Curcuminoids limit neutrophil-mediated reperfusion injury in experimental stroke by targeting the endothelium

Microcirculation

Volumn 20, Issue 6, 2013, Pages 544-554

  Funk, Janet L ^a,b   Frye, Jennifer B ^a   Davis Gorman, Grace ^b   Spera, Allison L ^a   Bernas, Michael J ^a   Witte, Marlys H ^a   Weinand, Martin E ^a   Timmermann, Barbaba N ^c   Mcdonagh, Paul F ^a,b   Ritter, Leslie ^b,d  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF KANSAS   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

Curcuminoids; Endothelium; Ischemia; Neutrophil; Reperfusion; Stroke

Indexed keywords

CD11B ANTIGEN; CURCUMIN; CURCUMINOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ITGAM PROTEIN, HUMAN; NONSTEROID ANTIINFLAMMATORY AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION SIZE; BRAIN MICROCIRCULATION; CELL ADHESION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CURCUMA LONGA; EDEMA; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKOCYTE ACTIVATION; MALE; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR RATE; SINGLE DRUG DOSE; TEMPORAL LOBE; VASCULAR ENDOTHELIUM; ANIMAL; CELL CULTURE; DRUG EFFECTS; ENDOTHELIUM CELL; LEUKOCYTE ROLLING; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIGENS, CD11B; CELLS, CULTURED; CURCUMIN; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; LEUKOCYTE ROLLING; MALE; NEUTROPHIL ACTIVATION; NEUTROPHILS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; STROKE;

EID: 84881487624     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12054     Document Type: Article

References (47)

