Label-free DNA imaging in vivo with stimulated Raman scattering microscopy

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

Volumn 112, Issue 37, 2015, Pages 11624-11629

  Lu, Fa Ke ^a   Basu, Srinjan ^b,d   Igras, Vivien ^c   Hoang, Mai P ^c   Ji, Minbiao ^a   Fu, Dan ^a   Holtom, Gary R ^a   Neel, Victor A ^c   Freudiger, Christian W ^a   Fisher, David E ^c,e   Xie, X Sunney ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e Invenio Imaging Inc   (United States)

Author keywords

Cell division; Label free histology; Mitotic rate; Skin cancer; Stimulated Raman scattering microscopy

Indexed keywords

CARBON; DNA; HYDROGEN; LIPID; PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER DIAGNOSIS; CELL COUNTING; CELL DIVISION; CELL NUCLEUS; CHROMOSOME; CONTROLLED STUDY; DECOMPOSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROGEN BOND; IN VITRO STUDY; IN VIVO STUDY; LABEL FREE DNA IMAGING; MICROSCOPY; MITOSIS RATE; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOUSE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SKIN CELL; STAINING; STIMULATED RAMAN SCATTERING MICROSCOPY; ANIMAL; CELL PROLIFERATION; CHEMISTRY; DIAGNOSTIC IMAGING; HELA CELL LINE; IMAGE PROCESSING; METABOLISM; MITOSIS; NUDE MOUSE; RAMAN SPECTROMETRY; SKIN NEOPLASMS;

ANIMALS; CELL DIVISION; CELL NUCLEUS; CELL PROLIFERATION; DIAGNOSTIC IMAGING; DNA; FEMALE; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIPIDS; MICE; MICE, NUDE; MICROSCOPY; MITOSIS; SKIN NEOPLASMS; SPECTRUM ANALYSIS, RAMAN;

EID: 84941624226     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1515121112     Document Type: Article

References (60)

