DNA studies using atomic force microscopy: Capabilities for measurement of short DNA fragments

Frontiers in Molecular Biosciences

Volumn 2, Issue JAN, 2015, Pages

  Pang, Dalong ^a   Thierry, Alain R ^b   Dritschilo, Anatoly ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b INSERM   (France)

Author keywords

AFM; Cell free DNA; DNA fragments; Ionizing Radiation (IR)

Indexed keywords

EID: 85015950110     PISSN: None     EISSN: 2296889X     Source Type: Journal    
DOI: 10.3389/fmolb.2015.00001     Document Type: Review

References (76)

1. Barendsen, G. W. (1990). Mechanisms of cell reproductive death and shapes of radiation dose-survival curves of mammalian cells. Int. J. Radiat. Biol. 57, 885-896. doi: 10.1080/09553009014551001
2. Binnig, G., Quate, C. F., and Gerber, C. (1986). Atomic force microscope. Phys. Rev. Lett. 56, 930-933. doi: 10.1103/PhysRevLett.56.930
3. Binning, G., Rohrer, H., and Gerber, C. (1986). The scanning tunneling microscope. Sci. Am. 253, 50-56. doi: 10.1038/scientificamerican0885-50
4. Blöcher, D. (1990). In CHEF electrophoresis a linear induction of dsb corresponds to a nonlinear fraction of extracted DNA with dose. Int. J. Radiat. Biol. 57, 7-12. doi: 10.1080/09553009014550291
5. Bradley, M. O., and Kohn, K. W. (1979). X-ray induced DNA double strand break production and repair in mammalian cells as measured by neutral filter elution. Nucleic Acids Res. 7, 793-804. doi: 10.1093/nar/7.3.793
6. Bremnes, R. M., Sirera, R., and Camps, C. (2005). Circulating tumour-derived DNA and RNA markers in blood: a tool for early detection, diagnostics, and follow-up? Lung Cancer 49, 1-12. doi: 10.1016/j.lungcan.2004.12.008
7. Bresler, S. E., Noskin, L. A., and Suslov, A. V. (1984). Induction by gamma irradiation of double-strand breaks of Escherichia coli chromosomes and their role in cell lethality. Biophys. J. 45, 749-754. doi: 10.1016/S0006-3495(84)84218-6
8. Brezeanu, M., Taucher-Scholz, G., Psonka, K., Träger, F., and Hubenthal, F. (2007). SFM studies of carbon ion induced damages in plasmid DNA. J. Mol. Recognit. 20, 502-507. doi: 10.1002/jmr.852
9. Brons, S., Psonka, K., Heiss, M., Gudowska-Nowak, E., Taucher-Scholz, G., and Neumann, R. (2004). Direct visualisation of heavy ion induced DNA fragmentation using atomic force microscopy. Radiother. Oncol. 73(Suppl. 2), S112-S114. doi: 10.1016/S0167-8140(04)80029-X
10. Cerreta, A., Vobornik, D., Di Santo, G., Tobenas, S., Alonso-Sarduy, L., Adamcik, J., et al. (2012). FM-AFM constant height imaging and force curves: high resolution study of DNA-tip interactions. J. Mol. Recognit. 25, 486-493. doi: 10.1002/jmr.2212
11. Chun, F. K., Müller, I., Lange, I., Friedrich, M. G., Erbersdobler, A., Karakiewicz, P. I., et al. (2006). Circulating tumour-associated plasma DNA represents an independent and informative predictor of prostate cancer. BJU Int. 98, 544-548. doi: 10.1111/j.1464-410X.2006.06352.x
12. Diehl, F., Schmidt, K., Choti, M. A., Romans, K., Goodman, S., Li, M., et al. (2008). Circulating mutant DNA to assess tumor dynamics. Nat. Med. 14, 985-990. doi: 10.1038/nm.1789
13. Dolezel, J., Bartoš, J., and Voglmayr, H., and Greilhuber, J. (2003). Nuclear DNA content and genome size of trout and human. Cytometry A 51, 127-128. doi: 10.1002/cyto.a.10013
