Cell membrane damage is involved in the impaired survival of bone marrow stem cells by oxidized low-density lipoprotein

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 12, 2014, Pages 2445-2453

  Li, Xin ^a,b   Xiao, Yuan ^b   Cui, Yuqi ^b   Tan, Tao ^b   Narasimhulu, Chandrakala A ^c   Hao, Hong ^b   Liu, Lingjuan ^b   Zhang, Jia ^b   He, Guanglong ^b   Verfaillie, Catherine M ^d   Lei, Minxiang ^a   Parthasarathy, Sampath ^c   Ma, Jianjie ^b   Zhu, Hua ^b   Liu, Zhenguo ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Cell survival; Membrane damage; Mesenchymal stem cells; MG53; Ox LDL

Indexed keywords

ACETYLCYSTEINE; CARRIER PROTEIN; FLUORESCENT DYE; FM1 43; LOW DENSITY LIPOPROTEIN; MITSUGUMIN 53, HUMAN; OXIDIZED LOW DENSITY LIPOPROTEIN; PYRIDINIUM DERIVATIVE; QUATERNARY AMMONIUM DERIVATIVE; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SCAVENGER;

ANIMAL; BONE MARROW CELL; CELL CULTURE; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CONFOCAL MICROSCOPY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MULTIPOTENT STEM CELL; RAT; TIME;

ACETYLCYSTEINE; ANIMALS; BONE MARROW CELLS; CARRIER PROTEINS; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT DYES; FREE RADICAL SCAVENGERS; HUMANS; LIPOPROTEINS, LDL; MICROSCOPY, CONFOCAL; MULTIPOTENT STEM CELLS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; TIME FACTORS;

EID: 84911427889     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12424     Document Type: Article

References (72)

