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Chemical Ecology Proc. Natl. Acad. Sci. USA Vol. 92, pp. 75-82, January 1995 Colloquium Paper This paper was presented at a coUoquium entitled "Chemical Ecology: The Chemistry ofBiotic Interaction, " organized by a committee chaired by Jerrold Meinwald and Thomas Eisner, held March 25 and 26, 1994, at the National Academy of Sciences, Washington, DC. Chemical ecology: A view from the pharmaceutical industry (molecular evolution/natural product screens/scaffold/genetic code/combinatorial chemistry) LYNN HELENA CAPORALE Merck Research Laboratories, P.O. Box 2000, Rahway, NJ 07065 ABSTRACT Biological diversity reflects an underlying ulcers, and many bacterial infections (for examples, see ref. 1). molecular diversity. The molecules found in nature may be For other devastating diseases, such as diabetes, cancer, AIDS, regarded as solutions to challenges that have been confronted stroke, and Alzheimer disease, at best only inadequate therapy and overcome during molecular evolution. As our understand- is available; new approaches to treat these diseases are sought ing ofthese solutions deepens, the efficiency with which we can intensively by researchers within the pharmaceutical industry discover and/or design new treatments for human disease and elsewhere. In the future, new infectious agents may be grows. Nature assists our drug discovery efforts in a variety expected to emerge as important threats, much as human ofways. Some compounds synthesized by microorganisms and immunodeficiency virus (HIV) has challenged us. Because of plants are used directly as drugs. Human genetic variations the magnitude of these challenges, we continue to seek to that predispose to (or protect against) certain diseases may improve the strategies by which we discover new drugs. point to important drug targets. Organisms that manipulate molecules within us to their benefit also may help us to Most of the effort to create and discover medicinal mole- recognize key biochemical control points. Drug design efforts cules occurs in the research laboratories of the pharmaceutical are expedited by knowledge ofthe biochemistry ofa target. To industry. Drug discovery demands a coordinated effort among supplement this knowledge, we screen compounds from people with diverse talents. Researchers who elucidate disease sources selected to maximize molecular diversity. Organisms mechanisms (which point to macromolecules that would make known to manipulate biochemical pathways of other organ- good drug discovery targets) work with those skilled in iso- isms can be sources of particular interest. By using high lating or synthesizing new molecules and with those who can throughput assays, pharmaceutical companies can rapidly determine the safety and effectiveness of these molecules. scan the contents of tens of thousands of extracts of micro- Pharmaceutical company researchers begin the search for organisms, plants, and insects. A screen may be designed to clues to the type of molecules that, for example, inhibit a search for compounds that affect the activity of an individual targeted enzyme, by testing diverse structures in their com- targeted human receptor, enzyme, or ion channel, or the pound collections. These collections consist of compounds screen might be designed to capture compounds that affect synthesized previously in the course of other research pro- any step in a targeted metabolic or biochemical signaling grams. Discovery is optimized by scanning as wide a range of pathway. While a natural product discovered by such a screen structural types as possible (within resource constraints), will itself only rarely become a drug (its potency, selectivity, including compounds found in nature. bioavailability, and/or stability may be inadequate), it may Drug discovery has benefited significantly from the study of suggest a type of structure that would interact with the target, compounds that organisms have evolved for their own pur- serving as a point of departure for a medicinal chemistry poses. All of the drugs discovered at the Merck Research effort-i.e., it may be a "lead." It is still beyond our capability Laboratories that became available to patients in the last to design, routinely, such lead structures, based simply upon decade emerged from programs that benefited from knowl- knowledge of the structure of our target. However, if a drug edge of biological diversity. Some drugs were discovered via discovery target contains regions of structure homologous to natural product screens (2, 3). Others emerged from medicinal that in other proteins, structures known to interact with those chemistry efforts that drew on knowledge such as how the proteins may prove useful as leads for a medicinal chemistry venom of a