Lysozyme M-positive monocytes mediate angiotensin ii-induced arterial hypertension and vascular dysfunction

Circulation

Volumn 124, Issue 12, 2011, Pages 1370-1381

  Wenzel, Philip ^a,d   Knorr, Maike ^a   Kossmann, Sabine ^a   Stratmann, Jan ^a   Hausding, Michael ^a,d   Schuhmacher, Swenja ^a,d   Karbach, Susanne H ^c   Schwenk, Melanie ^b,d   Yogev, Nir ^c   Schulz, Eberhard ^a   Oelze, Matthias ^a   Grabbe, Stephan ^b   Jonuleit, Helmut ^b   Becker, Christian ^b   Daiber, Andreas ^a   Waisman, Ari ^c   Münzel, Thomas ^a,d  

^a 2nd Medical Clinic   (Germany)

^b Department of Dermatology ^*  (Germany)

^c Institute for Molecular Medicine   (Germany)

^d UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

angiotensin II; blood vessels; hypertension; inflammation; oxidative stress

Indexed keywords

CYTOCHROME C; LYSOZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; BLOOD PRESSURE REGULATION; CHEMOLUMINESCENCE; CONTROLLED STUDY; FLOW CYTOMETRY; HYPERTENSION; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TELEMETRY; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULAR RING; VASODILATATION; WESTERN BLOTTING;

ANGIOTENSIN II; ANIMALS; ANTIGENS, CD11B; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; HYPERTENSION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCYTES; MURAMIDASE; MUSCLE, SMOOTH, VASCULAR; NEUTROPHILS; NITRIC OXIDE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, CHEMOKINE; RESPIRATORY BURST; VASCULITIS; VASOCONSTRICTOR AGENTS;

EID: 80052961896     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.034470     Document Type: Article

References (43)

