Nuclear receptor control of opposing macrophage phenotypes in cardiovascular disease

Frontiers in Bioscience

Volumn 17, Issue 5, 2012, Pages 1917-1930

  Frieler, Ryan A ^a   Ramnarayanan, Saiprasad ^a   Mortensen, Richard M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Alternative activation; Glucocorticoid receptor; Macrophage; Mineralocorticoid receptor; PPAR; Review

Indexed keywords

CELL RECEPTOR; HEME OXYGENASE 1;

ANIMAL; CARDIOVASCULAR DISEASE; ENZYMOLOGY; HUMAN; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLISM; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; REVIEW;

ANIMALS; CARDIOVASCULAR DISEASES; HEME OXYGENASE-1; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; PHENOTYPE; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84859255925     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4028     Document Type: Review

References (120)

1. S. Gordon: Alternative activation of macrophages. Nat Rev Immunol, 3 (1), 23-35 (2003). (Pubitemid 37328697)
2. C. A. Louis, V. Mody, W. L. Henry, Jr., J. S. Reichner and J. E. Albina: Regulation of arginase isoforms I and II by IL-4 in cultured murine peritoneal macrophages. Am J Physiol, 276 (1 Pt 2), R237-R42 (1999).
3. M. Stein, S. Keshav, N. Harris and S. Gordon: Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med, 176 (1), 287-92 (1992).
4. G. Raes, P. De Baetselier, W. Noel, A. Beschin, F. Brombacher and G. Hassanzadeh Gh: Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol, 71 (4), 597-602 (2002).
5. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi and M. Locati: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol, 25 (12), 677-86 (2004). (Pubitemid 39457982)
6. D. M. Mosser and J. P. Edwards: Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 8 (12), 958-69 (2008).
7. G. D. Barish, M. Downes, W. A. Alaynick, R. T. Yu, C. B. Ocampo, A. L. Bookout, D. J. Mangelsdorf and R. M. Evans: A Nuclear Receptor Atlas: macrophage activation. Mol Endocrinol, 19 (10), 2466-77 (2005). (Pubitemid 41362661)
8. T. Rhen and J. A. Cidlowski: Antiinflammatory action of glucocorticoids-new mechanisms for old drugs. N Engl J Med, 353 (16), 1711-23 (2005).
9. K. Kang, S. M. Reilly, V. Karabacak, M. R. Gangl, K. Fitzgerald, B. Hatano and C. H. Lee: Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab, 7 (6), 485-95 (2008). (Pubitemid 351729204)
10. J. I. Odegaard, R. R. Ricardo-Gonzalez, M. H. Goforth, C. R. Morel, V. Subramanian, L. Mukundan, A. R. Eagle, D. Vats, F. Brombacher, A. W. Ferrante and A. Chawla: Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature, 447 (7148), 1116-20 (2007). (Pubitemid 47014427)
11. C. Jiang, A. T. Ting and B. Seed: PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature, 391 (6662), 82-6 (1998). (Pubitemid 28079219)
12. M. Ricote, A. C. Li, T. M. Willson, C. J. Kelly and C.K. Glass: The peroxisome proliferator-activated receptorgamma is a negative regulator of macrophage activation. Nature, 391 (6662), 79-82 (1998). (Pubitemid 28079218)
13. M. A. Bouhlel, B. Derudas, E. Rigamonti, R. Dievart, J. Brozek, S. Haulon, C. Zawadzki, B. Jude, G. Torpier, N. Marx, B. Staels and G. Chinetti-Gbaguidi: PPARgamma activation primes human monocytes into alternative M2 macrophages with anti- inflammatory properties. Cell Metab, 6 (2), 137-43 (2007). (Pubitemid 47189091)
14. M. G. Usher, S. Z. Duan, C. Y. Ivaschenko, R. A. Frieler, S. Berger, G. Schutz, C. N. Lumeng and R. M. Mortensen: Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest, 120 (9), 3350-64 (2010).
