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http://pubs.acs.org/page/vi/2013/brain_initiative Chemistry and the BRAIN Initiative The Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative embraces the concept that deciphering brain function will depend on new means of interrogating large numbers of neurons and making sense of the resulting data. Undoubtedly, the contributions of chemists have been and will continue to be central to these efforts. This virtual issue highlights advances of relevance to the BRAIN Initiative and includes articles, letters, reviews, perspectives, and editorials recently published in ACS Chemical Neuroscience, ACS Nano, Analytical Chemistry, and the Journal of the American Chemical Society. These journals encourage continued submission of such high-quality, high impact manuscripts Synopses for this collection were written by Erika Gebel Berg, Eva J. Gordon, Deirdre Lockwood, Jenny Morber, and Jeffrey M. Perkel. Go to the JACS Select interviews page, where you can listen to the podcast interview with two of the guest editors of this JACS Select collection, Anne Andrews and Paul Weiss. Editorials Chemistry and the BRAIN Initiative Anne M. Andrews, Alanna Schepartz, Jonathan Sweedler, and Paul S. Weiss J. Am. Chem. Soc., Article ASAP DOI: 10.1021/ja4118347 Nano in the Brain: Nano-Neuroscience Anne M. Andrews and Paul S. Weiss ACS Nano, 2012, 6 (10), pp 8463–8464 DOI: 10.1021/nn304724q The BRAIN Initiative: Toward a Chemical Connectome Anne M. Andrews ACS Chem. Neurosci., 2012, 4(5), pp 645-645 DOI: 10.1021/cn4001044 Reviews 3D Imaging by Mass Spectrometry: A New Frontier Erin H. Seeley and Richard M. Caprioli* Anal. Chem., 2012, 84(5), pp 2105-2110 DOI: 10.1021/ac2032707 Unparalleled Control of Neural Activity Using Orthogonal Pharmacogenetics Mikhail G. Shapiro*, Shawnalea J. Frazier, and Henry A. Lester ACS Chem. Neurosci., 2012, 3(8), pp 619-629 DOI: 10.1021/cn300053q Genetically Engineered Fluorescent Voltage Reporters Hiroki Mutoh, Walther Akemann, and Thomas Knöpfel* ACS Chem. Neurosci., 2012, 3(8), pp 585-592 DOI: 10.1021/cn300041b In Vivo Application of Optogenetics for Neural Circuit Analysis Xue Han ACS Chem. Neurosci., 2012, 3(8), pp 577-584 DOI: 10.1021/cn300065j Ultrafast Detection and Quantification of Brain Signaling Molecules with Carbon Fiber Microelectrodes Rinchen D. Lama, Karl Charlson, Arun Anantharam, and Parastoo Hashemi* Anal. Chem., 2012, 84(19), pp 8096-8101 DOI: 10.1021/ac301670h Chemical Analysis of Single Cells Raphaël Trouillon, Melissa K. Passarelli, Jun Wang, Michael E. Kurczy, and Andrew G. Ewing* Anal. Chem., 2013, 85(2), pp 522-542 DOI: 10.1021/ac303290s Nanotools for Neuroscience and Brain Activity Mapping A. Paul Alivisatos, Anne M. Andrews, Edward S. Boyden, Miyoung Chun, George M. Church, Karl Deisseroth, John P. Donoghue, Scott E. Fraser, Jennifer Lippincott-Schwartz, Loren L. Looger, Sotiris Masmanidis*, Paul L. McEuen, Arto V. Nurmikko, Hongkun Park, Darcy S. Peterka, Clay Reid, Michael L. Roukes, Axel Scherer*, Mark Schnitzer, Terrence J. Sejnowski, Kenneth L. Shepard, Doris Tsao, Gina Turrigiano, Paul S. Weiss*, Chris Xu, Rafael Yuste*, and Xiaowei Zhuang ACS Nano, 2013, 7(3), pp 1850-1866 DOI: 10.1021/nn4012847 Articles Native Serotonin Membrane Receptors Recognize 5-Hydroxytryptophan-Functionalized Substrates: Enabling Small-Molecule Recognition Amit Vaish, Mitchell J. Shuster, Sarawut Cheunkar, Yogesh S. Singh, Paul S. Weiss and Anne M. Andrews* ACS Chem. Neurosci., 2010, 1(7), pp 495-504 DOI: 10.1021/cn1000205 Synposis: Anchoring small molecules, such as neurotransmitters, to surfaces is an important means by which to explore their interactions with large biomolecules, including proteins, lipids, and DNA. However, neurotransmitter receptors have evolved to recognize small-molecule partners as they diffuse freely through the cellular environment, posing an inherent challenge to the anchoring approach. Anne Andrews and co-workers overcome this challenge by nanoengineering surfaces capable of mimicking the neurotransmitter serotonin in solution. By attaching a slightly larger molecular precursor of serotonin, called 5-hydroxytryptophan, to gold surfaces with highly structured