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William E Royer PhD

TitleProfessor Emeritus
InstitutionUMass Chan Medical School
DepartmentBiochemistry and Molecular Biotechnology
AddressUMass Chan Medical School
364 Plantation Street LRB
Worcester MA 01605
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    Other Positions
    InstitutionT.H. Chan School of Medicine
    DepartmentBiochemistry and Molecular Biotechnology

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentBiochemistry and Molecular Biotechnology

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentMD/PhD Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentPostbaccalaureate Research Education Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentTranslational Science

    Collapse Biography 
    Collapse education and training
    Pennsylvania State University, College Park, PA, United StatesBSBiophysics
    Johns Hopkins University, Baltimore, MD, United StatesPHDBiophysics

    Collapse Overview 
    Collapse overview

    Academic Background

    William E. Royer, Jr. received his BS from Pennsylvania State University in 1976 and his PhD in biophysics from The Johns Hopkins University in 1984. He was a postdoctoral fellow in Dr. Wayne Hendrickson's laboratory at ColumbiaUniversity and became an associate of the Howard Hughes Medical Institute in 1986 and an associate research scientist at Columbia University in1988. He joined the faculty of the University of Massachusetts MedicalSchool in 1990. He was an established Investigator of the American Heart Association from 1994-1999.


    Photo: William E Royer

    Research Interests

    Our laboratory explores the structural basis by which intermolecular interactions regulate biological function in a number of systems.  One focus is how assembly of protein subunits regulates their function.  Two systems in this area of current interest are interferon regulatory factors, in which phosphorylation triggers dimeric assembly and nuclear translocation, and a dimeric hemoglobin, for which assembly results in substantial cooperative ligand binding.  A second focus is the structure-based development of inhibitors for a cancer target, CtBP.  These three research areas are described below.

    Structural regulation of interferon regulatory factors (IRFs) in the innate immune response

    IRF family members play important roles in innate immunity, inflammation and apoptosis.  Their clinical importance is evidenced by a strong link between IRF5 and autoimmune diseases, particularly lupus.  Our goal is to obtain a structural understanding of activation that will permit insight into approaches for inactivation that could inform development of future therapies in autoimmune disease.  The first step in IRF activation is triggered by phosphorylation of Ser/Thr residues in a C-terminal autoinhibitory region. Phosphylation stimulates dimerization, translocation into the nucleus and assembly with the coactivator CBP/p300 and other proteins to stimulate transcription of type I interferons and other target genes. In collaboration with Dr. Celia Schiffer (BMP) and Dr. Kate Fitzgerald (Medicine), we are continuing work on the structural basis for activation of IRFs that was pioneered by our extraordinary colleague, Dr. Kai Lin, prior his tragic death. Our crystal structure of dimeric pseudophosphorylated IRF-5, in comparison with structures of monomeric IRF-3 determined by Dr. Lin, has revealed how phosphorylation triggers a striking conformational rearrangement of the C-terminal region converting it from an autoinhibitory to a dimerization role. Activated dimers are then translocated into the nucleus, where they assemble with transcriptional coactivators to activate transcription.

    Figure 1 legend: The crystal structure of the IRF-5 dimer (PDB id code 3DSH) is shown as a ribbon diagram with one subunit in green and one in blue, except for the C-terminal autoinhibition/dimerization region, which is shown in purple for both subunits.  Likely phosphorylation sites are shown as small yellow spheres at their alpha-carbon positions.  Comparison of the IRF-5 structure with that of monomeric autoinhibited IRF-3 strongly suggests a common mechanism for activation of the interfereon regulatory factors in which phosphorylation triggers a dramatic structural transition of the C-terminal region, resulting in IRF dimerization and exposure of the CBP binding site.  These two effects are key steps leading to the transcriptional activation of type 1 interferons and other target genes (see Chen et al. (2008) NSMB 15, 1213-1220).


    Structure-based development of inhibitors against CtBP, a cancer target

    The paralogous transcription coregulators C-terminal Binding Proteins (CtBP) 1 and 2 are critical modulators of numerous cellular processes.  CtBP 1 and 2 have been shown to be overexpressed in many human cancers where they act to inhibit apoptosis and promote metastasis.  Unusual among transcription factors, CtBP harbors an essential D-isomer specific 2-hydroxyacid dehydrogenase (D2-HDH) catalytic domain that enables CtBP to be a redox sensor and provides an attractive target for small molecule inhibition. High (mM) concentrations of the CtBP substrate MTOB have been shown by our collaborator, Dr. Steven Grossman at Virginia Commonwealth University, to be able to inhibit tumor growth in cell culture and mouse studies providing proof of principle that CtBP could be an excellent cancer target.  By determining the crystal structures of CtBP 1 and 2 in complex with MTOB, we elucidated unique active site features and then used these to identify compounds with substantially higher affinity.  Among these features is a water filled hydrophilic cavity, shown below, that is not shared by other D2-HDH family members.  We are working to exploit such structural features to design potentially therapeutically useful inhibitors that bind specifically to CtBP with high affinity.