1. Lewington S, Clarke R, Qizilbash N, Peto R, Collins R. Age-specific relevance of usual blood pressure to vascular mortality: a meta-analysis of individual data for one million adults in 61 prospective studies. Lancet. 2002;360:1903-1913 (Pubitemid 35472129)
2. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol. 1996;271:C1424-C1437
3. Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal. 2006;8:691-728 (Pubitemid 44043102)
4. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204:2449-2460 (Pubitemid 47529329)
5. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. J Clin Invest. 1996;97:1916-1923
6. Vendrov AE, Hakim ZS, Madamanchi NR, Rojas M, Madamanchi C, Runge MS. Atherosclerosis is attenuated by limiting superoxide generation in both macrophages and vessel wall cells. Arterioscler Thromb Vasc Biol. 2007;27:2714-2721 (Pubitemid 350158927)
7. El Bekay R, Alvarez M, Monteseirin J, Alba G, Chacon P, Vega A, Martin-Nieto J, Jimenez J, Pintado E, Bedoya FJ, Sobrino F. Oxidative stress is a critical mediator of the angiotensin II signal in human neutrophils: involvement of mitogen-activated protein kinase, calcineurin, and the transcription factor NF-kappaB. Blood. 2003;102:662-671 (Pubitemid 36841990)
8. Kintscher U, Wakino S, Kim S, Fleck E, Hsueh WA, Law RE. Angiotensin II induces migration and Pyk2/paxillin phosphorylation of human monocytes. Hypertension. 2001;37:587-593 (Pubitemid 32199032)
9. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612-616
10. AbdAlla S, Lother H, Langer A, el Faramawy Y, Quitterer U. Factor XIIIA transglutaminase crosslinks AT1 receptor dimers of monocytes at the onset of atherosclerosis. Cell. 2004;119:343-354 (Pubitemid 39423837)
11. Liu J, Yang F, Yang XP, Jankowski M, Pagano PJ. NAD(P)H oxidase mediates angiotensin II-induced vascular macrophage infiltration and medial hypertrophy. Arterioscler Thromb Vasc Biol. 2003;23:776-782 (Pubitemid 36569243)
12. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res. 2001;89:408-414 (Pubitemid 34132656)
13. De Ciuceis C, Amiri F, Brassard P, Endemann DH, Touyz RM, Schiffrin EL. Reduced vascular remodeling, endothelial dysfunction, and oxidative stress in resistance arteries of angiotensin II-infused macrophage colonystimulating factor-deficient mice: evidence for a role in inflammation in angiotensin-induced vascular injury. Arterioscler Thromb Vasc Biol. 2005;25:2106-2113 (Pubitemid 41416308)
14. Cross M, Renkawitz R. Repetitive sequence involvement in the duplication and divergence of mouse lysozyme genes. EMBO J. 1990;9: 1283-1288
15. Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837-1845
16. Rotzius P, Soehnlein O, Kenne E, Lindbom L, Nystrom K, Thams S, Eriksson EE. ApoE(-/-)/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis. 2009;202:111-118
17. Rotzius P, Thams S, Soehnlein O, Kenne E, Tseng CN, Bjorkstrom NK, Malmberg KJ, Lindbom L, Eriksson EE. Distinct infiltration of neutrophils in lesion shoulders in ApoE-/-mice. Am J Pathol. 2010;177: 493-500
18. Goren I, Allmann N, Yogev N, Schurmann C, Linke A, Holdener M, Waisman A, Pfeilschifter J, Frank S. A transgenic mouse model of inducible macrophage depletion: effects of diphtheria toxin-driven lysozyme M-specific cell lineage ablation on wound inflammatory, angiogenic, and contractive processes. Am J Pathol. 2009;175:132-147
19. Buch T, Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, Jung S, Waisman A. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods. 2005;2: 419-426 (Pubitemid 40916560)
20. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8:265-277 (Pubitemid 29523965)
21. Suzuki Y, Ruiz-Ortega M, Lorenzo O, Ruperez M, Esteban V, Egido J. Inflammation and angiotensin II. Int J Biochem Cell Biol. 2003;35: 881-900 (Pubitemid 36379329)
22. Kubota Y, Takubo K, Shimizu T, Ohno H, Kishi K, Shibuya M, Saya H, Suda T. M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med. 2009;206:1089-1102
23. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999;21:70-71 (Pubitemid 29036285)
24. Elferink JG, de Koster BM. The stimulation of human neutrophil migration by angiotensin IL: its dependence on Ca2 and the involvement of cyclic GMP. Br J Pharmacol. 1997;121:643-648
25. Nabah YN, Mateo T, Estelles R, Mata M, Zagorski J, Sarau H, Cortijo J, Morcillo EJ, Jose PJ, Sanz MJ. Angiotensin II induces neutrophil accumulation in vivo through generation and release of CXC chemokines. Circulation. 2004;110:3581-3586 (Pubitemid 39612574)
