE; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; PIA MATER; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; REPERFUSION; STREPTOZOCIN DIABETES;

ANIMALS; BRAIN ISCHEMIA; CELL ADHESION; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; DIABETES MELLITUS, EXPERIMENTAL; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; GENE KNOCKDOWN TECHNIQUES; GLYCOSYLATION END PRODUCTS, ADVANCED; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENTRICULAR; LASER-DOPPLER FLOWMETRY; LEUKOCYTES; OLIGONUCLEOTIDES, ANTISENSE; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; TIME FACTORS; VENULES;

EID: 72249114024     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00445.2009     Document Type: Article

References (35)

1. Basta G. Receptor for advanced glycation endproducts and atherosclerosis: from basic mechanisms to clinical implications. Atherosclerosis 196: 9-21, 2008.
2. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, Stern DM, Nawroth PP. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83: 876-886, 2005.
3. Chavakis T, Bierhaus A, Al Fakhri N, Schneider D, Witte S, Linn T, Nagashima M, Morser J, Arnold B, Preissner KT, Nawroth PP. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment. J Exp Med 198: 1507-1515, 2003. (Pubitemid 37467165)
4. Chavakis T, Bierhaus A, Nawroth PP. RAGE (receptor for advanced glycation end products): a central player in the inflammatory response. Microbes Infect 6: 1219-1225, 2004. (Pubitemid 39370091)
5. Dattilo BM, Fritz G, Leclerc E, Kooi CW, Heizmann CW, Chazin WJ. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry 46: 6957-6970, 2007. (Pubitemid 46906424)
6. Dello Russo C, Gavrilyuk V, Weinberg G, Almeida A, Bolanos JP, Palmer J, Pelligrino D, Galea E, Feinstein DL. Peroxisome proliferatoractivated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J Biol Chem 278: 5828-5836, 2003. (Pubitemid 36800829)
7. Gavrilyuk V, Dello Russo C, Heneka MT, Pelligrino D, Weinberg G, Feinstein DL. Norepinephrine increases I kappa B alpha expression in astrocytes. J Biol Chem 277: 29662-29668, 2002.
8. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114: 597-605, 2006. (Pubitemid 44199649)
9. Grossin N, Wautier MP, Meas T, Guillausseau PJ, Massin P, Wautier JL. Severity of diabetic microvascular complications is associated with a low soluble RAGE level. Diabetes Metab 34: 392-395, 2008.
10. Hassid BG, Nair MN, Ducruet AF, Otten ML, Komotar RJ, Pinsky DJ, Schmidt AM, Yan SF, Connolly ES. Neuronal RAGE expression modulates severity of injury following transient focal cerebral ischemia. J Clin Neurosci 16: 302-306, 2009.
11. Herold K, Moser B, Chen Y, Zeng S, Yan SF, Ramasamy R, Emond J, Clynes R, Schmidt AM. Receptor for advanced glycation end products (RAGE) in a dash to the rescue: inflammatory signals gone awry in the primal response to stress. J Leukoc Biol 82: 204-212, 2007. (Pubitemid 47230628)
12. Huang JS, Guh JY, Chen HC, Hung WC, Lai YH, Chuang LY. Role of receptor for advanced glycation end-product (RAGE) and the JAK/STAT-signaling pathway in AGE-induced collagen production in NRK-49F cells. J Cell Biochem 81: 102-113, 2001.
13. Kaneko M, Bucciarelli L, Hwang YC, Lee L, Yan SF, Schmidt AM, Ramasamy R. Aldose reductase and AGE-RAGE pathways: key players in myocardial ischemic injury. Ann NY Acad Sci 1043: 702-709, 2005. (Pubitemid 41123963)
14. Lindauer U, Dreier J, Angstwurm K, Rubin I, Villringer A, Einhaupl KM, Dirnagl U. Role of nitric oxide synthase inhibition in leukocyteendothelium interaction in the rat pial microvasculature. J Cereb Blood Flow Metab 16: 1143-1152, 1996. (Pubitemid 26365365)
15. -ΔΔCT Method. Methods 25: 402-408, 2001.
16. Ma L, Carter RJ, Morton AJ, Nicholson LF. RAGE is expressed in pyramidal cells of the hippocampus following moderate hypoxic-ischemic brain injury in rats. Brain Res 966: 167-174, 2003. (Pubitemid 36255580)
