INTRACELLULAR MANIPULATION BY FEMTOSECOND LASERS: REVIEW

WATARU WATANABE; SACHIHIIRO MATSUNAGA; KIICHI FUKUI; KAZUYOSHI ITOH

[1] Denk, W., Strickler, J. H. and Webb, W. W., “Twophoton laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).

[2] K¨onig, K., “Laser tweezers and multiphoton microscopes in life science,” Histochem. Cell. Biol. 114, 79–92 (2000).

[3] Amy, R. L. and Storb, R., “Selective mitochondrial damage by a ruby laser microbeam: an electron microscope study,” Science 150, 756–757 (1965).

[4] Berns, M. W., Aist, J., Edwards, J., Strahs, K., Girton, J., McNeil, P., Rattner, J. B., Kitzes, M., Hammerwilson, M., Liaw, L. H., Siemens, A., Koonce, M., Peterson, S., Brenner, S., Burt, J.,Walter, R., Bryan, P. J.,Vandyk, D.,Couclombe, J., Cahill, T. and Bern, G. S., “Laser microsurgery in cell and developmental biology,” Science 213, 505–513 (1981).

[5] Berns, M. W., Write, W. H. and Steubing, R. W., “Laser microbeam as a tool in cell biology,” Int. Rev. Cytol. 129, 1–44 (1991).

[6] Colombelli, J., Grill, S. W. and Stelzer, E. H. K., “Ultraviolet diffraction limited nanosurgery of live biological tissues,” Rev. Sci. Instrum. 75, 472–478 (2004).

[7] Colombelli, J., Reynaud, E. G. and Stelzer, E. H. K., “Laser pulse energy conversion on sequencespecifically bound metal nanoparticles and its application for DNA manipulation,” Med. Laser Appl. 20, 217–222 (2005).

[8] K¨onig, K., Riemann, I., Fischer, P. and Halbhuber, K. H., “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell. Mol. Biol. 45, 195– 201 (1999).

[9] K¨onig, K., Riemann, I. and Fritzsche,W., “Nanodissection of human chromosomes with near-infrared femtosecond laser pulses,” Opt. Lett. 26, 819–821 (2001).

[10] Tirlapur, U. K. and K¨onig, K., “Targeted transfection by femtosecond laser,” Nature 418, 290–291 (2002).

[11] Stevenson, D., Agate, B., Tsampoula, X., Fischer, P., Brown, C. T. A., Sibbett, W., Riches, A., Gunn- Moore, F. and Dholakia, K., “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14, 7125–7133 (2006).

[12] Baumgart, J., Bintig, W., Ngezahayo, A., Willenbrock, S., Escobar, H. M., Ertmer, W., Lubatschovski, H. and Heisterkamp, A., “Quantified femtosecond laser based opto-perforation of living GFSHR-17 and MTH53 a cells,” Opt. Express 16, 3021–3031 (2008).

[13] Uchugonova, A., K¨onig, K., Bueckle, R., Isemann, A. and Tempea, G., “Targeted transfection of stem cells with sub-20 femtosecond laser pulses,” Opt. Express 16, 9357–9364 (2008).

[14] Zeira, E., Manevitch, A., Khatchatouriants, A., Pappo, O., Hyam, E., Darash-Yahana, M., Tavor, E., Honigman, A., Lewis, A. and Galun, E., “Femtosecond infrared laser: an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8, 342–350 (2003).

[15] Zeira, E., Manevitch, A., Manevitch, Z., Kedar, E., Gropp, M., Daudi, N., Barsuk, R., Harati, M., Yotvat, H., Troilo, P. J., Griffiths, T. G., Pacchione, S. J., Roden, D. F., Niu, Z., Nussbaum, O., Zamir, G., Papo, O., Hemo, I., Lewis, A. and Galun, E., “Femtosecond laser: a new intradermal DNA delivery method for efficient, long-term gene expression and genetic immunization,” Faseb J. 21, 3522–3533 (2007).

[16] Kohli, V., Elezzabi, A. and Acker, J. P., “Cell nanosurgery using ultrashort (femtosecond) laser pulses: applications to membrane surgery and cell isolation,” Lasers Surg. Med. 37, 227–230 (2005).

[17] Tirlapur, U. K. and K¨onig, K., “Femtosecond nearinfrared lasers as a novel tool for non-invasive real-time high-resolution time-lapse imaging of chloroplast division in living bundle sheath cells of Arabidopsis,” Planta 24, 1–10 (2001).

[18] Tirlapur, U. K. and K¨onig, K., “Femtosecond nearinfrared laser pulses as a versatile non-invasive tool for intra-tissue nanoprocessing in plants without compromising viability,” ThePlant J. 31, 365–374 (2002).

