864
Views
21
CrossRef citations to date
0
Altmetric
Research Paper

Infrared microspectroscopy identifies biomolecular changes associated with chronic oxidative stress in mammary epithelium and stroma of breast tissues from healthy young women

Implications for latent stages of breast carcinogenesis

, , , , , & show all
Pages 225-235 | Received 25 Apr 2013, Accepted 08 Oct 2013, Published online: 01 Nov 2013

References

  • Muir CS. Epidemiology of cancer in ethnic groups. Br J Cancer Suppl 1996; 29:S12 - 6; PMID: 8782793
  • Park SK, Kim Y, Kang D, Jung EJ, Yoo KY. Risk factors and control strategies for the rapidly rising rate of breast cancer in Korea. J Breast Cancer 2011; 14:79 - 87; http://dx.doi.org/10.4048/jbc.2011.14.2.79; PMID: 21847401
  • Pott P. Chirurgical observations. London: L Hawes, W Clark, and R Collins., 1775.
  • Selikoff IJ, Hammond EC, Seidman H. Latency of asbestos disease among insulation workers in the United States and Canada. Cancer 1980; 46:2736 - 40; http://dx.doi.org/10.1002/1097-0142(19801215)46:12<2736::AID-CNCR2820461233>3.0.CO;2-L; PMID: 7448712
  • Selikoff IJ. Lessons for living in a chemical world. Bull Environ Contam Toxicol 1984; 33:682 - 95; http://dx.doi.org/10.1007/BF01625600; PMID: 6394072
  • Weiss W. Cigarette smoking and lung cancer trends. A light at the end of the tunnel?. Chest 1997; 111:1414 - 6; http://dx.doi.org/10.1378/chest.111.5.1414; PMID: 9149602
  • Miyakawa M, Tachibana M, Miyakawa A, Yoshida K, Shimada N, Murai M, Kondo T. Re-evaluation of the latent period of bladder cancer in dyestuff-plant workers in Japan. Int J Urol 2001; 8:423 - 30; http://dx.doi.org/10.1046/j.1442-2042.2001.00342.x; PMID: 11555006
  • 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; http://dx.doi.org/10.1097/01.HP.0000133216.72557.ab; PMID: 15551786
  • Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, Mabuchi K, Kodama K. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res 2007; 168:1 - 64; http://dx.doi.org/10.1667/RR0763.1; PMID: 17722996
  • 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; http://dx.doi.org/10.1002/ajim.20881; PMID: 20672325
  • Karabela-Bouropoulou V, Liapi-Avgeri G, Iliopoulou E, Agnantis NJ. Histological findings in breast tissue specimens from reduction mammoplasties. Pathol Res Pract 1994; 190:792 - 8; http://dx.doi.org/10.1016/S0344-0338(11)80427-9; PMID: 7831156
  • Ishag MT, Bashinsky DY, Beliaeva IV, Niemann TH, Marsh WL Jr.. Pathologic findings in reduction mammaplasty specimens. Am J Clin Pathol 2003; 120:377 - 80; http://dx.doi.org/10.1309/4KD652HN739XTLM3; PMID: 14502800
  • 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; http://dx.doi.org/10.1097/01.PRS.0000122212.37703.6E; PMID: 15253187
  • 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; http://dx.doi.org/10.1177/1066896907307176; PMID: 18203780
  • Hassan FE, Pacifico MD. Should we be analysing breast reduction specimens? A systematic analysis of over 1,000 consecutive cases. Aesthetic Plast Surg 2012; 36:1105 - 13; http://dx.doi.org/10.1007/s00266-012-9919-9; PMID: 22678135
  • Brown MH, Weinberg M, Chong N, Levine R, Holowaty E. A cohort study of breast cancer risk in breast reduction patients. Plast Reconstr Surg 1999; 103:1674 - 81; PMID: 10323701
  • Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003; 42:318 - 43; http://dx.doi.org/10.1016/S0163-7827(03)00014-6; PMID: 12689622
