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Single-Particle/Single-Cell Ion Microbeams As Probes of Biological Mechanisms Alan W

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Single-Particle/Single-Cell Ion Microbeams As Probes of Biological Mechanisms Alan W 1424 IEEE TRANSACTIONS ON PLASMA SCIENCE, VOL. 36, NO. 4, AUGUST 2008 Single-Particle/Single-Cell Ion Microbeams as Probes of Biological Mechanisms Alan W. Bigelow, David J. Brenner, Guy Garty, and Gerhard Randers-Pehrson (Invited Paper) Abstract—An ion microbeam is a very narrow beam of charged-particle microbeams with subcellular resolution, where charged particles, typically protons, alpha particles, or heavier, the beam size is smaller than a cell nucleus. Coupled to an of micrometer/submicrometer size, corresponding to cellular/ endstation with imaging, location, and positioning techniques, subcellular dimensions. Together with integrated techniques for locating live cellular or subcellular targets, they allow rapid a microbeam is a powerful tool for controlled cell-irradiation sequential irradiation of these targets. This review covers both experiments. the technology involved in modern single-cell microbeams, as well Where cell-irradiation studies date back to studies in the as some current applications. The recent explosion of interest in 1950s [4], pioneers in the field of single-cell ion microbeam microbeams was initially driven by interest in the domestic radon irradiation include groups at Columbia University [5], the Gray problem, in which target cells are exposed either to zero or one alpha particle. Microbeams allow cells to be individually irradi- Cancer Institute (GCI) [6], [7], and the Pacific Northwest ated with exact numbers of particles. As microbeams were built, National Laboratory [8]. Since that time, the number of refined, and used, the biological questions that were addressed planned and operational microbeam facilities has significantly with them have considerably broadened, to encompass many increased. To provide a cohesive example of a microbeam aspects of damage signal transduction. Two areas in particular facility, this review article will first concentrate on the devel- have attracted much interest: One is the use of microbeams to address the sensitivity of subcellular targets, such as the cytoplasm opment of light ion microbeam technology at the Radiological or mitochondria. The other reflects the ability of the microbeam to Research Accelerator Facility (RARAF), Columbia University irradiate some cells, but not others, allowing a direct investigation and subsequently provide technical summaries of similar fa- of the so-called bystander effect, where signals from irradiated cilities. For a review on heavy ion microbeam facilities and cells can apparently cause biological responses in neighboring their applications, refer to the companion paper in this issue unirradiated cells. by Funayama et al. Index Terms—Accelerators, biological effects of radiation, imaging, particle beams. II. RARAF—A MICROBEAM FACILITY Microbeam technologies at RARAF are geared toward cell- I. INTRODUCTION irradiation experiments involving the bystander effect, genomic HAT HAPPENS to a mammalian cell, or a neighboring instability, and adaptive response. Researchers at RARAF W cell, when it is struck by ionizing radiation? This basic have developed a series of microbeam systems: Microbeam I, question has led to the development of single-particle single- Microbeam II, and the permanent magnetic microbeam (PMM), cell microbeam facilities for studying the biological effects of propagating those technical aspects that have proven useful particle irradiation. In order to study the effects of ionizing from one microbeam generation to the next. The following radiation on single cells, such as, the bystander effect [1], it overview of RARAF microbeams demonstrates merging novel is practical to have a device that can locate single-cell and concepts with successful established design. subcellular targets and deliver a prescribed specific dose [2] to each target. A minimum delivery of exactly one ion per cell A. Microbeam I nuclues demonstrates the precision of a single-particle single- cell ion microbeam and is particularly applicable to studying Initial microbeam development at RARAF was based on effects from radon exposure [3]. Particle accelerators with a vertical collimated beam from a model D1, 4.2-MV High specialized ion optics or collimators are capable of forming Voltage Engineering (HVE) Van de Graaff accelerator with a duoplasmatron ion source [5]. This particle accelerator, built in 1949, was originally the injector for the Cosmotron project Manuscript received November 10, 2007; revised February 6, 2008. This at Brookhaven National Laboratory and was moved to Nevis work was supported in part by the National Institute of Biomedical Imaging and Bioengineering under Grant NIBIB 5 P41 EB002033-12 and in part by