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Review Article Antibacterial Discovery and Development: from Gene to Product and Back Hindawi Publishing Corporation BioMed Research International Volume 2015, Article ID 591349, 16 pages http://dx.doi.org/10.1155/2015/591349 Review Article Antibacterial Discovery and Development: From Gene to Product and Back Victor Fedorenko,1 Olga Genilloud,2 Liliya Horbal,1 Giorgia Letizia Marcone,3,4 Flavia Marinelli,3,4 Yossi Paitan,5 and Eliora Z. Ron6,7 1 Department of Genetics and Biotechnology, Ivan Franko National University of Lviv, Lviv 79005, Ukraine 2Fundacion´ MEDINA, Health Sciences Technology Park, 18016 Granada, Spain 3Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy 4The Protein Factory, Interuniversity Centre Politecnico di Milano, ICRM CNR Milano, and University of Insubria, 21100 Varese, Italy 5Clinical Microbiology Laboratory, Meir Medical Center, 44281 Kfar Saba, Israel 6Department of Molecular Microbiology and Biotechnology, Tel Aviv University, 6997801 Tel Aviv, Israel 7Galilee Research Institute (MIGAL), 11016 Kiryat Shmona, Israel Correspondence should be addressed to Flavia Marinelli; [email protected] Received 30 October 2014; Revised 30 December 2014; Accepted 13 January 2015 Academic Editor: Metin Guru Copyright © 2015 Victor Fedorenko et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Concern over the reports of antibiotic-resistant bacterial infections in hospitals and in the community has been publicized in the media, accompanied by comments on the risk that we may soon run out of antibiotics as a way to control infectious disease. Infections caused by Enterococcus faecium, Staphylococcus aureus, Klebsiella species, Clostridium difficile, Acinetobacter baumannii, Pseudomonas aeruginosa, Escherichia coli, and other Enterobacteriaceae species represent a major public health burden. Despite the pharmaceutical sector’s lack of interest in the topic in the last decade, microbial natural products continue to represent one of the most interesting sources for discovering and developing novel antibacterials. Research in microbial natural product screening and development is currently benefiting from progress that has been made in other related fields (microbial ecology, analytical chemistry, genomics, molecular biology, and synthetic biology). In this paper, we review how novel and classical approaches can be integrated in the current processes for microbial product screening, fermentation, and strain improvement. 1. Introduction and Gram-positive bacteria represent the dominant process by which bacteria become multiresistant. The selective pres- Antibacterial therapy has saved millions of lives and consid- sure of antimicrobial use in hospitals, in communities, and in erably reduced the rate of premature death from bacterial agriculture comprises the engine driving this process. Nowa- infections. These achievements led to the assumption that days we are aware that bacterial resistance to all currently pathogenic bacteria and the high mortality due to infectious used antibiotics has emerged for both Gram-positive and diseases would be a thing of the past. Unfortunately, soon Gram-negative bacteria. This threatening situation urgently after the introduction of antibiotics, reports concerning the calls for a concerted international effort among governments, emergence of resistance started to accumulate. Antibiotic the pharmaceutical industry, biotechnology companies, and resistance mechanisms, which appear de novo or are trans- theacademicworldtoreactandsupportthedevelopment mitted among bacteria, have been well studied and described of new antibacterial agents. One example of such initiative in many reviews. These include detoxification of antibiotic effort is the Infectious Diseases Society of America (IDSA) molecules and mutations in the designated target or, as call to develop 10 new systemic antibacterial drugs by 2020 [2] described recently, are mediated by population-level resis- by targeting drug development against both Gram-positive tance mechanisms [1]. It is now apparent that interspecies and and Gram-negative bacteria. Unless serious action is taken, intraspecies horizontal gene transfer of both Gram-negative the acute and dangerous situation that exists today may send 2 BioMed Research International us back to the preantibiotic era, when there was no cure for Although the prevalence of Gram-negative bacteria is bacterial infections. If this happens, the prophecy of Louis currently somewhat lower than that of Gram-positive bacte- Pasteurwillbefulfilledand“microbeswillhavethelastword.” ria, it is well recognized that Gram-negative MDR infections are emerging as a threat to hospitalized patients with a