Identification of mammary epithelial cells subject to chronic oxidative stress in mammary epithelium of young women and teenagers living in USA: Implication for breast carcinogenesis

Cancer Biology and Therapy

Volumn 13, Issue 2, 2012, Pages 101-113

  Weisz, Judith ^a   Shearer, Debra A ^a   Murata, Erin ^c   Patrick, Susan D ^a,b   Han, Bing ^a   Berg, Arthur ^d   Clawson, Gary A ^a,b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b PENN STATE CANCER INSTITUTE   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; ANTIOXIDANT; DNA; GLUTATHIONE PEROXIDASE; PEROXIDASE; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ACUTE STRESS; ADOLESCENT; ADULT; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CELLULAR STRESS RESPONSE; CHRONIC STRESS; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE EXPRESSION; GENE FUNCTION; GROUPS BY AGE; HISTOLOGY; HOUSEKEEPING GENE; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MICROARRAY ANALYSIS; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNITED STATES; WESTERN BLOTTING;

ADOLESCENT; ADULT; ALDEHYDES; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; EPITHELIUM; FEMALE; GENE EXPRESSION PROFILING; GENES, ESSENTIAL; HUMANS; MAMMARY GLANDS, HUMAN; OXIDATIVE STRESS; REPRODUCIBILITY OF RESULTS; UNITED STATES; YOUNG ADULT;

EID: 84856692524     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.13.2.18873     Document Type: Article

References (101)

1. Selikoff IJ, Hammond EC, Seidman H. Latency of asbestos disease among insulation workers in the United States and Canada. Cancer 1980; 46:2736-40; PMID: 7448712; http://dx.doi.org/10.1002/1097-0142(19801215)46:12,2736::AID- CNCR2820461233.3.0.CO;2-L
2. Selikoff IJ. Lessons for living in a chemical world. Bull Environ Contam Toxicol 1984; 33:682-95; PMID: 6394072; http://dx.doi.org/10.1007/BF01625600
3. Weiss W. Cigarette smoking and lung cancer trends. A light at the end of the tunnel? Chest 1997; 111:1414-6; PMID:9149602; http://dx.doi.org/10.1378/ chest.111.5.1414
4. Miyakawa M, Tachibana M, Miyakawa A, Yoshida K, Shimada N, Murai M, et al. Re-evaluation of the latent period of bladder cancer in dyestuff-plant workers in Japan. Int J Urol 2001; 8:423-30; PMID:11555006; http://dx.doi.org/ 10.1046/j.1442-2042.2001.00342.x
5. Archer VE, Coons T, Saccomanno G, Hong DY. Latency and the lung cancer epidemic among United States uranium miners. Health Phys 2004; 87:480-9; PMID:15551786; http://dx.doi.org/10.1097/01.HP.0000133216.72557.ab
6. Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, et al. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res 2007; 168:1-64; PMID:17722996; http://dx.doi.org/10.1667/RR0763.1
7. Finkelstein MM. Absence of radiographic asbestosis and the risk of lung cancer among asbestos-cement workers: Extended follow-up of a cohort. Am J Ind Med 2010; 53:1065-9; PMID:20672325; http://dx.doi.org/10.1002/ajim.20881
8. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11: 81-128; PMID:1937131; http://dx.doi.org/10.1016/0891-5849(91)90192-6
9. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003; 42:318-43; PMID:12689622; http://dx.doi.org/10. 1016/S0163-7827(03)00014-6
10. Dubinina EE, Dadali VA. Role of 4-hydroxy-trans-2- nonenal in cell functions. Biochemistry (Mosc) 2010; 75:1069-87; PMID:21077827; http://dx.doi.org/10.1134/S0006297910090014
11. Jürgens G, Chen Q, Esterbauer H, Mair S, Ledinski G, Dinges HP. Immunostaining of human autopsy aortas with antibodies to modified apolipoprotein B and apoprotein(a). Arterioscler Thromb 1993; 13: 1689-99; PMID:7692957; http://dx.doi.org/10.1161/01.ATV.13.11.1689
12. Uchida K, Toyokuni S, Nishikawa K, Kawakishi S, Oda H, Hiai H, et al. Michael addition-type 4-hydroxy-2-nonenal adducts in modified low-density lipoproteins: markers for atherosclerosis. Biochemistry 1994; 33:12487-94; PMID:7918471; http://dx.doi.org/10.1021/bi00207a016
13. Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, et al. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 1999; 48:927-32; PMID:10102716; http://dx.doi.org/10.2337/diabetes.48.4.927
14. Guéraud F, Atalay M, Bresgen N, Cipak A, Eckl PM, Huc L, et al. Chemistry and biochemistry of lipid peroxidation products. Free Radic Res 2010; 44:1098-124; PMID:20836659; http://dx.doi.org/10.3109/10715762.2010.498477
15. Halliwell B. Oxidative stress and cancer: have we moved forward? Biochem J 2007; 401:1-11; PMID:17150040; http://dx.doi.org/10.1042/BJ20061131
16. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 2010; 38:96-109; PMID:20019356; http://dx.doi.org/10.1177/0192623309356453
17. Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A. DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res 2011; 711:13-27.
