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Structure-guided directed evolution of highly selective p450-based magnetic resonance imaging sensors for dopamine and serotonin.

Brustad EM, Lelyveld VS, Snow CD, Crook N, Jung ST, Martinez FM, Scholl TJ, Jasanoff A, Arnold FH
J Mol Biol 422 245-62 (2012)
Related entries: 4dtw, 4dty, 4dtz, 4du2, 4dua, 4duc, 4dud, 4due, 4duf

Cited: 25 times
EuropePMC logo PMID: 22659321

Abstract

New tools that allow dynamic visualization of molecular neural events are important for studying the basis of brain activity and disease. Sensors that permit ligand-sensitive magnetic resonance imaging (MRI) are useful reagents due to the noninvasive nature and good temporal and spatial resolution of MR methods. Paramagnetic metalloproteins can be effective MRI sensors due to the selectivity imparted by the protein active site and the ability to tune protein properties using techniques such as directed evolution. Here, we show that structure-guided directed evolution of the active site of the cytochrome P450-BM3 heme domain produces highly selective MRI probes with submicromolar affinities for small molecules. We report a new, high-affinity dopamine sensor as well as the first MRI reporter for serotonin, with which we demonstrate quantification of neurotransmitter release in vitro. We also present a detailed structural analysis of evolved cytochrome P450-BM3 heme domain lineages to systematically dissect the molecular basis of neurotransmitter binding affinity, selectivity, and enhanced MRI contrast activity in these engineered proteins.

Articles - 4dub mentioned but not cited (1)

  1. Structure-guided directed evolution of highly selective p450-based magnetic resonance imaging sensors for dopamine and serotonin. Brustad EM, Lelyveld VS, Snow CD, Crook N, Jung ST, Martinez FM, Scholl TJ, Jasanoff A, Arnold FH. J Mol Biol 422 245-262 (2012)


Reviews citing this publication (11)

  1. A review of responsive MRI contrast agents: 2005-2014. Hingorani DV, Bernstein AS, Pagel MD. Contrast Media Mol Imaging 10 245-265 (2015)
  2. Molecular fMRI. Bartelle BB, Barandov A, Jasanoff A. J Neurosci 36 4139-4148 (2016)
  3. Probing the brain with molecular fMRI. Ghosh S, Harvey P, Simon JC, Jasanoff A. Curr Opin Neurobiol 50 201-210 (2018)
  4. Metalloprotein-based MRI probes. Matsumoto Y, Jasanoff A. FEBS Lett 587 1021-1029 (2013)
  5. Strategies for sensing neurotransmitters with responsive MRI contrast agents. Angelovski G, Tóth É. Chem Soc Rev 46 324-336 (2017)
  6. Beyond the outer limits of nature by directed evolution. Molina-Espeja P, Viña-Gonzalez J, Gomez-Fernandez BJ, Martin-Diaz J, Garcia-Ruiz E, Alcalde M. Biotechnol Adv 34 754-767 (2016)
  7. Rational heme protein design: all roads lead to Rome. Lin YW, Sawyer EB, Wang J. Chem Asian J 8 2534-2544 (2013)
  8. A brief review of non-invasive brain imaging technologies and the near-infrared optical bioimaging. Kim B, Kim H, Kim S, Hwang YR. Appl Microsc 51 9 (2021)
  9. Lanthanide Complexes in Molecular Magnetic Resonance Imaging and Theranostics. Lacerda S, Tóth É. ChemMedChem 12 883-894 (2017)
  10. A Promiscuous Bacterial P450: The Unparalleled Diversity of BM3 in Pharmaceutical Metabolism. Thistlethwaite S, Jeffreys LN, Girvan HM, McLean KJ, Munro AW. Int J Mol Sci 22 11380 (2021)
  11. Molecular fMRI of neurochemical signaling. Wei H, Frey AM, Jasanoff A. J Neurosci Methods 364 109372 (2021)

Articles citing this publication (13)

  1. Navigating the protein fitness landscape with Gaussian processes. Romero PA, Krause A, Arnold FH. Proc Natl Acad Sci U S A 110 E193-201 (2013)
  2. Molecular-level functional magnetic resonance imaging of dopaminergic signaling. Lee T, Cai LX, Lelyveld VS, Hai A, Jasanoff A. Science 344 533-535 (2014)
  3. In vivo continuous evolution of genes and pathways in yeast. Crook N, Abatemarco J, Sun J, Wagner JM, Schmitz A, Alper HS. Nat Commun 7 13051 (2016)
  4. Local and global consequences of reward-evoked striatal dopamine release. Li N, Jasanoff A. Nature 580 239-244 (2020)
  5. Molecular fMRI of Serotonin Transport. Hai A, Cai LX, Lee T, Lelyveld VS, Jasanoff A. Neuron 92 754-765 (2016)
  6. Identification of Mechanism-Based Inactivation in P450-Catalyzed Cyclopropanation Facilitates Engineering of Improved Enzymes. Renata H, Lewis RD, Sweredoski MJ, Moradian A, Hess S, Wang ZJ, Arnold FH. J Am Chem Soc 138 12527-12533 (2016)
  7. Nanosensors for the Chemical Imaging of Acetylcholine Using Magnetic Resonance Imaging. Luo Y, Kim EH, Flask CA, Clark HA. ACS Nano 12 5761-5773 (2018)
  8. Porphyrin-substituted H-NOX proteins as high-relaxivity MRI contrast agents. Winter MB, Klemm PJ, Phillips-Piro CM, Raymond KN, Marletta MA. Inorg Chem 52 2277-2279 (2013)
  9. Neurotransmitter-Responsive Nanosensors for T2-Weighted Magnetic Resonance Imaging. Hsieh V, Okada S, Wei H, García-Álvarez I, Barandov A, Alvarado SR, Ohlendorf R, Fan J, Ortega A, Jasanoff A. J Am Chem Soc 141 15751-15754 (2019)
  10. P450 BM3 crystal structures reveal the role of the charged surface residue Lys/Arg184 in inversion of enantioselective styrene epoxidation. Shehzad A, Panneerselvam S, Linow M, Bocola M, Roccatano D, Mueller-Dieckmann J, Wilmanns M, Schwaneberg U. Chem Commun (Camb) 49 4694-4696 (2013)
  11. A Protein-Based Biosensor for Detecting Calcium by Magnetic Resonance Imaging. Ozbakir HF, Miller ADC, Fishman KB, Martins AF, Kippin TE, Mukherjee A. ACS Sens 6 3163-3169 (2021)
  12. A DNA-Based MRI Contrast Agent for Quantitative pH Measurement. Seo H, Ma KY, Tuttle EE, Calderon IAC, Buskermolen AD, Flask CA, Clark HA. ACS Sens 6 727-732 (2021)
  13. Designing Protein-Based Probes for Sensing Biological Analytes with Magnetic Resonance Imaging. Yun J, Baldini M, Chowdhury R, Mukherjee A. Anal Sens 2 e202200019 (2022)


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