single layers of organic molecules, the key elements of serotonin are preserved, allowing recognition by native serotonin receptors. This strategy can be extended to developing improved nanomaterials for other small molecules for molecular recognition studies and identifying artificial receptors for future use in brain nanobiosensing. Tunable Growth Factor Delivery from Injectable Hydrogels for Tissue Engineering Katarina Vulic and Molly S. Shoichet* J. Am. Chem. Soc., 2012, 134(2), pp 882-885 DOI: 10.1021/ja210638x Synposis: Protein therapeutics have been designed to treat a variety of diseases, but because they are unstable and easily degraded in the body and traditional encapsulation strategies, it is challenging to deliver them to patients. To overcome these hurdles, scientists have immobilized proteins in gel-like matrices to control release of the protein. Now Katarina Vulic and Molly Shoichet enhance this technique by preparing a polysaccharide gel that can deliver any protein at a tunable rate. The gel, which can be injected into any tissue or organ, including the spinal cord or brain, carries a peptide that binds a proline-rich regulatory protein domain. Once this domain is fused to a therapeutic protein, researchers can control its release rate by changing the peptide concentration or using peptides with different binding affinities. Sodium Sensing in Neurons with a Dendrimer-Based Nanoprobe Christophe M. Lamy*, Olivier Sallin, Céline Loussert, and Jean-Yves Chatton ACS Nano, 2012, 6(2), pp 1176-1187 DOI: 10.1021/nn203822t Synposis: Christophe Lamy and colleagues have created a particle that expands researchers’ ability to watch live neurons interact. Neurons transmit information through electrical signals that are generated when the cell shuttles charged particles called ions from one place to another. To "watch" such fundamental processes in living cells, researchers can tag ions with molecules that give off light, or fluoresce. Unfortunately, previous fluorescent sodium-ion probes leaked quickly out of cells. Using a form of polymer called a dendrimer that traps fluorescent dyes inside, the researchers create a sodium probe that spreads well, stays inside cells, and does not interfere with cell behavior. Combined Elemental and Biomolecular Mass Spectrometry Imaging for Probing the Inventory of Tissue at a Micrometer Scale Andreas Matusch, Larissa S. Fenn, Candan Depboylu, Martin Klietz, Sven Strohmer, John A. McLean, and J. Sabine Becker* Anal. Chem., 2012, 84(7), pp 3170-3178 DOI: 10.1021/ac203112c Synposis: Mass spectrometry imaging can create maps of tissues and reveal the location of vital biomolecules within a sample. Using more than one type of mass spectrometry to analyze a biological sample may provide complementary information. Sabine Becker and colleagues combine laser ablation inductively coupled plasma mass spectrometry, which detects elements and isotopes, with matrix-assisted laser desorption/ionization ion mobility mass spectrometry, which can identify biomolecules, to generate images of mouse brain sections with and without tumors. They combine the data from the two methods to generate maps with both elemental and biomolecular information. The researchers observe an increase in certain metals and a drop in lipids in the vicinity of brain lesions, offering new insights linking morphology and chemistry within the brain. Variations in Binding Among Several Agonists at Two Stoichiometries of the Neuronal, α4β2 Nicotinic Receptor Ximena Da Silva Tavares, Angela P. Blum, Darren T. Nakamura, Nyssa L. Puskar, Jai A. P. Shanata, Henry A. Lester, and Dennis A. Dougherty* J. Am. Chem. Soc., 2012, 134(28), pp 11474-11480 DOI: 10.1021/ja3011379 Synposis: A better understanding of the molecular basis of nicotine addiction could help to improve an unfortunate effect of the smoking pandemic—that half of all tobacco users die from smoking-related causes. The addictive properties of tobacco stem from the interaction between the small molecule nicotine and a protein in the brain called the α4β2 nicotinic acetylcholine receptor. Dennis Dougherty and co-workers examine the interactions between α4β2 and nicotine and three other compounds that bind