18. Maulik N, Yoshida T, Engelman RM, Deaton D, Flack JE, 3rd, Rousou JA, et al. Ischemic preconditioning attenuates apoptotic cell death associated with ischemia/reperfusion. Mol Cell Biochem 1998; 186: 139-45; PMID:9774195; http://dx.doi.org/10.1023/A:1006883717174
19. Ravati A, Ahlemeyer B, Becker A, Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 2000; 866:23-32; PMID:10825477; http://dx.doi.org/10.1016/S0006-8993(00)02210-1
20. Pohlman TH, Harlan JM. Adaptive responses of the endothelium to stress. J Surg Res 2000; 89:85-119; PMID:10720457; http://dx.doi.org/10.1006/jsre.1999. 5801
21. Eneman JD, Potts RJ, Osier M, Shukla GS, Lee CH, Chiu JF, et al. Suppressed oxidant-induced apoptosis in cadmium adapted alveolar epithelial cells and its potential involvement in cadmium carcinogenesis. Toxicology 2000; 147:215-28; PMID:10924803; http://dx.doi.org/10.1016/S0300-483X(00)00215-8
22. Rüdiger HA, Graf R, Clavien PA. Sub-lethal oxidative stress triggers the protective effects of ischemic preconditioning in the mouse liver. J Hepatol 2003; 39:972-7; PMID:14642614; http://dx.doi.org/10.1016/S0168-8278(03) 00415-X
23. Wu HH, Hsiao TY, Chien CT, Lai MK. Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced apoptosis and autophagy in the rat. J Biomed Sci 2009; 16:19; PMID: 19272187; http://dx.doi.org/10.1186/1423-0127-16-19
24. Wang L, Li W, Kang Z, Liu Y, Deng X, Tao H, et al. Hyperbaric oxygen preconditioning attenuates early apoptosis after spinal cord ischemia in rats. J Neurotrauma 2009; 26:55-66; PMID:19196076; http://dx.doi.org/10.1089/neu.2008. 0538
25. Sharma RK, Netland PA, Kedrov MA, Johnson DA. Preconditioning protects the retinal pigment epithelium cells from oxidative stress-induced cell death. Acta Ophthalmol 2009; 87:82-8; PMID:18494742; http:// dx.doi.org/10.1111/j.1755- 3768.2008.01170.x
26. Martyniuk CJ, Feswick A, Spade DJ, Kroll KJ, Barber DS, Denslow ND. Effects of acute dieldrin exposure on neurotransmitters and global gene transcription in largemouth bass (Micropterus salmoides) hypothalamus. Neurotoxicology 2010; 31:356-66; PMID:20438755; http://dx.doi.org/10.1016/j. neuro.2010.04.008
27. Martyniuk CJ, Kroll KJ, Doperalski NJ, Barber DS, Denslow ND. Genomic and proteomic responses to environmentally relevant exposures to dieldrin: indicators of neurodegeneration? Toxicol Sci 2010; 117: 190-9; PMID:20584760; http://dx.doi.org/10.1093/toxsci/kfq192
28. Yu HJ, Chien CT, Lai YJ, Lai MK, Chen CF, Levin RM, et al. Hypoxia preconditioning attenuates bladder overdistension-induced oxidative injury by up-regulation of Bcl-2 in the rat. J Physiol 2004; 554:815-28; PMID:14608004; http://dx.doi.org/10. 1113/jphysiol.2003.056002
29. Tang XQ, Feng JQ, Chen J, Chen PX, Zhi JL, Cui Y, et al. Protection of oxidative preconditioning against apoptosis induced by H2O2 in PC12 cells: mechanisms via MMP, ROS, and Bcl-2. Brain Res 2005; 1057:57-64; PMID:16129420; http://dx.doi.org/10.1016/j.brainres.2005.07.072
30. Halestrap AP, Clarke SJ, Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim Biophys Acta 2007; 1767:1007-1031; PMID:17631856; http://dx.doi.org/10.1016/j.bbabio.2007.05.008