  • 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; http://dx.doi.org/10.1161/01.ATV.13.11.1689; PMID: 7692957
  • Waeg G, Dimsity G, Esterbauer H. Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins. Free Radic Res 1996; 25:149 - 59; http://dx.doi.org/10.3109/10715769609149920; PMID: 8885333
  • Rosenfeld ME, Palinski W, Ylä-Herttuala S, Butler S, Witztum JL. Distribution of oxidation specific lipid-protein adducts and apolipoprotein B in atherosclerotic lesions of varying severity from WHHL rabbits. Arteriosclerosis 1990; 10:336 - 49; http://dx.doi.org/10.1161/01.ATV.10.3.336; PMID: 1693069
  • Yoritaka A, Hattori N, Uchida K, Tanaka M, Stadtman ER, Mizuno Y. Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc Natl Acad Sci U S A 1996; 93:2696 - 701; http://dx.doi.org/10.1073/pnas.93.7.2696; PMID: 8610103
  • Clawson GA, Benedict CM, Kelley MR, Weisz J. Focal nuclear hepatocyte response to oxidative damage following low dose thioacetamide intoxication. Carcinogenesis 1997; 18:1663 - 8; http://dx.doi.org/10.1093/carcin/18.8.1663; PMID: 9276646
  • Ando Y, Brännström T, Uchida K, Nyhlin N, Näsman B, Suhr O, Yamashita T, Olsson T, El Salhy M, Uchino M, et al. Histochemical detection of 4-hydroxynonenal protein in Alzheimer amyloid. J Neurol Sci 1998; 156:172 - 6; http://dx.doi.org/10.1016/S0022-510X(98)00042-2; PMID: 9588853
  • Meng J, Sakata N, Takebayashi S, Asano T, Futata T, Nagai R, Ikeda K, Horiuchi S, Myint T, Taniguchi N. Glycoxidation in aortic collagen from STZ-induced diabetic rats and its relevance to vascular damage. Atherosclerosis 1998; 136:355 - 65; http://dx.doi.org/10.1016/S0021-9150(97)00238-4; PMID: 9543107
  • Khan MF, Wu X, Tipnis UR, Ansari GA, Boor PJ. Protein adducts of malondialdehyde and 4-hydroxynonenal in livers of iron loaded rats: quantitation and localization. Toxicology 2002; 173:193 - 201; PMID: 11960672
  • Temma K, Shimoya K, Zhang Q, Kimura T, Wasada K, Kanzaki T, Azuma C, Koyama M, Murata Y. Effects of 4-hydroxy-2-nonenal, a marker of oxidative stress, on the cyclooxygenase-2 of human placenta in chorioamnionitis. Mol Hum Reprod 2004; 10:167 - 71; http://dx.doi.org/10.1093/molehr/gah030; PMID: 14981143
  • Dalfó E, Portero-Otín M, Ayala V, Martínez A, Pamplona R, Ferrer I. Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J Neuropathol Exp Neurol 2005; 64:816 - 30; http://dx.doi.org/10.1097/01.jnen.0000179050.54522.5a; PMID: 16141792
  • Rytilä P, Rehn T, Ilumets H, Rouhos A, Sovijärvi A, Myllärniemi M, Kinnula VL. Increased oxidative stress in asymptomatic current chronic smokers and GOLD stage 0 COPD. Respir Res 2006; 7:69; http://dx.doi.org/10.1186/1465-9921-7-69; PMID: 16646959
  • Chu J, Tong M, de la Monte SM. Chronic ethanol exposure causes mitochondrial dysfunction and oxidative stress in immature central nervous system neurons. Acta Neuropathol 2007; 113:659 - 73; http://dx.doi.org/10.1007/s00401-007-0199-4; PMID: 17431646
  • Hattoria N, Wanga M, Taka H, Fujimura T, Yoritaka A, Kubo S, Mochizuki H. Toxic effects of dopamine metabolism in Parkinson’s disease. Parkinsonism Relat Disord 2009; 15:Suppl 1 S35 - 8; http://dx.doi.org/10.1016/S1353-8020(09)70010-0; PMID: 19131041
  • Malins DC, Holmes EH, Polissar NL, Gunselman SJ. The etiology of breast cancer. Characteristic alteration in hydroxyl radical-induced DNA base lesions during oncogenesis with potential for evaluating incidence risk. Cancer 1993; 71:3036 - 43; http://dx.doi.org/10.1002/1097-0142(19930515)71:10<3036::AID-CNCR2820711025>3.0.CO;2-P; PMID: 8387875