15. P. R. Colville-Nash, S. S. Qureshi, D. Willis and D. A. Willoughby: Inhibition of inducible nitric oxide synthase by peroxisome proliferator- activated receptor agonists: correlation with induction of heme oxygenase 1. J Immunol, 161 (2), 978-84 (1998). (Pubitemid 28323565)
16. A. L. Hevener, J. M. Olefsky, D. Reichart, M. T. Nguyen, G. Bandyopadyhay, H. Y. Leung, M. J. Watt, C. Benner, M. A. Febbraio, A. K. Nguyen, B. Folian, S. Subramaniam, F. J. Gonzalez, C. K. Glass and M. Ricote: Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest, 117 (6), 1658- 69 (2007). (Pubitemid 46871350)
17. G. Majai, Z. Sarang, K. Csomos, G. Zahuczky and L. Fesus: PPARgamma- dependent regulation of human macrophages in phagocytosis of apoptotic cells. Eur J Immunol, 37 (5), 1343-54 (2007). (Pubitemid 46925318)
18. A. Berry, P. Balard, A. Coste, D. Olagnier, C. Lagane, H. Authier, F. Benoit-Vical, J. C. Lepert, J. P. Seguela, J. F. Magnaval, P. Chambon, D. Metzger, B. Desvergne, W. Wahli, J. Auwerx and B. Pipy: IL-13 induces expression of CD36 in human monocytes through PPARgamma activation. Eur J Immunol, 37 (6), 1642-52 (2007). (Pubitemid 46939499)
19. K. Asada, S. Sasaki, T. Suda, K. Chida and H. Nakamura: Antiinflammatory roles of peroxisome proliferator-activated receptor gamma in human alveolar macrophages. Am J Respir Crit Care Med, 169 (2), 195- 200 (2004). (Pubitemid 38114534)
20. J. I. Odegaard, R. R. Ricardo-Gonzalez, A. Red Eagle, D. Vats, C. R. Morel, M. H. Goforth, V. Subramanian, L. Mukundan, A. W. Ferrante and A. Chawla: Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab, 7 (6), 496- 507 (2008). (Pubitemid 351729205)
21. L. Mukundan, J. I. Odegaard, C. R. Morel, J. E. Heredia, J. W. Mwangi, R. R. Ricardo-Gonzalez, Y. P. Goh, A. R. Eagle, S. E. Dunn, J. U. Awakuni, K. D. Nguyen, L. Steinman, S. A. Michie and A. Chawla: PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat Med, 15 (11), 1266-72 (2009).
22. H. Shu, B. Wong, G. Zhou, Y. Li, J. Berger, J. W. Woods, S. D. Wright and T. Q. Cai: Activation of PPARalpha or gamma reduces secretion of matrix metalloproteinase 9 but not interleukin 8 from human monocytic THP-1 cells. Biochem Biophys Res Commun, 267 (1), 345-9 (2000). (Pubitemid 30072554)
23. M. A. Bouhlel, J. Brozek, B. Derudas, C. Zawadzki, B. Jude, B. Staels and G. Chinetti-Gbaguidi: Unlike PPARgamma, PPARalpha or PPARbeta/delta activation does not promote human monocyte differentiation toward alternative macrophages. Biochem Biophys Res Commun, 386 (3), 459-62 (2009).
24. R. Genolet, W. Wahli and L. Michalik: PPARs as drug targets to modulate inflammatory responses? Current drug targets. Inflammation and allergy, 3 (4), 361-75 (2004). (Pubitemid 39534773)
25. L. D. Hazlett, S. A. McClellan, R. P. Barrett, X. Huang, Y. Zhang, M. Wu, N. van Rooijen and E. Szliter: IL-33 shifts macrophage polarization, promoting resistance against Pseudomonas aeruginosa keratitis. Investigative ophthalmology visual science, 51 (3), 1524-32 (2010).
26. M. Kurowska-Stolarska, B. Stolarski, P. Kewin, G. Murphy, C. J. Corrigan, S. Ying, N. Pitman, A. Mirchandani, B. Rana, N. van Rooijen, M. Shepherd, C. McSharry, I. B. McInnes, D. Xu and F. Y. Liew: IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. Journal of immunology, 183 (10), 6469-77 (2009).
27. R. A. Ahokas, K. J. Warrington, I. C. Gerling, Y. Sun, L. A. Wodi, P. A. Herring, L. Lu, S. K. Bhattacharya, A. E. Postlethwaite and K. T. Weber: Aldosteronism and peripheral blood mononuclear cell activation: a neuroendocrine-immune interface. Circ Res, 93 (10), e124- 35 (2003).
