Mei Hong (chemist)

Last updated
Mei Hong Mei Hong MIT.png
Mei Hong

Mei Hong (born 1970) is a Chinese-American biophysical chemist and professor of chemistry at the Massachusetts Institute of Technology. [1] She is known for her creative development and application of solid-state nuclear magnetic resonance (ssNMR) spectroscopy to elucidate the structures and mechanisms of membrane proteins, plant cell walls, and amyloid proteins. She has received a number of recognitions for her work, including the American Chemical Society Nakanishi Prize in 2021, Günther Laukien Prize in 2014, [2] the Protein Society Young Investigator award in 2012, and the American Chemical Society’s Pure Chemistry award in 2003.

Contents

Education and career

Hong grew up in China and completed her B.A. degree in chemistry from Mount Holyoke College ( summa cum laude ) in 1992 and a Ph.D. degree from the University of California, Berkeley in 1996. There she worked in the laboratory of Alexander Pines to investigate phospholipid structure and dynamics using variable-angle-spinning NMR. After a one-year postdoctoral stint in the laboratory of Robert G. Griffin at the Massachusetts Institute of Technology, she went to University of Massachusetts Amherst and developed biosynthetic isotopic labeling approaches to advance protein structure determination by ssNMR. She started an assistant professorship at Iowa State University in 1999, became an associate professor in 2002 and full professor in 2004, and held the first John D. Corbett Professorship from 2007 to 2010. In 2014, she returned to the Massachusetts Institute of Technology as a professor of chemistry. [1]

Research

Hong's research focuses on elucidating the structure, dynamics and mechanism of membrane proteins using ssNMR. She is particularly known for her in-depth study of the Matrix-2 (M2) proteins of influenza A viruses, which are responsible for all flu pandemics in history. M2 is an acid-activated proton channel and a membrane scission protein of the influenza virus. [3] Hong's ssNMR studies have provided insights into the proton-conduction mechanism of this channel, by quantifying the proton transfer rates and equilibria between water and the proton-selective histidine residue. [4] [5] She showed that the antiviral drug amantadine inhibits proton conduction by direct occlusion of the channel pore. [6] She determined the cholesterol-binding structure of the M2 protein, which sheds light on how cholesterol mediates M2's membrane scission function. [7] In 2020 she determined both the influenza B M2 protein structure [8] and the SARS-CoV-2 envelope protein structure, [9] the latter in rapid response to COVID-19. The 1.5 Å BM2 structures in the closed and open states revealed different activation mechanisms of BM2 compared to influenza AM2. The 2.1 Å SARS-CoV-2 envelope protein structure forms the basis for antiviral drug design.

Other membrane proteins that Hong's group has studied include β-hairpin antimicrobial peptides, [10] channel-forming colicins, [11] and viral fusion proteins. [12] She determined the structure of the membrane toroidal pores formed by the antimicrobial peptide protegrin-1, [10] which explained the membrane-disruptive mechanism of this peptide. She showed that the transmembrane domain of viral fusion proteins can be conformationally plastic, and the β-sheet conformation can correlate with the generation of membrane curvature and membrane dehydration, which are necessary for virus-cell fusion. [12]

Hong has also investigated the structure and dynamics of amyloid proteins, including full-length tau [13] and Aβ peptides involved in neurodegenerative diseases [14] as well as amyloid fibrils formed by designed peptides. [15] She showed that the peptide hormone glucagon fibrillizes into an antiparallel hydrogen-bonded β-sheet with two coexisting molecular conformations. [16] These studies shed light on the origin of structural polymorphism, water interaction, [17] and metal ion binding.

Hong pioneered the study of plant cell walls using multidimensional ssNMR. [18] These studies revealed the molecular interactions of the polysaccharides in plant cell walls, and helped to revise the conventional model of the primary cell wall structure by proposing a single-network model where cellulose, hemicellulose and pectins all interact with each other. [19] She determined the binding target of the protein expansin to be hemicellulose-enriched regions of cellulose microfibrils, [20] thus giving insight into the mechanism of wall loosening by expansin.  