14. Drew, M. E., Chworos, A., Oroudjev, E., Hansma, H., and Yamakoshi, Y. (2010). A tripod molecular tip for single molecule ligand-receptor force spectroscopy by AFM. Langmuir 26, 7117-7125. doi: 10.1021/la904151h
15. Elsässer, T., Brons, S., Psonka, K., Scholz, M., Gudowska-Nowak, E., and Taucher-Scholz, G. (2008). Biophysical modeling of fragment length distributions of DNA plasmids after X and heavy-ion irradiation analyzed by atomic force microscopy. Radiat. Res. 169, 649-659. doi: 10.1667/RR1028.1
16. Esnault, C., Chnais, B., Casse, N., Delorme, N., Louarn, G., and Pilard, J. (2013). Electrochemically modified carbon and chromium surfaces for AFM imaging of double-strand DNA interaction with transposase protein. Chem. Phys. Chem. 14, 338-345. doi: 10.1002/cphc.201200885
17. Frankenberg-Schwager, M., and Frankenberg, D. (1990). DNA double-strand breaks: their repair and relationship to cell killing in yeast. Int. J. Radiat. Biol. 58, 569-575. doi: 10.1080/09553009014551931
18. González, L. N., Arruda-Neto, J. D., Cotta, M. A., Carrer, H., Garcia, F., Silva, R. A., et al. (2012). DNA fragmentation by gamma radiation and electron beams using atomic force microscopy. J. Biol. Phys. 38, 531-542. doi: 10.1007/s10867-012-9270-z
19. Goodman, F. O., and Garcia, N. (1991). Roles of the attractive and repulsive forces in atomic-force microscopy. Phys. Rev. B Condens. Matter. 43, 4728-4731. doi: 10.1103/PhysRevB.43.4728
20. Gormally, E., Hainaut, P., Caboux, E., Airoldi, L., Autrup, H., Malaveille, C., et al. (2004). Amount of DNA in plasma and cancer risk: a prospective study. Int. J. Cancer. 111, 746-749. doi: 10.1002/ijc.20327
21. Gudowska-Nowak, E., Psonka-Antonczyk, K., Weron, K., Elsässer, T., and Taucher-Scholz, G. (2009). Distribution of DNA fragment sizes after irradiation with ions. Eur. Phys. J. E Soft Matter 30, 317-324. doi: 10.1140/epje/i2009-10522-7
22. Hall, E., and Giaccia, A. (2011). Radiobiology for the Radiologist, 7th Edn. Philadelphia, PA: Lippincott Williams & Wilkins
23. Hamon, L., Pastré, D., Dupaigne, P., Le Breton, C., Le Cam, E., and Piétrement, O. (2007). High-resolution AFM imaging of single-stranded DNA-binding (SSB) protein-DNA complexes. Nucleic Acids Res. 35, e58. doi: 10.1093/nar/gkm147
24. Hansma, H. G., Kasuya, K., and Oroudjev, E. (2004). Atomic force microscopy imaging and pulling of nucleic acids. Curr. Opin. Struct. Biol. 14, 380-385. doi: 10.1016/j.sbi.2004.05.005
25. Hansma, H. G., Laney, D. E., Bezanilla, M., Sinsheimer, R. L., and Hansma, P. K. (1995). Applications for atomic force microscopy of DNA. Biophys. J. 68, 1672-1677. doi: 10.1016/S0006-3495(95)80343-7
26. Hansma, H. G., Pietrasanta, L. I., Golan, R., Sitko, J. C., Viani, M. B., Paloczi, G. T., et al. (2000). Recent highlights from atomic force microscopy of DNA. J. Biomol. Struct. Dyn. 17(Suppl. 1), 271-275. doi: 10.1080/07391102.2000.10506631
27. Hawkes, P. W. (1985). The Beginning of Electron Microscope. Orlando, FL: Academic Press
28. Herrera, L. J., Raja, S., Gooding, W. E., El-Hefnawy, T., Kelly, L., Luketich, J. D., et al. (2005). Quantitative analysis of circulating plasma DNA as a tumor marker in thoracic malignancies. Clin. Chem. 51, 113-118. doi: 10.1373/clinchem.2004.039263
29. Holdenrieder, S., Burges, A., Reich, O., Spelsberg, F. W., and Stieber, P. (2008). DNA integrity in plasma and serum of patients with malignant and benign diseases. Ann. N.Y. Acad. Sci. 1137, 162-170. doi: 10.1196/annals.1448.013