28. S. Keidar, M. Kaplan, E. Pavlotzky, R. Coleman, T. Hayek, S. Hamoud and M. Aviram: Aldosterone administration to mice stimulates macrophage NADPH oxidase and increases atherosclerosis development: a possible role for angiotensin-converting enzyme and the receptors for angiotensin II and aldosterone. Circulation, 109 (18), 2213-20 (2004). (Pubitemid 38625399)
29. K. Bendtzen, P. R. Hansen and K. Rieneck: Spironolactone inhibits production of proinflammatory cytokines, including tumour necrosis factor-alpha and interferon- gamma, and has potential in the treatment of arthritis. Clin Exp Immunol, 134 (1), 151-8 (2003). (Pubitemid 37186601)
30. B. Pitt, W. Remme, F. Zannad, J. Neaton, F. Martinez, B. Roniker, R. Bittman, S. Hurley, J. Kleiman and M. Gatlin: Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med, 348 (14), 1309-21 (2003). (Pubitemid 36384098)
31. B. Pitt, F. Zannad, W. J. Remme, R. Cody, A. Castaigne, A. Perez, J. Palensky and J. Wittes: The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med, 341 (10), 709-17 (1999). (Pubitemid 29407370)
32. K. Nagata, K. Obata, J. Xu, S. Ichihara, A. Noda, H. Kimata, T. Kato, H. Izawa, T. Murohara and M. Yokota: Mineralocorticoid receptor antagonism attenuates cardiac hypertrophy and failure in low-aldosterone hypertensive rats. Hypertension, 47 (4), 656-64 (2006). (Pubitemid 43740235)
33. G. M. Kuster, E. Kotlyar, M. K. Rude, D. A. Siwik, R. Liao, W. S. Colucci and F. Sam: Mineralocorticoid receptor inhibition ameliorates the transition to myocardial failure and decreases oxidative stress and inflammation in mice with chronic pressure overload. Circulation, 111 (4), 420-7 (2005). (Pubitemid 40204425)
34. D. G. Veliotes, G. R. Norton, R. J. Correia, H. Strijdom, D. Badenhorst, R. Brooksbank and A. J. Woodiwiss: Impact of aldosterone receptor blockade on the deleterious cardiac effects of adrenergic activation in hypertensive rats. Journal of cardiovascular pharmacology, 56 (2), 203-11 (2010).
35. A. J. Rickard, J. Morgan, G. Tesch, J. W. Funder, P. J. Fuller and M. J. Young: Deletion of mineralocorticoid receptors from macrophages protects against deoxycorticosterone/salt-induced cardiac fibrosis and increased blood pressure. Hypertension, 54 (3), 537-43 (2009).
36. S. M. Haffner, A. S. Greenberg, W. M. Weston, H. Chen, K. Williams and M. I. Freed: Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation, 106 (6), 679-84 (2002). (Pubitemid 34851926)
37. P. Mohanty, A. Aljada, H. Ghanim, D. Hofmeyer, D. Tripathy, T. Syed, W. Al-Haddad, S. Dhindsa and P. Dandona: Evidence for a potent antiinflammatory effect of rosiglitazone. J Clin Endocrinol Metab, 89 (6), 2728-35 (2004).
38. A. Raji, E. W. Seely, S. A. Bekins, G. H. Williams and D. C. Simonson: Rosiglitazone improves insulin sensitivity and lowers blood pressure in hypertensive patients. Diabetes Care, 26 (1), 172-8 (2003). (Pubitemid 36929012)
39. M. H. Tan, D. Johns, J. Strand, J. Halse, S. Madsbad, J. W. Eriksson, J. Clausen, C. S. Konkoy and M. Herz: Sustained effects of pioglitazone vs. glibenclamide on insulin sensitivity, glycaemic control, and lipid profiles in patients with Type 2 diabetes. Diabet Med, 21 (8), 859-66 (2004). (Pubitemid 39036999)
40. J. P. van Wijk, E. J. de Koning, E. P. Martens and T. J. Rabelink: Thiazolidinediones and blood lipids in type 2 diabetes. Arterioscler Thromb Vasc Biol, 23 (10), 1744-9 (2003). (Pubitemid 37254857)
41. C. Yosefy, E. Magen, A. Kiselevich, R. Priluk, D. London, L. Volchek and R. J. Viskoper, Jr.: Rosiglitazoneimproves, while Glibenclamide worsens blood pressure control in treated hypertensive diabetic and dyslipidemic subjects via modulation of insulin resistance and sympathetic activity. J Cardiovasc Pharmacol, 44 (2), 215-22 (2004). (Pubitemid 38982165)
42. T. Shiomi, H. Tsutsui, S. Hayashidani, N. Suematsu, M. Ikeuchi, J. Wen, M. Ishibashi, T. Kubota, K. Egashira and A. Takeshita: Pioglitazone, a peroxisome proliferatoractivated receptor-gamma agonist, attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation, 106 (24), 3126-32 (2002). (Pubitemid 35440299)
43. E. Caglayan, B. Stauber, A. R. Collins, C. J. Lyon, F. Yin, J. Liu, S. Rosenkranz, E. Erdmann, L. E. Peterson, R. S. Ross, R. K. Tangirala and W. A. Hsueh: Differential roles of cardiomyocyte and macrophage peroxisome proliferator-activated receptor gamma in cardiac fibrosis. Diabetes, 57 (9), 2470-9 (2008).