To address these questions, Hong has developed isotopic labeling strategies, [21] multidimensional NMR correlation experiments, [22] polarization transfer techniques, [23] [24] and computational methods for resonance assignment of NMR spectra. [25]

Selected awards and honors

Related Research Articles

<span class="mw-page-title-main">Beta sheet</span> Protein structural motif

The beta sheet is a common motif of the regular protein secondary structure. Beta sheets consist of beta strands (β-strands) connected laterally by at least two or three backbone hydrogen bonds, forming a generally twisted, pleated sheet. A β-strand is a stretch of polypeptide chain typically 3 to 10 amino acids long with backbone in an extended conformation. The supramolecular association of β-sheets has been implicated in the formation of the fibrils and protein aggregates observed in amyloidosis, Alzheimer's disease and other proteinopathies.

<span class="mw-page-title-main">Amyloid</span> Insoluble protein aggregate with a fibrillar morphology

Amyloids are aggregates of proteins characterised by a fibrillar morphology of typically 7–13 nm in diameter, a β-sheet secondary structure and ability to be stained by particular dyes, such as Congo red. In the human body, amyloids have been linked to the development of various diseases. Pathogenic amyloids form when previously healthy proteins lose their normal structure and physiological functions (misfolding) and form fibrous deposits within and around cells. These protein misfolding and deposition processes disrupt the healthy function of tissues and organs.

<span class="mw-page-title-main">Amylin</span> Peptide hormone that plays a role in glycemic regulation

Amylin, or islet amyloid polypeptide (IAPP), is a 37-residue peptide hormone. It is co-secreted with insulin from the pancreatic β-cells in the ratio of approximately 100:1 (insulin:amylin). Amylin plays a role in glycemic regulation by slowing gastric emptying and promoting satiety, thereby preventing post-prandial spikes in blood glucose levels.

<span class="mw-page-title-main">Nuclear magnetic resonance spectroscopy</span> Laboratory technique

Nuclear magnetic resonance spectroscopy, most commonly known as NMR spectroscopy or magnetic resonance spectroscopy (MRS), is a spectroscopic technique based on re-orientation of atomic nuclei with non-zero nuclear spins in an external magnetic field. This re-orientation occurs with absorption of electromagnetic radiation in the radio frequency region from roughly 4 to 900 MHz, which depends on the isotopic nature of the nucleus and increased proportionally to the strength of the external magnetic field. Notably, the resonance frequency of each NMR-active nucleus depends on its chemical environment. As a result, NMR spectra provide information about individual functional groups present in the sample, as well about connections between nearby nuclei in the same molecule. As the NMR spectra are unique or highly characteristic to individual compounds and functional groups, NMR spectroscopy is one of the most important methods to identify molecular structures, particularly of organic compounds.

<span class="mw-page-title-main">Amyloid beta</span> Group of peptides

Amyloid beta denotes peptides of 36–43 amino acids that are the main component of the amyloid plaques found in the brains of people with Alzheimer's disease. The peptides derive from the amyloid-beta precursor protein (APP), which is cleaved by beta secretase and gamma secretase to yield Aβ in a cholesterol-dependent process and substrate presentation. Aβ molecules can aggregate to form flexible soluble oligomers which may exist in several forms. It is now believed that certain misfolded oligomers can induce other Aβ molecules to also take the misfolded oligomeric form, leading to a chain reaction akin to a prion infection. The oligomers are toxic to nerve cells. The other protein implicated in Alzheimer's disease, tau protein, also forms such prion-like misfolded oligomers, and there is some evidence that misfolded Aβ can induce tau to misfold.

<span class="mw-page-title-main">Solid-state nuclear magnetic resonance</span>

Solid-state NMR (ssNMR) spectroscopy is a technique for characterizing atomic level structure in solid materials e.g. powders, single crystals and amorphous samples and tissues using nuclear magnetic resonance (NMR) spectroscopy. The anisotropic part of many spin interactions are present in solid-state NMR, unlike in solution-state NMR where rapid tumbling motion averages out many of the spin interactions. As a result, solid-state NMR spectra are characterised by larger linewidths than in solution state NMR, which can be utilized to give quantitative information on the molecular structure, conformation and dynamics of the material. Solid-state NMR is often combined with magic angle spinning to remove anisotropic interactions and improve the resolution as well as the sensitivity of the technique.

<span class="mw-page-title-main">M2 proton channel</span>

The Matrix-2 (M2) protein is a proton-selective viroporin, integral in the viral envelope of the influenza A virus. The channel itself is a homotetramer, where the units are helices stabilized by two disulfide bonds, and is activated by low pH. The M2 protein is encoded on the seventh RNA segment together with the M1 protein. Proton conductance by the M2 protein in influenza A is essential for viral replication.