[19] K¨onig, K., Riemann, I., Stracke, F. and Le Harzic, R., “Nanoprocessing with nanojoule near-infrared femtosecond laser pulses,” Med. Laser Appl. 20, 169–184 (2005).

[20] Shimada, T., Watanabe, W., Matsunaga, S., Higashi, T., Ishii, H., Fukui, K., Isobe, K. and Itoh, K., “Intracellular disruption of mitochondria in living HeLa cells with a 76-MHz femtosecond laser oscillator,” Opt. Express 13, 9869–9880 (2005).

[21] Supatto, W., Debarre, D., Moulia, B., Brouzes, E., Martin, J. L., Farge, E. and Beaurepaire, E., In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses,” Proc. Natl. Acad. Sci. USA 102, 1047–1052 (2005).

[22] Sacconi, L., Toli′c-N rrelykke, I. M., Antolini, R. and Pavone, F. S., “Combined intracellular threedimensional imaging and selective nanosurgery by a nonlinear microscope, J. Biomed. Opt. 10, 014002 (2005).

[23] Shen, N., Datta, D., Schaffer, C. B., LeDuc, P., Ingber, D. E. and Mazur, E., “Ablation of cytoskeletal filaments and mitochondria in live cells using a femtosecond laser nanoscissor,” Mech. Chem. Biosyst. 2, 17–25 (2005).

[24] Maxwell, I., Chung, C. and Mazur, E., “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

[25] Kumar, S., Maxwell, I. Z., Heisterkamp, A., Polte, T. R., Lele, T. P., Salanga, M., Mazur, E. and Ingber, D. E., “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophysical J. 90, 3762–3773 (2006).

[26] Heisterkamp, A., Maxwell, I. Z., Mazur, E., Underwood, J. M., Nickerson, J. A., Kumar, S. and Ingber, D. E., “Pulse energy dependence of subcellular dissection by femtosecond laser pulses,” Opt. Express 13, 3690–3696 (2005).

[27] Watanabe, W., Arakawa, N., Matsunaga, S., Higashi, T., Fukui, K., Isobe, K. and Itoh, K., “Femtosecond laser disruption of subcellular organelles in a living cell,” Opt. Express 12, 4203–4213 (2004).

[28] Watanabe, W., Matsunaga, S., Shimada, T., Higashi, T., Fukui, K. and Itoh, K., “Femtosecond laser disruption of mitochondria in living cells,” Med. Laser Appl. 20, 185–191 (2005).

[29] Yanik, M. F., Cinar, H., Cinar, H. N., Chisholm, A. D., Jin, Y. and Ben-Yakar, A., “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).

[30] Bourgeois, F. and Ben-Yakar, A., “Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C.elegans,” Opt. Express 15, 8521–8531 (2007).

[31] Yanik, M. F., Cinar, H., Cinar, H. N., Gibby, A., Chisholm, A. D., Jin, Y. S. and Ben-Yakar, A., “Nerve regeneration in Caenorhabditis elegans after femtosecond laser axotomy,” IEEE J. Sel. Top. Quant. 12, 1283–1291 (2006).

[32] Vogel, A., Noack, J., Huttman, G. and Paltauf, G., “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).

[33] Lukyanov, K. A., Chudakov, D. M., Lukyanov, S. and Verkhusha, V. V., “Photoactivatable fluorescent proteins,” Nat. Rev. Mo. Cell Bio. 6, 885–891 (2005).

[34] Patterson, G. H. and Lippincott-Schwartz, J., “A photoactivatable GFP for selective photolabeling of proteins and cells,” Science 297, 1873–1877 (2002).

[35] Chudakov, D. M., Belousov, V. V., Zaraisky, A. G., Novoselov, V. V., Staroverov, D. B., Zorov, D. B., Lukyanov, S. and Lukyanov, K. A., “Kindling fluorescent proteins for precise in vivo photolabeling,” Nature Biotechnol. 21, 191–194 (2003).

[36] Schneider, M., Barozzi, S., Testa, I., Faretta, M. and Diaspro, A., “Two-photon activation and excitation properties of PA-GFP in the 720–920nm region,” Biophys. J. 89, 1346–1352 (2005).

[37] Tsutsui, H., Karasawa, S., Shimizu, H., Nukina, N. and Miyawaki, A., “Semi-rational engineering of a coral fluorescent protein into an efficient highlighter,” EMBO Rep. 6, 233–238 (2005).