signif- icantimpactonlengthofhospitalization,mortality,andcost 2. Medical Needs for Novel Antibacterials [14, 15]. These include multiresistant nonfermenters, such as Pseudomonas aeruginosa and Acinetobacter baumannii,or Multidrug-resistant bacterial infections represent a major multiresistant, extended-spectrum -lactamase-producing public health burden, not only in terms of morbidity and Enterobacteriaceae and more recently carbapenem-resistant mortality, but also in increased expenses for managing Enterobacteriaceae (CRE) of different types. Emerging resis- patients and implementing extensive infection control mea- tance is due to the spread of the Klebsiella pneumoniae carba- sures. Mortality due to multidrug-resistant bacterial infec- penemase (KPC) and to the novel New Delhi metallo-- tions is high. In 2002 it was reported that 1.7 million health- lactamase (NDM-1). The rising crisis of multidrug-resistant care-associated infections occur each year in American hos- Gram-negativebacteriahaspromptedtheuseofsalvage pitals and were associated with about 99,000 deaths [3]. This therapy with colistin, an older polymyxin known to be neuro- represents a huge increase from a previous estimation, which toxic and nephrotoxic [16, 17]. However, there are already reported that in 1992 about 13,300 people died from hospital- reports describing isolates of several Gram-negative bacteria acquired infection [4]. It is estimated that in the EU, Iceland, that are resistant to all available antibiotics, including poly- and Norway about 37,000 patients die as a direct result of a myxins [18, 19]. hospital-acquired infection each year; an additional 111,000 die as an indirect result of hospital-acquired infection [5]; and about25,000patientsdiefromamultidrug-resistantbacterial 3. Natural Product Discovery: The Screening infection. Ingredients to Exploit Microbial Diversity Presently, the most frequent multidrug resistance (MDR) Despite the pharmaceutical sector’s lack of interest in bacteria are Enterococcus faecium, Staphylococcus aureus, addressing the topic in the last decade, microbial products Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomo- continue to represent one of the most interesting sources nas aeruginosa,andEnterobacter spp. which therefore were for the discovery of novel antibacterials today and research termed “ESKAPE” after initially being reported6 [ ], with in the field is currently benefiting from progress that has several reports adding Clostridium difficile or other Enter- been made in other related fields (microbial ecology, metage- obacteriaceae [7]. Gram-positive pathogens, such as Staphylo- nomics, metabolomics, or synthetic biology), fields which coccus, Streptococcus, Enterococcus,andClostridium, account have provided a deeper understanding of the microbiome and for a large proportion of serious infections worldwide. An thus the development of new tools to foster the discovery of increasing percentage of such Gram-positive isolates exhibit novel compounds. Among living organisms, microorganisms reduced susceptibility to first-line therapies [8–10], resulting (actinobacteria, cyanobacteria, myxobacteria, and fungi) in poor clinical outcomes in both community and hospital represent one of the most prolific sources for the production settings [10–13]; this has a significant impact on overall of antibiotics. For decades, exploitation of their specialized healthcare utilization and costs [10, 11]. Staphylococcus aureus (commonly termed secondary) metabolism has guaranteed and Enterococcus spp. were found to be among the most the discovery of novel antibiotics and other compounds with commonly isolated pathogens in the hospital environment, unprecedented chemical characteristics and biological prop- and being frequently resistant to multiple drugs complicates erties that do not exist in the screening libraries of synthetic therapy. The representative hospital “superbugs,” methicillin- compounds [20, 21]. In this section, we examine the current resistant S. aureus (MRSA) and vancomycin-resistant ente- trends in microbial product screening for discovering novel rococci (VRE), frequently attract mass-media attention and, antibiotics. A flow diagram showing the overall screening in many countries, pressure is increasing to reduce MRSA operation is reported in Figure 1. and VRE infection rates. Resistance to anti-MRSA and anti- VRE drugs is uncommon; however, infections by MRSA 3.1. Microbial Product Libraries. Microbial natural product strains resistant to glycopeptides, daptomycin, or linezolid libraries rely on the quality and diversity of novel microbial (common anti-MRSA drugs) and by VRE strains resistant strains and the approaches used to exploit their
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