Senescent cells expose and secrete an oxidized form of membrane-bound vimentin as revealed by a natural polyreactive antibody

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 9, 2017, Pages E1668-E1677

  Frescas, David ^a   Roux, Christelle M ^a   Aygun Sunar, Semra ^a   Gleiberman, Anatoli S ^a   Krasnov, Peter ^a   Kurnasov, Oleg V ^b   Strom, Evguenia ^a   Virtuoso, Lauren P ^a   Wrobel, Michelle ^a   Osterman, Andrei L ^b   Antoch, Marina P ^c   Mett, Vadim ^a   Chernov, Olga B ^a   Gudkov, Andrei V ^a,c  

^a Everon Biosciences   (United States)

^b BURNHAM INSTITUTE   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Aging; Biomarker; Malondialdehyde; Oxidative posttranslational modifications; SAMP8

Indexed keywords

IMMUNOGLOBULIN M ANTIBODY; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; VIMENTIN; ANTIBODY; BETA GALACTOSIDASE; BIOLOGICAL MARKER; IMMUNOGLOBULIN M;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL AGING; CELL FRACTIONATION; CELL SURFACE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; INNATE IMMUNITY; INTERMEDIATE FILAMENT; LUNG FIBROBLAST; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; SENESCENCE; SKIN FIBROBLAST; SURFACE PROPERTY; TISSUE CULTURE CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; FIBROBLAST; HUMORAL IMMUNITY; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIBODIES; BETA-GALACTOSIDASE; BIOMARKERS; CELL MEMBRANE; CELLS, CULTURED; CELLULAR SENESCENCE; FEMALE; FIBROBLASTS; IMMUNITY, HUMORAL; IMMUNITY, INNATE; IMMUNOGLOBULIN M; INTERMEDIATE FILAMENTS; MALONDIALDEHYDE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; REACTIVE OXYGEN SPECIES; VIMENTIN;

EID: 85014248635     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1614661114     Document Type: Article

References (108)

1. Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621.
2. Bodnar AG, et al. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279(5349):349-352.
3. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88(5):593-602.
4. Rodier F, et al. (2009) Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11(8):973-979.
5. Coppé JP, et al. (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6(12):2853-2868.
6. Kuilman T, Peeper DS (2009) Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 9(2):81-94.
7. Brack AS, et al. (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807-810.
8. Krtolica A, et al. (2011) GROα regulates human embryonic stem cell self-renewal or adoption of a neuronal fate. Differentiation 81(4):222-232.
9. Pricola KL, Kuhn NZ, Haleem-Smith H, Song Y, Tuan RS (2009) Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. J Cell Biochem 108(3):577-588.
10. Krizhanovsky V, et al. (2008) Senescence of activated stellate cells limits liver fibrosis. Cell 134(4):657-667.
11. Xue W, et al. (2007) Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445(7128):656-660.
12. Lawless C, et al. (2010) Quantitative assessment of markers for cell senescence. Exp Gerontol 45(10):772-778.
13. van Deursen JM (2014) The role of senescent cells in ageing. Nature 509(7501):439-446.
14. Kang C, et al. (2015) The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 349(6255):aaa5612.
15. Sagiv A, Krizhanovsky V (2013) Immunosurveillance of senescent cells: The bright side of the senescence program. Biogerontology 14(6):617-628.
16. Grönwall C, Vas J, Silverman GJ (2012) Protective roles of natural IgM antibodies. Front Immunol 3:66.
17. Vas J, Grönwall C, Silverman GJ (2013) Fundamental roles of the innate-like repertoire of natural antibodies in immune homeostasis. Front Immunol 4:4.
18. Panda S, Ding JL (2015) Natural antibodies bridge innate and adaptive immunity. J Immunol 194(1):13-20.
19. Lutz HU, Binder CJ, Kaveri S (2009) Naturally occurring auto-antibodies in homeostasis and disease. Trends Immunol 30(1):43-51.
20. Grönwall C, et al. (2012) IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin Immunol 142(3):390-398.
21. Lujambio A, et al. (2013) Non-cell-autonomous tumor suppression by p53. Cell 153(2):449-460.
22. Shimizu S, Sugai S, Konda S, Yamanaka Y, Setoyama M (1986) A monoclonal surface immunoglobulin (IgM/D-L) with specificity for surface antigen of ox red blood cells in a patient with leukemic lymphosarcoma. J Clin Immunol 6(5):397-401.
23. Satelli A, Li S (2011) Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 68(18):3033-3046.
24. Binder CJ (2012) Naturally occurring IgM antibodies to oxidation-specific epitopes. Adv Exp Med Biol 750:2-13.
25. Pastan I, et al. (1993) PR1-A monoclonal antibody that reacts with an antigen on the surface of normal and malignant prostate cells. J Natl Cancer Inst 85(14):1149-1154.
26. Inagaki T, et al. (1993) [Effective removal of the contaminating host fibroblasts for establishment of human-tumor cultured lines]. Hum Cell 6(2):137-142. Japanese.
27. Tsiantoulas D, Diehl CJ, Witztum JL, Binder CJ (2014) B cells and humoral immunity in atherosclerosis. Circ Res 114(11):1743-1756.
28. Belmokhtar CA, Hillion J, Ségal-Bendirdjian E (2001) Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene 20(26):3354-3362.
29. Shaw PX, et al. (2000) Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest 105(12):1731-1740.
30. Chou MY, et al. (2009) Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest 119(5):1335-1349.
31. Amir S, et al. (2012) Peptide mimotopes of malondialdehyde epitopes for clinical applications in cardiovascular disease. J Lipid Res 53(7):1316-1326.
32. Tuominen A, et al. (2006) A natural antibody to oxidized cardiolipin binds to oxidized low-density lipoprotein, apoptotic cells, and atherosclerotic lesions. Arterioscler Thromb Vasc Biol 26(9):2096-2102.
33. Esterre P, Melin M, Serrar M, Grimaud JA (1992) New specific markers of human and mouse fibroblasts. Cell Mol Biol 38(3):297-301.
34. Nishio K, Inoue A, Qiao S, Kondo H, Mimura A (2001) Senescence and cytoskeleton: Overproduction of vimentin induces senescent-like morphology in human fibroblasts. Histochem Cell Biol 116(4):321-327.