Brazilian viper lowers blood pressure (4-6). effort. The specificity of a lead for a target may be optimized Another program was inspired by a human genetic variation by directing structural variation to specificity-determining that indicated that a particular enzyme would be a good drug sites and away from those sites required for interaction with target (7). conserved features of the targeted protein structure. Strate- gies that facilitate recognition and exploration of sites at Selection of Drug Discovery Targets which variation is most likely to generate a novel function increase the efficiency with which useful molecules can be A key step in the process of selecting a molecular target for a created. drug discovery program involves a demonstration that altering the activity of the proposed target should affect the disease. This is illustrated by the choice of the HIV protease as a target. Drug Discovery and Its Relationship to Chemical Ecology When the HIV genome was sequenced, Asp-Thr-Gly was recognized, based on previous work with other organisms, as Effective medical treatments are available for many diseases. a sequence found in aspartyl proteases. Viral-encoded pro- Recent discoveries include drugs that treat hypertension, teases are known to free active proteins from a viral polypro- tein precursor. Therefore, it was considered possible that The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in Abbreviations: HIV, human immunodeficiency virus; HMG, hy- accordance with 18 U.S.C. §1734 solely to indicate this fact. droxymethylglutaryl. 75 Downloaded by guest on September 24, 2021 76 Colloquium Paper: Caporale Proc. Natl. Acad Sci USA 92 (1995) inactivating the proposed HIV aspartyl protease might prevent isolation and characterization of unstable molecules present in the formation of viable virus and, thus, that the HIV protease minute quantities in source organisms, such as the potent would be an important target for a drug discovery effort (8). broad-spectrum antibiotic thienamycin (3). To test this hypothesis, a genetic approach was taken to As our understanding of biology deepens, we are increas- inactivate the aspartyl protease, changing the proposed active ingly able to select (and obtain in sufficient quantities) a site Asp to Asn. This mutation did indeed inactivate the HIV specific protein target for a drug discovery effort (18). Iden- protease; further, mutant HIV, lacking an active protease, was tification of human genes that predispose to diseases of not viable (Fig. 1). With this proof of concept in hand, an complex etiology, such as Alzheimer disease (19), may provide intensive effort was mounted to find an HIV protease inhib- clues to biochemical sites of intervention. Thus, many future itor. This proof of concept has been reinforced as small therapies may be targeted to (i.e., discovered by screening molecule inhibitors of the HIV protease have subsequently against) not the most common human sequence at a locus but been found to block the spread of the virus in tissue culture (9). disease-associated alleles. Progress in cloning DNA has placed The search for inhibitors of the HIV protease began with in our hands an array of receptor subtypes and of isozymes. compounds that had been prepared during prior work to [For example, there are at least 14 human serotonin receptor inhibit related proteases, notably renin, an aspartyl protease subtypes (20).] Different receptor subtypes may couple the involved in blood pressure regulation (9, 10). While new action of the signaling ligand (which might be a hormone or a structures that inhibit the HIV protease have emerged from neurotransmitter) to different second messenger systems (e.g., natural product screens (11, 12) [one structure that inhibits activating adenyl cyclase or opening a potassium channel). aspartyl proteases, the statine moiety, had been discovered Subtypes typically have distinct tissue distribution (i.e., one bacterial natural before the emer- may be found in the brain, another in the heart, or both may through screening products be in the same region of the brain, but one may be postsynaptic gence of HIV (10)], the most significant advances in this of have come an extensive medicinal and the other presynaptic). Consequently, the effects drugs program through chemistry to activate or inhibit one can be effort that built upon prior work with aspartyl proteases. designed selectively subtype Inhibitors had to be found that other confined to a subset of the functions of the endogenous ligand. spared important pro- are to teases as A more difficult was to Many side effects of older drugs caused by binding (such renin). challenge one discover nontoxic molecules that are bioavailable and have a nontarget
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