44. M. Iglarz, R. M. Touyz, E. C. Viel, P. Paradis, F. Amiri, Q. N. Diep and E. L. Schiffrin: Peroxisome proliferator-activated receptor-alpha and receptor-gamma activators prevent cardiac fibrosis in mineralocorticoiddependent hypertension. Hypertension, 42 (4), 737-43 (2003). (Pubitemid 37237318)
45. S. Z. Duan, C. Y. Ivashchenko, M. W. Russell, D. S. Milstone and R. M. Mortensen: Cardiomyocyte-specific knockout and agonist of peroxisome proliferator-activated receptor-gamma both induce cardiac hypertrophy in mice. Circ Res, 97 (4), 372-9 (2005). (Pubitemid 41216142)
46. N. H. Son, S. Yu, J. Tuinei, K. Arai, H. Hamai, S. Homma, G. I. Shulman, E. D. Abel and I. J. Goldberg: PPARgamma-induced cardiolipotoxicity in mice is ameliorated by PPARalpha deficiency despite increases in fatty acid oxidation. J Clin Invest, 120 (10), 3443-54 (2010).
47. Y. Guan, C. Hao, D. R. Cha, R. Rao, W. Lu, D. E. Kohan, M. A. Magnuson, R. Redha, Y. Zhang and M. D. Breyer: Thiazolidinediones expand body fluid volume through PPARgamma stimulation of ENaC-mediated renal salt absorption. Nat Med, 11 (8), 861-6 (2005). (Pubitemid 41161118)
48. P. D. Home, S. J. Pocock, H. Beck-Nielsen, R. Gomis, M. Hanefeld, N. P. Jones, M. Komajda and J. J. McMurray: Rosiglitazone evaluated for cardiovascular outcomes-an interim analysis. N Engl J Med, 357 (1), 28-38 (2007). (Pubitemid 47026732)
49. A. M. Lincoff, K. Wolski, S. J. Nicholls and S. E. Nissen: Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: a meta-analysis of randomized trials. JAMA, 298 (10), 1180-8 (2007). (Pubitemid 47403104)
50. C. Troidl, H. Mollmann, H. Nef, F. Masseli, S. Voss, S. Szardien, M. Willmer, A. Rolf, J. Rixe, K. Troidl, S. Kostin, C. Hamm and A. Elsasser: Classically and alternatively activated macrophages contribute to tissue remodelling after myocardial infarction. J Cell Mol Med, 13 (9B), 3485-96 (2009).
51. S. J. McSweeney, P. W. Hadoke, A. M. Kozak, G. R. Small, H. Khaled, B. R. Walker and G. A. Gray: Improved heart function follows enhanced inflammatory cell recruitment and angiogenesis in 11betaHSD1-deficient mice post-MI. Cardiovasc Res, 88 (1), 159-67 (2010).
52. N. S. Wayman, Y. Hattori, M. C. McDonald, H. Mota-Filipe, S. Cuzzocrea, B. Pisano, P. K. Chatterjee and C. Thiemermann: Ligands of the peroxisome proliferatoractivated receptors (PPAR-gamma and PPAR-alpha) reduce myocardial infarct size. FASEB J, 16 (9), 1027-40 (2002). (Pubitemid 34753509)
53. D. Fraccarollo, P. Galuppo, S. Hildemann, M. Christ, G. Ertl and J. Bauersachs: Additive improvement of left ventricular remodeling and neurohormonal activation by aldosterone receptor blockade with eplerenone and ACE inhibition in rats with myocardial infarction. J Am Coll Cardiol, 42 (9), 1666-73 (2003). (Pubitemid 37378451)
54. K. Schmidt, R. Tissier, B. Ghaleh, T. Drogies, S. B. Felix and T. Krieg: Cardioprotective effects of mineralocorticoid receptor antagonists at reperfusion. Eur Heart J, 31 (13), 1655-62 (2010).
55. J. Khallou-Laschet, A. Varthaman, G. Fornasa, C. Compain, A. T. Gaston, M. Clement, M. Dussiot, O. Levillain, S. Graff-Dubois, A. Nicoletti and G. Caligiuri: Macrophage plasticity in experimental atherosclerosis. PLoS One, 5 (1), e8852 (2010).
56. J. E. Feig, J. X. Rong, R. Shamir, M. Sanson, Y. Vengrenyuk, J. Liu, K. Rayner, K. Moore, M. Garabedian and E. A. Fisher: HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc Natl Acad Sci U S A, 108 (17), 7166-71 (2011).
57. J. E. Feig, S. Parathath, J. X. Rong, S. L. Mick, Y. Vengrenyuk, L. Grauer, S. G. Young and E. A. Fisher: Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques. Circulation, 123 (9), 989-98 (2011).