to α4β2: the neurotransmitter acetylcholine and two smoking cessation drugs, varenicline and cytisine. Using electrophysiology and protein engineering methods, the authors identify subtle differences in how each compound interacts with different forms of α4β2. These findings could help in the design of new agents to help people quit smoking. Seeing Citrulline: Development of a Phenylglyoxal-Based Probe To Visualize Protein Citrullination Kevin L. Bicker, Venkataraman Subramanian, Alexander A. Chumanevich, Lorne J. Hofseth, and Paul R. Thompson* J. Am. Chem. Soc., 2012, 134(41), pp 17015-17018 DOI: 10.1021/ja308871v Synposis: In a host of diseases including cancer, multiple sclerosis, and Alzheimer’s disease, researchers have observed abnormally high rates of a biochemical process called citrullination, in which residues of the amino acid arginine are hydrolyzed to citrulline. But the role of citrullination in these diseases is still unclear because citrulline is challenging and expensive to trace with chemical methods. Paul Thompson and co-workers have devised a new way to visualize citrullination using a sensitive, versatile, and easily synthesized molecular probe. Under acidic conditions, the probe, a rhodamine-phenylglyoxal conjugate, fluorescently labels protein residues that have been converted to citrulline. The method could help scientists clarify the role and targets of citrullination in diseases and identify potential disease biomarkers. Chemical Gradients within Brain Extracellular Space Measured using Low Flow Push–Pull Perfusion Sampling in Vivo Thomas R. Slaney, Omar S. Mabrouk, Kirsten A. Porter-Stransky, Brandon J. Aragona, and Robert T. Kennedy* ACS Chem. Neurosci., 2013, 4(2), pp 321-329 DOI: 10.1021/cn300158p Synposis: Brain heterogeneity at the cellular level is characterized by the fact that neurons use many different types of chemicals to carry out interneuronal signaling. However, chemical neurotransmitters function outside cells at low concentrations, making it difficult to measure their abundance with high spatial resolution. Robert Kennedy and colleagues describe a method to measure neurotransmitter levels with nanoliter precision. The team develops a "low flow push-pull perfusion" system comprising two fused silica capillaries in a polyimide sheath, and they use it to measure neurotransmitter and metabolite concentrations via liquid chromatography-mass spectrometry in anesthetized and awake animals. With these advances, the authors observe sharp concentration gradients over distances as small as 200 m in some cases. "The results show that gradients in basal concentrations of neurotransmitters and metabolites can exist between adjacent brain regions less than 1 mm apart," the authors conclude. Single Molecule Quantum-Confined Stark Effect Measurements of Semiconductor Nanoparticles at Room Temperature KyoungWon Park, Zvicka Deutsch, J. Jack Li, Dan Oron, and Shimon Weiss* ACS Nano, 2012, 6(11), pp 10013-10023 DOI: 10.1021/nn303719m Synposis: Nanoparticles and nanorods could serve as local high-resolution voltage sensors, according to this study by Shimon Weiss and his team. The technique relies on the quantum-confined Stark effect (QCSE), in which an external electric field changes the wavelengths of light absorbed and emitted by small particles. The study considers whether nanoparticles can yield a sizable QCSE at room temperature, and if the effect can be measured, and quickly, on a single particle. With a combination of numerical calculations and experiments, the researchers measure and simulate wavelength shifts for eight different nanoparticle formulations at the single-molecule scale. A Fluorescent Sensor for GABA and Synthetic GABAB Receptor Ligands Anastasiya Masharina, Luc Reymond, Damien Maurel, Keitaro Umezawa, and Kai Johnsson* J. Am. Chem. Soc., 2012, 134(46), pp 19026-19034 DOI: 10.1021/ja306320s Synposis: γ-Aminobutyric acid, or GABA, is the chief inhibitory neurotransmitter in the brain. GABA plays vital roles in neuronal communication and brain development, and numerous important drugs, including antidepressants, antianxiety agents, and anticonvulsants, work by enhancing its activity. Despite these key functions, few