  • Malins DC, Polissar NL, Nishikida K, Holmes EH, Gardner HS, Gunselman SJ. The etiology and prediction of breast cancer. Fourier transform-infrared spectroscopy reveals progressive alterations in breast DNA leading to a cancer-like phenotype in a high proportion of normal women. Cancer 1995; 75:503 - 17; http://dx.doi.org/10.1002/1097-0142(19950115)75:2<503::AID-CNCR2820750213>3.0.CO;2-0; PMID: 7812921
  • Malins DC, Polissar NL, Schaefer S, Su Y, Vinson M. A unified theory of carcinogenesis based on order-disorder transitions in DNA structure as studied in the human ovary and breast. Proc Natl Acad Sci U S A 1998; 95:7637 - 42; http://dx.doi.org/10.1073/pnas.95.13.7637; PMID: 9636202
  • Malins DC, Anderson KM, Jaruga P, Ramsey CR, Gilman NK, Green VM, Rostad SW, Emerman JT, Dizdaroglu M. Oxidative changes in the DNA of stroma and epithelium from the female breast: potential implications for breast cancer. Cell Cycle 2006; 5:1629 - 32; http://dx.doi.org/10.4161/cc.5.15.3098; PMID: 16880742
  • Anderson KM, Jaruga P, Ramsey CR, Gilman NK, Green VM, Rostad SW, Emerman JT, Dizdaroglu M, Malins DC. Structural alterations in breast stromal and epithelial DNA: the influence of 8,5′-cyclo-2′-deoxyadenosine. Cell Cycle 2006; 5:1240 - 4; http://dx.doi.org/10.4161/cc.5.11.2816; PMID: 16760644
  • Malins DC, Anderson KM, Gilman NK, Green VM, Barker EA, Hellström KE. Development of a cancer DNA phenotype prior to tumor formation. Proc Natl Acad Sci U S A 2004; 101:10721 - 5; http://dx.doi.org/10.1073/pnas.0403888101; PMID: 15249662
  • Malins DC, Haimanot R. 4,6-Diamino-5-formamidopyrimidine, 8-hydroxyguanine and 8-hydroxyadenine in DNA from neoplastic liver of English sole exposed to carcinogens. Biochem Biophys Res Commun 1990; 173:614 - 9; http://dx.doi.org/10.1016/S0006-291X(05)80079-8; PMID: 2175601
  • Malins DC, Gunselman SJ. Fourier-transform infrared spectroscopy and gas chromatography-mass spectrometry reveal a remarkable degree of structural damage in the DNA of wild fish exposed to toxic chemicals. Proc Natl Acad Sci U S A 1994; 91:13038 - 41; http://dx.doi.org/10.1073/pnas.91.26.13038; PMID: 7809168
  • Malins DC, Polissar NL, Garner MM, Gunselman SJ. Mutagenic DNA base modifications are correlated with lesions in nonneoplastic hepatic tissue of the English sole carcinogenesis model. Cancer Res 1996; 56:5563 - 5; PMID: 8971153
  • Malins DC, Polissar NL, Gunselman SJ. Infrared spectral models demonstrate that exposure to environmental chemicals leads to new forms of DNA. Proc Natl Acad Sci U S A 1997; 94:3611 - 5; http://dx.doi.org/10.1073/pnas.94.8.3611; PMID: 9108025
  • Malins DC, Stegeman JJ, Anderson JW, Johnson PM, Gold J, Anderson KM. Structural changes in gill DNA reveal the effects of contaminants on Puget Sound fish. Environ Health Perspect 2004; 112:511 - 5; http://dx.doi.org/10.1289/ehp.6719; PMID: 15064153
  • Malins DC, Anderson KM, Stegeman JJ, Jaruga P, Green VM, Gilman NK, Dizdaroglu M. Biomarkers signal contaminant effects on the organs of English sole (Parophrys vetulus) from Puget Sound. Environ Health Perspect 2006; 114:823 - 9; http://dx.doi.org/10.1289/ehp.8544; PMID: 16759979
  • Weisz J, Shearer DA, Murata E, Patrick SD, Han B, Berg A, Clawson GA. 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 Biol Ther 2012; 13:101 - 13; http://dx.doi.org/10.4161/cbt.13.2.18873; PMID: 22231390