35. Chen C, Stenzel-Poore MP, Rittenberg MB (1991) Natural auto- and polyreactive antibodies differing from antigen-induced antibodies in the H chain CDR3. J Immunol 147(7):2359-2367.
36. Tsiantoulas D, et al. (2015) Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies. J Lipid Res 56(2):440-448.
37. Horkovics-Kovats S, Traub P (1990) Specific interaction of the intermediate filament protein vimentin and its isolated N-terminus with negatively charged phospholipids as determined by vesicle aggregation, fusion, and leakage measurements. Biochemistry 29(37):8652-8657.
38. Perides G, Harter C, Traub P (1987) Electrostatic and hydrophobic interactions of the intermediate filament protein vimentin and its amino terminus with lipid bilayers. J Biol Chem 262(28):13742-13749.
39. Bilalic S, et al. (2012) Lymphocyte activation induces cell surface expression of an immunogenic vimentin isoform. Transpl Immunol 27(2-3):101-106.
40. Huet D, et al. (2006) SC5 mAb represents a unique tool for the detection of extracellular vimentin as a specific marker of Sezary cells. J Immunol 176(1):652-659.
41. Mitra A, et al. (2015) Cell-surface vimentin: A mislocalized protein for isolating csVimentin(+) CD133(-) novel stem-like hepatocellular carcinoma cells expressing EMT markers. Int J Cancer 137(2):491-496.
42. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM (2003) Vimentin is secreted by activated macrophages. Nat Cell Biol 5(1):59-63.
43. Moisan E, Girard D (2006) Cell surface expression of intermediate filament proteins vimentin and lamin B1 in human neutrophil spontaneous apoptosis. J Leukoc Biol 79(3):489-498.
44. Kueper T, et al. (2007) Vimentin is the specific target in skin glycation. Structural prerequisites, functional consequences, and role in skin aging. J Biol Chem282(32):23427-23436.
45. Pamplona R, et al. (2005) Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. Effects of Alzheimer disease and identification of lipoxidation targets. J Biol Chem 280(22):21522-21530.
46. Spurny R, et al. (2007) Oxidation and nitrosylation of cysteines proximal to the intermediate filament (IF)-binding site of plectin: Effects on structure and vimentin binding and involvement in IF collapse. J Biol Chem 282(11):8175-8187.
47. Rogers KR, Morris CJ, Blake DR (1991) Oxidation of thiol in the vimentin cytoskeleton. Biochem J 275(Pt 3):789-791.
48. Pérez-Sala D, et al. (2015) Vimentin filament organization and stress sensing depend on its single cysteine residue and zinc binding. Nat Commun 6:7287.
49. Garzón B, Oeste CL, Díez-Dacal B, Pérez-Sala D (2011) Proteomic studies on protein modification by cyclopentenone prostaglandins: Expanding our view on electrophile actions. J Proteomics 74(11):2243-2263.
50. Traub P, Perides G, Kühn S, Scherbarth A (1987) Efficient interaction of nonpolar lipids with intermediate filaments of the vimentin type. Eur J Cell Biol 43(1):55-64.
51. Bhattacharya R, et al. (2009) Recruitment of vimentin to the cell surface by beta3 integrin and plectin mediates adhesion strength. J Cell Sci 122(Pt 9):1390-1400.
52. Morley JE, Farr SA, Kumar VB, Armbrecht HJ (2012) The SAMP8 mouse: A model to develop therapeutic interventions for Alzheimer's disease. Curr Pharm Des 18(8):1123-1130.
53. He XL, Zhou WQ, Bi MG, Du GH (2010) Neuroprotective effects of icariin on memory impairment and neurochemical deficits in senescence-accelerated mouse prone 8 (SAMP8) mice. Brain Res 1334:73-83.
54. Akbor MM, et al. (2013) Possible involvement of Hcn1 ion channel in learning and memory dysfunction in SAMP8 mice. Biochem Biophys Res Commun 441(1):25-30.
55. Nomura Y, Okuma Y (1999) Age-related defects in lifespan and learning ability in SAMP8 mice. Neurobiol Aging 20(2):111-115.
56. Tomobe K, Nomura Y (2009) Neurochemistry, neuropathology, and heredity in SAMP8: A mouse model of senescence. Neurochem Res 34(4):660-669.
57. Tomobe K, Shinozuka T, Kawashima T, Kawashima-Ohya Y, Nomura Y (2013) Agerelated changes of forkhead transcription factor FOXO1 in the liver of senescenceaccelerated mouse SAMP8. Arch Gerontol Geriatr 57(3):417-422.
58. Tomobe K, Shinozuka T, Kuroiwa M, Nomura Y (2012) Age-related changes of Nrf2 and phosphorylated GSK-3β in a mouse model of accelerated aging (SAMP8). Arch Gerontol Geriatr 54(2):e1-e7.