31. Choi H, Kim SH, Chun YS, Cho YS, Park JW, Kim MS. In vivo hyperoxic preconditioning prevents myocardial infarction by expressing bcl-2. Exp Biol Med (Maywood) 2006; 231:463-72; PMID:16565442
32. Goodman MF. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 2002; 71:17-50; PMID:12045089; http://dx.doi.org/ 10.1146/annurev.biochem.71.083101.124707
33. Clémenson C, Marsolier-Kergoat MC. DNA damage checkpoint inactivation: adaptation and recovery. DNA Repair (Amst) 2009; 8:1101-9; PMID:19464963; http://dx.doi.org/10.1016/j.dnarep.2009.04.008
34. Chang DJ, Cimprich KA. DNA damage tolerance: when it's OK to make mistakes. Nat Chem Biol 2009; 5:82-90; PMID:19148176; http://dx.doi.org/10.1038/ nchembio.139
35. Muir CS. Epidemiology of cancer in ethnic groups. Br J Cancer Suppl 1996; 29:S12-6; PMID:8782793
36. President's Cancer Panel 2008-2009 Annual Report: April 2010,
37. Hellmold H, Rylander T, Magnusson M, Reihner E, Warner M, Gustafsson JA. Characterization of cytochrome P450 enzymes in human breast tissue from reduction mammaplasties. J Clin Endocrinol Metab 1998; 83:886-95; PMID:9506744; http://dx.doi.org/10.1210/jc.83.3.886
38. Tannheimer SL, Barton SL, Ethier SP, Burchiel SW. Carcinogenic polycyclic aromatic hydrocarbons increase intracellular Ca2+ and cell proliferation in primary human mammary epithelial cells. Carcinogenesis 1997; 18:1177-82; PMID:9214600; http://dx.doi.org/10.1093/carcin/18.6.1177
39. Williams JA, Stone EM, Millar BC, Gusterson BA, Grover PL, Phillips DH. Determination of the enzymes responsible for activation of the heterocyclic amine 2-amino-3-methylimidazo[4,5-f]quinoline in the human breast. Pharmacogenetics 1998; 8: 519-28; PMID:9918136; http://dx.doi.org/10.1097/ 00008571-199812000-00009
40. Jefcoate CR, Liehr JG, Santen RJ, Sutter TR, Yager JD, Yue W, et al. Tissue-specific synthesis and oxidative metabolism of estrogens. J Natl Cancer Inst Monogr 2000; 27:95-112; PMID:10963622
41. Haas S, Pierl C, Harth V, Pesch B, Rabstein S, Bruning T, et al. Expression of xenobiotic and steroid hormone metabolizing enzymes in human breast carcinomas. Int J Cancer 2006; 119:1785-91; PMID: 16721811; http://dx.doi.org/10.1002/ijc.21915
42. Triano EA, Slusher LB, Atkins TA, Beneski JT, Gestl SA, Zolfaghari R, et al. Class I alcohol dehydrogenase is highly expressed in normal human mammary epithelium but not in invasive breast cancer: implications for breast carcinogenesis. Cancer Res 2003; 63:3092-100; PMID:12810634
43. Jonker JW, Merino G, Musters S, van Herwaarden AE, Bolscher E, Wagenaar E, et al. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 2005; 11:127-9; PMID:15685169; http://dx.doi.org/10.1038/nm1186
44. van Herwaarden AE, Wagenaar E, Merino G, Jonker JW, Rosing H, Beijnen JH, et al. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Mol Cell Biol 2007; 27:1247-53; PMID:17145775; http://dx.doi.org/10.1128/MCB.01621-06
45. Martin FL, Carmichael PL, Crofton-Sleigh C, Venitt S, Phillips DH, Grover PL. Genotoxicity of human mammary lipid. Cancer Res 1996; 56:5342-6; PMID: 8968081