  • 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; http://dx.doi.org/10.1016/j.neuro.2010.04.008; PMID: 20438755
  • 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; http://dx.doi.org/10.1093/toxsci/kfq192; PMID: 20584760
  • 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; http://dx.doi.org/10.1186/1755-1536-2-5; PMID: 19912645
  • Cunha GR, Ricke WA. A historical perspective on the role of stroma in the pathogenesis of benign prostatic hyperplasia. Differentiation 2011; 82:168 - 72; http://dx.doi.org/10.1016/j.diff.2011.04.002; PMID: 21723032
  • Howlett AR, Bissell MJ. The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial Cell Biol 1993; 2:79 - 89; PMID: 8353596
  • Rønnov-Jessen L, Petersen OW, Bissell MJ. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev 1996; 76:69 - 125; PMID: 8592733
  • Rønnov-Jessen L, Bissell MJ. Breast cancer by proxy: can the microenvironment be both the cause and consequence?. Trends Mol Med 2009; 15:5 - 13; http://dx.doi.org/10.1016/j.molmed.2008.11.001; PMID: 19091631
  • Haviv I, Polyak K, Qiu W, Hu M, Campbell I. Origin of carcinoma associated fibroblasts. Cell Cycle 2009; 8:589 - 95; http://dx.doi.org/10.4161/cc.8.4.7669; PMID: 19182519
  • Hu M, Polyak K. Microenvironmental regulation of cancer development. Curr Opin Genet Dev 2008; 18:27 - 34; http://dx.doi.org/10.1016/j.gde.2007.12.006; PMID: 18282701
  • Ricke EA, Williams K, Lee YF, Couto S, Wang Y, Hayward SW, Cunha GR, Ricke WA. Androgen hormone action in prostatic carcinogenesis: stromal androgen receptors mediate prostate cancer progression, malignant transformation and metastasis. Carcinogenesis 2012; 33:1391 - 8; http://dx.doi.org/10.1093/carcin/bgs153; PMID: 22535887
  • Kelly JG, Trevisan J, Scott AD, Carmichael PL, Pollock HM, Martin-Hirsch PL, Martin FL. Biospectroscopy to metabolically profile biomolecular structure: a multistage approach linking computational analysis with biomarkers. J Proteome Res 2011; 10:1437 - 48; http://dx.doi.org/10.1021/pr101067u; PMID: 21210632
  • Patel II, Martin FL. Discrimination of zone-specific spectral signatures in normal human prostate using Raman spectroscopy. Analyst 2010; 135:3060 - 9; http://dx.doi.org/10.1039/c0an00518e; PMID: 20949203
  • Pang W, Li J, Ahmadzai AA, Heppenstall LD, Llabjani V, Trevisan J, Qiu X, Martin FL. Identification of benzo[a]pyrene-induced cell cycle-associated alterations in MCF-7 cells using infrared spectroscopy with computational analysis. Toxicology 2012; 298:24 - 9; http://dx.doi.org/10.1016/j.tox.2012.04.009; PMID: 22561278
  • Miller LM, Dumas P. From structure to cellular mechanism with infrared microspectroscopy. Curr Opin Struct Biol 2010; 20:649 - 56; http://dx.doi.org/10.1016/j.sbi.2010.07.007; PMID: 20739176
  • Miller LM, Dumas P. Chemical imaging of biological tissue with synchrotron infrared light. Biochim Biophys Acta 2006; 1758:846 - 57
  • German MJ, Pollock HM, Zhao B, Tobin MJ, Hammiche A, Bentley A, Cooper LJ, Martin FL, Fullwood NJ. Characterization of putative stem cell populations in the cornea using synchrotron infrared microspectroscopy. Invest Ophthalmol Vis Sci 2006; 47:2417 - 21; http://dx.doi.org/10.1167/iovs.05-1254; PMID: 16723451
