Source: PURDUE UNIVERSITY submitted to NRP
DRUG REPURPOSING FOR IDENTIFICATION OF NOVEL ANTIBIOTICS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1013508
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2017
Project End Date
Nov 13, 2020
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
PURDUE UNIVERSITY
(N/A)
WEST LAFAYETTE,IN 47907
Performing Department
Veterinary Comparative Pathobiology
Non Technical Summary
The current costly and time-consuming drug discovery process is ill-equipped to combat rapidly emerging multidrug resistant pathogens. There is a pressing need for the identification of novel strategies to develop antibiotics quickly and efficiently to deal with the rapid emergence of multidrug resistance pathogens. One strategy which warrants more attention as a unique method for identifying new antimicrobials is drug repurposing. Repurposing FDA-approved drugs, with well-characterized toxicology and pharmacology, to find new applications outside the scope of the original medical indication is a novel way to reduce both the time and cost associated with antimicrobial innovation. The FDA-approved drugs represent an untapped reservoir for new antibiotic leads that may lead to identification of new targets that will guide the future development of improved antimicrobial/anti-infective agents. Thus, in addition to the discovery of potential novel drugs and drug targets, the impact will be multiplied by research laboratories/pharmaceutical companies worldwide, using the resulting data to follow up on "hits" from our screening.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
31140101100100%
Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
4010 - Bacteria;

Field Of Science
1100 - Bacteriology;
Goals / Objectives
Our long term research goal is to discover and develop novel antimicrobials with novel mechanism of action from approved human and veterinary non-antimicrobial drugs (drug repurposing) that can be repurposed as therapeutics agents in the treatment of human and animal infections caused by bacterial and fungal pathogens. Recently, drug repurposing is gaining momentum as it has resulted in successes in a number of disease areas and has accounted for approximately 30% of newly approved FDA drugs and vaccines (Ashburn and Thor, 2004; Chong and Sullivan, 2007b; Jin and Wong, 2013). Repurposing existing approved drugs permits companies to bypass much of the preclinical work and early stage clinical trials required for new compounds (particularly toxicological and pharmacological analysis of drugs) thus cutting into the cost associated with bringing a drug to the marketplace (DiMasi et al., 2003). In addition to lower drug discovery-associated costs, repurposing approved drugs (particularly for identification of new antimicrobials) has several additional benefits. Given these drugs have already been tested in animals and human, valuable information pertaining to, toxicity, pharmacokinetic and pharmacodynamic parameters are known. This permits a better understanding of the overall pharmacology of the drug, potential routes of administration, tissue distribution and establishing an appropriate dosing regimen.Our objectives in this proposal are:To assemble library of all approved drugs/clinical molecules (~ 4,000)Screen the library against bacterial and fungal pathogens and Identifying drugs/molecules with promising activityIdentifying the mechanism of action (MOA) and target(s) of the non-antimicrobial drugs
Project Methods
1-Assembling the library of clinical drugs: A major challenge to repurposing approved drugs pertains to the lack of accessibility to libraries containing clinical drug collections. No single collection of the nearly 10,000 known drugs/clinical safe compounds currently exists (Chong and Sullivan, 2007b). Only 40% (~ 4,000 drugs) of the total known approved drugs/clinical safe compounds are available for screening and these drugs are dispersed throughout several different collections. We have already assembled 50% of the commercially available compounds (~ 2,000 drugs: from: 727-NIH Clinical Collections 1 and 2, 1,600-Pharmakon from Microsource, and few small libraries). We identified the remaining 50% of the drugs (the National