Physalaemin is a tachykinin peptide obtained from the Physalaemus frog, closely related to substance P. Its structure was first elucidated in 1964.

Adriaan "Ad" Bax is a Dutch-American molecular biophysicist. He was born in the Netherlands and is the Chief of the Section on Biophysical NMR Spectroscopy at the National Institutes of Health. He is known for his work on the methodology of biomolecular NMR spectroscopy.

<span class="mw-page-title-main">Insulin-degrading enzyme</span> Mammalian protein found in Homo sapiens

Insulin-degrading enzyme, also known as IDE, is an enzyme.

<span class="mw-page-title-main">William DeGrado</span>

William (Bill) DeGrado is a professor at the University of California, San Francisco, where he is the Toby Herfindal Presidential Professor of Entrepreneurship and Innovation in the Department of Pharmaceutical Chemistry. As an early pioneer of protein design, he coined the term de novo protein design. He is also active in discovery of small molecule drugs for a variety of human diseases. He is a member of the U.S. National Academy of Sciences (1999), American Academy of Arts & Sciences (1997) and National Academy of Inventors. He also is a scientific cofounder of Pliant therapeutics.

Nucleic acid NMR is the use of nuclear magnetic resonance spectroscopy to obtain information about the structure and dynamics of nucleic acid molecules, such as DNA or RNA. It is useful for molecules of up to 100 nucleotides, and as of 2003, nearly half of all known RNA structures had been determined by NMR spectroscopy.

Robert Tycko is an American biophysicist whose research primarily involves solid state NMR, including the development of new methods and applications to various areas of physics, chemistry, and biology. He is a member of the Laboratory of Chemical Physics in the National Institute of Diabetes and Digestive and Kidney Diseases at the National Institutes of Health in Bethesda, Maryland, USA. He was formerly a member of the Physical Chemistry Research and Materials Chemistry Research departments of AT&T Bell Labs in Murray Hill, New Jersey. His work has contributed to our understanding of geometric phases in spectroscopy, physical properties of fullerenes, skyrmions in 2D electron systems, protein folding, and amyloid fibrils associated with Alzheimer’s disease and prions.

<span class="mw-page-title-main">G. Marius Clore</span> Molecular biophysicist, structural biologist

G. Marius Clore MAE, FRSC, FRS is a British-born, Anglo-American molecular biophysicist and structural biologist. He was born in London, U.K. and is a dual U.S./U.K. Citizen. He is a Member of the National Academy of Sciences, a Fellow of the Royal Society, a NIH Distinguished Investigator, and the Chief of the Molecular and Structural Biophysics Section in the Laboratory of Chemical Physics of the National Institute of Diabetes and Digestive and Kidney Diseases at the U.S. National Institutes of Health. He is known for his foundational work in three-dimensional protein and nucleic acid structure determination by biomolecular NMR spectroscopy, for advancing experimental approaches to the study of large macromolecules and their complexes by NMR, and for developing NMR-based methods to study rare conformational states in protein-nucleic acid and protein-protein recognition. Clore's discovery of previously undetectable, functionally significant, rare transient states of macromolecules has yielded fundamental new insights into the mechanisms of important biological processes, and in particular the significance of weak interactions and the mechanisms whereby the opposing constraints of speed and specificity are optimized. Further, Clore's work opens up a new era of pharmacology and drug design as it is now possible to target structures and conformations that have been heretofore unseen.

Marc Baldus is a physicist and professor of NMR spectroscopy at Utrecht University. He is especially known for his work in the field of structural biology using solid-state nuclear magnetic resonance (ssNMR) spectroscopy. He applies ssNMR methods to establish structure-function relationships in complex biomolecular systems including membrane and Amyloid proteins. In addition, he develops cellular NMR methods to study large molecular transport and insertion systems in bacteria as well as signal transduction mechanisms in eukaryotic cells.

The ion channel hypothesis of Alzheimer’s disease (AD), also known as the channel hypothesis or the amyloid beta ion channel hypothesis, is a more recent variant of the amyloid hypothesis of AD, which identifies amyloid beta (Aβ) as the underlying cause of neurotoxicity seen in AD. While the traditional formulation of the amyloid hypothesis pinpoints insoluble, fibrillar aggregates of Aβ as the basis of disruption of calcium ion homeostasis and subsequent apoptosis in AD, the ion channel hypothesis in 1993 introduced the possibility of an ion-channel-forming oligomer of soluble, non-fibrillar Aβ as the cytotoxic species allowing unregulated calcium influx into neurons in AD.