46. Phillips DH, Martin FL, Williams JA, Wheat LM, Nolan L, Cole KJ, et al. Mutagens in human breast lipid and milk: the search for environmental agents that initiate breast cancer. Environ Mol Mutagen 2002; 39:143-9; PMID:11921182; http://dx.doi.org/10.1002/em.10049
47. Martin FL. Genotoxins and the initiation of sporadic breast cancer. Mutagenesis 2001; 16:155-61; PMID: 11230559; http://dx.doi.org/10.1093/mutage/ 16.2.155
48. Mattson MP. Dietary factors, hormesis and health. Ageing Res Rev 2008; 7:43-8; PMID:17913594; http://dx.doi.org/10.1016/j.arr.2007.08.004
49. Hulbert AJ. Metabolism and longevity: is there a role for membrane fatty acids? Integr Comp Biol 2010; 50:808-17; PMID:21558243; http://dx.doi.org/10. 1093/icb/icq007
50. Boice JD, Jr., Friis S, McLaughlin JK, Mellemkjaer L, Blot WJ, Fraumeni JF, et al. Cancer following breast reduction surgery in Denmark. Cancer Causes Control 1997; 8:253-8; PMID:9134250; http://dx.doi.org/10.1023/A:1018484616598
51. Colwell AS, Kukreja J, Breuing KH, Lester S, Orgill DP. Occult breast carcinoma in reduction mammaplasty specimens: 14-year experience. Plast Reconstr Surg 2004; 113:1984-8; PMID:15253187; http://dx.doi.org/10.1097/01.PRS. 0000122212.37703.6E
52. Dotto J, Kluk M, Geramizadeh B, Tavassoli FA. Frequency of clinically occult intraepithelial and invasive neoplasia in reduction mammoplasty specimens: a study of 516 cases. Int J Surg Pathol 2008; 16: 25-30; PMID:18203780; http://dx.doi.org/10.1177/1066896907307176
53. Karpinets TV, Foy BD. Tumorigenesis: the adaptation of mammalian cells to sustained stress environment by epigenetic alterations and succeeding matched mutations. Carcinogenesis 2005; 26:1323-34; PMID: 15802302; http://dx.doi.org/ 10.1093/carcin/bgi079
54. Heng HH, Stevens JB, Bremer SW, Ye KJ, Liu G, Ye CJ. The evolutionary mechanism of cancer. J Cell Biochem 2010; 109:1072-84; PMID:20213744
55. Hart BA, Potts RJ, Watkin RD.**Cadmium adaptation in the lung - a double-edged sword? Toxicology 2001; 160:65-70; PMID:11246125; http://dx.doi.org/10.1016/S0300-483X(00)00436-4
56. Thijssen S, Cuypers A, Maringwa J, Smeets K, Horemans N, Lambrichts I, et al. Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 2007; 236:29-41; PMID: 17499415; http://dx.doi.org/10.1016/ j.tox.2007.03.022
57. Zoller LC, Weisz J. A demonstration of regional differences in lysosome membrane permeability in the membrana granulosa of Graafian follicles in cryostat sections of the rat ovary: a quantitative cytochemical study. Endocrinology 1980; 106:871-7; PMID: 7353547; http://dx.doi.org/10.1210/endo- 106-3-871
58. Palinski W, Yla-Herttuala S, Rosenfeld ME, Butler SW, Socher SA, Parthasarathy S, et al. Antisera and monoclonal antibodies specific for epitopes generated during oxidative modification of low density lipoprotein. Arteriosclerosis 1990; 10:325-35; PMID: 1693068; http://dx.doi.org/10.1161/01. ATV.10.3.325
59. Russo J, Russo IH. Influence of differentiation and cell kinetics on the susceptibility of the rat mammary gland to carcinogenesis. Cancer Res 1980; 40:2677-87; PMID:7388818
60. Kenney NJ, Smith GH, Lawrence E, Barrett JC, Salomon DS. Identification of stem cell units in the terminal end bud and duct of the mouse mammary gland. J Biomed Biotechnol 2001; 1:133-43; PMID:12488607; http://dx.doi.org/10.1155/ S1110724301000304