1. Kagey MH, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467(7314):430-435.
2. Apostolou E, Hochedlinger K (2013) Chromatin dynamics during cellular reprogramming. Nature 502(7472):462-471.
3. Jannink I, Risberg B, Van Diest PJ, Baak JPA (1996) Heterogeneity of mitotic activity in breast cancer. Histopathology 29(5):421-428.
4. Aasi SZ, Leffel DJ, Lazova RZ (2012) Atlas of practical mohs histopathology (Springer, New York).
5. Freudiger CW, et al. (2008) Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy. Science 322(5909):1857-1861.
6. Nandakumar P, Kovalev A, Volkmer A (2009) Vibrational imaging based on stimulated Raman scattering microscopy. New J Phys 11:033026.
7. Ideguchi T, et al. (2013) Coherent Raman spectro-imaging with laser frequency combs. Nature 502(7471):355-358.
8. Berto P, Andresen ER, Rigneault H (2014) Background-free stimulated Raman spectroscopy and microscopy. Phys Rev Lett 112(5):053905.
9. Bégin S, Bélanger E, Laffray S, Vallée R, Côté D (2009) In vivo optical monitoring of tissue pathologies and diseases with vibrational contrast. J Biophotonics 2(11): 632-642.
10. Saar BG, et al. (2010) Video-rate molecular imaging in vivo with stimulated Raman scattering. Science 330(6009):1368-1370.
11. Ji M, et al. (2013) Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy. Sci Transl Med 5(201):201ra119.
12. Mittal R, et al. (2013) Evaluation of stimulated Raman scattering microscopy for identifying squamous cell carcinoma in human skin. Lasers Surg Med 45(8):496-502.
13. Fu D, et al. (2014) Imaging the intracellular distribution of tyrosine kinase inhibitors in living cells with quantitative hyperspectral stimulated Raman scattering. Nat Chem 6(7):614-622.
14. Wei L, et al. (2014) Live-cell imaging of alkyne-tagged small biomolecules by stimulated Raman scattering. Nat Methods 11(4):410-412.
15. Yue S, et al. (2014) Cholesteryl ester accumulation induced by PTEN loss and PI3K/AKT activation underlies human prostate cancer aggressiveness. Cell Metab 19(3):393-406.
16. Freudiger CW, et al. (2011) Highly specific label-free molecular imaging with spectrally tailored excitation stimulated Raman scattering (STE-SRS) microscopy. Nat Photonics 5(2):103-109.
17. Fu D, et al. (2012) Quantitative chemical imaging with multiplex stimulated Raman scattering microscopy. J Am Chem Soc 134(8):3623-3626.
18. Ozeki Y, et al. (2012) High-speed molecular spectral imaging of tissue with stimulated Raman scattering. Nat Photonics 6(12):844-850.
19. Wang K, et al. (2013) Time-lens based hyperspectral stimulated Raman scattering imaging and quantitative spectral analysis. J Biophotonics 6(10):815-820.
20. Freudiger CW, et al. (2012) Multicolored stain-free histopathology with coherent Raman imaging. Lab Invest 92(10):1492-1502.
21. Lu FK, et al. (2012) Multicolor stimulated Raman scattering (SRS) microscopy. Mol Phys 110(15-16):1927-1932.
22. Zhang X, et al. (2012) Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy. ChemPhysChem 13(4):1054-1059.
23. Klein K, et al. (2012) Label-free live-cell imaging with confocal Raman microscopy. Biophys J 102(2):360-368.
24. Cheng J-X, Xie XS (2013) Coherent Raman scattering microscopy (CRC Press, Boca Raton).
25. Jeppsson K, Kanno T, Shirahige K, Sjögren C (2014) The maintenance of chromosome structure: Positioning and functioning of SMC complexes. Nat Rev Mol Cell Biol 15(9): 601-614.
26. Rodriguez-Puebla ML, Robles AI, Johnson DG, LaCava M, & Conti CJ (1998) Synchronized proliferation induced by 12-O-tetradecanoylphorbol-13-acetate treatment of mouse skin: An in vivo model for cell cycle regulation. Cell growth & differentiation: the molecular biology journal of the American Association for Cancer Research 9(1):31-39.
27. Tentler JJ, et al. (2012) Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 9(6):338-350.
28. Madan V, Lear JT, Szeimies RM (2010) Non-melanoma skin cancer. Lancet 375(9715): 673-685.
29. Petter G, Haustein UF (1998) Squamous cell carcinoma of the skin-histopathological features and their significance for the clinical outcome. J Eur Acad Dermatol Venereol 11(1):37-44.
30. Warner CL, Cockerell CJ (2011) The new seventh edition American Joint Committee on Cancer staging of cutaneous non-melanoma skin cancer: A critical review. Am J Clin Dermatol 12(3):147-154.
31. Marusyk A, Almendro V, Polyak K (2012) Intra-tumour heterogeneity: A looking glass for cancer? Nat Rev Cancer 12(5):323-334.
32. Konig K, Riemann I (2003) High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution. J Biomed Opt 8(3): 432-439.
33. Chen X, Grégoire S, Formanek F, Galey JB, Rigneault H (2015) Quantitative 3D molecular cutaneous absorption in human skin using label free nonlinear microscopy. J Control Release 200:78-86.
34. Frans SD, Harris JM (1985) Selection of Analytical Wavelengths for Multicomponent Spectrophotometric Determinations. Anal Chem 57(13):2680-2684.
35. Sasaki K, Kawata S, Minami S (1986) Optimal Wavelength Selection for Quantitative- Analysis. Appl Spectrosc 40(2):185-190.
36. Osborne SD, Jordan RB, Kunnemeyer R (1997) Method of wavelength selection for partial least squares. Analyst (Lond) 122(12):1531-1537.
37. Martin RM, Leonhardt H, & Cardoso MC (2005) DNA labeling in living cells. Cytometry. Part A: the journal of the International Society for Analytical Cytology 67(1):45-52.
38. Peng CY, et al. (1997) Mitotic and G2 checkpoint control: Regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277(5331):1501-1505.
39. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911-917.
40. Papenfuss HD, Gross JF, Intaglietta M, Treese FA (1979) A transparent access chamber for the rat dorsal skin fold. Microvasc Res 18(3):311-318.
41. Huang Q, et al. (1999) Noninvasive visualization of tumors in rodent dorsal skin window chambers. Nat Biotechnol 17(10):1033-1035.
42. Palmer GM, et al. (2011) In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters. Nat Protoc 6(9):1355-1366.
43. Slaga TJ, Fischer SM, Weeks CE, Klein-Szanto AJ, Reiners J (1982) Studies on the mechanisms involved in multistage carcinogenesis in mouse skin. J Cell Biochem 18(1): 99-119.
44. Argyris TS (1980) Epidermal growth following a single application of 12-O-tetradecanoyl- phorbol-13-acetate in mice. Am J Pathol 98(3):639-648.
45. Morton CL, Houghton PJ (2007) Establishment of human tumor xenografts in immunodeficient mice. Nat Protoc 2(2):247-250.
46. Orth JD, et al. (2011) Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics. Cancer Res 71(13):4608-4616.
47. Puppels GJ, et al. (1990) Studying single living cells and chromosomes by confocal Raman microspectroscopy. Nature 347(6290):301-303.
48. Thomas GJ, Jr (1999) Raman spectroscopy of protein and nucleic acid assemblies. Annu Rev Biophys Biomol Struct 28:1-27.
49. Huang Z, et al. (2003) Near-infrared Raman spectroscopy for optical diagnosis of lung cancer. Int J Cancer 107(6):1047-1052.
50. Uzunbajakava N, et al. (2003) Nonresonant confocal Raman imaging of DNA and protein distribution in apoptotic cells. Biophys J 84(6):3968-3981.
51. Jess PR, et al. (2007) Early detection of cervical neoplasia by Raman spectroscopy. International journal of cancer. Journal international du cancer 121(12):2723-2728.
52. Chowdary MV, et al. (2009) Biochemical correlation of Raman spectra of normal, benign and malignant breast tissues: A spectral deconvolution study. Biopolymers 91(7):539-546.
53. Jachtenberg JW, et al. (2013) Raman spectroscopy can discriminate distinct glioma subtypes as defined by RNA expression profiling. J Raman Spectrosc 44(9):1217-1221.
54. Chen Y, et al. (2014) Raman spectroscopy analysis of the biochemical characteristics of molecules associated with the malignant transformation of gastric mucosa. PLoS One 9(4):e93906.
55. Okotrub KA, Surovtsev NV, Semeshin VF, & Omelyanchuk LV (2015) Raman spectroscopy for DNA quantification in cell nucleus. Cytometry. Part A: the journal of the International Society for Analytical Cytology 87(1):68-73.
56. Parker FS (1983) Applications of Infrared, Raman, and Resonance Raman Spectroscopy in Biochemistry (Plenum Press, New York).
57. Matthäus C, Boydston-White S, Miljkovic M, Romeo M, Diem M (2006) Raman and infrared microspectral imaging of mitotic cells. Appl Spectrosc 60(1):1-8.
58. Mallidis C, et al. (2011) In situ visualization of damaged DNA in human sperm by Raman microspectroscopy. Hum Reprod 26(7):1641-1649.
59. Fu D, Xie XS (2014) Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data. Anal Chem 86(9):4115-4119.
60. Liao C-S, et al. (2015) Microsecond scale vibrational spectroscopic imaging by multiplex stimulated Raman scattering microscopy. Light Sci Appl 4:e265.