the Laboratories in 1980, where it was used to pioneer single- National Cancer Institute under Grant 5P01-CA049062-16. cell single-particle microbeam studies at RARAF. The duoplas- The authors are with the Radiological Research Accelerator Facility, Center matron is a hot-cathode magnetic ion source, which typically for Radiological Research, Columbia University, Irvington, NY 10533 USA (e-mail: [email protected]). produces ions of hydrogen and helium isotopes [9]. In the Digital Object Identifier 10.1109/TPS.2008.927268 duoplasmatron design, an innovative electromagnet–electrode 0093-3813/$25.00 © 2008 IEEE BIGELOW et al.: SINGLE-PARTICLE/SINGLE-CELL ION MICROBEAMS AS PROBES OF BIOLOGICAL MECHANISMS 1425 combination forms plasma primarily at the exit hole of the ion of the scaler attached to the input of a high-voltage ampli- source [10]. fier (Technisches Büro S. Fischer, Ober-Ramstadt, Germany), The first-generation collimated microbeam at RARAF, now where the output drove electrostatic deflection plates to shutter decommissioned and referred to as Microbeam I, was ini- the ion beam. The shutter (stainless steel plates: 53.3-cm length, tially used for biology experiments starting in February 1994. 5.7-cm height, and 1.3-cm gap) was positioned approximately Apertures for beam collimation consisted of a 2-mm-diameter 6.4-m upstream from the exit window. aperture located 1.3 m before a final collimating pair of Several design aspects became RARAF standards since the apertures. The final consecutive collimating apertures were successful operation of Microbeam I. For one, a vertical ion 5- and 6-µm-diameter laser-drilled holes in 12.5-µm-thick beam for irradiation has a practical advantage when working stainless steel sheets, separated by 300 µm. The 6-µm-diameter with plated cells covered by a very thin nominally uniform aperture acted as an antiscatter element, to limit the particle layer of medium. Also, cell-dish transfer between the biologist irradiation to an area smaller than the nucleus of a human and the microbeam operator is expedited by having a biology cell. Nevertheless, a small fraction of the particles (8%) ar- workbench and incubator in the same room and adjacent to rived outside of the prescribed target region. This is a general the irradiator. For biology experiments, such as mutation and characteristic of all collimated microbeams and is overcome by oncogenic transformation studies [1], [3], [12]–[15], available using a focusing system. Two actuators were used to adjust high throughput of about 11 000 cells per hour was vital for the alignment of the final collimator, which was mounted in obtaining statistically relevant numbers of irradiated samples. a spherical gimbal. This decommissioned collimator assembly is currently located at the McMaster Accelerator Laboratory B. Microbeam II (McMaster University, Hamilton, ON, Canada) for microbeam development in that facility. The essential change from Microbeam I to Microbeam II Accurate cell imaging and targeting were facilitated through was to progress from a collimated beam to a focused ion a program written for real-time image analysis and stage po- beam on a dedicated beamline with a double-focusing magnet. sitioning. Developed in Visual Basic under the Windows NT The Microbeam II endstation incorporates a Nikon Eclipse operating system, the irradiation algorithm was essentially: 600FN microscope that rests in a kinetic mount and is also 1) with a low-magnification objective lens, acquire a series of attached to a pivot arm for online and offline positioning. adjacent images for coarse cellular location, and 2) under high Sample illumination is regulated with an adjustable light-guide- magnification, reimage each region that contains at least one coupled shuttered UV lamp. Ion beam scatter at the vacuum cell in the coarse image, then locate, position, and irradiate exit window is minimized by using a 100-nm-thick SiN exit cells. For each cell to be irradiated, a mechanical stage moves window. A precision xyz-stage incorporated into the endsta- the cell target to the coordinates of the ion beam, previously tion of Microbeam II comprises two components: a custom determined by imaging the profile of laser transmission through coarse xy-stage, designed and constructed in-house, coupled the final collimator. Tried and established on Microbeam I, this to a three-axis piezoelectric-actuated fine-motion stage, the control program has served as the base for further generations LP-200 low-profile nanopositioner from Mad City Laboratory of microbeam system development at RARAF. (Madison, WI) [16]. Each microbeam experiment includes an irradiation protocol A microbeam formed with focusing elements brought a with 1) a prescribed number of particles (as low as one) per promise of a smaller beam spot size, which matched the bio- targeted cell, 2) a percentage of cells to be targeted,
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