61. Bai L, Rohrschneider LR. s-SHIP promoter expression marks activated stem cells in developing mouse mammary tissue. Genes Dev 2010; 24:1882-92; PMID: 20810647; http://dx.doi.org/10.1101/gad.1932810
62. Wood CE, Hester JM, Cline JM. Mammary gland development in early pubertal female macaques. Toxicol Pathol 2007; 35:795-805; PMID:17943653; http://dx.doi.org/10.1080/01926230701584213
63. Grune T, Michel P, Sitte N, Eggert W, Albrecht-Nebe H, Esterbauer H, et al. Increased levels of 4-hydroxynonenal modified proteins in plasma of children with autoimmune diseases. Free Radic Biol Med 1997; 23: 357-60; PMID:9214570; http://dx.doi.org/10.1016/S0891-5849(96)00586-2
64. Waeg G, Dimsity G, Esterbauer H. Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins. Free Radic Res 1996; 25:149-59; PMID:8885333; http://dx.doi.org/10.3109/10715769609149920
65. Chua PJ, Yip GW, Bay BH. Cell cycle arrest induced by hydrogen peroxide is associated with modulation of oxidative stress related genes in breast cancer cells. Exp Biol Med (Maywood) 2009; 234:1086-94; PMID: 19596828; http://dx.doi.org/10.3181/0903-RM-98
66. Feltens R, Mogel I, Roder-Stolinski C, Simon JC, Herberth G, Lehmann I. Chlorobenzene induces oxidative stress in human lung epithelial cells in vitro. Toxicol Appl Pharmacol 2010; 242:100-8; PMID: 19800902; http://dx.doi.org/10. 1016/j.taap.2009.09.020
67. Huang CC, Aronstam RS, Chen DR, Huang YW. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol In Vitro 2010; 24:45-55; PMID:19755143; http://dx.doi.org/10.1016/j.tiv.2009.09.007
68. Higgins LG, Hayes JD. Mechanisms of induction of cytosolic and microsomal glutathione transferase (GST) genes by xenobiotics and pro-inflammatory agents. Drug Metab Rev 2011; 43:92-137; PMID:21495793; http:// dx.doi.org/10.3109/ 03602532.2011.567391
69. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, et al. A novel p53- inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF). FEBS Lett 2002; 524:163-71; PMID:12135761; http://dx.doi.org/10.1016/S0014-5793(02)03049-1
70. Josephy PD. The role of peroxidase-catalyzed activation of aromatic amines in breast cancer. Mutagenesis 1996; 11:3-7; PMID:8671708; http://dx.doi.org/10.1093/mutage/11.1.3
71. Gorlewska-Roberts KM, Teitel CH, Lay JO, Jr., Roberts DW, Kadlubar FF. Lactoperoxidase-catalyzed activation of carcinogenic aromatic and heterocyclic amines. Chem Res Toxicol 2004; 17:1659-66; PMID: 15606142; http://dx.doi.org/10. 1021/tx049787n
72. Ghibaudi EM, Laurenti E, Beltramo P, Ferrari RP. Can estrogenic radicals, generated by lactoperoxidase, be involved in the molecular mechanism of breast carcinogenesis? Redox Rep 2000; 5:229-35; PMID:10994878; http://dx.doi.org/10. 1179/135100000101535672
73. Ogden CA, deCathelineau A, Hoffmann PR, Bratton D, Ghebrehiwet B, Fadok VA, et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001; 194:781-95; PMID: 11560994; http://dx.doi.org/10.1084/jem.194.6. 781
74. Nauta AJ, Raaschou-Jensen N, Roos A, Daha MR, Madsen HO, Borrias-Essers MC, et al. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol 2003; 33:2853-63; PMID: 14515269; http://dx.doi.org/10. 1002/eji.200323888