  • Patel II, Harrison WJ, Kerns JG, Filik J, Wehbe K, Carmichael PL, Scott AD, Philpott MP, Frogley MD, Cinque G, et al. Isolating stem cells in the inter-follicular epidermis employing synchrotron radiation-based Fourier-transform infrared microspectroscopy and focal plane array imaging. Anal Bioanal Chem 2012; 404:1745 - 58; http://dx.doi.org/10.1007/s00216-012-6314-y; PMID: 22945554
  • Walsh MJ, Hammiche A, Fellous TG, Nicholson JM, Cotte M, Susini J, Fullwood NJ, Martin-Hirsch PL, Alison MR, Martin FL. Tracking the cell hierarchy in the human intestine using biochemical signatures derived by mid-infrared microspectroscopy. Stem Cell Res 2009; 3:15 - 27; http://dx.doi.org/10.1016/j.scr.2009.02.003; PMID: 19393589
  • Walsh MJ, Singh MN, Pollock HM, Cooper LJ, German MJ, Stringfellow HF, Fullwood NJ, Paraskevaidis E, Martin-Hirsch PL, Martin FL. ATR microspectroscopy with multivariate analysis segregates grades of exfoliative cervical cytology. Biochem Biophys Res Commun 2007; 352:213 - 9; http://dx.doi.org/10.1016/j.bbrc.2006.11.005; PMID: 17141660
  • Fogarty SW, Patel II, Trevisan J, Nakamura T, Hirschmugl CJ, Fullwood NJ, Martin FL. Sub-cellular spectrochemical imaging of isolated human corneal cells employing synchrotron radiation-based Fourier-transform infrared microspectroscopy. Analyst 2013; 138:240 - 8; http://dx.doi.org/10.1039/c2an36197c; PMID: 23152953
  • Walsh MJ, Fellous TG, Hammiche A, Lin WR, Fullwood NJ, Grude O, Bahrami F, Nicholson JM, Cotte M, Susini J, et al. Fourier transform infrared microspectroscopy identifies symmetric PO(2)(-) modifications as a marker of the putative stem cell region of human intestinal crypts. Stem Cells 2008; 26:108 - 18; http://dx.doi.org/10.1634/stemcells.2007-0196; PMID: 17901405
  • Lee LS, Lin SY, Chi CW, Liu HC, Cheng CL. Non-destructive analysis of the protein conformational structure of human pituitary adenomas using reflectance FT-IR microspectroscopy. Cancer Lett 1995; 94:65 - 9; http://dx.doi.org/10.1016/0304-3835(95)03825-H; PMID: 7621446
  • Dukor RK, Liebman MN, Johnson BL. A new, non-destructive method for analysis of clinical samples with FT-IR microspectroscopy. Breast cancer tissue as an example. Cell Mol Biol (Noisy-le-grand) 1998; 44:211 - 7; PMID: 9551652
  • Lasch P, Haensch W, Naumann D, Diem M. Imaging of colorectal adenocarcinoma using FT-IR microspectroscopy and cluster analysis. Biochim Biophys Acta 2004; 1688:176 - 86; http://dx.doi.org/10.1016/j.bbadis.2003.12.006; PMID: 14990348
  • Krafft C, Steiner G, Beleites C, Salzer R. Disease recognition by infrared and Raman spectroscopy. J Biophotonics 2009; 2:13 - 28; http://dx.doi.org/10.1002/jbio.200810024; PMID: 19343682
  • Diem M, Papamarkakis K, Schubert J, Bird B, Romeo MJ, Miljković M. The infrared spectral signatures of disease: extracting the distinguishing spectral features between normal and diseased states. Appl Spectrosc 2009; 63:307A - 18A; http://dx.doi.org/10.1366/000370209789806894; PMID: 19891826
  • Heraud P, Caine S, Campanale N, Karnezis T, McNaughton D, Wood BR, Tobin MJ, Bernard CC. Early detection of the chemical changes occurring during the induction and prevention of autoimmune-mediated demyelination detected by FT-IR imaging. Neuroimage 2010; 49:1180 - 9; http://dx.doi.org/10.1016/j.neuroimage.2009.09.053; PMID: 19796690
  • Kelly JG, Nakamura T, Kinoshita S, Fullwood NJ, Martin FL. Evidence for a stem-cell lineage in corneal squamous cell carcinoma using synchrotron-based Fourier-transform infrared microspectroscopy and multivariate analysis. Analyst 2010; 135:3120 - 5; http://dx.doi.org/10.1039/c0an00507j; PMID: 20886154