molecular tools are available to detect GABA in live cells. To this end, Kai Johnsson and co-workers report the creation of a fluorescent sensor for GABA, called GABA-Snifit. The sensor is capable of detecting GABA on the surface of live cells with high spatiotemporal resolution. This capability facilitates exploration of GABA biology and the potential of related compounds, including possible drug leads, to modulate the GABA signaling pathway. Light-Triggered Modulation of Cellular Electrical Activity by Ruthenium Diimine Nanoswitches Joyce G. Rohan, Y. Rose Citron, Alec C. Durrell, Lionel E. Cheruzel, Harry B. Gray, Robert H. Grubbs, Mark Humayun, Kathrin L. Engisch, Victor Pikov, and Robert H. Chow* ACS Chem. Neurosci., 2013, 4(4), pp 585-593 DOI: 10.1021/cn300213f Synposis: The ability to control neural function with light could enable future therapies aimed at inactivating debilitating memories or improving learning under conditions of cognitive impairment. Researchers have made important advances in the ability to control neuronal firing using light-actuated switches. The process is referred to as optogenetics, which often requires hacking genes to produce light-sensitive proteins. Now Robert Chow and co-workers present a technique that uses a man-made chemical compound and cell-friendly blue light to switch neurons on and off. Because previous methods required either high levels of foreign proteins or cell-damaging UV light, this new method brings us closer to the day that such technologies might be used treat human conditions like post-traumatic stress disorder or Alzheimer’s disease. Structure of Inclusions of Huntington’s Disease Brain Revealed by Synchrotron Infrared Microspectroscopy: Polymorphism and Relevance to Cytotoxicity William André, Christophe Sandt, Paul Dumas, Philippe Djian*, and Guylaine Hoffner* Anal. Chem., 2013, 85(7), pp 3765-3773 DOI: 10.1021/ac400038b Synposis: Huntington’s disease is an incurable genetic disorder related to the proliferation of protein clumps in the brain. Little is known about what the protein aggregates look like or how their structure contributes to disease, which has stymied attempts to develop targeted therapies. Philippe Djian, Guylaine Hoffner, and colleagues use synchrotron infrared microspectroscopy to tease out structural details of Huntington’s disease protein aggregates embedded in brain tissue samples. They discover that the aggregate structures vary, depending on their location in the brain. Plus, the protein clumps in the most severely damaged regions of the brain have a particular look, suggesting that these may represent the most toxic varieties. Improved Orange and Red Ca2+ Indicators and Photophysical Considerations for Optogenetic Applications Jiahui Wu, Lin Liu, Tomoki Matsuda, Yongxin Zhao, Aleksander Rebane, Mikhail Drobizhev, Yu-Fen Chang, Satoko Araki, Yoshiyuki Arai, Kelsey March, Thomas E. Hughes, Ken Sagou, Takaki Miyata, Takeharu Nagai*, Wen-hong Li*, and Robert E. Campbell* ACS Chem. Neurosci., 2013, 4(6), pp 963-972 DOI: 10.1021/cn400012b Synposis: In an emerging and powerful area of neuroscience, researchers have developed genetically encoded chemical switches that can control neuronal activity with light. These optogenetic tools are generally triggered at wavelengths in the ultraviolet to green range of the spectrum. But those wavelengths present a challenge for researchers who want to monitor calcium ion concentrations in cells during optogenetic activation. The excitation wavelengths of many imaging agents for calcium overlap with the active spectrum of optogenetic tools. Here, Takeharu Nagai, Wen-hong Li, Robert Campbell, and colleagues report on the development of genetically encoded calcium ion indicators that are excited in the orange to red range of the spectrum, circumventing issues associated with combined optogenetic and calcium imaging studies. This work is anticipated to advance high-resolution neural circuitry imaging by extending the spectral palette available for carrying out these studies. Optically Selective Two-Photon Uncaging of Glutamate at 900 nm Jeremy P. Olson, Hyung-Bae Kwon, Kevin T. Takasaki, Chiayu Q. Chiu, Michael J. Higley, Bernardo L. Sabatini, and