1. Lalu MM, McIntyre L, Pugliese C, et al. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS ONE. 2012; 7: e47559.
2. Mundra V, Gerling IC, Mahato RI. Mesenchymal stem cell-based therapy. Mol Pharm. 2013; 10: 77-89.
3. Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res. 2011; 109: 923-40.
4. Djouad F, Bouffi C, Ghannam S, et al. Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases. Nat Rev Rheumatol. 2009; 5: 392-9.
5. Garcia-Castro J, Trigueros C, Madrenas J, et al. Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool. J Cell Mol Med. 2008; 12: 2552-65.
6. Parekkadan B, Milwid JM. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng. 2010; 12: 87-117.
7. Hong KU, Li QH, Guo Y, et al. A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol. 2013; 108: 346.
8. Laflamme MA, Murry CE. Regenerating the heart. Nat Biotechnol. 2005; 23: 845-56.
9. Muller-Ehmsen J, Peterson KL, Kedes L, et al. Rebuilding a damaged heart: long-term survival of transplanted neonatal rat cardiomyocytes after myocardial infarction and effect on cardiac function. Circulation. 2002; 105: 1720-6.
10. Muller-Ehmsen J, Whittaker P, Kloner RA, et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol. 2002; 34: 107-16.
11. Gao J, Dennis JE, Muzic RF, et al. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 2001; 169: 12-20.
12. Lee JW, Gupta N, Serikov V, et al. Potential application of mesenchymal stem cells in acute lung injury. Expert Opin Biol Ther. 2009; 9: 1259-70.
13. Lee RH, Pulin AA, Seo MJ, et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell. 2009; 5: 54-63.
14. Schrepfer S, Deuse T, Reichenspurner H, et al. Stem cell transplantation: the lung barrier. Transplant Proc. 2007; 39: 573-6.
15. Imazu M, Ono K, Tadehara F, et al. Plasma levels of oxidized low density lipoprotein are associated with stable angina pectoris and modalities of acute coronary syndrome. Int Heart J. 2008; 49: 515-24.
16. Itabe H, Ueda M. Measurement of plasma oxidized low-density lipoprotein and its clinical implications. J Atheros Thromb. 2007; 14: 1-11.
17. Yamashita H, Ehara S, Yoshiyama M, et al. Elevated plasma levels of oxidized low-density lipoprotein relate to the presence of angiographically detected complex and thrombotic coronary artery lesion morphology in patients with unstable angina. Circ J. 2007; 71: 681-7.
18. Tie G, Yan J, Yang Y, et al. Oxidized low-density lipoprotein induces apoptosis in endothelial progenitor cells by inactivating the phosphoinositide 3-kinase/Akt pathway. J Vasc Res. 2010; 47: 519-30.
19. Wu Y, Wang Q, Cheng L, et al. Effect of oxidized low-density lipoprotein on survival and function of endothelial progenitor cell mediated by p38 signal pathway. J Cardiovas Pharmacol. 2009; 53: 151-6.
20. Hamed S, Brenner B, Abassi Z, et al. Hyperglycemia and oxidized-LDL exert a deleterious effect on endothelial progenitor cell migration in type 2 diabetes mellitus. Thromb Res. 2010; 126: 166-74.
21. Di Santo S, Diehm N, Ortmann J, et al. Oxidized low density lipoprotein impairs endothelial progenitor cell function by downregulation of E-selectin and integrin alpha(v)beta5. Biochem Biophys Res Commun. 2008; 373: 528-32.
22. Ma FX, Zhou B, Chen Z, et al. Oxidized low density lipoprotein impairs endothelial progenitor cells by regulation of endothelial nitric oxide synthase. J Lipid Res. 2006; 47: 1227-37.
23. Wang X, Chen J, Tao Q, et al. Effects of ox-LDL on number and activity of circulating endothelial progenitor cells. Drug Chem Toxicol. 2004; 27: 243-55.
24. Imanishi T, Hano T, Sawamura T, et al. Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin Exp Pharmacol Physiol. 2004; 31: 407-13.
25. Zhou B, Ma FX, Liu PX, et al. Impaired therapeutic vasculogenesis by transplantation of OxLDL-treated endothelial progenitor cells. J Lipid Res. 2007; 48: 518-27.
26. Imanishi T, Hano T, Matsuo Y, et al. Oxidized low-density lipoprotein inhibits vascular endothelial growth factor-induced endothelial progenitor cell differentiation. Clin Exp Pharmacol Physiol. 2003; 30: 665-70.
27. Yang H, Mohamed AS, Zhou SH. Oxidized low density lipoprotein, stem cells, and atherosclerosis. Lipids Health Dis. 2012; 11: 85.
28. Chu L, Hao H, Luo M, et al. Ox-LDL modifies the behaviour of bone marrow stem cells and impairs their endothelial differentiation via inhibition of Akt phosphorylation. J Cell Mol Med. 2011; 15: 423-32.
29. Lu T, Parthasarathy S, Hao H, et al. Reactive oxygen species mediate oxidized low-density lipoprotein-induced inhibition of oct-4 expression and endothelial differentiation of bone marrow stem cells. Antioxid Redox Signal. 2010; 13: 1845-56.
30. Cai C, Masumiya H, Weisleder N, et al. MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol. 2009; 11: 56-64.
31. Ozato K, Shin DM, Chang TH, et al. TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol. 2008; 8: 849-60.
32. Weisleder N, Takizawa N, Lin P, et al. Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy. Science Transl Med. 2012; 4: 139ra85.
33. Auge N, Nikolova-Karakashian M, Carpentier S, et al. Role of sphingosine 1-phosphate in the mitogenesis induced by oxidized low density lipoprotein in smooth muscle cells via activation of sphingomyelinase, ceramidase, and sphingosine kinase. J Biol Chem. 1999; 274: 21533-8.
34. Cominacini L, Garbin U, Davoli A, et al. A simple test for predisposition to LDL oxidation based on the fluorescence development during copper-catalyzed oxidative modification. J Lipid Res. 1991; 32: 349-58.
35. Zhu H, Lin P, De G, et al. Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J Biol Chem. 2011; 286: 12820-4.
36. Breyer A, Estharabadi N, Oki M, et al. Multipotent adult progenitor cell isolation and culture procedures. Exp Hematol. 2006; 34: 1596-601.
37. Ulloa-Montoya F, Kidder BL, Pauwelyn KA, et al. Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol. 2007; 8: R163.