59. Cuesta S, et al. (2010) Melatonin improves inflammation processes in liver of senescence- accelerated prone male mice (SAMP8). Exp Gerontol 45(12):950-956.
60. Crisby M, Henareh L, Agewall S (2014) Relationship between oxidized LDL, IgM, and IgG autoantibodies to ox-LDL levels with recurrent cardiovascular events in Swedish patients with previous myocardial infarction. Angiology 65(10):932-936.
61. van Leeuwen M, et al. (2009) The IgM response to modified LDL in experimental atherosclerosis: hypochlorite-modified LDL IgM antibodies versus classical natural T15 IgM antibodies. Ann N Y Acad Sci 1173:274-279.
62. Su J, et al. (2006) Antibodies of IgM subclass to phosphorylcholine and oxidized LDL are protective factors for atherosclerosis in patients with hypertension. Atherosclerosis 188(1):160-166.
63. Ravandi A, et al. (2011) Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: Results from the EPIC-Norfolk Study. J Lipid Res 52(10):1829-1836.
64. Garrido-Sánchez L, Chinchurreta P, García-Fuentes E, Mora M, Tinahones FJ (2010) a higher level of IgM anti-oxidized LDL antibodies is associated with a lower severity of coronary atherosclerosis in patients on statins. Int J Cardiol 145(2):263-264.
65. de Faire U, et al. (2010) Low levels of IgM antibodies to phosphorylcholine predict cardiovascular disease in 60-year old men: Effects on uptake of oxidized LDL in macrophages as a potential mechanism. J Autoimmun 34(2):73-79.
66. Klein-Schneegans AS, Kuntz L, Trembleau S, Fonteneau P, Loor F (1990) Serum concentrations of IgM, IgG1, IgG2b, IgG3 and IgA in C57BL/6 mice and their congenics at the nu(nude)locus. Thymus 16(1):45-54.
67. Singer KH, et al. (1989) Removal of fibroblasts from human epithelial cell cultures with use of a complement fixing monoclonal antibody reactive with human fibroblasts and monocytes/macrophages. J Invest Dermatol 92(2):166-170.
68. Jackson KJ, et al. (2012) Divergent human populations show extensive shared IGK rearrangements in peripheral blood B cells. Immunogenetics 64(1):3-14.
69. Hardy RR (2006) B-1 B cell development. J Immunol 177(5):2749-2754.
70. Ochsenbein AF, et al. (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286(5447):2156-2159.
71. deCathelineau AM, Henson PM (2003) The final step in programmed cell death: Phagocytes carry apoptotic cells to the grave. Essays Biochem 39:105-117.
72. Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ (2003) The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neoantigens and apoptotic cells. J Immunol 170(12):6151-6157.
73. Litvack ML, et al. (2010) Natural IgM and innate immune collectin SP-D bind to late apoptotic cells and enhance their clearance by alveolar macrophages in vivo. Mol Immunol 48(1-3):37-47.
74. Litvack ML, Post M, Palaniyar N (2011) IgM promotes the clearance of small particles and apoptotic microparticles by macrophages. PLoS One 6(3):e17223.
75. Starr AE, Bellac CL, Dufour A, Goebeler V, Overall CM (2012) Biochemical characterization and N-terminomics analysis of leukolysin, the membrane-type 6 matrix metalloprotease (MMP25): Chemokine and vimentin cleavages enhance cell migration and macrophage phagocytic activities. J Biol Chem 287(16):13382-13395.
76. Boilard E, Bourgoin SG, Bernatchez C, Surette ME (2003) Identification of an autoantigen on the surface of apoptotic human T cells as a new protein interacting with inflammatory group IIA phospholipase A2. Blood 102(8):2901-2909.
77. IseH, GotoM, Komura K, Akaike T (2012) Engulfment and clearance of apoptotic cells based on a GlcNAc-binding lectin-like property of surface vimentin. Glycobiology 22(6):788-805.
78. Chen Y, Park YB, Patel E, Silverman GJ (2009) IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J Immunol 182(10):6031-6043.
79. Kofler R, Dixon FJ, Theofilopoulos AN (1987) The genetic origin of autoantibodies. Immunol Today 8(12):374-380.
80. Leibundgut G, et al. (2012) Oxidized phospholipids are present on plasminogen, affect fibrinolysis, and increase following acutemyocardial infarction. J AmColl Cardiol 59(16):1426-1437.
81. Oeste CL, Pérez-Sala D (2014) Modification of cysteine residues by cyclopentenone prostaglandins: Interplay with redox regulation of protein function. Mass Spectrom Rev 33(2):110-125.
