Reversal of hypoxia in murine atherosclerosis prevents necrotic core expansion by enhancing efferocytosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 12, 2014, Pages 2545-2553

  Marsch, Elke ^a   Theelen, Thomas L ^a   Demandt, Jasper A F ^a   Jeurissen, Mike ^a   Van Gink, Mathijs ^a   Verjans, Robin ^a   Janssen, Anique ^a   Cleutjens, Jack P ^a   Meex, Steven J R ^b   Donners, Marjo M ^a   Haenen, Guido R ^b   Schalkwijk, Casper G ^c   Dubois, Ludwig J ^d   Lambin, Philippe ^d   Mallat, Ziad ^e,f,g   Gijbels, Marion J ^a,b   Heemskerk, Johan W M ^a   Fisher, Edward A ⁱ   Biessen, Erik A L ^a   Janssen, Ben J ^a   Daemen, Mat J A P ^h   Sluimer, Judith C ^a   more..

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b Department of Clinical Chemistry ^*  (United Kingdom)

^c CARIM   (United States)

^d GROW   (Netherlands)

^e MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^f PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h ACADEMIC MEDICAL CENTER   (Netherlands)

ⁱ NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Carbogen; Hypoxia; Macrophages

Indexed keywords

CARBOGEN; CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; PIMONIDAZOLE; CARBON DIOXIDE; CD36 ANTIGEN; MERTK PROTEIN, MOUSE; ONCOPROTEIN; OXYGEN; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; AORTA ROOT; ARTERIAL BLOOD; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW DERIVED MACROPHAGE; CELL DEATH; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE COURSE; EFFEROCYTOSIS; HEMATOPOIESIS; HYPOXIA; IN VITRO STUDY; MOUSE; MURINAE; NICK END LABELING; NONHUMAN; OXYGEN TENSION; PHENOTYPE; ANIMAL; ANOXIA; APOPTOSIS; BLOOD; C57BL MOUSE; DEFICIENCY; GENETICS; HUMAN; KNOCKOUT MOUSE; MACROPHAGE; MALE; METABOLISM; NECROSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; PLAQUE, ATHEROSCLEROTIC;

ANIMALS; ANOXIA; ANTIGENS, CD36; APOPTOSIS; CARBON DIOXIDE; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; OXYGEN; PHAGOCYTOSIS; PLAQUE, ATHEROSCLEROTIC; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, LDL;

EID: 84918827233     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304023     Document Type: Article

References (43)

1. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438:932-936.
2. Fong CC, Zhang Q, Shi YF, Wu RS, Fong WF, Yang M. Effect of hypoxia on R.A.W264.7 macrophages apoptosis and signaling. Toxicology. 2007;235:52-61.
3. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
4. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10:36-46.
5. Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the unstable plaque. Prog Cardiovasc Dis. 2002;44:349-356.
6. Sluimer JC, Gasc JM, Van Wanroij JL, Kisters N, Groeneweg M, Sollewijn Gelpke MD, Cleutjens JP, Van den Akker LH, Corvol P, Wouters BG, Daemen MJ, Bijnens AP. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol. 2008;51:1258-1265.
7. Sluimer JC, Daemen MJ. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J Pathol. 2009;218:7-29.
8. Björnheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol. 1999;19:870-876.
9. Ramkhelawon B, Yang Y, Van Gils JM, Hewing B, Rayner KJ, Parathath S, Guo L, Oldebeken S, Feig JL, Fisher EA, Moore KJ. Hypoxia induces netrin-1 and Unc5b in atherosclerotic plaques: mechanism for macrophage retention and survival. Arterioscler Thromb Vasc Biol. 2013;33:1180-1188.
10. Parathath S, Mick SL, Feig JE, Joaquin V, Grauer L, Habiel DM, Gassmann M, Gardner LB, Fisher EA. Hypoxia is present in murine atherosclerotic plaques and has multiple adverse effects on macrophage lipid metabolism. Circ Res. 2011;109:1141-1152.
11. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol. 2005;175:6257-6263.
12. Burke B, Giannoudis A, Corke K.P., Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol. 2003;163:1233-1243.
13. Dubois LJ, Lieuwes NG, Janssen MH, Peeters WJ, Windhorst AD, Walsh JC, Kolb HC, Ollers MC, Bussink J, Van Dongen GA, Van Der Kogel A, Lambin P. Preclinical evaluation and validation of [18F]HX4, a promising hypoxia marker for PET imaging. Proc Natl Acad Sci U S A. 2011;108:14620-14625.
14. Jordan BF, Magat J, Colliez F, et al. Mapping of oxygen by imaging lipids relaxation enhancement: a potential sensitive endogenous MRI contrast to map variations in tissue oxygenation. Magn Reson Med. 2012;70:732-744.
15. Van Laarhoven HW, Bussink J, Lok J, Verhagen I, Punt CJ, Heerschap A, Kaanders JH, Van Der Kogel AJ. Modulation of hypoxia in murine liver metastases of colon carcinoma by nicotinamide and carbogen. Radiat Res. 2005;164:245-249.
16. Kaanders JH, Bussink J, Van Der Kogel AJ. ARCON: a novel biologybased approach in radiotherapy. Lancet Oncol. 2002;3:728-737.
17. Chou SC, Azuma Y, Varia M.A., Raleigh JA. Evidence that involucrin, a marker for differentiation, is oxygen regulated in human squamous cell carcinomas. Br J Cancer. 2004;90:728-735.
18. Seijkens T, Hoeksema M.A., Beckers L, Smeets E, Meiler S, Levels J, Tjwa M, de Winther MP, Lutgens E. Hypercholesterolemia-induced priming of hematopoietic stem and progenitor cells aggravates atherosclerosis. FASEB J. 2014;28:2202-2213.
19. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:1256-1261.
20. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/-mice. Arterioscler Thromb Vasc Biol. 2008;28:1421-1428.
21. Borissoff JI, Heeneman S, Kilinç E, Kassák P, Van Oerle R, Winckers K, Govers-Riemslag JW, Hamulyák K, Hackeng TM, Daemen MJ, ten Cate H, Spronk HM. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation. 2010;122:821-830.
22. Zizzo G, Hilliard BA, Monestier M, Cohen PL. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J Immunol. 2012;189:3508-3520.
23. Li Y, Gerbod-Giannone MC, Seitz H, Cui D, Thorp E, Tall AR, Matsushima GK, Tabas I. Cholesterol-induced apoptotic macrophages elicit an inflammatory response in phagocytes, which is partially attenuated by the Mer receptor. J Biol Chem. 2006;281:6707-6717.
24. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R, Offenstadt G, Lesèche G, Cohen PL, Tedgui A, Mallat Z. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:1429-1431.
25. Kennedy AS, Raleigh JA, Perez GM, Calkins DP, Thrall D.E., Novotny DB, Varia M.A. Proliferation and hypoxia in human squamous cell carcinoma of the cervix: first report of combined immunohistochemical assays. Int J Radiat Oncol Biol Phys. 1997;37:897-905.
26. Lee YA, Kim JY, Hong SJ, Lee S.H., Yoo MC, Kim KS, Yang HI. Synovial proliferation differentially affects hypoxia in the joint cavities of rheumatoid arthritis and osteoarthritis patients. Clin Rheumatol. 2007;26:2023-2029.
27. Haroon ZA, Raleigh JA, Greenberg CS, Dewhirst MW. Early wound healing exhibits cytokine surge without evidence of hypoxia. Ann Surg. 2000;231:137-147.
28. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (Lond). 2008;32:451-463.
29. Rist RJ, Naftalin RJ. Glucose-and phorbol myristate acetate-stimulated oxygen consumption and superoxide production in rat peritoneal macrophages is inhibited by dexamethasone. Biochem J. 1993;291 (pt 2):509-514.
30. Wagner BA, Venkataraman S, Buettner GR. The rate of oxygen utilization by cells. Free Radic Biol Med. 2011;51:700-712.
31. Folco EJ, Sheikine Y, Rocha VZ, Christen T, Shvartz E, Sukhova GK, Di Carli MF, Libby P. Hypoxia but not inflammation augments glucose uptake in human macrophages: implications for imaging atherosclerosis with 18fluorine-labeled 2-deoxy-D-glucose positron emission tomography. J Am Coll Cardiol. 2011;58:603-614.
32. Levin M, Leppänen O, Evaldsson M, Wiklund O, Bondjers G, Björnheden T. Mapping of ATP, glucose, glycogen, and lactate concentrations within the arterial wall. Arterioscler Thromb Vasc Biol. 2003;23:1801-1807.
33. Kawaguchi T, Veech RL, Uyeda K. Regulation of energy metabolism in macrophages during hypoxia. Roles of fructose 2,6-bisphosphate and ribose 1,5-bisphosphate. J Biol Chem. 2001;276:28554-28561.
34. Fujisaka S, Usui I, Ikutani M, Aminuddin A, Takikawa A, Tsuneyama K, Mahmood A, Goda N, Nagai Y, Takatsu K, Tobe K. Adipose tissue hypoxia induces inflammatory M1 polarity of macrophages in an HIF-1?-dependent and HIF-1?-independent manner in obese mice. Diabetologia. 2013;56:1403-1412.
35. Van Overmeire E, Laoui D, Keirsse J, Van Ginderachter JA. Hypoxia and tumor-associated macrophages: a deadly alliance in support of tumor progression. Oncoimmunology. 2014;3:e27561.
36. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev. 2008;88:887-918.
37. Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey R.A., Earp HS, Matsushima G, Reap EA. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med. 2002;196:135-140
38. Brizel DM, Lin S, Johnson JL, Brooks J, Dewhirst MW, Piantadosi C.A. The mechanisms by which hyperbaric oxygen and carbogen improve tumour oxygenation. Br J Cancer. 1995;72:1120-1124.
39. Kergoat H, Faucher C. Effects of oxygen and carbogen breathing on choroidal hemodynamics in humans. Invest Ophthalmol Vis Sci. 1999;40:2906-2911.
40. Hoskin P, Rojas A, Saunders M. Accelerated radiotherapy, carbogen, and nicotinamide (ARCON) in the treatment of advanced bladder cancer: mature results of a Phase II nonrandomized study. Int J Radiat Oncol Biol Phys. 2009;73:1425-1431.
41. Lipsky BA, Berendt AR. Hyperbaric oxygen therapy for diabetic foot wounds: has hope hurdled hype? Diabetes Care. 2010;33:1143-1145.
42. Drager LF, Bortolotto L.A., Figueiredo AC, Krieger EM, Lorenzi GF. Effects of continuous positive airway pressure on early signs of atherosclerosis in obstructive sleep apnea. Am J Respir Crit Care Med. 2007;176:706-712.
43. Silvola JM, Saraste A, Forsback S, Laine VJ, Saukko P, Heinonen SE, Ylä-Herttuala S, Roivainen A, Knuuti J. Detection of hypoxia by [18F] EF5 in atherosclerotic plaques in mice. Arterioscler Thromb Vasc Biol. 2011;31:1011-1015.