<span class="mw-page-title-main">Viroporin</span> Viral proteins that modify cellular membranes

Viroporins are small and usually hydrophobic multifunctional viral proteins that modify cellular membranes, thereby facilitating virus release from infected cells. Viroporins are capable of assembling into oligomeric ion channels or pores in the host cell's membrane, rendering it more permeable and thus facilitating the exit of virions from the cell. Many viroporins also have additional effects on cellular metabolism and homeostasis mediated by protein-protein interactions with host cell proteins. Viroporins are not necessarily essential for viral replication, but do enhance growth rates. They are found in a variety of viral genomes but are particularly common in RNA viruses. Many viruses that cause human disease express viroporins. These viruses include hepatitis C virus, HIV-1, influenza A virus, poliovirus, respiratory syncytial virus, and SARS-CoV.

<span class="mw-page-title-main">Hartmut Oschkinat</span> German structural biologist and professor

Hartmut Oschkinat is a German structural biologist and professor for chemistry at the Free University of Berlin. His research focuses on the study of biological systems with solid-state nuclear magnetic resonance.

<span class="mw-page-title-main">James J. Chou</span> American chemist

James J. Chou (周界文) is a Chinese American scientist and Professor of Biological Chemistry and Molecular Pharmacology at the Harvard Medical School. He is known for pioneering the use of Nuclear Magnetic Resonance (NMR) Spectroscopy to reveal the structural details of the membrane regions of cell surface proteins, particularly those of immune receptors and viral membrane proteins.

Suzana K. Straus is a Canadian chemist who is a professor at the University of British Columbia. Her research focuses on host defense peptides (HDPs), as well as protein-protein and protein-ligand interactions.