Institute of Neurological Disorders and Stroke (NINDS) collection of 1,040 compounds, the Prestwick Chemical Library of 1,280 drugs, and the Johns Hopkins Clinical Compound Library of more than 1,500 compounds) (Chong and Sullivan, 2007b). Combined with other drug collections available in our lab, these collections will represent all drugs/clinical molecules (~ 4,000) available for commercial purchase. However, there is redundancy and overlap between these different libraries, which presents an additional problem as a compound may be present in more than one collection making screening these compounds more difficult. Non-redundant collection containing (~ 4,000 drugs) will be assembled at 1 mM concentration in 384 well plates to facilitate the high throughput screening (HTS). 2 Whole-cell screening against multidrug resistant pathogens: The assembled library above will be screened (Cheng et al., 2010) against multidrug resistant pathogens. We will start with ESKAPE pathogens (E. faecium, S. aureus, K. pneumoniae, A. baumannii, P. aeruginosa, and E. coli), which can be later expanded to any other pathogen, in 384-well plates at 8 µM concentration in triplicate in a High Throughput Screening Facility at Purdue University. The identified hits (drugs) will be subjected to a secondary manual screen in 96-well plates and according to guidelines of the Clinical and Laboratory Standards (CLSI) (NCCLS, 2012) to determine minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of the drugs against ESKAPE. Drugs with direct antimicrobial activity will be identified and screening against additional pathogens of veterinary important. Our findings in ESKAPE pathogens will be broadly relevant to other pathogens and should significantly impact and inform efforts to repurpose therapies against multidrug resistant pathogens.3-dentifying the mechanism of action (MOA) and target(s) of the non-antimicrobial drugsUnderstanding the mechanism of action of a novel antibiotic is an essential step in drug development research. Connecting an antimicrobial compound to its cellular target is a critical step for improving the affinity, selectivity, and antibacterial properties of the drug.Our approach toward identifying the MOA and target will focus mutation and mapping of the mutants. Bacterial Mutants resistant to the drug will be generated in-vitro by two methods: a) large volume of logarithmic culture of the bacteria will be concentrated to 1011-1012 CFU/ml and added to IsoSensitest agar containing 2X, 4X, 10X and 20X MIC drug (MacLeod et al., 2009; Martinez and Baquero, 2000; O'Neill et al., 2001; Zurenko et al., 1996). 10 plates will be used for each concentration (With 10 agar plates, mutations could potentially be detected at frequencies of 1 in 1011 (O'Neill et al., 2001)).b) Using an alternative approach, drug mutants will be isolated by multiple passage methods through progressively increasing concentration of drug in liquid culture (Lama et al., 2012; Peleg et al., 2012). Bacterial cultures that grew at the highest concentrations of drug will be used as an inoculum for the subsequent culture. Colonies from a&b methods above will be selected and stable mutants to the drug will be confirmed (MacLeod et al., 2009; Martinez and Baquero, 2000).Genomic DNA will be isolated from single colonies using standard methods (Skovgaard et al., 2011). Bar coded indexed sequencing libraries will be constructed using standard kits. The Illumina HiSeq 2500 platform (Purdue University Genome Facility) will be used to sequence the mutants and the parenteral strain on one lane using Rapid Run mode that would result in 9-10 million reads per sample. Mapping and Assembly with Qualities software (Purdue University Bioinformatics Facility) will be utilized to map the reads produced by the Illumina sequencer to the reference genome (parental reference strain). Individual high-confidence SNP will be identified. Genetic variant annotation and effect prediction software (snpEff and snpSift) will be utilized to predict the impact of a specific mutation on protein function (Comas et al., 2012; Ng and Henikoff, 2003). Select SNPs will be confirmed independently by PCR amplifying and sequencing of the PCR product.