30. Ido, S., Kimura, K., Oyabu, K., Kobayashi, K., Tsukada, M., Matsushige, K., et al. (2013). Beyond the helix pitch: direct visualization of native DNA in aqueous solution. ACS Nano 7, 1817-1822. doi: 10.1021/nn400071n
31. Jenner, T. J., Belli, M., Goodhead, D. T., Ianzini, F., Simone, G., and Tabocchini, M. A. (1992). Direct comparison of biological effectiveness of protons and alpha-particles of the same LET. III. Initial yield of DNA double-strand breaks in V79 cells. Int. J. Radiat. Biol. 61, 631-637. doi: 10.1080/09553009214551441
32. Jung, K., Fleischhacker, M., and Rabien, A. (2010). Cell-free DNA in the blood as a solid tumor biomarker-a critical appraisal of the literature. Clin. Chim. Acta 411, 1611-1624. doi: 10.1016/j.cca.2010.07.032
33. Kamat, A. A., Baldwin, M., Urbauer, D., Dang, D., Han, L. Y., Godwin, A., et al. (2010). Plasma cell-free DNA in ovarian cancer: an independent prognostic biomarker. Cancer 116, 1918-1925. doi: 10.1002/cncr.24997
34. Kamat, A. A., Bischoff, F. Z., Dang, D., Baldwin, M. F., Han, L. Y., Lin, Y. G., et al. (2006). Circulating cell-free DNA: a novel biomarker for response to therapy in ovarian carcinoma. Cancer Biol. Ther. 5, 1369-1374. doi: 10.4161/cbt.5.10.3240
35. Ke, C., Jiang, Y., Mieczkowski, P. A., Muramoto, G. G., Chute, J. P., and Marszalek, P. E. (2008). Nanoscale detection of ionizing radiation damage to DNA by atomic force microscopy. Small. 4, 288-294. doi: 10.1002/smll.200700527
36. Kobayashi, M., Sumitomo, K., and Torimitsu, K. (2007). Real-time imaging of DNA-streptavidin complex formation in solution using a high-speed atomic force microscope. Ultramicroscopy 107, 184-190. doi: 10.1016/j.ultramic.2006.07.008
37. Lal, R., and John, S. A. (1994). Biological applications of atomic force microscopy. Am. J. Physiol. 266(1 Pt 1), C1-C21
38. Lea, D. E. (1955). Actions of Radiations on Living Cells, 2nd Edn. New York, NY: Cambridge University Press
39. Lee, G., Muramoto, G. G., Chute, J. P., and Marszalek, P. E. (2009). Nanomechanical fingerprints of gamma radiation damage to DNA. J. Nanosci. Nanotechnol. 9, 7359-7363. doi: 10.1166/jnn.2009.1776
40. Lett, J. T. (1992). Damage to cellular DNA from particulate radiations, the efficacy of its processing and the radiosensitivity of mammalian cells. Emphasis on DNA double strand breaks and chromatin breaks. Radiat. Environ. Biophys. 31, 257-277. doi: 10.1007/BF01210207
41. Levin, D., and Hutchinson, F. (1973). Neutral sucrose sedimentation of very large DNA from Bacillus subtilis. I. Effect of random double-strand breaks and centrifuge speed on sedimentation. J. Mol. Biol. 75, 455-478. doi: 10.1016/0022-2836(73)90454-3
42. Lyubchenko, Y. L., Gall, A. A., and Shlyakhtenko, L. S. (2014). Visualization of DNA and protein-DNA complexes with atomic force microscopy. Methods Mol. Biol. 1117, 367-384. doi: 10.1007/978-1-62703-776-1_17
43. Marzese, D. M., Hirose, H., and Hoon, D. S. (2013). Diagnostic and prognostic value of circulating tumor-related DNA in cancer patients. Expert Rev. Mol. Diagn. 13, 827-844. doi: 10.1586/14737159.2013.845088
44. Mazur, A. K., and Maaloum, M. (2014). Atomic force microscopy study of DNA flexibility on short length scales: smooth bending versus kinking. Nucleic Acids Res. 42, 14006-14012. doi: 10.1093/nar/gku1192
45. Mead, R., Duku, M., Bhandari, P., and Cree, I. A. (2011). Circulating tumour markers can define patients with normal colons, benign polyps, and cancers. Br. J. Cancer 105, 239-245. doi: 10.1038/bjc.2011.230