1. Ahmad M, Theofanidis P, Medford RM. Role of activating protein-1 in the regulation of the vascular cell adhesion molecule-1 gene expression by tumor necrosis factor-alpha. J Biol Chem 273: 4616-4621, 1998.
2. Begum AN, Jones MR, Lim GP, Morihara T, Kim P, Heath DD, Rock CL, Pruitt MA, Yang F, Hudspeth B, Hu S, Faull KF, Teter B, Cole GM, Frautschy SA. Curcumin structure-function, bioavailability, and efficacy in models of neuroinflammation and Alzheimer's disease. J Pharmacol Exp Ther 326: 196-208, 2008.
3. Bernas MJ, Cardoso FL, Daley SK, Weinand ME, Campos AR, Ferreira AJ, Hoying JB, Witte MH, Brites D, Persidsky Y, Ramirez SH, Brito MA. Establishment of primary cultures of human brain microvascular endothelial cells to provide an in vitro cellular model of the blood-brain barrier. Nat Protoc 5: 1265-1272, 2010.
4. Buck BH, Liebeskind DS, Saver JL, Bang OY, Yun SW, Starkman S, Ali LK, Kim D, Villablanca JP, Salamon N, Razinia T, Ovbiagele B. Early neutrophilia is associated with volume of ischemic tissue in acute stroke. Stroke 39: 355-360, 2008.
5. del Zoppo GJ. Microvascular responses to cerebral ischemia/inflammation. Ann N Y Acad Sci 823: 132-147, 1997.
6. Dhillon N, Aggarwal BB, Newman RA, Wolff RA, Kunnumakkara AB, Abbruzzese JL, Ng CS, Badmaev V, Kurzrock R. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin Cancer Res 14: 4491-4499, 2008.
7. Dohare P, Garg P, Jain V, Nath C, Ray M. Dose dependence and therapeutic window for the neuroprotective effects of curcumin in thromboembolic model of rat. Behav Brain Res 193: 289-297, 2008.
8. Duilio C, Ambrosio G, Kuppusamy P, DiPaula A, Becker LC, Zweier JL. Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am J Physiol Heart Circ Physiol 280: H2649-H2657, 2001.
9. Epstein J, Sanderson IR, Macdonald TT. Curcumin as a therapeutic agent: the evidence from in vitro, animal and human studies. Br J Nutr 103: 1545-1557, 2010.
10. Funk JL, Migliati E, Chen G, Wei H, Wilson J, Downey KJ, Mullarky PJ, Coull BM, McDonagh PF, Ritter LS. PTHrP induction in focal stroke: a neuroprotective vascular peptide. Am J Physiol Regul Integr Comp Physiol 284: R1021-R1030, 2003.
11. Funk JL, Frye JB, Oyarzo JN, Chen G, Lantz RC, Jolad SD, Solyom AM, Timmermann BN. Efficacy and mechanism of action of turmeric supplements in the treatment of experimental arthritis. Arthritis Rheum 54: 3452-3464, 2006.
12. Funk JL. Turmeric. In: Encyclopedia of Dietary Supplements, 2nd edition, edited by Coates P, Betz JM, Blackman MR, Cragg GM, Levine M, White JD, Moss J, Levine MA. London, UK: Informa Healthcare, 2010.
13. Hammad FT, Al-Salam S, Lubbad L. Curcumin provides incomplete protection of the kidney in ischemia reperfusion injury. Physiol Res 61: 503-511, 2012 (Epub).
14. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 87: 779-789, 2010.
15. Karatepe O, Gulcicek OB, Ugurlucan M, Adas G, Battal M, Kemik A, Kamali G, Altug T, Karahan S. Curcumin nutrition for the prevention of mesenteric ischemia-reperfusion injury: an experimental rodent model. Transplant Proc 41: 3611-3616, 2009.
16. Kilgore KS, Schmid E, Shanley TP, Flory CM, Maheswari V, Tramontini NL, Cohen H, Ward PA, Friedl HP, Warren JS. Sublytic concentrations of the membrane attack complex of complement induce endothelial interleukin-8 and monocyte chemoattractant protein-1 through nuclear factor-kappa B activation. Am J Pathol 150: 2019-2031, 1997.
17. Kim YS, Ahn Y, Hong MH, Joo SY, Kim KH, Sohn IS, Park HW, Hong YJ, Kim JH, Kim W, Jeong MH, Cho JG, Park JC, Kang JC. Curcumin attenuates inflammatory responses of TNF-alpha-stimualted human endothelial cells. J Cardiovasc Pharmacol 50: 41-49, 2007.
18. Kurd SK, Smith N, VanVoorhees A, Troxel AB, Badmaev V, Seykora JT, Gelfand JM. Oral curcumin in the treatment of moderate to severe psoriasis vulgaris: A prospective clinical trial. J Am Acad Dematol 58: 625-631, 2008.
19. Lao CD, Ruffin MT 4th, Normolle D, Heath DD, Murray SI, Bailey JM, Boggs ME, Crowell J, Rock CL, Brenner DE. Dose escalation of a curcuminoid formulation. BMC Complement Altern Med 6: 10, 2006.
20. Liu T, Young PR, McDonnell PC, White RF, Barone FC, Feuerstein GZ. Cytokine-induced neutrophil chemoattractant mRNA expressed in cerebral ischemia. Neurosci Lett 164: 125-128, 1993.
21. Liu F, McCullough LD. Middle cerebral artery occlusion model in rodents: methods and potential pitfalls. J Biomed Biotechnol 2011: 464701, 2011.
22. Lukita-Atmadja W, Ito Y, Baker GL, McCuskey RS. Effects of curcuminoids as anti-inflammatory agents on the hepatic microvascular response to endotoxin. Shock 17: 399-403, 2002.
23. Matsuo Y, Onodera H, Shiga Y, Shozuhara H, Ninomiya M, Kihara T, Tamatani T, Miyasaka M, Kogure K. Role of cell adhesion molecules in brain injury after transient middle cerebral artery occlusion in the rat. Brain Res 656: 344-352, 1994.