58. A. C. Li, K. K. Brown, M. J. Silvestre, T. M. Willson, W. Palinski and C. K. Glass: Peroxisome proliferatoractivated receptor gamma ligands inhibit development of atherosclerosis in LDL receptor-deficient mice. J Clin Invest, 106 (4), 523-31 (2000). (Pubitemid 30666385)
59. Z. Chen, S. Ishibashi, S. Perrey, J. Osuga, T. Gotoda, T. Kitamine, Y. Tamura, H. Okazaki, N. Yahagi, Y. Iizuka, F. Shionoiri, K. Ohashi, K. Harada, H. Shimano, R. Nagai and N. Yamada: Troglitazone inhibits atherosclerosis in apolipoprotein E-knockout mice: pleiotropic effects on CD36 expression and HDL. Arterioscler Thromb Vasc Biol, 21 (3), 372-7 (2001). (Pubitemid 32199118)
60. V. R. Babaev, P. G. Yancey, S. V. Ryzhov, V. Kon, M. D. Breyer, M. A. Magnuson, S. Fazio and M. F. Linton: Conditional knockout of macrophage PPARgammaincreases atherosclerosis in C57BL/6 and low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol, 25 (8), 1647-53 (2005). (Pubitemid 41098935)
61. S. Keidar, T. Hayek, M. Kaplan, E. Pavlotzky, S. Hamoud, R. Coleman and M. Aviram: Effect of eplerenone, a selective aldosterone blocker, on blood pressure, serum and macrophage oxidative stress, and atherosclerosis in apolipoprotein E-deficient mice. J Cardiovasc Pharmacol, 41 (6), 955-63 (2003). (Pubitemid 36706146)
62. S. Rajagopalan, D. Duquaine, S. King, B. Pitt and P. Patel: Mineralocorticoid receptor antagonism in experimental atherosclerosis. Circulation, 105 (18), 2212-6 (2002). (Pubitemid 34517167)
63. S. Takai, D. Jin, M. Muramatsu, K. Kirimura, H. Sakonjo and M. Miyazaki: Eplerenone inhibits atherosclerosis in nonhuman primates. Hypertension, 46 (5), 1135-9 (2005). (Pubitemid 41533016)
64. M. P. Bowes, R. Rothlein, S. C. Fagan and J. A. Zivin: Monoclonal antibodies preventing leukocyte activation reduce experimental neurologic injury and enhance efficacy of thrombolytic therapy. Neurology, 45 (4), 815-9 (1995).
65. E. S. Connolly, Jr., C. J. Winfree, T. A. Springer, Y. Naka, H. Liao, S. D. Yan, D. M. Stern, R. A. Solomon, J. C. Gutierrez-Ramos and D. J. Pinsky: Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest, 97 (1), 209-16 (1996). (Pubitemid 26021710)
66. S. A. Loddick and N. J. Rothwell: Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab, 16 (5), 932-40 (1996). (Pubitemid 26292060)
67. S. G. Soriano, A. Coxon, Y. F. Wang, M. P. Frosch, S. A. Lipton, P. R. Hickey and T. N. Mayadas: Mice deficient in Mac-1 (CD11b/CD18) are less susceptible to cerebral ischemia/reperfusion injury. Stroke, 30 (1), 134-9 (1999). (Pubitemid 29029454)
68. P. A. Spera, J. A. Ellison, G. Z. Feuerstein and F. C. Barone: IL-10 reduces rat brain injury following focal stroke. Neurosci Lett, 251 (3), 189-92 (1998). (Pubitemid 28381079)
69. R. A. Frieler, H. Meng, S. Z. Duan, S. Berger, G. Schutz, Y. He, G. Xi, M. M. Wang and R. M. Mortensen: Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke, 42 (1), 179-85 (2011).
70. J. Iwanami, M. Mogi, S. Okamoto, X. Y. Gao, J. M. Li, L. J. Min, A. Ide, K. Tsukuda, M. Iwai and M. Horiuchi: Pretreatment with eplerenone reduces stroke volume in mouse middle cerebral artery occlusion model. Eur J Pharmacol, 566 (1-3), 153-9 (2007). (Pubitemid 46782806)
71. N. Oyamada, M. Sone, K. Miyashita, K. Park, D. Taura, M. Inuzuka, T. Sonoyama, H. Tsujimoto, Y. Fukunaga, N. Tamura, H. Itoh and K. Nakao: The role of mineralocorticoid receptor expression in brain remodeling after cerebral ischemia. Endocrinology, 149 (8), 3764-77 (2008).
72. X. Xiong, G. E. Barreto, L. Xu, Y. B. Ouyang, X. Xie and R. G. Giffard: Increased Brain Injury and Worsened Neurological Outcome in Interleukin-4 Knockout Mice After Transient Focal Cerebral Ischemia. Stroke (2011).