46. Mladenov, E., Magin, S., Soni, A., and Iliakis, G. (2013). DNA double-strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy. Front. Oncol. 10:113. doi: 10.3389/fonc.2013.00113
47. Mouliere, F., El Messaoudi, S., Gongora, C., Guedj, A. S., Robert, B., Del Rio, M., et al. (2013). Circulating cell-free DNA from colorectal cancer patients may reveal high KRAS or BRAF mutation load. Transl. Oncol. 6, 319-328. doi: 10.1593/tlo.12445
48. Mouliere, F., El Messaoudi, S., Pang, D., Dritschilo, A., and Thierry, A. R. (2014). Multi-marker analysis of circulating cell-free DNA toward personalized medicine for colorectal cancer. Mol. Oncol. 8, 927-941. doi: 10.1016/j.molonc.2014.02.005
49. Mouliere, F., Robert, B., Arnau Peyrotte, E., Del Rio, M., Ychou, M., Molina, F., et al. (2011). High fragmentation characterizes tumour-derived circulating DNA. PLoS ONE 6:e23418. doi: 10.1371/journal.pone.0023418
50. Mouliere, F., and Thierry, A. R. (2012). The importance of examining the proportion of circulating DNA originating from tumor, microenvironment and normal cells in colorectal cancer patients. Expert Opin. Biol. Ther. 12(Suppl. 1), S209-S215. doi: 10.1517/14712598.2012.688023
51. Murakami, M., Hirokawa, H., and Hayata, I. (2000). Analysis of radiation damage of DNA by atomic force microscopy in comparison with agarose gel electrophoresis studies. J. Biochem. Biophys. Methods 44, 31-40. doi: 10.1016/S0165-022X(00)00049-X
52. Nikjoo, H., Charlton, D. E., and Goodhead, D. T. (1994). Monte Carlo track structure studies of energy deposition and calculation of initial DSB and RBE. Adv. Space Res. 14, 161-180. doi: 10.1016/0273-1177(94)90466-9
53. Nygaard, A. D., Garm Spindler, K. L., Pallisgaard, N., Andersen, R. F., and Jakobsen, A. (2013). The prognostic value of KRAS mutated plasma DNA in advanced non-small cell lung cancer. Lung Cancer 79, 312-317. doi: 10.1016/j.lungcan.2012.11.016
54. Olive, P. L. (2002). The comet assay. An overview of techniques. Methods Mol. Biol. 203, 179-194. doi: 10.1385/1-59259-179-5:179
55. Ormerod, M. G., and Lehmann, A. R. (1971). Artefacts arising from the sedimentation of high molecular weight DNA on sucrose gradients. Biochim. Biophys. Acta 247, 369-372. doi: 10.1016/0005-2787(71)90021-9
56. Oxnard, G. R., Paweletz, C. P., Kuang, Y., Mach, S. L., O'Connell, A., Messineo, M. M., et al. (2014). Noninvasive detection of response and resistance in EGFR-mutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin. Cancer Res. 20, 1698-1705. doi: 10.1158/1078-0432.CCR-13-2482
57. Painter, R. B. (1975). Repair in mammalian cells: overview. Basic Life Sci. 5B, 595-600
58. Pang, D., Berman, B. L., Chasovskikh, S., Rodgers, J. E., and Dritschilo, A. (1998). Investigation of neutron-induced damage in DNA by atomic force microscopy: experimental evidence of clustered DNA lesions. Radiat. Res. 150, 612-618. doi: 10.2307/3579883
59. Pang, D., Rodgers, J. E., Berman, B. L., Chasovskikh, S., and Dritschilo, A. (2005). Spatial distribution of radiation-induced double-strand breaks in plasmid DNA as resolved by atomic force microscopy. Radiat. Res. 164, 755-765. doi: 10.1667/RR3425.1
60. Pilch, D. R., Sedelnikova, O. A., Redon, C., Celeste, A., Nussenzweig, A., and Bonner, W. M. (2003). Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 81, 123-129. doi: 10.1139/o03-042