References

  1. 1 2 "Professor Mei Hong – Hong Lab MIT" . Retrieved 2019-05-21.
  2. Ernst, Richard R. (April 2005). "The Günther Laukien Prize". Journal of Magnetic Resonance. 173 (2): 188–191. Bibcode:2005JMagR.173..188E. doi:10.1016/j.jmr.2005.02.006. ISSN   1090-7807. PMID   15780911.
  3. Hong, Mei; DeGrado, William F. (2012-10-09). "Structural basis for proton conduction and inhibition by the influenza M2 protein". Protein Science. 21 (11): 1620–1633. doi:10.1002/pro.2158. PMC   3527700 . PMID   23001990.
  4. Hu, F.; Luo, W.; Hong, M. (2010-10-21). "Mechanisms of Proton Conduction and Gating in Influenza M2 Proton Channels from Solid-State NMR". Science. 330 (6003): 505–508. Bibcode:2010Sci...330..505H. doi:10.1126/science.1191714. ISSN   0036-8075. PMC   4102303 . PMID   20966251.
  5. Hu, Fanghao; Schmidt-Rohr, Klaus; Hong, Mei (2011-10-21). "NMR Detection of pH-Dependent Histidine–Water Proton Exchange Reveals the Conduction Mechanism of a Transmembrane Proton Channel". Journal of the American Chemical Society. 134 (8): 3703–3713. doi:10.1021/ja2081185. ISSN   0002-7863. PMC   3288706 . PMID   21974716.
  6. Cady, Sarah D.; Schmidt-Rohr, Klaus; Wang, Jun; Soto, Cinque S.; DeGrado, William F.; Hong, Mei (2010). "Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers". Nature. 463 (7281): 689–692. Bibcode:2010Natur.463..689C. doi:10.1038/nature08722. ISSN   0028-0836. PMC   2818718 . PMID   20130653.
  7. Elkins, Matthew R.; Williams, Jonathan K.; Gelenter, Martin D.; Dai, Peng; Kwon, Byungsu; Sergeyev, Ivan V.; Pentelute, Bradley L.; Hong, Mei (2017-11-20). "Cholesterol-binding site of the influenza M2 protein in lipid bilayers from solid-state NMR". Proceedings of the National Academy of Sciences. 114 (49): 12946–12951. Bibcode:2017PNAS..11412946E. doi: 10.1073/pnas.1715127114 . ISSN   0027-8424. PMC   5724280 . PMID   29158386.
  8. Mandala, Venkata S.; Loftis, Alexander R.; Shcherbakov, Alexander A.; Pentelute, Bradley L.; Hong, Mei (2020-02-03). "Atomic structures of closed and open influenza B M2 proton channel reveal the conduction mechanism". Nature Structural & Molecular Biology. 27 (2): 160–167. doi:10.1038/s41594-019-0371-2. ISSN   1545-9985. PMC   7641042 . PMID   32015551. S2CID   211017938.
  9. Mandala, Venkata S.; McKay, Matthew J.; Shcherbakov, Alexander A.; Dregni, Aurelio J.; Kolocouris, Antonios; Hong, Mei (December 2020). "Structure and drug binding of the SARS-CoV-2 envelope protein transmembrane domain in lipid bilayers". Nature Structural & Molecular Biology. 27 (12): 1202–1208. doi: 10.1038/s41594-020-00536-8 . ISSN   1545-9985. PMC   7718435 . PMID   33177698.
  10. 1 2 Mani, R.; Cady, S. D.; Tang, M.; Waring, A. J.; Lehrer, R. I.; Hong, M. (2006-10-23). "Membrane-dependent oligomeric structure and pore formation of a beta-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR". Proceedings of the National Academy of Sciences. 103 (44): 16242–16247. Bibcode:2006PNAS..10316242M. doi: 10.1073/pnas.0605079103 . ISSN   0027-8424. PMC   1637567 . PMID   17060626.
  11. Luo, Wenbin; Yao, Xiaolan; Hong, Mei (2005). "Large Structure Rearrangement of Colicin Ia Channel Domain after Membrane Binding from 2D13C Spin Diffusion NMR". Journal of the American Chemical Society. 127 (17): 6402–6408. doi:10.1021/ja0433121. ISSN   0002-7863. PMID   15853348.
  12. 1 2 Yao, Hongwei; Lee, Michelle W.; Waring, Alan J.; Wong, Gerard C. L.; Hong, Mei (2015-08-17). "Viral fusion protein transmembrane domain adopts β-strand structure to facilitate membrane topological changes for virus–cell fusion". Proceedings of the National Academy of Sciences. 112 (35): 10926–10931. Bibcode:2015PNAS..11210926Y. doi: 10.1073/pnas.1501430112 . ISSN   0027-8424. PMC   4568205 . PMID   26283363.
  13. Dregni, Aurelio J.; Mandala, Venkata S.; Wu, Haifan; Elkins, Matthew R.; Wang, Harrison K.; Hung, Ivan; DeGrado, William F.; Hong, Mei (2019-08-13). "In vitro 0N4R tau fibrils contain a monomorphic β-sheet core enclosed by dynamically heterogeneous fuzzy coat segments". Proceedings of the National Academy of Sciences. 116 (33): 16357–16366. Bibcode:2019PNAS..11616357D. doi: 10.1073/pnas.1906839116 . ISSN   0027-8424. PMC   6697781 . PMID   31358628.