17. Mukherjee TK, Reynolds PR, Hoidal JR. Differential effect of estrogen receptor alpha and beta agonists on the receptor for advanced glycation end product expression in human microvascular endothelial cells. Biochim Biophys Acta 1745: 300-309, 2005.
18. Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 22: 3716-3727, 2008.
19. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333, 2002. (Pubitemid 34761611)
20. Santizo R, Pelligrino DA. Estrogen reduces leukocyte adhesion in the cerebral circulation of female rats. J Cereb Blood Flow Metab 19: 1061-1065, 1999. (Pubitemid 30167755)
21. Santizo RA, Koenig HM, Pelligrino DA. Estrogen and leukocyte adhesion following transient forebrain ischemia in rats. Stroke 31: 2231-2235, 2000. (Pubitemid 30702798)
22. Santizo RA, Xu HL, Galea E, Muyskens S, Baughman VL, Pelligrino DA. Combined endothelial nitric oxide synthase upregulation and caveolin- 1 downregulation decrease leukocyte adhesion in pial venules of ovariectomized female rats. Stroke 33: 613-616, 2002. (Pubitemid 34123415)
23. Santizo RA, Xu HL, Ye S, Baughman VL, Pelligrino DA. Loss of benefit from estrogen replacement therapy in diabetic ovariectomized female rats subjected to transient forebrain ischemia. Brain Res 956: 86-95, 2002. (Pubitemid 35335560)
24. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108: 949-955, 2001.
25. Shepherd CE, Goyette J, Utter V, Rahimi F, Yang Z, Geczy CL, Halliday GM. Inflammatory S100A9 and S100A12 proteins in Alzheimer's disease. Neurobiol Aging 27: 1554-1563, 2006. (Pubitemid 44344843)
26. Stern DM, Yan SD, Yan SF, Schmidt AM. Receptor for advanced glycation endproducts (RAGE) and the complications of diabetes. Ageing Res Rev 1: 1-15, 2002. (Pubitemid 38340348)
27. Tanaka N, Yonekura H, Yamagishi S, Fujimori H, Yamamoto Y, Yamamoto H. The receptor for advanced glycation end products is induced by the glycation products themselves and tumor necrosis factoralpha through nuclear factor-kappa B, and by 17beta-estradiol through Sp-1 in human vascular endothelial cells. J Biol Chem 275: 25781-25790, 2000. (Pubitemid 30687083)
28. Thangthaeng N, Sumien N, Forster MJ. Dissociation of functional status from accrual of CML and RAGE in the aged mouse brain. Exp Gerontol 43: 1077-1085, 2008.
29. Trauernicht AK, Sun H, Patel KP, Mayhan WG. Enalapril prevents impaired nitric oxide synthase-dependent dilatation of cerebral arterioles in diabetic rats. Stroke 34: 2698-2703, 2003. (Pubitemid 37392770)
30. Ulloa L, Messmer D. High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev 17: 189-201, 2006. (Pubitemid 43949075)
31. Wang Q, Santizo R, Baughman VL, Pelligrino DA. Estrogen provides neuroprotection in transient forebrain ischemia through perfusion-independent mechanisms in rats. Stroke 30: 630-637, 1999. (Pubitemid 29115403)
32. Xu HL, Baughman VL, Pelligrino DA. Estrogen replacement treatment in diabetic ovariectomized female rats potentiates postischemic leukocyte adhesion in cerebral venules. Stroke 35: 1974-1978, 2004.
33. Xu HL, Galea E, Santizo RA, Baughman VL, Pelligrino DA. The key role of caveolin-1 in estrogen-mediated regulation of endothelial nitric oxide synthase function in cerebral arterioles in vivo. J Cereb Blood Flow Metab 21: 907-913, 2001. (Pubitemid 32729826)
34. Xu HL, Salter-Cid L, Linnik MD, Wang EY, Paisansathan C, Pelligrino DA. Vascular adhesion protein-1 plays an important role in postischemic inflammation and neuropathology in diabetic, estrogen-treated ovariectomized female rats subjected to transient forebrain ischemia. J Pharmacol Exp Ther 317: 19-29, 2006.
35. Zhai DX, Kong QF, Xu WS, Bai SS, Peng HS, Zhao K, Li GZ, Wang DD, Sun B, Wang JH, Wang GY, Li HL. RAGE expression is upregulated in human cerebral ischemia and pMCAO rats. Neurosci Lett 445: 117-121, 2008.