61. Pogozelski, W. K., Xapsos, M. A., and Blakely, W. F. (1999). Quantitative assessment of the contribution of clustered damage to DNA double-strand breaks induced by 60Co gamma rays and fission neutrons. Radiat. Res. 151, 442-448. doi: 10.2307/3579831
62. Prise, K. M., Folkard, M., Newman, H. C., and Michael, B. D. (1994). Effect of radiation quality on lesion complexity in cellular DNA. Int. J. Radiat. Biol. 66, 537-542. doi: 10.1080/09553009414551581
63. Psonka, K., Brons, S., Heiss, M., Gudowska-Nowak, E., and Taucher-Scholz, G. (2005). Induction of DNA damage by heavy ions measured by atomic force microscopy. J. Phys. Condens. Matter 17, 1443-1446. doi: 10.1088/0953-8984/17/18/002
64. Psonka-Antonczyk, K., Elsässer, T., Gudowska-Nowak, E., and Taucher-Scholz, G. (2009). Distribution of double-strand breaks induced by ionizing radiation at the level of single DNA molecules examined by atomic force microscopy. Radiat. Res. 172, 288-295. doi: 10.1667/RR1772.1
65. Rydberg, B. (1996). Clusters of DNA damage induced by ionizing radiation: formation of short DNA fragments. II. Experimental detection. Radiat Res. 145, 200-209. doi: 10.2307/3579175
66. Santos, S., Barcons, V., Christenson, H. K., Billingsley, D., Bonass, W. A., Font, J., et al. (2013). Stability, resolution, and ultra-low wear amplitude modulation atomic force microscopy of DNA: small amplitude small set-point imaging. Appl. Phys. Lett. 103, 063702. doi: 10.1063/1.4817906
67. Schafer, M., Schmitz, C., and Bucker, H. (1994). Heavy ion induced DNA double strand breaks in cells of E. coli. Adv. Space. Res. 14, 203-206. doi: 10.1016/0273-1177(94)90468-5
68. Schwartz, D. C., and Cantor, C. R. (1984). Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 37, 67-75. doi: 10.1016/0092-8674(84)90301-5
69. Schwarzenbach, H., Hoon, D. S., and Pantel, K. (2011). Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 11, 426-437. doi: 10.1038/nrc3066
70. Sedelnikova, O. A., Pilch, D. R., Redon, C., and Bonner, W. M. (2003). Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2, 233-235. doi: 10.4161/cbt.2.3.373
71. Sorel, I., Piétrement, O., Hamon, L., Baconnais, S., Cam, E. L., and Pastré, D. (2006). The EcoRI-DNA complex as a model for investigating protein-DNA interactions by atomic force microscopy. Biochemistry 45, 14675-14682. doi: 10.1021/bi060293u
72. Stroun, M., Lyautey, J., Lederrey, C., Olson-Sand, A., and Anker, P. (2001). About the possible origin and mechanism of circulating DNA: apoptosis and active DNA release. Clin. Chim. Acta 313, 139-142. doi: 10.1016/S0009-8981(01)00665-9
73. Taucher-Scholz, G., Heilmann, J., Schneider, M., and Kraft, G. (1995). Detection of heavy-ion-induced DNA double-strand breaks using static-field gel electrophoresis. Radiat. Environ. Biophys. 34, 101-106. doi: 10.1007/BF01275214
74. Town, C. D., Smith, K. C., and Kaplan, H. S. (1971). DNA polymerase required for rapid repair of x-ray-induced DNA strand breaks in vivo. Science. 172, 851-854. doi: 10.1126/science.172.3985.851
75. Wang, B. G., Huang, H. Y., Chen, Y. C., Bristow, R. E., Kassauei, K., Cheng, C. C., et al. (2003). Increased plasma DNA integrity in cancer patients. Cancer Res. 63, 3966-3968
76. Ward, J. F. (1994). The complexity of DNA damage: relevance to biological consequences. Int. J. Radiat. Biol. 66, 427-432. doi: 10.1080/09553009414551401