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Positron Emission Tomography Provides Molecular Imaging of Biological Processes

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Positron Emission Tomography Provides Molecular Imaging of Biological Processes Positron emission tomography provides molecular imaging of biological processes Michael E. Phelps* Department of Molecular and Medical Pharmacology, Department of Energy Laboratory of Structural Biology and Molecular Medicine and Crump Institute for Molecular Imaging, University of California Los Angeles School of Medicine, Box 951735, Los Angeles, CA 90095-1735 This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected on April 27, 1999. Contributed by Michael E. Phelps, April 3, 2000 Diseases are biological processes, and molecular imaging with Molecular imaging technologies use molecular probes or positron emission tomography (PET) is sensitive to and informative of interactions with molecules. Many different technologies have these processes. This is illustrated by detection of biological abnor- been and continue to be developed to image the structure and malities in neurological disorders with no computed tomography or function of systems, such as x-ray diffraction, electron micros- MRI anatomic changes, as well as even before symptoms are ex- copy, autoradiography, optical imaging, positron emission to- pressed. PET whole body imaging in cancer provides the means to (i) mography (PET), magnetic resonance imaging (MRI), x-ray identify early disease, (ii) differentiate benign from malignant lesions, computed tomography (CT), and single photon emission com- (iii) examine all organs for metastases, and (iv) determine therapeutic puted tomography, with unique applications, as well as advan- effectiveness. Diagnostic accuracy of PET is 8–43% higher than tages and limitations to each. conventional procedures and changes treatment in 20–40% of the This article focuses on one of these molecular imaging technol- patients, depending on the clinical question, in lung and colorectal ogies, PET, and its role in imaging integrative mammalian biology cancers, melanoma, and lymphoma, with similar findings in breast, of organ systems and whole organisms from mouse to human in the ovarian, head and neck, and renal cancers. A microPET scanner for context of living, functioning systems. Normal biological processes mice, in concert with human PET systems, provides a novel technol- and their failure in disease are the targets of PET. An overview is ogy for molecular imaging assays of metabolism and signal trans- provided with examples to illustrate specific points. duction to gene expression, from mice to patients: e.g., PET reporter gene assays are used to trace the location and temporal level of Principles of PET. PET is an analytical imaging technology developed expression of therapeutic and endogenous genes. PET probes and (1–5) to use compounds labeled with positron emitting radioiso- drugs are being developed together—in low mass amounts, as topes as molecular probes to image and measure biochemical molecular imaging probes to image the function of targets without processes of mammalian biology in vivo (Fig. 1). The only radio- disturbing them, and in mass amounts to modify the target’s function isotopes of oxygen (14O, 15O), nitrogen (13N), and carbon (11C) that as a drug. Molecular imaging by PET, optical technologies, magnetic can be administered to a subject and detected externally are all resonance imaging, single photon emission tomography, and other positron emitters. There is no positron emitter of hydrogen, so technologies are assisting in moving research findings from in vitro fluorine-18 is used as a hydrogen substitute. Positron emitters of biology to in vivo integrative mammalian biology of disease. Cu, Zn, K, Br, Rb, I, P, Fe, Ga and others are also used. Molecular probes for PET are developed by first identifying atson and Crick’s elucidation of DNA in 1958 initiated a a target process to be studied and then synthesizing a positron Wtime in which biological and physical scientists would labeled molecule through which an assay can be performed. strive to unravel the genetic code and its regulated expression Because PET cannot provide direct chemical analysis of that is the basis of development and maintenance of phenotypic reaction products in tissue, labeled molecules are used that function of all cells of an organism. At this time, there is an trace a small number of steps (i.e., one to four) of a biochem- intense exploration to determine patterns of gene expression ical process so that kinetic analysis can be used to estimate the that encode for normal biological processes such as replication, concentration of reactants and products over time and, from migration, signal transduction of cell communication, and many this, reaction rates. The fundamental principles of assays