Progress 10/01/17 to 11/13/20

Outputs
Target Audience:Local scientific communities and investigators in academic units (College of Science, Veterinary Medicine, Chemistry,Agriculture and food science), related disciplines (Pharmacy, Agriculture, and College of Medicine) in West Lafayettecampus, Bindley Bioscience Center, and Birck Nanotechnology Center, Purdue Center for Cancer Research. Also public audience through news letter and podcast. Changes/Problems:Dr. Seleem left Purdue University during the reporting period. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Antimicrobial resistance among bacterial and fungal pathogens has caused a severe shortage of effective drugs to treat infections. One strategy to address this is to test the antimicrobial activity of existing drugs used non-infectious disease indications. Such drugs usually have well known safety and pharmaceutical profiles. Dr. Seleem's research group has screened large libraries of drugs for toxicity against various human and animal bacterial and fungal pathogens. This "repurposing" approach has identified several drugs with antimicrobial activity. Further chemical and structural modifications of these drugs are pursued to improve the efficacy of the identified compounds.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: AbdelKhalek A, Seleem MN.Repurposing the Veterinary Antiprotozoal Drug Ronidazole for the Treatment of Clostridioides difficile Infection. Int J Antimicrob Agents. 2020 Oct 9:106188. doi: 10.1016/j.ijantimicag.2020.106188. Online ahead of print. PMID: 33045352
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Eldesouky HE, Salama EA, Lanman NA, Hazbun TR, Seleem MN.Potent synergistic interactions between lopinavir and azole antifungal drugs against emerging multidrug-resistant Candida auris. Antimicrob Agents Chemother. 2020 Oct 12:AAC.00684-20. doi: 10.1128/AAC.00684-20. Online ahead of print. PMID: 33046487
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Seong YJ, Alhashimi M, Mayhoub A, Mohammad H, Seleem MN. Repurposing Fenamic Acid Drugs To Combat Multidrug-Resistant Neisseria gonorrhoeae. Antimicrob Agents Chemother. 2020 Jun 23;64(7):e02206-19. doi: 10.1128/AAC.02206-19. Print 2020 Jun 23.PMID: 32393483
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Abutaleb NS, Seleem MN. Auranofin, at clinically achievable dose, protects mice and prevents recurrence from Clostridioides difficile infection. Sci Rep. 2020 May 7;10(1):7701. doi: 10.1038/s41598-020-64882-9. PMID: 32382070 Free PMC article.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Eldesouky HE, Salama EA, Li X, Hazbun TR, Mayhoub AS, Seleem MN.Repurposing approach identifies pitavastatin as a potent azole chemosensitizing agent effective against azole-resistant Candida species. Sci Rep. 2020 May 5;10(1):7525. doi: 10.1038/s41598-020-64571-7. PMID: 32372011 Free PMC article.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Mohammad H, Abutaleb NS, Seleem MN. Auranofin Rapidly Eradicates Methicillin-resistant Staphylococcus aureus (MRSA) in an Infected Pressure Ulcer Mouse Model. Sci Rep. 2020 Apr 29;10(1):7251. doi: 10.1038/s41598-020-64352-2. PMID: 32350417 Free PMC article.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Eldesouky HE, Salama EA, Hazbun TR, Mayhoub AS, Seleem MN. Ospemifene displays broad-spectrum synergistic interactions with itraconazole through potent interference with fungal efflux activities. Sci Rep. 2020 Apr 8;10(1):6089. doi: 10.1038/s41598-020-62976-y. PMID: 32269301 Free PMC article.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Abutaleb NS, Seleem MN. Repurposing the Antiamoebic Drug Diiodohydroxyquinoline for Treatment of Clostridioides difficile Infections. Antimicrob Agents Chemother. 2020 May 21;64(6):e02115-19. doi: 10.1128/AAC.02115-19. Print 2020 May 21. PMID: 32253206
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Pal R, Seleem MN. Screening of Natural Products and Approved Oncology Drug Libraries for Activity against Clostridioides difficile. Sci Rep. 2020 Apr 6;10(1):5966. doi: 10.1038/s41598-020-63029-0. PMID: 32249833 Free PMC article.


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:Local scientific communities and investigators in academic units (College of Science, Veterinary Medicine, Chemistry,Agriculture and food science), related disciplines (Pharmacy, Agriculture, and College of Medicine) in West Lafayettecampus, Bindley Bioscience Center, and Birck Nanotechnology Center, Purdue Center for Cancer Research. Also public audience through news letter and podcast Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?The results were shared with local scientific communities, collaborators and interested academic units. The results also were published in peer reviewed journals. Several podcast and news reports were made available to the public to disseminate the information. What do you plan to do during the next reporting period to accomplish the goals?Screen the library against additional bacterial and fungal pathogens andIdentifying drugs/molecules with promising activity. Synthesis more potent compoudns