82. Gharbi S, Garzón B, Gayarre J, Timms J, Pérez-Sala D (2007) Study of protein targets for covalent modification by the antitumoral and anti-inflammatory prostaglandin PGA1: Focus on vimentin. J Mass Spectrom 42(11):1474-1484.
83. Hong SH, et al. (2006) Identification of a specific vimentin isoform that induces an antibody response in pancreatic cancer. Biomark Insights 1:175-183.
84. Satelli A, Brownlee Z, Mitra A, Meng QH, Li S (2015) Circulating tumor cell enumeration with a combination of epithelial cell adhesion molecule- and cell-surface vimentin-based methods for monitoring breast cancer therapeutic response. Clin Chem 61(1):259-266.
85. Satelli A, et al. (2014) Universal marker and detection tool for human sarcoma circulating tumor cells. Cancer Res 74(6):1645-1650.
86. Darvin K, et al. (2014) Plasma protein biomarkers of the geriatric syndrome of frailty. J Gerontol A Biol Sci Med Sci 69(2):182-186.
87. Shamsi KS, et al. (2012) Proteomic screening of glycoproteins in human plasma for frailty biomarkers. J Gerontol A Biol Sci Med Sci 67(8):853-864.
88. Tanisawa K, et al. (2013) Exome sequencing of senescence-accelerated mice (SAM) reveals deleterious mutations in degenerative disease-causing genes. BMC Genomics 14:248.
89. Smith CG, et al. (2013) Role of the oxidative DNA damage repair gene OGG1 in colorectal tumorigenesis. J Natl Cancer Inst 105(16):1249-1253.
90. Smith TB, et al. (2013) The presence of a truncated base excision repair pathway in human spermatozoa that is mediated by OGG1. J Cell Sci 126(Pt 6):1488-1497.
91. Choi JY, et al. (1999) Thermolabile 8-hydroxyguanine DNA glycosylase with low activity in senescence-accelerated mice due to a single-base mutation. Free Radic Biol Med 27(7-8):848-854.
92. Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143-166.
93. Krokan HE, et al. (2014) Error-free versus mutagenic processing of genomic uracil- Relevance to cancer. DNA Repair (Amst) 19:38-47.
94. Baker DJ, et al. (2004) BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36(7):744-749.
95. Kapanidou M, Lee S, Bolanos-Garcia VM (2015) BubR1 kinase: Protection against aneuploidy and premature aging. Trends Mol Med 21(6):364-372.
96. Salminen A, et al. (2011) Astrocytes in the aging brain express characteristics of senescence- associated secretory phenotype. Eur J Neurosci 34(1):3-11.
97. Gan W, et al. (2012) Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: Urinary 8-oxoguanosine as a novel biomarker of aging. Free Radic Biol Med 52(9):1700-1707.
98. Miller YI, Tsimikas S (2013) Oxidation-specific epitopes as targets for biotheranostic applications in humans: Biomarkers, molecular imaging and therapeutics. Curr Opin Lipidol 24(5):426-437.
99. Fruhwirth GO, Loidl A, Hermetter A (2007) Oxidized phospholipids: From molecular properties to disease. Biochim Biophys Acta 1772(7):718-736.
100. Holt PG, et al. (1985) Preparation of interstitial lung cells by enzymatic digestion of tissue slices: Preliminary characterization by morphology and performance in functional assays. Immunology 54(1):139-147.
101. Lyadova I, et al. (1998) An ex vivo study of T lymphocytes recovered from the lungs of I/St mice infected with and susceptible to Mycobacterium tuberculosis. Infect Immun 66(10):4981-4988.
102. Baglole CJ, et al. (2005) Isolation and phenotypic characterization of lung fibroblasts. Methods Mol Med 117:115-127.
103. Seluanov A, Vaidya A, Gorbunova V (2010) Establishing primary adult fibroblast cultures from rodents. J Vis Exp (44):2033.
104. Kapina MA, Rubakova EI, Majorov KB, Logunova NN, Apt AS (2013) Capacity of lung stroma to educate dendritic cells inhibiting mycobacteria-specific T-cell response depends upon genetic susceptibility to tuberculosis. PLoS One 8(8):e72773.
105. Di Leonardo A, Linke SP, Clarkin K, Wahl GM (1994) DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev 8(21):2540-2551.
106. Aoshiba K, Tsuji T, Nagai A (2003) Bleomycin induces cellular senescence in alveolar epithelial cells. Eur Respir J 22(3):436-443.
107. Frescas D, Guardavaccaro D, Bassermann F, Koyama-Nasu R, Pagano M (2007) JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature 450(7167):309-313.
108. Xu B, et al. (2004) The endothelial cell-specific antibody PAL-E identifies a secreted form of vimentin in the blood vasculature. Mol Cell Biol 24(20):9198-9206.