73. F. A. Wagener, H. D. Volk, D. Willis, N. G. Abraham, M. P. Soares, G. J. Adema and C. G. Figdor: Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev, 55 (3), 551-71 (2003). (Pubitemid 37013215)
74. J. P. Roach, E. E. Moore, D. A. Partrick, S. S. Damle, C. C. Silliman, R. C. McIntyre, Jr. and A. Banerjee: Heme oxygenase-1 induction in macrophages by a hemoglobinbased oxygen carrier reduces endotoxin-stimulated cytokine secretion. Shock, 31 (3), 251-7 (2009).
75. T. S. Lee and L. Y. Chau: Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med, 8 (3), 240-6 (2002).
76. Y. Drechsler, A. Dolganiuc, O. Norkina, L. Romics, W. Li, K. Kodys, F. H. Bach, P. Mandrekar and G. Szabo: Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J Immunol, 177 (4), 2592-600 (2006). (Pubitemid 44201018)
77. L. E. Otterbein, F. H. Bach, J. Alam, M. Soares, H. Tao Lu, M. Wysk, R. J. Davis, R. A. Flavell and A. M. Choi: Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med, 6 (4), 422-8 (2000). (Pubitemid 30208159)
78. A. Kadl, A. K. Meher, P. R. Sharma, M. Y. Lee, A. C. Doran, S. R. Johnstone, M. R. Elliott, F. Gruber, J. Han, W. Chen, T. Kensler, K. S. Ravichandran, B. E. Isakson, B. R. Wamhoff and N. Leitinger: Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res, 107 (6), 737-46 (2010).
79. K. M. Choi, P. C. Kashyap, N. Dutta, G. J. Stoltz, T. Ordog, T. Shea Donohue, A. J. Bauer, D. R. Linden, J. H. Szurszewski, S. J. Gibbons and G. Farrugia: CD206- positive M2 macrophages that express heme oxygenase- 1 protect against diabetic gastroparesis in mice. Gastroenterology, 138 (7), 2399-409, 2409 e1 (2010).
80. N. Weis, A. Weigert, A. von Knethen and B. Brune: Heme oxygenase-1 contributes to an alternative macrophage activation profile induced by apoptotic cell supernatants. Mol Biol Cell, 20 (5), 1280-8 (2009).
81. M. P. Soares and F. H. Bach: Heme oxygenase-1: from biology to therapeutic potential. Trends Mol Med, 15 (2), 50-8 (2009).
82. D. A. Ferenbach, N. C. Nkejabega, J. McKay, A. K. Choudhary, M. A. Vernon, M. F. Beesley, S. Clay, B. C. Conway, L. P. Marson, D. C. Kluth and J. Hughes: The induction of macrophage hemeoxygenase-1 is protective during acute kidney injury in aging mice. Kidney Int, 79 (9), 966-76 (2011).
83. H. Christou, T. Morita, C. M. Hsieh, H. Koike, B. Arkonac, M. A. Perrella and S. Kourembanas: Prevention of hypoxia-induced pulmonary hypertension by enhancement of endogenous heme oxygenase-1 in the rat. Circ Res, 86 (12), 1224-9 (2000). (Pubitemid 30436662)
84. L. Devey, D. Ferenbach, E. Mohr, K. Sangster, C. O. Bellamy, J. Hughes and S. J. Wigmore: Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol Ther, 17 (1), 65-72 (2009).
85. Y. Liu, B. Zhu, L. Luo, P. Li, D. W. Paty and M. S. Cynader: Heme oxygenase-1 plays an important protective role in experimental autoimmune encephalomyelitis. Neuroreport, 12 (9), 1841-5 (2001). (Pubitemid 32553694)
86. S. Tzima, P. Victoratos, K. Kranidioti, M. Alexiou and G. Kollias: Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. J Exp Med, 206 (5), 1167-79 (2009).
87. K. Ishikawa, D. Sugawara, X. Wang, K. Suzuki, H. Itabe, Y. Maruyama and A. J. Lusis: Heme oxygenase-1 inhibits atherosclerotic lesion formation in ldl-receptor knockout mice. Circ Res, 88 (5), 506-12 (2001). (Pubitemid 32240914)
88. S. H. Juan, T. S. Lee, K. W. Tseng, J. Y. Liou, S. K. Shyue, K. K. Wu and L. Y. Chau: Adenovirus-mediated heme oxygenase-1 gene transfer inhibits the development of atherosclerosis in apolipoprotein E-deficient mice. Circulation, 104 (13), 1519-25 (2001). (Pubitemid 32917345)
89. C. Cheng, A. M. Noordeloos, V. Jeney, M. P. Soares, F. Moll, G. Pasterkamp, P. W. Serruys and H. J. Duckers: Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque. Circulation, 119 (23), 3017-27 (2009).
