Erythrocyte Efferocytosis by the Arterial Wall Promotes Oxidation in Early-Stage Atheroma in Humans

Frontiers in Cardiovascular Medicine

Volumn 4, Issue , 2017, Pages

  Delbosc, Sandrine ^a,b   Bayles, Richard Graham ^a,b   Laschet, Jamila ^a,b   Ollivier, Veronique ^a,b   Ho Tin Noé, Benoit ^a,b   Touat, Ziad ^a,b   Deschildre, Catherine ^a,b   Morvan, Marion ^a,b   Louedec, Liliane ^a,b   Gouya, Laurent ^b,c   Guedj, Kevin ^a,b   Nicoletti, Antonino ^a,b   Michel, Jean Baptiste ^a,b  

^a INSERM   (France)

^b Département Hospitalo Universitaire DHU PROTECT   (France)

^c CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

Author keywords

atherosclerosis; fatty streaks; hemoglobin; iron; oxidative stress; smooth muscle cells; translational studies; vascular biology

Indexed keywords

EID: 85033599265     PISSN: None     EISSN: 2297055X     Source Type: Journal    
DOI: 10.3389/fcvm.2017.00043     Document Type: Article

References (60)

1. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation (2007) 116:1832–44.10.1161/CIRCULATIONAHA.106.67689017938300
2. Biasetti J, Spazzini PG, Hedin U, Gasser TC. Synergy between shear-induced migration and secondary flows on red blood cells transport in arteries: considerations on oxygen transport. J R Soc Interface (2014) 11:20140403.10.1098/rsif.2014.040324850907
3. Tarbell JM. Mass transport in arteries and the localization of atherosclerosis. Annu Rev Biomed Eng (2003) 5:79–118.10.1146/annurev.bioeng.5.040202.12152912651738
4. Mohamied Y, Rowland EM, Bailey EL, Sherwin SJ, Schwartz MA, Weinberg PD. Change of direction in the biomechanics of atherosclerosis. Ann Biomed Eng (2015) 43:16–25.10.1007/s10439-014-1095-425138165
5. White SJ, Newby AC, Johnson TW. Endothelial erosion of plaques as a substrate for coronary thrombosis. Thromb Haemost (2016) 115:509–19.10.1160/TH15-09-076526791872
6. Yla-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S, Carew TE, Butler S, et al. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest (1989) 84:1086–95.10.1172/JCI1142712794046
7. Geer JC, Catsulis C, Mcgill HC, Jr Stron JP. Fine structure of the baboon aortic fatty streak. Am J Pathol (1968) 52:265–86.
8. Allahverdian S, Chehroudi AC, Mcmanus BM, Abraham T, Francis GA. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation (2014) 129:1551–9.10.1161/CIRCULATIONAHA.113.005015
9. Ho-Tin-Noe B, Vo S, Bayles R, Ferriere S, Ladjal H, Toumi S, et al. Cholesterol crystallization in human atherosclerosis is triggered in smooth muscle cells during the transition from fatty streak to fibroatheroma. J Pathol (2017) 241:671–82.
10. Feil S, Fehrenbacher B, Lukowski R, Essmann F, Schulze-Osthoff K, Schaller M, et al. Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis. Circ Res (2014) 115:662–7.10.1161/CIRCRESAHA.115.304634
11. Shankman LS, Gomez D, Cherepanova OA, Salmon M, Alencar GF, Haskins RM, et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med (2015) 21:628–37.10.1038/nm.3866
12. Chappell J, Harman JL, Narasimhan VM, Yu H, Foote K, Simons BD, et al. Extensive proliferation of a subset of differentiated, yet plastic, medial vascular smooth muscle cells contributes to neointimal formation in mouse injury and atherosclerosis models. Circ Res (2016) 119:1313–23.10.1161/CIRCRESAHA.116.309799
13. Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB. The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res (2012) 95:194–204.10.1093/cvr/cvs135
14. Ross R. Atherosclerosis – an inflammatory disease. N Engl J Med (1999) 340:115–26.10.1056/NEJM199901143400207
15. Massberg S, Brand K, Gruner S, Page S, Muller E, Muller I, et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med (2002) 196:887–96.10.1084/jem.2001204412370251
16. Jeney V, Balla G, Balla J. Red blood cell, hemoglobin and heme in the progression of atherosclerosis. Front Physiol (2014) 5:379.10.3389/fphys.2014.0037925324785
17. Balla G, Vercellotti GM, Muller-Eberhard U, Eaton J, Jacob HS. Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab Invest (1991) 64:648–55.
18. Balla G, Jacob HS, Eaton JW, Belcher JD, Vercellotti GM. Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler Thromb (1991) 11:1700–11.10.1161/01.ATV.11.6.1700