75. Palaniyar N, Clark H, Nadesalingam J, Shih MJ, Hawgood S, Reid KB. Innate immune collectin surfactant protein D enhances the clearance of DNA by macrophages and minimizes anti-DNA antibody generation. J Immunol 2005; 174:7352-8; PMID: 15905582
76. Litvack ML, Palaniyar N. Review: Soluble innate immune pattern-recognition proteins for clearing dying cells and cellular components: implications on exacerbating or resolving inflammation. Innate Immun 2010; 16:191-200; PMID:20529971; http://dx.doi.org/10.1177/1753425910369271
77. Rajawat YS, Hilioti Z, Bossis I. Aging: central role for autophagy and the lysosomal degradative system. Ageing Res Rev 2009; 8:199-213; PMID:19427410; http://dx.doi.org/10.1016/j.arr.2009.05.001
78. Kaarniranta K, Salminen A, Eskelinen EL, Kopitz J. Heat shock proteins as gatekeepers of proteolytic pathways-Implications for age-related macular degeneration (AMD). Ageing Res Rev 2009; 8:128-39; PMID: 19274853; http://dx.doi.org/10.1016/j.arr.2009.01.001
79. Pivtoraiko VN, Stone SL, Roth KA, Shacka JJ. Oxidative stress and autophagy in the regulation of lysosome-dependent neuron death. Antioxid Redox Signal 2009; 11:481-96; PMID:18764739; http://dx.doi.org/10.1089/ars.2008.2263
80. Jung T, Hohn A, Catalgol B, Grune T. Age-related differences in oxidative protein-damage in young and senescent fibroblasts. Arch Biochem Biophys 2009; 483:127-35; PMID:19135972; http://dx.doi.org/10.1016/j.abb.2008.12.007
81. Miller LM, Dumas P. Chemical imaging of biological tissue with synchrotron infrared light. Biochim Biophys Acta 2006; 1758:846-857; PMID:16781664; http://dx.doi.org/10.1016/j.bbamem.2006.04.010
82. Krishna CM, Sockalingum GD, Bhat RA, Venteo L, Kushtagi P, Pluot M, et al. FTIR and Raman microspectroscopy of normal, benign, and malignant formalin-fixed ovarian tissues. Anal Bioanal Chem 2007; 387:1649-56; PMID:17043798; http://dx.doi.org/10.1007/s00216-006-0827-1
83. Walsh MJ, Hammiche A, Fellous TG, Nicholson JM, Cotte M, Susini J, et al. Tracking the cell hierarchy in the human intestine using biochemical signatures derived by mid-infrared microspectroscopy. Stem Cell Res 2009; In press; PMID:19393589; http://dx.doi.org/10.1016/j.scr.2009.02.003
84. Nakamura T, Kelly JG, Trevisan J, Cooper LJ, Bentley AJ, Carmichael PL, et al. Microspectroscopy of spectral biomarkers associated with human corneal stem cells. Mol Vis 2010; 16:359-68; PMID:20520745
85. Schubert W, Gieseler A, Krusche A, Hillert R. Toponome mapping in prostate cancer: detection of 2000 cell surface protein clusters in a single tissue section and cell type specific annotation by using a three symbol code. J Proteome Res 2009; 8:2696-707; PMID:19275201; http://dx.doi.org/10.1021/ pr800944f
86. Schubert W, Friedenberger M, Bode M, Krusche A, Hillert R. Functional architecture of the cell nucleus: towards comprehensive toponome reference maps of apoptosis. Biochim Biophys Acta 2008; 1783:2080-2088; PMID:18718492; http://dx.doi.org/10.1016/j.bbamcr.2008.07.019