90. K. Ishikawa, D. Sugawara, J. Goto, Y. Watanabe, K. Kawamura, M. Shiomi, H. Itabe and Y. Maruyama: Heme oxygenase-1 inhibits atherogenesis in Watanabe heritable hyperlipidemic rabbits. Circulation, 104 (15), 1831-6 (2001). (Pubitemid 32963350)
91. S. F. Yet, M. D. Layne, X. Liu, Y. H. Chen, B. Ith, N. E. Sibinga and M. A. Perrella: Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J, 17 (12), 1759-61 (2003).
92. Y. G. Li, D. M. Wang, S. M. Chen, X. R. Tan, X. Y. Fang, J. W. Wu, G. H. Zhang and R. Q. Mai: Haem oxygenase-1 expression and coronary heart disease- association between levels of haem oxygenase-1 expression and angiographic morphology as well as the quantity of coronary lesions. Acta Cardiol, 61 (3), 295-300 (2006).
93. K. A. Niese, A. R. Collier, A. R. Hajek, S. D. Cederbaum, W. E. O'Brien, M. Wills- Karp, M. E. Rothenberg and N. Zimmermann: Bone marrow cell derived arginase I is the major source of allergen-induced lung arginase but is not required for airway hyperresponsiveness, remodeling and lung inflammatory responses in mice. BMC Immunol, 10, 33 (2009).
94. E. Vergadi, M. S. Chang, C. Lee, O. D. Liang, X. Liu, A. Fernandez-Gonzalez, S. A. Mitsialis and S. Kourembanas: Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension. Circulation, 123 (18), 1986-95 (2011).
95. T. Minamino, H. Christou, C. M. Hsieh, Y. Liu, V. Dhawan, N. G. Abraham, M. A.Perrella, S. A. Mitsialis and S. Kourembanas: Targeted expression of heme oxygenase- 1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci U S A, 98 (15), 8798-803 (2001). (Pubitemid 32678107)
96. S. F. Yet, M. A. Perrella, M. D. Layne, C. M. Hsieh, K. Maemura, L. Kobzik, P. Wiesel, H. Christou, S. Kourembanas and M. E. Lee: Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest, 103 (8), R23-9 (1999). (Pubitemid 29207256)
97. B. S. Zuckerbraun, B. Y. Chin, B. Wegiel, T. R. Billiar, E. Czsimadia, J. Rao, L. Shimoda, E. Ifedigbo, S. Kanno and L. E. Otterbein: Carbon monoxide reverses established pulmonary hypertension. J Exp Med, 203 (9), 2109-19 (2006). (Pubitemid 44352232)
98. L. Sun, M. C. Louie, K. M. Vannella, C. A. Wilke, A. M. LeVine, B. B. Moore and T. P. Shanley: New concepts of IL-10-induced lung fibrosis: fibrocyte recruitment and M2 activation in a CCL2/CCR2 axis. Am J Physiol Lung Cell Mol Physiol, 300 (3), L341-53 (2011).
99. G. G. Brusselle, J. C. Kips, J. H. Tavernier, J. G. van der Heyden, C. A. Cuvelier, R. A. Pauwels and H. Bluethmann: Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin Exp Allergy, 24 (1), 73-80 (1994). (Pubitemid 24210819)
100. G. Grunig, M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley and D. B. Corry: Requirement for IL-13 independently of IL-4 in experimental asthma. Science, 282 (5397), 2261-3 (1998). (Pubitemid 29004075)
101. D. R. Herbert, C. Holscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, B. Claussen, I. Forster and F. Brombacher: Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity, 20 (5), 623-35 (2004). (Pubitemid 38659504)
102. J. E. Kolodsick, G. B. Toews, C. Jakubzick, C. Hogaboam, T. A. Moore, A. McKenzie, C. A. Wilke, C. J. Chrisman and B. B. Moore: Protection from fluorescein isothiocyanate-induced fibrosis in IL-13-deficient, but not IL-4-deficient, mice results from impaired collagen synthesis by fibroblasts. J Immunol, 172 (7), 4068-76 (2004). (Pubitemid 38375218)
103. S. Miyata, T. Matsuyama, T. Kodama, Y. Nishioka, K. Kuribayashi, K. Takeda, S. Akira and M. Sugita: STAT6 deficiency in a mouse model of allergen-induced airways inflammation abolishes eosinophilia but induces infiltration of CD8+ T cells. Clin Exp Allergy, 29 (1), 114-23 (1999). (Pubitemid 29067660)
104. D. S. Straus and C. K. Glass: Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol, 28 (12), 551-8 (2007). (Pubitemid 350101420)
105. C. H. Lee, A. Chawla, N. Urbiztondo, D. Liao, W. A. Boisvert, R. M. Evans and L. K. Curtiss: Transcriptional repression of atherogenic inflammation: modulation by PPARdelta. Science, 302 (5644), 453-7 (2003) doi:10.1126/science. 1087344. (Pubitemid 37296272)
106. F. J. Schopfer, Y. Lin, P. R. Baker, T. Cui, M. Garcia-Barrio, J. Zhang, K. Chen, Y. E. Chen and B. A. Freeman: Nitrolinoleic acid: an endogenous peroxisome proliferator activated receptor gamma ligand. Proceedings of the National Academy of Sciences of the United States of America, 102 (7), 2340-5 (2005). (Pubitemid 40279377)
107. J. L. Arriza, R. B. Simerly, L. W. Swanson and R. M. Evans: The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron, 1 (9), 887- 900 (1988).