  14. Elkins, Matthew R.; Wang, Tuo; Nick, Mimi; Jo, Hyunil; Lemmin, Thomas; Prusiner, Stanley B.; DeGrado, William F.; Stöhr, Jan; Hong, Mei (2016-07-28). "Structural Polymorphism of Alzheimer's β-Amyloid Fibrils as Controlled by an E22 Switch: A Solid-State NMR Study". Journal of the American Chemical Society. 138 (31): 9840–9852. doi:10.1021/jacs.6b03715. hdl:1721.1/113318. ISSN   0002-7863. PMC   5149419 . PMID   27414264.
  15. Lee, M.; Wang, T.; Makhlynets, O.V.; Wu, Y.; Polizzi, N.; Wu, H.; Gosavi, P.M.; Korendovych, I.V.; DeGrado, W.F. (2017-05-31). "Zinc-Binding Structure of a Catalytic Amyloid from Solid-State NMR Spectroscopy". doi:10.2210/pdb5ugk/pdb.{{cite journal}}: Cite journal requires |journal= (help)
  16. Gelenter, Martin D.; Smith, Katelyn J.; Liao, Shu-Yu; Mandala, Venkata S.; Dregni, Aurelio J.; Lamm, Matthew S.; Tian, Yu; Pochan, Darrin J.; Tucker, Thomas J.; Su, Yongchao; Hong, Mei (2019-06-24). "The peptide hormone glucagon forms amyloid fibrils with two coexisting β-strand conformations". Nature Structural & Molecular Biology. 26 (7): 592–598. doi:10.1038/s41594-019-0238-6. hdl: 1721.1/125383 . ISSN   1545-9985. PMC   6609468 . PMID   31235909.
  17. Wang, Tuo; Jo, Hyunil; DeGrado, William F.; Hong, Mei (2017-04-21). "Water Distribution, Dynamics, and Interactions with Alzheimer's β-Amyloid Fibrils Investigated by Solid-State NMR". Journal of the American Chemical Society. 139 (17): 6242–6252. doi:10.1021/jacs.7b02089. ISSN   0002-7863. PMC   5808936 . PMID   28406028.
  18. Wang, Tuo; Hong, Mei (2015-09-09). "Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls". Journal of Experimental Botany. 67 (2): 503–514. doi:10.1093/jxb/erv416. ISSN   0022-0957. PMC   6280985 . PMID   26355148.
  19. Pérez García, Marilú; Zhang, Yuan; Hayes, Jennifer; Salazar, Andre; Zabotina, Olga A.; Hong, Mei (2011-02-15). "Structure and Interactions of Plant Cell-Wall Polysaccharides by Two- and Three-Dimensional Magic-Angle-Spinning Solid-State NMR". Biochemistry. 50 (6): 989–1000. doi:10.1021/bi101795q. ISSN   0006-2960. PMID   21204530. S2CID   42980200.
  20. Wang, T.; Park, Y. B.; Caporini, M. A.; Rosay, M.; Zhong, L.; Cosgrove, D. J.; Hong, M. (2013-09-24). "Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls". Proceedings of the National Academy of Sciences. 110 (41): 16444–16449. Bibcode:2013PNAS..11016444W. doi: 10.1073/pnas.1316290110 . ISSN   0027-8424. PMC   3799313 . PMID   24065828.
  21. Hong, M.; Jakes, K. (1999-05-01). "Selective and extensive 13C labeling of a membrane protein for solid-state NMR investigations". Journal of Biomolecular NMR. 14 (1): 71–74. doi:10.1023/A:1008334930603. ISSN   1573-5001. PMID   10382307. S2CID   41194972.
  22. Hong, Mei (1999-09-01). "Resonance assignment of 13C/15N labeled solid proteins by two- and three-dimensional magic-angle-spinning NMR". Journal of Biomolecular NMR. 15 (1): 1–14. doi:10.1023/A:1008334204412. ISSN   1573-5001. PMID   10549131. S2CID   1474913.
  23. Hong, Mei; Schmidt-Rohr, Klaus (2013-02-07). "Magic-Angle-Spinning NMR Techniques for Measuring Long-Range Distances in Biological Macromolecules". Accounts of Chemical Research. 46 (9): 2154–2163. doi:10.1021/ar300294x. ISSN   0001-4842. PMC   3714308 . PMID   23387532.
  24. Roos, Matthias; Mandala, Venkata S.; Hong, Mei (2018-09-13). "Determination of Long-Range Distances by Fast Magic-Angle-Spinning Radiofrequency-Driven 19F–19F Dipolar Recoupling NMR". The Journal of Physical Chemistry B. 122 (40): 9302–9313. doi:10.1021/acs.jpcb.8b06878. ISSN   1520-6106. PMC   6314681 . PMID   30211552.
  25. Fritzsching, K. J.; Yang, Y.; Schmidt-Rohr, K.; Hong, Mei (2013-04-28). "Practical use of chemical shift databases for protein solid-state NMR: 2D chemical shift maps and amino-acid assignment with secondary-structure information". Journal of Biomolecular NMR. 56 (2): 155–167. doi:10.1007/s10858-013-9732-z. ISSN   0925-2738. PMC   4048757 . PMID   23625364.
  26. "The ISMAR Organization | ISMAR". www.weizmann.ac.il. Retrieved 2019-05-21.
  27. "Monday at ENC: Laukien Prize Winners 2014". The Resonance. 2014-03-25. Retrieved 2019-05-21.
  28. "ICMRBS Founders Medal". www.icmrbs.org. Retrieved 2019-05-21.
  29. "Elected Fellows". American Association for the Advancement of Science. Retrieved 2019-05-21.
  30. "ACS Award in Pure Chemistry". American Chemical Society. Retrieved 2019-05-21.