A functional group-guided approach to aptamers for small molecules
Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of individual functional groups on small molecules to binding within 27 target-aptamer pairs, identifying potential hindrances to receptor isolatio...
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| Published in | Science (American Association for the Advancement of Science) Vol. 380; no. 6648; pp. 942 - 948 |
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| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
02.06.2023
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of individual functional groups on small molecules to binding within 27 target-aptamer pairs, identifying potential hindrances to receptor isolation-for example, negative cooperativity between sterically hindered functional groups. To increase the probability of aptamer isolation for important targets, such as leucine and voriconazole, for which multiple previous selection attempts failed, we designed tailored strategies focused on overcoming individual structural barriers to successful selections. This approach enables us to move beyond standardized protocols into functional group-guided searches, relying on sequences common to receptors for targets and their analogs to serve as anchors in regions of vast oligonucleotide spaces wherein useful reagents are likely to be found. |
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| AbstractList | Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of individual functional groups on small molecules to binding within 27 target-aptamer pairs, identifying potential hindrances to receptor isolation—for example, negative cooperativity between sterically hindered functional groups. To increase the probability of aptamer isolation for important targets, such as leucine and voriconazole, for which multiple previous selection attempts failed, we designed tailored strategies focused on overcoming individual structural barriers to successful selections. This approach enables us to move beyond standardized protocols into functional group–guided searches, relying on sequences common to receptors for targets and their analogs to serve as anchors in regions of vast oligonucleotide spaces wherein useful reagents are likely to be found.
Developing highly selective aptamers, folded RNA or DNA oligonucleotides that bind to ligands, is a challenge because the sequence space is difficult to explore efficiently, nucleotides have limited chemical functionality, and methods for predicting RNA structure are not very accurate. Yang
et al
. developed an approach for sequential optimization of aptamers by modifying the target molecule with various functional groups. To design a sensor for the amino acid leucine, they used multiple derivatives to isolate aptamers with high affinity and selectivity. They then used a stepwise approach based on substructure to generate an aptamer for the antifungal drug voriconazole. —Michael A. Funk
Concepts from organic and medicinal chemistry guide isolation of aptamers for small-molecule targets. Editor’s summaryDeveloping highly selective aptamers, folded RNA or DNA oligonucleotides that bind to ligands, is a challenge because the sequence space is difficult to explore efficiently, nucleotides have limited chemical functionality, and methods for predicting RNA structure are not very accurate. Yang et al. developed an approach for sequential optimization of aptamers by modifying the target molecule with various functional groups. To design a sensor for the amino acid leucine, they used multiple derivatives to isolate aptamers with high affinity and selectivity. They then used a stepwise approach based on substructure to generate an aptamer for the antifungal drug voriconazole. —Michael A. Funk Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of individual functional groups on small molecules to binding within 27 target-aptamer pairs, identifying potential hindrances to receptor isolation-for example, negative cooperativity between sterically hindered functional groups. To increase the probability of aptamer isolation for important targets, such as leucine and voriconazole, for which multiple previous selection attempts failed, we designed tailored strategies focused on overcoming individual structural barriers to successful selections. This approach enables us to move beyond standardized protocols into functional group-guided searches, relying on sequences common to receptors for targets and their analogs to serve as anchors in regions of vast oligonucleotide spaces wherein useful reagents are likely to be found. Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of individual functional groups on small molecules to binding within 27 target-aptamer pairs, identifying potential hindrances to receptor isolation, for example, negative cooperativity between sterically hindered functional groups. To increase the probability of aptamer isolation for important targets, such as leucine and voriconazole, where multiple previous selection attempts failed, we designed tailored strategies focused on overcoming individual structural barriers to successful selections. This approach enables us to move beyond standardized protocols into functional group-guided searches, relying on sequences common to receptors for targets and their analogs to serve as anchors in regions of vast oligonucleotide spaces wherein useful reagents are likely to be found. Concepts from organic and medicinal chemistry guide isolation of aptamers for small molecule targets. |
| Author | Sajjath, Sairaj Yang, Kyungae Zhang, Yameng Worgall, Tilla S Taylor, Steven Stevens, Jacob Banerjee, Saswata Kostic, Aleksandra M Wong, Isabel Mitchell, Noelle M Cheng, Zhenzhuang Andrews, Anne M Mohan, Sumit Landry, Donald W Stojanovic, Milan N |