108. J. L. Arriza, C. Weinberger, G. Cerelli, T. M. Glaser, B. L. Handelin, D. E. Housman and R. M. Evans: Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science, 237 (4812), 268-75 (1987). (Pubitemid 17095145)
109. A. S. Mihailidou, T. Y. Loan Le, M. Mardini and J. W. Funder: Glucocorticoids activate cardiac mineralocorticoid receptors during experimental myocardial infarction. Hypertension, 54 (6), 1306-12 (2009).
110. J. T. Pesce, T. R. Ramalingam, M. M. Mentink-Kane, M. S. Wilson, K. C. El Kasmi, A. M. Smith, R. W. Thompson, A. W. Cheever, P. J. Murray and T. A. Wynn: Arginase-1- expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog, 5 (4), e1000371 (2009).
111. T. Bagnost, L. Ma, R. F. da Silva, R. Rezakhaniha, C. Houdayer, N. Stergiopulos, C. Andre, Y. Guillaume, A. Berthelot and C. Demougeot: Cardiovascular effects of arginase inhibition in spontaneously hypertensive rats with fully developed hypertension. Cardiovascular research, 87 (3), 569-77 (2010).
112. C. N. Lumeng, J. L. Bodzin and A. R. Saltiel: Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest, 117 (1), 175-84 (2007) doi:10.1172/JCI29881. (Pubitemid 46048464)
113. G. Trujillo, E. C. O'Connor, S. L. Kunkel and C. M. Hogaboam: A novel mechanism for CCR4 in the regulation of macrophage activation in bleomycin-induced pulmonary fibrosis. Am J Pathol, 172 (5), 1209-21 (2008). (Pubitemid 351671535)
114. A. L. Mora, E. Torres-Gonzalez, M. Rojas, C. Corredor, J. Ritzenthaler, J. Xu, J. Roman, K. Brigham and A. Stecenko: Activation of alveolar macrophages via the alternative pathway in herpesvirus-induced lung fibrosis. Am J Respir Cell Mol Biol, 35 (4), 466-73 (2006). (Pubitemid 44477646)
115. D. A. Ferenbach, V. Ramdas, N. Spencer, L. Marson, I. Anegon, J. Hughes and D. C. Kluth: Macrophages expressing heme oxygenase-1 improve renal function in ischemia/reperfusion injury. Mol Ther, 18 (9), 1706-13 (2010).
116. I. Nakamichi, A. Habtezion, B. Zhong, C. H. Contag, E. C. Butcher and M. B. Omary: Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Invest, 115 (11), 3007-14 (2005). (Pubitemid 41567566)
117. T. P. Weber, A. Meissner, P. Boknik, M. G. Hartlage, T. Mollhoff, H. Van Aken and N. Rolf: Hemin, inducer of heme-oxygenase 1, improves functional recovery from myocardial stunning in conscious dogs. J Cardiothorac Vasc Anesth, 15 (4), 422-7 (2001). (Pubitemid 32756200)
118. Q. Ye, Y. Dalavanga, N. Poulakis, S. U. Sixt, J. Guzman and U. Costabel: Decreased expression of haem oxygenase-1 by alveolar macrophages in idiopathic pulmonary fibrosis. Eur Respir J, 31 (5), 1030-6 (2008).
119. M. John, S. Lim, J. Seybold, P. Jose, A. Robichaud, B. O'Connor, P. J. Barnes and K. F. Chung: Inhaled corticosteroids increase interleukin-10 but reduce macrophage inflammatory protein-1alpha, granulocytemacrophage colony-stimulating factor, and interferongamma release from alveolar macrophages in asthma. Am J Respir Crit Care Med, 157 (1), 256-62 (1998). (Pubitemid 28071290)
120. C. Iadecola and J. Anrather: The immunology of stroke: from mechanisms to translation. Nat Med, 17 (7), 796-808 (2011).