87. Schubert W, Bode M, Hillert R, Krusche A, Friedenberger M. Toponomics and neurotoponomics: a new way to medical systems biology. Expert Rev Proteomics 2008; 5:361-9; PMID:18466063; http:// dx.doi.org/10.1586/14789450.5.2.361
88. Bartow SA, Pathak DR, Black WC, Key CR, Teaf SR. Prevalence of benign, atypical, and malignant breast lesions in populations at different risk for breast cancer. A forensic autopsy study. Cancer 1987; 60:2751-60; PMID: 3677009; http://dx.doi.org/10.1002/1097-0142(19871201)60:11,2751::AID-CNCR2820601127. 3.0.CO;2-M
89. Ivanovic Z. Hypoxia or in situ normoxia: The stem cell paradigm. J Cell Physiol 2009; 219:271-5; PMID: 19160417; http://dx.doi.org/10.1002/jcp.21690
90. Freeman TA, Parvizi J, Della Valle CJ, Steinbeck MJ. Reactive oxygen and nitrogen species induce protein and DNA modifications driving arthrofibrosis following total knee arthroplasty. Fibrogenesis Tissue Repair 2009; 2:5; PMID:19912645; http://dx.doi.org/10.1186/1755-1536-2-5
91. Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci USA 1998; 95:4882-7; PMID:9560197; http://dx.doi.org/10.1073/pnas.95.9.4882
92. Wang M, Dhingra K, Hittelman WN, Liehr JG, de Andrade M, Li D. Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissues. Cancer Epidemiol Biomarkers Prev 1996; 5:705-10;PMID:8877062
93. Ishii T, Kumazawa S, Sakurai T, Nakayama T, Uchida K. Mass spectroscopic characterization of protein modification by malondialdehyde. Chem Res Toxicol 2006; 19:122-9; PMID:16411665; http://dx.doi.org/10.1021/tx050231p
94. Nair U, Bartsch H, Nair J. Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic Biol Med 2007; 43:1109-20; PMID: 17854706; http://dx.doi.org/10.1016/j.freeradbiomed.2007.07.012
95. Strong JP. Landmark perspective: Coronary atherosclerosis in soldiers. A clue to the natural history of atherosclerosis in the young. JAMA 1986; 256:2863-6; PMID:3534337; http://dx.doi.org/10.1001/jama.1986.03380200101029
96. Sens MA, Somji S, Garrett SH, Beall CL, Sens DA. Metallothionein isoform 3 overexpression is associated with breast cancers having a poor prognosis. Am J Pathol 2001; 159:21-6; PMID:11438449; http://dx.doi.org/10.1016/S0002-9440(10) 61668-9
97. Bindoli A, Fukuto JM, Forman HJ. Thiol chemistry in peroxidase catalysis and redox signaling. Antioxid Redox Signal 2008; 10:1549-64; PMID:18479206; http://dx.doi.org/10.1089/ars.2008.2063
98. Wonsey DR, Zeller KI, Dang CV. The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc Natl Acad Sci USA 2002; 99:6649-54; PMID:12011429; http://dx. doi.org/10.1073/pnas.102523299
99. Nonn L, Berggren M, Powis G. Increased expression of mitochondrial peroxiredoxin-3 (thioredoxin peroxidase-2) protects cancer cells against hypoxia and drug-induced hydrogen peroxide-dependent apoptosis. Mol Cancer Res 2003; 1:682-9; PMID:12861054
100. Chua PJ, Lee EH, Yu Y, Yip GW, Tan PH, Bay BH. Silencing the Peroxiredoxin III gene inhibits cell proliferation in breast cancer. Int J Oncol 2010; 36:359-64; PMID:20043069
101. Glynn SA, Boersma BJ, Dorsey TH, Yi M, Yfantis HG, Ridnour LA, et al. Increased NOS2 predicts poor survival in estrogen receptor-negative breast cancer patients. J Clin Invest 2010; 120:3843-54; PMID: 20978357; http://dx.doi.org/10.1172/JCI42059