| AuthorAffiliation | 6 Departments of Biomedical Engineering, Fu Foundation School of Engineering and Applied Science, and Systems Biology, Columbia University Irving Medical Center, New York, NY 10032, USA 1 Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA 4 Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, NY 10032, USA 5 Department of Psychiatry & Biobehavioral Sciences and Hatos Center for Neuropharmacology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA 2 Department of Chemistry & Biochemistry and California Nanosystems Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA 3 Department of Epidemiology, Mailman School of Public Health, New York, NY 10032, USA |
| AuthorAffiliation_xml | – name: 6 Departments of Biomedical Engineering, Fu Foundation School of Engineering and Applied Science, and Systems Biology, Columbia University Irving Medical Center, New York, NY 10032, USA – name: 5 Department of Psychiatry & Biobehavioral Sciences and Hatos Center for Neuropharmacology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA – name: 4 Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, NY 10032, USA – name: 1 Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – name: 3 Department of Epidemiology, Mailman School of Public Health, New York, NY 10032, USA – name: 2 Department of Chemistry & Biochemistry and California Nanosystems Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA |
| Author_xml | – sequence: 1 givenname: Kyungae orcidid: 0000-0001-5575-4107 surname: Yang fullname: Yang, Kyungae organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 2 givenname: Noelle M orcidid: 0009-0002-0263-240X surname: Mitchell fullname: Mitchell, Noelle M organization: Department of Chemistry and Biochemistry and California Nanosystems Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA – sequence: 3 givenname: Saswata orcidid: 0009-0000-5686-5087 surname: Banerjee fullname: Banerjee, Saswata organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 4 givenname: Zhenzhuang surname: Cheng fullname: Cheng, Zhenzhuang organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 5 givenname: Steven surname: Taylor fullname: Taylor, Steven organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 6 givenname: Aleksandra M orcidid: 0000-0003-4525-2773 surname: Kostic fullname: Kostic, Aleksandra M organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 7 givenname: Isabel orcidid: 0009-0007-8783-3054 surname: Wong fullname: Wong, Isabel organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 8 givenname: Sairaj orcidid: 0000-0002-7156-3279 surname: Sajjath fullname: Sajjath, Sairaj organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 9 givenname: Yameng orcidid: 0009-0005-7038-7049 surname: Zhang fullname: Zhang, Yameng organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 10 givenname: Jacob orcidid: 0000-0001-9614-1673 surname: Stevens fullname: Stevens, Jacob organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 11 givenname: Sumit orcidid: 0000-0002-5305-9685 surname: Mohan fullname: Mohan, Sumit organization: Department of Epidemiology, Mailman School of Public Health, New York, NY 10032, USA – sequence: 12 givenname: Donald W orcidid: 0000-0003-4046-5665 surname: Landry fullname: Landry, Donald W organization: Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 13 givenname: Tilla S orcidid: 0000-0002-0587-5223 surname: Worgall fullname: Worgall, Tilla S organization: Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, NY 10032, USA – sequence: 14 givenname: Anne M orcidid: 0000-0002-1961-4833 surname: Andrews fullname: Andrews, Anne M organization: Department of Psychiatry and Biobehavioral Sciences and Hatos Center for Neuropharmacology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA – sequence: 15 givenname: Milan N orcidid: 0000-0001-6340-0982 surname: Stojanovic fullname: Stojanovic, Milan N organization: Departments of Biomedical Engineering, Fu Foundation School of Engineering and Applied Science, and Systems Biology, Columbia University Irving Medical Center, New York, NY 10032, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37262137$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current affiliation: Rutgers New Jersey Medical School, Newark, NJ, USA. Current affiliation: Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, NY, USA. Current affiliation: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA. Author contributions: K.Y. and M.N.S. conceptualized the approach and designed the experiments; K.Y. isolated all aptamers for amines and amino acids, S.B. isolated aptamers for two amides, under her supervision. Z.C. synthesized voriconazole analogs. A.K. was a high-school student supported by the NSF and I.W. was an undergraduate student on an NSF REU (CCF1518715, 1763632). They both optimized and characterized aptamers. S.S. worked on epinephrine aptamers and Y.Z. was an undergraduate student who worked on isolating methylene blue aptamers, while supervised by S.T and K.Y. D.W.L. initiated research on aptamers in general, helped formulate an early version of this manuscript and suggested experiments, while J.S. and S.M. initiated the research on voriconazole aptamers and helped design parameters of initial selection experiments. T.S.W. initiated research on amino acids and ammonia and helped design early selection experiments with these targets. N.M.M. and A.M.A. produced and analyzed isothermal calorimetry data, while A.M.A also helped define neurotransmitter targets and parameters for selections. M.N.S. is responsible for all free energy calculations, he initially drafted the manuscript, while M.N.S., K.Y., N.M.M., and A.M.A. produced the final manuscript form, with input and approval from all authors. |
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| Snippet | Aptameric receptors are important biosensor components, yet our ability to identify them depends on the target structures. We analyzed the contributions of... Editor’s summaryDeveloping highly selective aptamers, folded RNA or DNA oligonucleotides that bind to ligands, is a challenge because the sequence space is... |
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| SubjectTerms | Amino acids Aptamers Functional groups Fungicides Leucine Nucleotide sequence Nucleotides Oligonucleotides Optimization Ribonucleic acid RNA Voriconazole |
| Title | A functional group-guided approach to aptamers for small molecules |
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