and other functions cells perform. There is also a growing basis for molecular probes used in them typically originate from bio- diseases resulting from alterations in normal regulation of gene chemical, biological, and pharmaceutical sciences. Biochem- expression that transition cells to phenotypes of disease. These ists develop them to isolate and accurately measure a limited alterations in gene expression can result from interactions with number of steps in a biochemical pathway. Drugs are designed the environment, hereditary deficits, developmental errors, and to have limited interactions because the goal is to modify the aging processes. As a result, physical, biological and medical function of a key step in a biological process with minimal sciences are working together to identify fundamental errors of interaction with other processes. disease and develop molecular corrections for them. The name In a typical molecular assay, a positron-labeled probe is injected given to this broad field of endeavor is ‘‘Molecular Medicine.’’ intravenously, and PET scans provide measures of the tissue As part of the evolving concept of molecular medicine, molecular concentration of the probe and labeled products over time. These imaging technologies are being developed to examine the integra- data are combined with a measure of the time course of the plasma tive functions of molecules, cells, organ systems, and whole organ- probe concentration, representing its delivery to tissue, and pro- isms. The organisms range from viruses and bacteria to higher order cessed with a compartmental model containing equations describ- species, including humans, but in each case molecular imaging is ing the transport and reaction processes the probe undergoes. The used to examine the structure and regulatory mechanisms of their organized functions. The system studied may be a protein with affector sites through which functions of the protein are altered by Abbreviations: PET, positron emission tomography; CT, computed tomography; FDG, 2-[F- 18]fluoro-2-deoxy-D-glucose; DG, 2-deoxy-D-[C-14]glucose; FLT, 3Ј-deoxy-3Јfluorothymi- interactions with other molecules, or an organ system such as liver dine; PRG, PET reporter gene; PRP, PET reporter probe; HSV1-TK, herpes simplex virus or brain, in which collections of cells function as an integrated thymidine kinase; MPTP, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine; FGCV, 8-[F- system based on molecular mechanisms through which intra- and 18]fluoroganciclovir; FESP, [F-18]fluoroethylspiperone; FPCV, [F-18]fluoropenciclovir. intercellular functions are performed. *E-mail: [email protected]. 9226–9233 ͉ PNAS ͉ August 1, 2000 ͉ vol. 97 ͉ no. 16 Downloaded by guest on September 25, 2021 Fig. 1. Principles of PET. A biologically active molecule is labeled with a positron Fig. 2. Tracer kinetic models for FDG and FLT. Arrows show forward and emitting radioisotope as in the example FDG. FDG is injected intravenously, reverse transport between plasma and tissue, phosphorylation and dephos- distributes throughout the body via bloodstream, and enters into organs, where phorylation. Both FDG and FLT phosphates are not significant substrates for it traces transport and phosphorylation of glucose. Positrons emitted from the dephosphorylation or further metabolism at normal imaging times of 40–60 nucleus of F-18 are antielectrons that travel a short distance and combine with an min after injection. Models taking dephosphorylation reaction into account at electron, and annihilation occurs with their masses converted into their energy much later imaging times have been developed (7, 9). Images are 6-mm-thick equivalent (E ϭ mc2) through emission of two 511-keV photons 180° apart. The longitudinal tomographic sections of a patient with a lung tumor (arrows), two 511-keV photons are electronically detected as a coincidence event when with high glucose metabolism and DNA replication. The rest of the images they strike opposing detectors simultaneously. The figure illustrates one line of show normal distribution of glucose utilization and DNA replication, excep- coincidence detection, but in an actual tomograph, 6–70 million detector pair tions being clearance of both tracers to bladder (arrowhead) and, in the case combinations record events from many different angles around subject simulta- of FLT, the glucuronidation by hepatocytes (12) in liver. neously. After correction for photon attenuation, tomographic images of tissue concentration are reconstructed. ‘‘Blocks’’ of detectors are arranged around the circumference, with each containing 32–64 detector elements, for a total of tens that produce pharmacologic effects. FDG is commonly used with of thousands of elements. PET scanners provide hundreds of tomographic image PET to image normal and altered metabolic states of disease planes
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