19. Baek JH, D’agnillo F, Vallelian F, Pereira CP, Williams MC, Jia Y, et al. Hemoglobin-driven pathophysiology is an in vivo consequence of the red blood cell storage lesion that can be attenuated in guinea pigs by haptoglobin therapy. J Clin Invest (2012) 122:1444–58.10.1172/JCI5977022446185
20. Arbustini E, Morbini P, D’armini AM, Repetto A, Minzioni G, Piovella F, et al. Plaque composition in plexogenic and thromboembolic pulmonary hypertension: the critical role of thrombotic material in pultaceous core formation. Heart (2002) 88:177–82.10.1136/heart.88.2.17712117850
21. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med (2003) 349:2316–25.10.1056/NEJMoa03565514668457
22. Nagy E, Eaton JW, Jeney V, Soares MP, Varga Z, Galajda Z, et al. Red cells, hemoglobin, heme, iron, and atherogenesis. Arterioscler Thromb Vasc Biol (2010) 30:1347–53.10.1161/ATVBAHA.110.20643320378845
23. Kolb S, Vranckx R, Huisse MG, Michel JB, Meilhac O. The phosphatidylserine receptor mediates phagocytosis by vascular smooth muscle cells. J Pathol (2007) 212:249–59.10.1002/path.219017534843
24. Llorente-Cortes V, Otero-Vinas M, Camino-Lopez S, Costales P, Badimon L. Cholesteryl esters of aggregated LDL are internalized by selective uptake in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol (2006) 26:117–23.10.1161/01.ATV.0000193618.32611.8b16254205
25. Bennett MR, Gibson DF, Schwartz SM, Tait JF. Binding and phagocytosis of apoptotic vascular smooth muscle cells is mediated in part by exposure of phosphatidylserine. Circ Res (1995) 77:1136–42.10.1161/01.RES.77.6.11367586226
26. Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W, Jr Rosenfeld ME, et al. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation (1994) 89:2462–78.10.1161/01.CIR.89.5.2462
27. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res (2014) 114:1852–66.10.1161/CIRCRESAHA.114.302721
28. Delbosc S, Diallo D, Dejouvencel T, Lamiral Z, Louedec L, Martin-Ventura JL, et al. Impaired high-density lipoprotein anti-oxidant capacity in human abdominal aortic aneurysm. Cardiovasc Res (2013) 100:307–15.10.1093/cvr/cvt19423955602
29. Hyafil F, Laissy JP, Mazighi M, Tchetche D, Louedec L, Adle-Biassette H, et al. Ferumoxtran-10-enhanced MRI of the hypercholesterolemic rabbit aorta: relationship between signal loss and macrophage infiltration. Arterioscler Thromb Vasc Biol (2006) 26:176–81.10.1161/01.ATV.0000194098.82677.5716269663
30. Tziakas D, Chalikias G, Kapelouzou A, Tentes I, Schafer K, Karayannakos P, et al. Erythrocyte membrane cholesterol and lipid core growth in a rabbit model of atherosclerosis: modulatory effects of rosuvastatin. Int J Cardiol (2013) 170:173–81.10.1016/j.ijcard.2013.10.07024215985
31. Clowes AW, Karnowsky MJ. Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature (1977) 265:625–6.10.1038/265625a0
32. Seligman AM, Karnovsky MJ, Wasserkrug HL, Hanker JS. Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB). J Cell Biol (1968) 38:1–14.10.1083/jcb.38.1.14300067
33. Nguyen-Legros J, Bizot J, Bolesse M, Pulicani JP. [“Diaminobenzidine black” as a new histochemical demonstration of exogenous iron (author’s transl)]. Histochemistry (1980) 66:239–44.10.1007/BF00495737
34. Meguro R, Asano Y, Odagiri S, Li C, Iwatsuki H, Shoumura K. Nonheme-iron histochemistry for light and electron microscopy: a historical, theoretical and technical review. Arch Histol Cytol (2007) 70:1–19.10.1679/aohc.70.117558140
35. Mitchinson MJ, Hothersall DC, Brooks PN, De Burbure CY. The distribution of ceroid in human atherosclerosis. J Pathol (1985) 145:177–83.10.1002/path.17114502053973770
36. Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood (1993) 81:1607–13.7680921
37. Rong JX, Shapiro M, Trogan E, Fisher EA. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci U S A (2003) 100:13531–6.10.1073/pnas.173552610014581613
38. Silva G, Jeney V, Chora A, Larsen R, Balla J, Soares MP. Oxidized hemoglobin is an endogenous proinflammatory agonist that targets vascular endothelial cells. J Biol Chem (2009) 284:29582–95.10.1074/jbc.M109.04534419700768