24. Mazzoni MC, Schmid-Schönbein GW. Mechanisms and consequences of cell activation in the microcirculation. Cardiovasc Res 32: 709-719, 1996.
25. Morrison H, McKee D, Ritter L. Systemic Neutrophil Activation in a Mouse Model of Ischemic Stroke and Reperfusion. Biol Res Nurs 13: 154-163, 2011.
26. Oda M, Han JY, Nakamura M. Endothelial cell dysfunction in microvasculature: relevance to disease processes. Clin Hemorheol Microcirc 23: 199-211, 2000.
27. Pendurthi UR, Williams JT, Rao LV. Inhibition of tissue factor gene activation in cultured endothelial cells by curcumin. Suppression of activation of transcription factors Egr-1, AP-1, and NF-kappa B. Arterioscler Thromb Vasc Biol 17: 3406-3413, 1997.
28. Rathore P, Dohare P, Varma S, Ray A, Sharma U, Jagannathan NR, Ray M. Curcuma oil: reduces early accumulation of oxidative product and is anti-apoptogenic in transient focal ischemia in rat brain. Neurochem Res 33: 1672-1682, 2008.
29. Ritter LS, Orozco JA, Coull BM, McDonagh PF, Rosenblum WI. Leukocyte accumulation and hemodynamic changes in the cerebral microcirculation during early reperfusion after stroke. Stroke 31: 1153-1161, 2000.
30. Ritter LS, Stempel KM, Coull BM, McDonagh PF. Leukocyte-platelet aggregates in rat peripheral blood after ischemic stroke and reperfusion. Biol Res Nurs 6: 281-288, 2005.
31. Ritter L, Funk J, Schenkel L, Tipton A, Downey K, Wilson J, Coull B, McDonagh P. Inflammatory and hemodynamic changes in the cerebral microcirculation of aged rats after global cerebral ischemia and reperfusion. Microcirculation 15: 297-310, 2008.
32. Ritter L, Davidson L, Henry M, Davis-Gorman G, Morrison H, Frye JB, Cohen Z, Chandler S, McDonagh P, Funk JL. Exaggerated Neutrophil-Mediated Reperfusion Injury after Ischemic Stroke in a Rodent Model of Type 2 Diabetes. Microcirculation 18: 552-561, 2011.
33. Ruehl ML, Orozco JA, Stoker MB, McDonagh PF, Coull BM, Ritter LS. Protective effects of inhibiting both blood and vascular selectins after stroke and reperfusion. Neurol Res 24: 226-232, 2002.
34. Schmid-Schonbein GW. The damaging potential of leukocyte activation in the microcirculation. Angiology 44: 45-56, 1993.
35. Sharma RA, McLelland HR, Hill KA, Ireson CR, Euden SA, Manson MM, Pirmohamed M, Marnett LJ, Gescher AJ, Steward WP. Pharmacodynamic and pharmacokinetic study of oral Curcuma extract in patients with colorectal cancer. Clin Cancer Res 7: 1894-1900, 2001.
36. Shukla PK, Khanna VK, Ali MM, Khan MY, Srimal RC. Anti-ischemic effect of curcumin in rat brain. Neurochem Res 33: 1036-1043, 2008.
37. Stanimirovic DB, Wong J, Shapiro A, Durkin JP. Increase in surface expression of ICAM-1, VCAM-1 and E-selectin in human cerebromicrovascular endothelial cells subjected to ischemia-like insults. Acta Neurochir Suppl 70: 12-16, 1997.
38. Thiyagarajan M, Sharma SS. Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci 74: 969-985, 2004.
39. Vachharajani V, Wang SW, Mishra N, El Gazzar M, Yoza B, McCall C. Curcumin modulates leukocyte and platelet adhesion in murine sepsis. Microcirculation 17: 407-416, 2010.
40. Vareed SK, Kakarala M, Ruffin MT, Crowell JA, Normolle DP, Djuric Z, Brenner DE. Pharmacokinetics of curcumin conjugate metabolites in healthy human subjects. Cancer Epidemiol Biomarkers Prev 17: 1411-1417, 2008.
41. Voraberger G, Schäfer R, Stratowa C. Cloning of the human gene for intercellular adhesion molecule 1 and analysis of its 5'-regulatory region. Induction by cytokines and phorbol ester. J Immunol 147: 2777-2786, 1991.
42. Wang CX, Shuaib A. Neuroprotective effects of free radical scavengers in stroke. Drugs Aging 24: 537-546, 2007.
43. Wang Q, Sun AY, Simonyi A, Jensen MD, Shelat PB, Rottinghaus GE, MacDonald RS, Miller DK, Lubahn DE, Weisman GA, Sun GY. Neuroprotective mechanisms of curcumin against cerebral ischemia-induced neuronal apoptosis and behavioral deficits. J Neurosci Res 82: 138-148, 2005.
44. Worthmann H, Tryc AB, Goldbecker A, Ma YT, Tountopoulou A, Hahn A, Dengler R, Lichtinghagen R, Weissenborn K. The temporal profile of inflammatory markers and mediators in blood after acute ischemic stroke differs depending on stroke outcome. Cerebrovasc Dis 30: 85-92, 2010.
45. Yeh CH, Chen TP, Wu YC, Lin YM. Jing Lin P. Inhibition of NFkappaB activation with curcumin attenuates plasma inflammatory cytokines surge andcardiomyocytic apoptosis following cardiac ischemia/reperfusion. J Surg Res 125: 109-116, 2005.
46. Zhang RL, Chopp M, Li Y, Zaloga C, Jiang N, Jones ML, Miyasaka M, Ward PA. Anti-ICAM-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in the rat. Neurology 44: 1747-1751, 1994.
47. Zhao J, Zhao Y, Zheng W, Lu Y, Feng G, Yu S. Neuroprotective effect of curcumin on transient focal cerebral ischemia in rats. Brain Res 1229: 224-232, 2008.