Impacts
What was accomplished under these goals? Antifungal Drug Discovery: We developed a robust whole-cell screening assay to explore the ability of FDA-approved drugs in restoring the antifungal activity of fluconazole against a multidrug-resistant emerging pathogen Candida auris Our screen revealed several drugs with potent activity including, lopinavir (HIV antiviral) and aprepitant (an antiemetic) with ability to restore the fluconazole susceptibility in C. auris Lopinavir and aprepitant displayed broad-spectrum synergistic interactions with itraconazole against all the tested C. auris isolates. These potent synergistic interactions were validated in vivo in a Caenorhabditis elegans infection model. Moreover, combinations of itraconazole and lopinavir (or aprepitant) displayed a significant broad-spectrum antifungal activity against other Candida species such as C. albicans, C. glabrata, C. krusie, C. tropicalis, and C. parapsilosis. Our preliminary data indicate a significant ability of lopinavir to interfere with both ABC and MFS efflux activities in C. albicans. We are moving forward with mechanistic study and preliminary in vivo mice experiment to support our R01 application Antibacterial Drug Discovery: We will report our repurposing progress in two bacterial pathogens (Vancomycin resistant enterococci-VRE and Neisseria gonorrhoeae) Vancomycin resistant enterococci Our initial screen of ~ 3,800 FDA approved drugs and clinical molecules against vancomycin- resistant enterococcus species identified carbonic anhydrase inhibitors (CAIs) with potent and specific anti-enterococcal activity within clinical range (acetazolamide, dorzolamide, brinzolamide, ethoxzolamide, methazolamide, and dichlorphenamide) Our team has also identified a potential unique target in enterococcus by isolating resistant bacteria to acetazolamide. Our team has begun medicinal chemistry structure-activity relationship (SAR) studies to optimize acetazolamide for improved potency versus enterococcus species while maintaining selectivity over the normal gut microbiota To date we have synthesized and tested 29 analogs of AZM versus VRE and improved the potency of the scaffold versus VRE by approximately 570-fold. The goal of synthesis of these molecules was to optimize AZM for improved potency versus enterococcus species while maintaining selectivity over the normal gut microbiota. Also we wanted to have molecules with less absorption in the intestinal tract to be tested for VRE intestinal decolonization. While the PK for these new analogs yet to be defined, molecule 8 was scaled-up (~200 mg) and an in vivo efficacy study and toxicity study were performed. Acetazolamide analogs were superior to linezolid and acetazolamide in reducing VRE in feces, caeca and ilea of infected mice. R01 application and DoD application were submitted and both were awarded and we decided to accept R01 application ($3,717,432) and decline DOD.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Abdelkhalek A., N. Abutaleb, H. Mohammad & M. N. Seleem. (2019). Antibacterial and antivirulence activities of auranofin against Clostridium difficile. International Journal of Antimicrobial Agents 53: 54-62 M. Alhashimi, A. Mayhoub & M. N. Seleem. (2019). Repurposing salicylamide for combating multidrug-resistant Neisseria gonorrhoeae. Antimicrobial Agents and Chemotherapy. 10.1128/AAC.01225-19 N. S. Abutaleb & M. N. Seleem. (2019). Antivirulence activity of auranofin against vancomycin-resistant enterococci: in vitro and in vivo studies. International Journal of Antimicrobial Agents. 26 October 2019. PMID:31669742 D. Mody, A. Athamneh, & M. N. Seleem. (2019). Curcumin: A natural derivative with antibacterial activity against Clostridium difficile. Journal of Global Antimicrobial Resistance. 2019 Oct 14. pii: S2213-7165(19)30259-0. PubMed PMID: 316226839


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:local scientific communities and investigators in academic units (College of Science, Veterinary Medicine, Chemistry, Agriculture and food science), related disciplines (Pharmacy, Agriculture, and College of Medicine) in West Lafayette campus, Bindley Bioscience Center, and Birck Nanotechnology Center, Purdue Center for Cancer Research Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?The results were shared with local scientific communities, collaborators and interested academic units. The results also were published in open access peer reviewed journals such as Plos One and Nature scientific reports What do you plan to do during the next reporting period to accomplish the goals?Confirm the identify of each drug in the library and screen the library against additional bacterial and fungal pathogens and Identifying drugs/molecules with promising activity. Move to animal testing.

Impacts
What was accomplished under these goals? We accomplished first goal and were able to assembled library of all approved drugs/clinical molecules (~ 4,000). Also we were able to screen the library against some important microorganisms such as vancomycin resistant enterococci and candida albicans. We identified promising molecules that were tested further against these clinical isolates. The promising molecules (such as niclosamide, auranofin, ebselen) showed potent activity against all test pathogens. Some of the molecules such as niclosamide and auranofin, the microorganisms failed to form resistant against them and they could be move forward to animal testing. All the drugs tested for toxicity and proved to be not toxic at the concentration that kills bacteria.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: A. Abdelkhalek, N. Abutaleb, H. Mohammad, M. N. Seleem*. (2018). Repurposing ebselen for decolonization of vancomycin-resistant enterococci (VRE). Plos One 13 (6), e0199710 A. Abdelkhalek, N. Abutaleb, K. Elmagarmid, M. N. Seleem. (2018). Repurposing Auranofin as an Intestinal Decolonizing Agent for Vancomycin-Resistant Enterococci. Scientific Reports 8 (1), 8353 H. Mohammad, A. Abdelkhalek, N. Abutaleb, and M. N. Seleem*. (2018). Evaluation of the Anthelmintic Drug Niclosamide for Intestinal Decolonization of Vancomycin-resistant Enterococci" International Journal of Antimicrobial Agents 51 (6), 897-904. H. Eldesouky, A. Mayhoub, T. R. Hazbun, and M. N. Seleem*. (2018). Reversal of azole resistance in Candida albicans by sulfa antibacterial drugs. Antimicrobial Agents and Chemotherapy 62 (3), e00701-17.