Tumor necrosis factor-α inhibition attenuates middle cerebral artery remodeling but increases cerebral ischemic damage in hypertensive rats

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 5, 2014, Pages

  Pires, Paulo W ^a   Girgla, Saavia S ^a   Moreno, Guillermo ^a   McClain, Jonathon L ^a   Dorrance, Anne M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cerebral vascular remodeling; Hypertension; Ischemic stroke; Macrophages microglia; Tumor necrosis factor

Indexed keywords

CEREBRAL VASCULAR REMODELING; HYPERTENSION; ISCHEMIC STROKE; MACROPHAGES/MICROGLIA; TUMOR NECROSIS FACTOR-Α;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BLOOD PRESSURE; HYPERTENSION; IMMUNOGLOBULIN G; INFARCTION, MIDDLE CEREBRAL ARTERY; MACROPHAGES; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY; RATS; RATS, INBRED SHR; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA; VASODILATION;

EID: 84906902771     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00018.2014     Document Type: Article

References (52)

1. Barone FC, Arvin B, White RF, Miller A, Webb CL, Willette RN, Lysko PG, Feuerstein GZ. Tumor necrosis factor-alpha. A mediator of focal ischemic brain injury. Stroke 28: 1233-1244, 1997.
2. Baumbach GL, Hajdu MA. Mechanics and composition of cerebral arterioles in renal and spontaneously hypertensive rats. Hypertension 21: 816-826, 1993.
3. Briet M, Schiffrin EL. Vascular actions of aldosterone. J Vasc Res 50: 89-99, 2013.
4. Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med 2: 788-794, 1996.
5. Capria A, De Nardo D, Baffetti FR, Barbini U, Violo A, Tondo T, Fontana L. Long-term anti-TNF-alpha treatments reverse the endothelial dysfunction in rheumatoid arthritis: the biological coherence between synovial and endothelial inflammation. Int J Immunopathol Pharmacol 23: 255-262, 2010.
6. Castro MM, Rizzi E, Prado CM, Rossi MA, Tanus-Santos JE, Gerlach RF. Imbalance between matrix metalloproteinases and tissue inhibitor of metalloproteinases in hypertensive vascular remodeling. Matrix Biol 29: 194-201, 2010.
7. Chan SL, Chapman AC, Sweet JG, Gokina NI, Cipolla MJ. Effect of PPARgamma inhibition during pregnancy on posterior cerebral artery function and structure. Front Physiol 1: 130, 2010.
8. Coucha M, Li W, Ergul A. The effect of endothelin receptor A antagonism on basilar artery endothelium-dependent relaxation after ischemic stroke. Life Sci 91: 676-680, 2012.
9. Dorrance AM, Osborn HL, Grekin R, Webb RC. Spironolactone reduces cerebral infarct size and EGF-receptor mRNA in stroke-prone rats. Am J Physiol Regul Integr Comp Physiol 281: R944-R950, 2001.
10. Elmarakby AA, Quigley JE, Imig JD, Pollock JS, Pollock DM. TNF-α inhibition reduces renal injury in DOCA-salt hypertensive rats. Am J Physiol Regul Integr Comp Physiol 294: R76-R83, 2008.
11. Elmarakby AA, Quigley JE, Pollock DM, Imig JD. Tumor necrosis factor alpha blockade increases renal Cyp2c23 expression and slows the progression of renal damage in salt-sensitive hypertension. Hypertension 47: 557-562, 2006.
12. Galarraga B, Belch JJ, Pullar T, Ogston S, Khan F. Clinical improvement in rheumatoid arthritis is associated with healthier microvascular function in patients who respond to antirheumatic therapy. J Rheumatol 37: 521-528, 2010.
13. Gary DS, Bruce-Keller AJ, Kindy MS, Mattson MP. Ischemic and excitotoxic brain injury is enhanced in mice lacking the p55 tumor necrosis factor receptor. J Cereb Blood Flow Metab 18: 1283-1287, 1998.
14. Gillham JC, Myers JE, Baker PN, Taggart MJ. TNF-alpha alters nitric oxide-and endothelium-derived hyperpolarizing factor-mediated vasodilatation in human omental arteries. Hypertens Pregnancy 27: 29-38, 2008.
15. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127: e6-e245, 2013.
16. Hayashi K, Naiki T. Adaptation and remodeling of vascular wall; biomechanical response to hypertension. J Mech Behav Biomed Mater 2: 3-19, 2009.
17. Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, Gao Y, Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 43: 3063-3070, 2012.
18. Iademarco MF, Barks JL, Dean DC. Regulation of vascular cell adhesion molecule-1 expression by IL-4 and TNF-alpha in cultured endothelial cells. J Clin Invest 95: 264-271, 1995.
19. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 87: 779-789, 2010.
20. Lee SJ, Kim WJ, Moon SK. TNF-alpha regulates vascular smooth muscle cell responses in genetic hypertension. Int Immunopharmacol 9: 837-843, 2009.
21. Li JS, Lariviere R, Schiffrin EL. Effect of a nonselective endothelin antagonist on vascular remodeling in deoxycorticosterone acetate-salt hypertensive rats. Evidence for a role of endothelin in vascular hypertrophy. Hypertension 24: 183-188, 1994.
22. Li YY, Feng YQ, Kadokami T, McTiernan CF, Draviam R, Watkins SC, Feldman AM. Myocardial extracellular matrix remodeling in transgenic mice overexpressing tumor necrosis factor alpha can be modulated by anti-tumor necrosis factor alpha therapy. Proc Natl Acad Sci USA 97: 12746-12751, 2000.
23. Lin CP, Huang PH, Tsai HS, Wu TC, Leu HB, Liu PL, Chen YH. Monascus purpureus-fermented rice inhibits tumor necrosis factor-alphainduced upregulation of matrix metalloproteinase 2 and 9 in human aortic smooth muscle cells. J Pharm Pharmacol 63: 1587-1594, 2011.
24. Lin YC, Chiang CH, Chang LT, Sun CK, Leu S, Shao PL, Hsieh MC, Tsai TH, Chua S, Chung SY, Kao YH, Yip HK. Simvastatin attenuates the additive effects of TNF-alpha and IL-18 on the connexin 43 upregulation and over-proliferation of cultured aortic smooth muscle cells. Cytokine 62: 341-351, 2013.
25. -ΔΔCT method. Methods 25: 402-408, 2001.
26. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91, 1989.
27. Mabuchi T, Kitagawa K, Ohtsuki T, Kuwabara K, Yagita Y, Yanagihara T, Hori M, Matsumoto M. Contribution of microglia/macrophages to expansion of infarction and response of oligodendrocytes after focal cerebral ischemia in rats. Stroke 31: 1735-1743, 2000.
28. Marchesi C, Paradis P, Schiffrin EL. Role of the renin-angiotensin system in vascular inflammation. Trends Pharmacol Sci 29: 367-374, 2008.
29. Marrelli SP, Khorovets A, Johnson TD, Childres WF, Bryan RM Jr. P2 purinoceptor-mediated dilations in the rat middle cerebral artery after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 276: H33-H41, 1999.
30. Martinez-Revelles S, Jimenez-Altayo F, Caracuel L, Perez-Asensio FJ, Planas AM, Vila E. Endothelial dysfunction in rat mesenteric resistance artery after transient middle cerebral artery occlusion. J Pharmacol Exp Ther 325: 363-369, 2008.
31. Mathiassen ON, Buus NH, Sihm I, Thybo NK, Morn B, Schroeder AP, Thygesen K, Aalkjaer C, Lederballe O, Mulvany MJ, Christensen KL. Small artery structure is an independent predictor of cardiovascular events in essential hypertension. J Hypertens 25: 1021-1026, 2007.
32. McCoy MK, Tansey MG. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation 5: 45, 2008.
33. Picchi A, Gao X, Belmadani S, Potter BJ, Focardi M, Chilian WM, Zhang C. Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99: 69-77, 2006.
34. Pires PW, Deutsch C, McClain JL, Rogers CT, Dorrance AM. Tempol, a superoxide dismutase mimetic, prevents cerebral vessel remodeling in hypertensive rats. Microvasc Res 80: 445-452, 2010.