[38] Ivanchenko, S., R¨ocker, C., Oswald, F., Wiedenmann, J. and Nienhaus, U., “Targeted green-red photoconversion of EosFP, a fluorescent marker protein,” J. Biol. Phys. 31, 249–259 (2005).

[39] Chen, Y., Macdonald, P. J., Skinner, J. P., Patterson, G. H. and Muller, J. D., “Probing nucleocytoplasmic transport by two-photon activation of PA-GFP,” Microscopic Res. Tech. 69, 220–226 (2006).

[40] Watanabe, W., Shimada, T., Matsunaga, S., Kurihara, D., Arimura, S., Tsutsumi, N., Fukui, K., Isobe, K. and Itoh, K., “Single organelle tracking by two-photon conversion,” Opt. Express 15, 2490– 2498 (2007).

[41] Watanabe, W., Matsunaga, S., Higashi, T., Fukui, K. and Itoh, K., “In vivo manipulation of fluorescently labeled organelles in living cells by multiphoton excitation,” J. Biomed. Opt. 13, 031213 (2008).

[42] Kohli, V. and Elezzabi, A. Y., “Laser surgery of zebrafish (Danio rerio) embryos using femtosecond laser pulses: optimal parameters for exogenous material delivery, and the laser’s effect on shortand long-term development,” BMC Biotechnol. 8, 7 (2008).

[43] Uchugonova, A., Isemann A., Gorjup, E., Tempe, G., B¨uckle, R., Watanabe, W. and K¨onig, K., “Optical knock out of stem cells with extremely ultrashort femtosecond laser pulses,” J. Biophotonics 1, 463– 469 (2008).

[44] Iwanaga, S., Smith, N., Fujita, K., Kawata, S. and Nakamura, O., “Single-pulse cell stimulation with a near-infrared picosecond laser,” Appl. Phys. Lett. 87, 243901 (2005).

[45] Tanabe, T., Oyamada, M., Fujita, K., Dai, P., Tanaka, H. and Takamatsu, T., “Multiphoton excitation evoked chromophore-assisted laser inactivation using green fluorescent protein,” Nature Methods 2, 503–505 (2005).

[46] Garwe, F., Csaki, A., Maubach, G., Steinbruck, A., Weise, A., K¨onig, K. and Fritzsche, W., “Laser pulse energy conversion on sequence-specifically bound metal nanoparticles and its application for DNA manipulation,” Med. Laser Appl. 20, 201–206 (2005).

[47] Csaki, A., Garwe, F., Steinbrueck, A., Maubach, G., Festag, G., Weise, A., Riemann, I., K¨onig, K. and Fritzsche, W., “A parallel approach for subwavelength molecular surgery using gene-specific positioned metal nanoparticles as laserlight antennas,” Nano Lett. 7, 247–253 (2007).

[48] Ben-Yakar, A., “Plasmonic laser nanosurgery of cells using femtosecond laser ablation in the nearfield of gold nanoparticles,” LPM2008 (The 9th International Symposium on Laser Precision Microfabrication), Quebec City, Canada (2008).

[49] Guo, S. X., Bourgeois, F., Chokshi, T., Durr, N., Hilliard, N. J. M., Chronis, N. and Ben-Yakar, A., “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nature Methods 5, 531–533 (2008).

[50] Rohde, C. B., Zeng, F., Gonzalez-Rubio, R., Angel, M. and Yanik, M. F., “Microfluidic system for on-chip high-throughput whole-animal sorting and screening at sub-cellular resolution,” Proc. Natl. Acad Sci. USA 104, 13891 (2007).

[51] Zei, F., Rohde, C. and Yanik, M. F., “Sub-cellular precision on-chip small-animal immobilization, multiphoton imaging and femtosecond laser manipulation, Lab on a Chip 8, 653 (2008).

[52] K¨onig, K., Krauss, O. and Riemann, I., “Intratissue surgery with 80MHz nanojoule femtosecond laser pulses in the near infrared,” Opt. Express 10, 171– 176 (2002).

[53] Juhasz, T., Frieder, H., Kurtz, R. M., Horvath, C., Bille, J. F. and Mourou, G., “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quant. 5, 902–910 (1999).

[54] Lubatschowski, H., Maatz, G., Heisterkamp, A., Hetzel, U., Drommer, W., Welling, H. and Ertmer, W., “Application of ultrashort laser pulses for intrastromal refractive surgery,” Graf. Arch. Clin. Exp. 238, 33–39 (2000).

[55] Nishimura, N., Schaffer, C. B., Friedman, B., Tsai, P. S., Lyden, P. D. and Kleinfeld, D., “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nature Methods 3, 99 (2006).