26. Oelze M, Mollnau H, Hoffmann N, Warnholtz A, Bodenschatz M, Smolenski A, Walter U, Skatchkov M, Meinertz T, Munzel T. Vasodilatorstimulated phosphoprotein serine 239 phosphorylation as a sensitive monitor of defective nitric oxide/cGMP signaling and endothelial dysfunction. Circ Res. 2000;87:999-1005
27. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M, Ullrich V, Mulsch A, Schulz E, Keaney JF Jr, Stamler JS, Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest. 2004;113: 482-489 (Pubitemid 38544192)
28. Wenzel P, Hink U, Oelze M, Schuppan S, Schaeuble K, Schildknecht S, Ho KK, Weiner H, Bachschmid M, Munzel T, Daiber A. Role of reduced lipoic acid in the redox regulation of mitochondrial aldehyde dehydrogenase (ALDH-2) activity. Implications for mitochondrial oxidative stress and nitrate tolerance. J Biol Chem. 2007;282:792-799 (Pubitemid 47076617)
29. Weber M, Lauer N, Mulsch A, Kojda G. The effect of peroxynitrite on the catalytic activity of soluble guanylyl cyclase. Free Radic Biol Med. 2001;31:1360-1367 (Pubitemid 33145305)
30. Soehnlein O, Zernecke A, Eriksson EE, Rothfuchs AG, Pham CT, Herwald H, Bidzhekov K, Rottenberg ME, Weber C, Lindbom L. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008;112:1461-1471
31. Sasmono RT, Ehrnsperger A, Cronau SL, Ravasi T, Kandane R, Hickey MJ, Cook AD, Himes SR, Hamilton JA, Hume DA. Mouse neutrophilic granulocytes express mRNA encoding the macrophage colonystimulating factor receptor (CSF-1R) as well as many other macrophagespecific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1. J Leukoc Biol. 2007;82:111-123 (Pubitemid 47026422)
32. Ishibashi M, Hiasa K, Zhao Q, Inoue S, Ohtani K, Kitamoto S, Tsuchihashi M, Sugaya T, Charo IF, Kura S, Tsuzuki T, Ishibashi T, Takeshita A, Egashira K. Critical role of monocyte chemoattractant protein-1 receptor CCR2 on monocytes in hypertension-induced vascular inflammation and remodeling. Circ Res. 2004;94:1203-1210 (Pubitemid 38659633)
33. Bush E, Maeda N, Kuziel WA, Dawson TC, Wilcox JN, DeLeon H, Taylor WR. CC chemokine receptor 2 is required for macrophage infiltration and vascular hypertrophy in angiotensin II-induced hypertension. Hypertension. 2000;36:360-363
34. Keshav S, Chung P, Milon G, Gordon S. Lysozyme is an inducible marker of macrophage activation in murine tissues as demonstrated by in situ hybridization. J Exp Med. 1991;174:1049-1058
35. Gordon S, Todd J, Cohn ZA. In vitro synthesis and secretion of lysozyme by mononuclear phagocytes. J Exp Med. 1974;139:1228-1248
36. Scheinecker C, Strobl H, Fritsch G, Csmarits B, Krieger O, Majdic O, Knapp W. Granulomonocyte-associated lysosomal protein expression during in vitro expansion and differentiation of CD34+ hematopoietic progenitor cells. Blood. 1995;86:4115-4123
37. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity. 2005;22:285-294 (Pubitemid 40387471)
38. Dale DC, Boxer L, Liles WC. The phagocytes: neutrophils and monocytes. Blood. 2008;112:935-945
39. Rey FE, Li XC, Carretero OA, Garvin JL, Pagano PJ. Perivascular superoxide anion contributes to impairment of endothelium-dependent relaxation: role of gp91(phox). Circulation. 2002;106:2497-2502 (Pubitemid 35278808)
40. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H, Yabe-Nishimura C. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation. 2005;112:2677-2685 (Pubitemid 41532605)
41. Morton J, Coles B, Wright K, Gallimore A, Morrow JD, Terry ES, Anning PB, Morgan BP, Dioszeghy V, Kuhn H, Chaitidis P, Hobbs AJ, Jones SA, O'Donnell VB. Circulating neutrophils maintain physiological blood pressure by suppressing bacteria and IFNgamma-dependent iNOS expression in the vasculature of healthy mice. Blood. 2008;111: 5187-5194
42. Rudolph V, Andrie RP, Rudolph TK, Friedrichs K, Klinke A, Hirsch-Hoffmann B, Schwoerer AP, Lau D, Fu X, Klingel K, Sydow K, Didie M, Seniuk A, von Leitner EC, Szoecs K, Schrickel JW, Treede H, Wenzel U, Lewalter T, Nickenig G, Zimmermann WH, Meinertz T, Boger RH, Reichenspurner H, Freeman BA, Eschenhagen T, Ehmke H, Hazen SL, Willems S, Baldus S. Myeloperoxidase acts as a profibrotic mediator of atrial fibrillation. Nat Med. 2010;16:470-474
43. Shimizu K, Libby P, Shubiki R, Sakuma M, Wang Y, Asano K, Mitchell RN, Simon DI. Leukocyte integrin Mac-1 promotes acute cardiac allograft rejection. Circulation. 2008;117:1997-2008 (Pubitemid 351543476)