38. Zhu X, Zuo L, Cardounel AJ, et al. Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium. Antioxid Redox Signal. 2007; 9: 447-55.
39. McNeil PL, Miyake K, Vogel SS. The endomembrane requirement for cell surface repair. Proc Natl Acad Sci USA. 2003; 100: 4592-7.
40. He B, Tang RH, Weisleder N, et al. Enhancing muscle membrane repair by gene delivery of MG53 ameliorates muscular dystrophy and heart failure in delta-Sarcoglycan-deficient hamsters. Mol Ther. 2012; 20: 727-35.
41. Cai CX, Weisleder N, Ko JK, et al. Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3, and dysferlin. J Biol Chem. 2009; 284: 15894-902.
42. Cao CM, Zhang Y, Weisleder N, et al. MG53 constitutes a primary determinant of cardiac ischemic preconditioning. Circulation. 2010; 121: 2565-74.
43. Wang X, Xie W, Zhang Y, et al. Cardioprotection of ischemia/reperfusion injury by cholesterol-dependent MG53-mediated membrane repair. Circ Res. 2010; 107: 76-83.
44. Kohr MJ, Evangelista AM, Ferlito M, et al. S-nitrosylation of TRIM72 at cysteine 144 is critical for protection against oxidation-induced protein degradation and cell death. J Mol Cell Cardiol. 2014; 69: 67-74.
45. X'Avia Chan CY, Wang D, Cadeiras M, et al. S-nitrosylation of TRIM72 mends the broken heart: a molecular modifier-mediated cardioprotection. J Mol Cell Cardiol. 2014; 72C: 292-5.
46. Pervaiz S, Taneja R, Ghaffari S. Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal. 2009; 11: 2777-89.
47. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation. 2003; 108: 457-63.
48. Rizzo M, Kotur-Stevuljevic J, Berneis K, et al. Atherogenic dyslipidemia and oxidative stress: a new look. Transl Res. 2009; 153: 217-23.
49. Rodriguez C, Slevin M, Rodriguez-Calvo R, et al. Modulation of endothelium and endothelial progenitor cell function by low-density lipoproteins: implication for vascular repair, angiogenesis and vasculogenesis. Pathobiology. 2009; 76: 11-22.
50. Sakai M, Miyazaki A, Hakamata H, et al. Lysophosphatidylcholine plays an essential role in the mitogenic effect of oxidized low density lipoprotein on murine macrophages. J Biol Chem. 1994; 269: 31430-5.
51. Salvayre R, Auge N, Benoist H, et al. Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta. 2002; 1585: 213-21.
52. Stocker R, Keaney JF Jr. Role of oxidative modifications in atherosclerosis. Physiol Rev. 2004; 84: 1381-478.
53. Zhang F, Wang C, Jing S, et al. Lectin-like oxidized LDL receptor-1 expresses in mouse bone marrow-derived mesenchymal stem cells and stimulates their proliferation. Exp Cell Res. 2013; 319: 1054-9.
54. Zhang F, Wang C, Wang H, et al. Ox-LDL promotes migration and adhesion of bone marrow-derived mesenchymal stem cells via regulation of MCP-1 expression. Mediators Inflamm. 2013; 2013: 691023.
55. Eto H, Miyata M, Kume N, et al. Expression of lectin-like oxidized LDL receptor-1 in smooth muscle cells after vascular injury. Biochem Biophys Res Commun. 2006; 341: 591-8.
56. Hamilton JA, Myers D, Jessup W, et al. Oxidized LDL can induce macrophage survival, DNA synthesis, and enhanced proliferative response to CSF-1 and GM-CSF. Arterioscler Thromb Vasc Biol. 1999; 19: 98-105.
57. Hundal RS, Salh BS, Schrader JW, et al. Oxidized low density lipoprotein inhibits macrophage apoptosis through activation of the PI 3-kinase/PKB pathway. J Lipid Res. 2001; 42: 1483-91.
58. Matsumura T, Sakai M, Kobori S, et al. Two intracellular signaling pathways for activation of protein kinase C are involved in oxidized low-density lipoprotein-induced macrophage growth. Arterioscler Thromb Vasc Biol. 1997; 17: 3013-20.
59. Namgaladze D, Kollas A, Brune B. Oxidized LDL attenuates apoptosis in monocytic cells by activating ERK signaling. J Lipid Res. 2008; 49: 58-65.
60. Yang CM, Chiu CT, Wang CC, et al. Activation of mitogen-activated protein kinase by oxidized low-density lipoprotein in canine cultured vascular smooth muscle cells. Cell Signal. 2000; 12: 205-14.
61. Chen J, Mehta JL, Haider N, et al. Role of caspases in Ox-LDL-induced apoptotic cascade in human coronary artery endothelial cells. Circ Res. 2004; 94: 370-6.
62. Chen XP, Xun KL, Wu Q, et al. Oxidized low density lipoprotein receptor-1 mediates oxidized low density lipoprotein-induced apoptosis in human umbilical vein endothelial cells: role of reactive oxygen species. Vascul Pharmacol. 2007; 47: 1-9.
63. Bedel A, Negre-Salvayre A, Heeneman S, et al. E-cadherin/beta-catenin/T-cell factor pathway is involved in smooth muscle cell proliferation elicited by oxidized low-density lipoprotein. Circ Res. 2008; 103: 694-701.
64. Deambrosis I, Scalabrino E, Deregibus MC, et al. CD40-dependent activation of phosphatidylinositol 3-kinase/AKT pathway inhibits apoptosis of human cultured mesangial cells induced by oxidized LDL. Int J Immunopathol Pharmacol. 2005; 18: 327-37.
65. Vasconcelos EM, Degasperi GR, de Oliveira HC, et al. Reactive oxygen species generation in peripheral blood monocytes and oxidized LDL are increased in hyperlipidemic patients. Clin Biochem. 2009; 42: 1222-7.
66. Glover L, Brown RH Jr. Dysferlin in membrane trafficking and patch repair. Traffic. 2007; 8: 785-94.
67. Idone V, Tam C, Andrews NW. Two-way traffic on the road to plasma membrane repair. Trends Cell Biol. 2008; 18: 552-9.
68. Martin KA, Siefert JL, Yerrapragada S, et al. Cyanobacterial signature genes. Photosynth Res. 2003; 75: 211-21.
69. McNeil PL, Kirchhausen T. An emergency response team for membrane repair. Nat Rev Mol Cell Biol. 2005; 6: 499-505.
70. Levitan I, Gooch KJ. Lipid rafts in membrane-cytoskeleton interactions and control of cellular biomechanics: actions of oxLDL. Antioxid Redox Signal. 2007; 9: 1519-34.
71. Levitan I, Shentu TP. Impact of oxLDL on cholesterol-rich membrane rafts. J Lipids. 2011; 2011: 730209.
72. Shentu TP, Titushkin I, Singh DK, et al. oxLDL-induced decrease in lipid order of membrane domains is inversely correlated with endothelial stiffness and network formation. Am J Physiol Cell Physiol. 2010; 299: C218-29.