39. Geer JC. Fine structure of human aortic intimal thickening and fatty streaks. Lab Invest (1965) 14:1764–83.
40. Wen Y, Leake DS. Low density lipoprotein undergoes oxidation within lysosomes in cells. Circ Res (2007) 100:1337–43.10.1161/CIRCRESAHA.107.15170417446432
41. Kurz T, Terman A, Brunk UT. Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch Biochem Biophys (2007) 462:220–30.10.1016/j.abb.2007.01.01317306211
42. Lee FY, Lee TS, Pan CC, Huang AL, Chau LY. Colocalization of iron and ceroid in human atherosclerotic lesions. Atherosclerosis (1998) 138:281–8.10.1016/S0021-9150(98)00033-19690911
43. Li W, Ostblom M, Xu LH, Hellsten A, Leanderson P, Liedberg B, et al. Cytocidal effects of atheromatous plaque components: the death zone revisited. FASEB J (2006) 20:2281–90.10.1096/fj.06-6114com17077305
44. Haka AS, Kramer JR, Dasari RR, Fitzmaurice M. Mechanism of ceroid formation in atherosclerotic plaque: in situ studies using a combination of Raman and fluorescence spectroscopy. J Biomed Opt (2011) 16:011011.10.1117/1.352430421280898
45. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, et al. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem (1992) 267:18148–53.1517245
46. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA (1993) 90:9285–9.1517245
47. Soe-Lin S, Apte SS, Andriopoulos B, Jr Andrews MC, Schranzhofer M, Kahawita T, et al. Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo. Proc Natl Acad Sci U S A (2009) 106:5960–5.10.1073/pnas.090080810619321419
48. Pang JH, Jiang MJ, Chen YL, Wang FW, Wang DL, Chu SH, et al. Increased ferritin gene expression in atherosclerotic lesions. J Clin Invest (1996) 97:2204–12.10.1172/JCI1186618636399
49. Lane DJ, Merlot AM, Huang ML, Bae DH, Jansson PJ, Sahni S, et al. Cellular iron uptake, trafficking and metabolism: key molecules and mechanisms and their roles in disease. Biochim Biophys Acta (2015) 1853:1130–44.10.1016/j.bbamcr.2015.01.02125661197
50. Musci G, Polticelli F, Bonaccorsi di Patti MC. Ceruloplasmin-ferroportin system of iron traffic in vertebrates. World J Biol Chem (2014) 5:204–15.10.4331/wjbc.v5.i2.20424921009
51. Freeman GJ, Casasnovas JM, Umetsu DT, Dekruyff RH. TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol Rev (2010) 235:172–89.10.1111/j.0105-2896.2010.00903.x20536563
52. Gratchev A, Ovsiy I, Manousaridis I, Riabov V, Orekhov A, Kzhyshkowska J. Novel monocyte biomarkers of atherogenic conditions. Curr Pharm Des (2013) 19:5859–64.10.2174/138161281131933000423438959
53. Habib A, Finn AV. The role of iron metabolism as a mediator of macrophage inflammation and lipid handling in atherosclerosis. Front Pharmacol (2014) 5:195.10.3389/fphar.2014.0019525221512
54. Gomez D, Owens GK. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc Res (2012) 95:156–64.10.1093/cvr/cvs11522406749
55. Rosenfeld ME, Ross R. Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis (1990) 10:680–7.10.1161/01.ATV.10.5.6802403295
56. Nakayama M, Takahashi K, Komaru T, Fukuchi M, Shioiri H, Sato K, et al. Increased expression of heme oxygenase-1 and bilirubin accumulation in foam cells of rabbit atherosclerotic lesions. Arterioscler Thromb Vasc Biol (2001) 21:1373–7.10.1161/hq0801.09359211498468
57. Lee TS, Lee FY, Pang JH, Chau LY. Erythrophagocytosis and iron deposition in atherosclerotic lesions. Chin J Physiol (1999) 42:17–23.10405767
58. Unruh D, Srinivasan R, Benson T, Haigh S, Coyle D, Batra N, et al. Red blood cell dysfunction induced by high-fat diet: potential implications for obesity-related atherosclerosis. Circulation (2015) 132:1898–908.10.1161/CIRCULATIONAHA.115.01731326467254
59. Tziakas DN, Chalikias GK, Stakos D, Tentes IK, Papazoglou D, Thomaidi A, et al. Independent and additive predictive value of total cholesterol content of erythrocyte membranes with regard to coronary artery disease clinical presentation. Int J Cardiol (2011) 150:22–7.10.1016/j.ijcard.2010.02.02220223535
60. Pretorius E, Du Plooy JN, Soma P, Keyser I, Buys AV. Smoking and fluidity of erythrocyte membranes: a high resolution scanning electron and atomic force microscopy investigation. Nitric Oxide (2013) 35:42–6.10.1016/j.niox.2013.08.00323973530