35. Pires PW, Girgla SS, McClain JL, Kaminski NE, van Rooijen N, Dorrance AM. Improvement in middle cerebral artery structure and endothelial function in stroke-prone spontaneously hypertensive rats after macrophage depletion. Microcirculation 20: 650-661, 2013.
36. Pires PW, Rogers CT, McClain JL, Garver HS, Fink GD, Dorrance AM. Doxycycline, a matrix metalloprotease inhibitor, reduces vascular remodeling and damage after cerebral ischemia in stroke-prone spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 301: H87-H97, 2011.
37. Rajesh M, Mukhopadhyay P, Hasko G, Huffman JW, Mackie K, Pacher P. CB2 cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br J Pharmacol 153: 347-357, 2008.
38. Rigsby CS, Ergul A, Portik Dobos V, Pollock DM, Dorrance AM. Effects of spironolactone on cerebral vessel structure in rats with sustained hypertension. Am J Hypertens 24: 708-715, 2011.
39. Rigsby CS, Pollock DM, Dorrance AM. Spironolactone improves structure and increases tone in the cerebral vasculature of male spontaneously hypertensive stroke-prone rats. Microvasc Res 73: 198-205, 2007.
40. Sandoo A, Panoulas VF, Toms TE, Smith JP, Stavropoulos-Kalinoglou A, Metsios GS, Gasparyan AY, Carroll D, Veldhuijzen van Zanten JJ, Kitas GD. Anti-TNFalpha therapy may lead to blood pressure reductions through improved endothelium-dependent microvascular function in patients with rheumatoid arthritis. J Hum Hypertens 25: 699-702, 2011.
41. Schiffrin EL. Vascular endothelin in hypertension. Vascul Pharmacol 43: 19-29, 2005.
42. Schilling M, Besselmann M, Muller M, Strecker JK, Ringelstein EB, Kiefer R. Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: an investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 196: 290-297, 2005.
43. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314, 1994.
44. Sriramula S, Haque M, Majid DS, Francis J. Involvement of tumor necrosis factor-alpha in angiotensin II-mediated effects on salt appetite, hypertension, and cardiac hypertrophy. Hypertension 51: 1345-1351, 2008.
45. Sumbria RK, Boado RJ, Pardridge WM. Brain protection from stroke with intravenous TNFalpha decoy receptor-Trojan horse fusion protein. J Cereb Blood Flow Metab 32: 1933-1938, 2012.
46. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10: 290-293, 1990.
47. Todd MM, Weeks J. Comparative effects of propofol, pentobarbital, and isoflurane on cerebral blood flow and blood volume. J Neurosurg Anesthesiol 8: 296-303, 1996.
48. Touyz RM. Intracellular mechanisms involved in vascular remodelling of resistance arteries in hypertension: role of angiotensin II. Exp Physiol 90: 449-455, 2005.
49. Yang GY, Gong C, Qin Z, Liu XH, Lorris Betz A. Tumor necrosis factor alpha expression produces increased blood-brain barrier permeability following temporary focal cerebral ischemia in mice. Brain Res Mol Brain Res 69: 135-143, 1999.
50. Yang J, Noyan-Ashraf MH, Meissner A, Voigtlaender-Bolz J, Kroetsch JT, Foltz W, Jaffray D, Kapoor A, Momen A, Heximer SP, Zhang H, van Eede M, Henkelman RM, Matthews SG, Lidington D, Husain M, Bolz SS. Proximal cerebral arteries develop myogenic responsiveness in heart failure via tumor necrosis factor-alpha-dependent activation of sphingosine-1-phosphate signaling. Circulation 126: 196-206, 2012.
51. Yilmaz G, Granger DN. Cell adhesion molecules and ischemic stroke. Neurol Res 30: 783-793, 2008.
52. You J, Johnson TD, Childres WF, Bryan RM Jr. Endothelial-mediated dilations of rat middle cerebral arteries by ATP and ADP. Am J Physiol Heart Circ Physiol 273: H1472-H1477, 1997.