  • Caine S, Heraud P, Tobin MJ, McNaughton D, Bernard CC. The application of Fourier transform infrared microspectroscopy for the study of diseased central nervous system tissue. Neuroimage 2012; 59:3624 - 40; http://dx.doi.org/10.1016/j.neuroimage.2011.11.033; PMID: 22119649
  • Pijanka J, Sockalingum GD, Kohler A, Yang Y, Draux F, Parkes G, Lam KP, Collins D, Dumas P, Sandt C, et al. Synchrotron-based FTIR spectra of stained single cells. Towards a clinical application in pathology. Lab Invest 2010; 90:797 - 807; http://dx.doi.org/10.1038/labinvest.2010.8; PMID: 20125083
  • Patel II, Trevisan J, Singh PB, Nicholson CM, Krishnan RK, Matanhelia SS, Martin FL. Segregation of human prostate tissues classified high-risk (UK) versus low-risk (India) for adenocarcinoma using Fourier-transform infrared or Raman microspectroscopy coupled with discriminant analysis. Anal Bioanal Chem 2011; 401:969 - 82; http://dx.doi.org/10.1007/s00216-011-5123-z; PMID: 21643857
  • Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer 2007; 121:2381 - 6; http://dx.doi.org/10.1002/ijc.23192; PMID: 17893868
  • Evans RG, Naidu B, Rajpoot NM, Epstein D, Khan M. Toponome imaging system: multiplex biomarkers in oncology. Trends Mol Med 2012; 18:723 - 31; http://dx.doi.org/10.1016/j.molmed.2012.10.003; PMID: 23122853
  • Rohner TC, Staab D, Stoeckli M. MALDI mass spectrometric imaging of biological tissue sections. Mech Ageing Dev 2005; 126:177 - 85; http://dx.doi.org/10.1016/j.mad.2004.09.032; PMID: 15610777
  • Balluff B, Schöne C, Höfler H, Walch A. MALDI imaging mass spectrometry for direct tissue analysis: technological advancements and recent applications. Histochem Cell Biol 2011; 136:227 - 44; http://dx.doi.org/10.1007/s00418-011-0843-x; PMID: 21805154
  • Setou M, Kurabe N. Mass microscopy: high-resolution imaging mass spectrometry. J Electron Microsc (Tokyo) 2011; 60:47 - 56; http://dx.doi.org/10.1093/jmicro/dfq079; PMID: 21109523
  • Lagarrigue M, Lavigne R, Guével B, Com E, Chaurand P, Pineau C. Matrix-assisted laser desorption/ionization imaging mass spectrometry: a promising technique for reproductive research. Biol Reprod 2012; 86:74; http://dx.doi.org/10.1095/biolreprod.111.094896; PMID: 22156474
  • Schubert W, Gieseler A, Krusche A, Serocka P, Hillert R. Next-generation biomarkers based on 100-parameter functional super-resolution microscopy TIS. N Biotechnol 2012; 29:599 - 610; http://dx.doi.org/10.1016/j.nbt.2011.12.004; PMID: 22209707
  • Palinski W, Koschinsky T, Butler SW, Miller E, Vlassara H, Cerami A, Witztum JL. Immunological evidence for the presence of advanced glycosylation end products in atherosclerotic lesions of euglycemic rabbits. Arterioscler Thromb Vasc Biol 1995; 15:571 - 82; http://dx.doi.org/10.1161/01.ATV.15.5.571; PMID: 7749871
  • Trevisan J, Angelov PP, Scott AD, Carmichael PL, Martin FL. IRootLab: a free and open-source MATLAB toolbox for vibrational biospectroscopy data analysis. Bioinformatics 2013; 29:1095 - 7; http://dx.doi.org/10.1093/bioinformatics/btt084; PMID: 23422340
  • Setou M, Shrivas K, Sroyraya M, Yang H, Sugiura Y, Moribe J, Kondo A, Tsutsumi K, Kimura Y, Kurabe N. Developments and applications of mass microscopy. Med Mol Morphol 2010; 43:1 - 5; http://dx.doi.org/10.10007/s00795-009-0489-0; PMID: 20339999

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.