Graham C. R. Ellis-Davies* J. Am. Chem. Soc., 2013, 135(16), pp 5954-5957 DOI: 10.1021/ja4019379 Synposis: "Caged" neurotransmitters are inactive until irradiated with a specific wavelength of light. Such molecules provide spatial and temporal control of neuronal signaling, yet they are difficult to multiplex. Now Graham Ellis-Davies and colleagues demonstrate a new caged glutamate that overcomes this limitation. DEAC450-Glu is efficiently activated under two-photon excitation at 900 nm but remains caged at 720 nm, where several other caged compounds work. This difference enables simultaneous studies of, for instance, glutamate and GABA signaling. "For synaptic physiology, this technological advance is an important breakthrough, as it may allow the study of how excitatory and inhibitory transmitters sculpt dendritic integration with single-synapse resolution," the authors conclude. Two-Photon Optical Interrogation of Individual Dendritic Spines with Caged Dopamine Roberto Araya, Victoria Andino-Pavlovsky, Rafael Yuste*, and Roberto Etchenique* ACS Chem. Neurosci., 2013, 4(8), pp 1163-1167 DOI: 10.1021/cn4000692 Synposis: The neurotransmitter dopamine has been implicated in normal neurophysiological and disease processes associated with reward/addiction and movement/Parkinson’s disease. Yet tools to study dopamine neurotransmission with high spatial resolution and across integrated brain circuits have not existed. Now Rafael Yuste, Roberto Etchenique, and colleagues rectify this issue with a novel photocaged dopamine. RuBi-Dopa, a ruthenium-bipyridine derivative, is inactive as a neurotransmitter until uncaged by two-photon excitation at 820 nm. Using RuBi-Dopa and a fluorescent calcium indicator, the authors observed rapid dopamine-induced physiological changes in individual dendritic spines that would have been possible using standard neurochemical and electrophysiology approaches. "This novel compound together with state-of-the-art techniques such as two-photon excitation and calcium imaging allows the mapping of functional dopamine receptors in brain tissue with exquisite spatial resolution in a noninvasive way," the authors conclude. Optical Strategies for Sensing Neuronal Voltage Using Quantum Dots and Other Semiconductor Nanocrystals Jesse D. Marshall* and Mark J. Schnitzer* ACS Nano, 2013, 7(5), pp 4601-4609 DOI: 10.1021/nn401410k Synposis: To understand how the brain works, we have to watch it in action. Necessary capabilities include high-speed data gathering, the ability to zoom in, and sensitivity to interactions over long distances. Researchers have made headway with optical reporters based on photosensitive dyes and fluorescent proteins, but fundamental constraints limit their use. Citing the many attributes of quantum dots for high-resolution voltage sensing, Jesse Marshall and Mark Schnitzer use a holistic theory-based approach to examine how nanocrystals’ voltage sensitivity depends on their material and structural properties. The researchers find that inhomogeneous particles often perform better than their more conventional counterparts. ExoSensor 517: A Dual-Analyte Fluorescent Chemosensor for Visualizing Neurotransmitter Exocytosis Jessica L. Klockow, Kenneth S. Hettie, and Timothy E. Glass* ACS Chem. Neurosci., 2013, 4(10), pp 1334-1338 DOI: 10.1021/cn400128s Synposis: Neurotransmitters, chemicals that transmit signals between neurons and their target cells, encode information critical to neural processes involving learning, memory, sleep, and movement. While inside the neuron, neurotransmitters are housed in vesicles, which carry them to the cell membrane and then expel them into the synaptic cleft, or the space between neurons and receptive cells. Timothy Glass and co-workers develop a sensor—referred to as ExoSensor 517—that fluoresces when neurotransmitters are released from the neurons. The sensor design exploits high neurotransmitter concentrations in vesicles and the difference in pH between the interior of vesicles and the extracellular space. This type of sensor is anticipated to advance investigation of the complex molecular processes governing neurotransmission. |
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