    Figure 2 legend: The active site hydrophilic cavity in CtBP1, with the protein cavity surface shown in gray.  Four crystallographically observed water molecules, W1-W4, link substrate MTOB (cyan carbon atoms) with an NAD+ (yellow) phosphate.  This cavity is not present in other members of the D2-HDH family.  Therefore, creating inhibitors with functional groups that bind in this cavity should both gain affinity and specificity for CtBP. (See Hilbert et al. (2014) FEBS Lett. 588, 1743-1748)

    Time-resolved crystallographic analysis of cooperative ligand binding

    Invertebrate hemoglobins provide a number of useful model systems for exploring how protein subunits communicate.  We have investigated systems ranging from the simplest possible allosteric systems to much more complex protein assemblages.  As part of our efforts, we determined crystal structures of respiratory proteins with molecular masses of 3.6 x 106 Da comprising 180 different subunits.  (Our crystal structure of Lumbricus erythrocruorin was highlighted as the March, 2013 molecule of the month at the protein data bank – see http://www.rcsb.org/pdb/101/motm.do?momID=159.) Our current efforts are focused on applying sub-ns time-resolved crystallographic analysis to a dimeric hemoglobin (Scapharca HbI) to dissect the time-dependent ligand-linked structural changes that underlie cooperative ligand binding.  These experiments are being carried out at BioCARS (Advanced Photon Source) in collaboration with Dr. Vukica Srajer and Dr. Zhong Ren.  They have already led to a new understanding of the role of water molecules in intersubunit communication as well as permitting the development of a novel dynamic model that incorporates a direct linkage between two active sites.  In collaboration with Dr. Francesca Massi (BMP), we are combining the crystallographic results with NMR experiments that investigate the role of interface dynamics in cooperative behavior.


    Collapse Rotation Projects

    Potential Rotation Projects

    Project #1: Probing the structural basis for cooperativity in a dimeric hemoglobin: Scapharca dimeric hemoglobin is an elegantly simple model system for exploring the structural basis for intersubunit communication. Our analysis to date has established a new paradigm for cooperativity in which tightly bound water molecules are used as sensors for ligand state.

    In this project, the student will first mutate the gene for the native hemoglobin at a residue that is suspected of playing a role in the intersubunit communication. The mutated protein will then be expressed in E. coli and purified and subjected to functional analysis of oxygen binding. Using conditions already established for the native protein, the mutant hemoglobin will then be crystallized and subjected to preliminary x-ray analysis.

    This project will provide the student with an introduction to two of the most powerful techniques for investigating the structure and function of proteins: site-directed mutagenesis and x-ray crystallography. Additionally, valuable experience in protein purification will be obtained.

    Project #2: Structural analysis of the polymerization of sickle-cell hemoglobin Sickle cell disease results from the pathological polymerization of deoxygenated hemoglobin S (ß6E->V) within erythrocytes. This polymerization depends upon a complicated interplay of multiple interactions between tetramers. Our high resolution crystal structure of this molecule has elucidated details of some of the important interactions. Several projects are available for rotation students. These include crystallization of sickle-cell hemoglobin in the presence of an inhibitor to identify its binding site, site-directed mutagenesis of hemoglobin S and crystallization of mutants that show altered polymerization characteristics.

    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    1. Erlandsen H, Jecrois AM, Nichols JC, Cole JL, Royer WE. NADH/NAD+ binding and linked tetrameric assembly of the oncogenic transcription factors CtBP1 and CtBP2. FEBS Lett. 2022 02; 596(4):479-490. PMID: 34997967.
      Citations: 1     Fields:    Translation:HumansCells
    2. Nichols JC, Schiffer CA, Royer WE. NAD(H) phosphates mediate tetramer assembly of human C-terminal binding protein (CtBP). J Biol Chem. 2021 Jan-Jun; 296:100351. PMID: 33524397.
      Citations: 3     Fields:    Translation:HumansCells
    3. Jecrois AM, Dcona MM, Deng X, Bandyopadhyay D, Grossman SR, Schiffer CA, Royer WE. Cryo-EM structure of CtBP2 confirms tetrameric architecture. Structure. 2021 04 01; 29(4):310-319.e5. PMID: 33264605.
      Citations: 9     Fields:    Translation:HumansCells
    4. Lockbaum GJ, Leidner F, Royer WE, Kurt Yilmaz N, Schiffer CA. Optimizing the refinement of merohedrally twinned P61 HIV-1 protease-inhibitor cocrystal structures. Acta Crystallogr D Struct Biol. 2020 Mar 01; 76(Pt 3):302-310. PMID: 32133994.
    5. Dcona MM, Damle PK, Zarate-Perez F, Morris BL, Nawaz Z, Dennis MJ, Deng X, Korwar S, Singh SJ, Ellis KC, Royer WE, Bandyopadhyay D, Escalante C, Grossman SR. Active-Site Tryptophan, the Target of Antineoplastic C-Terminal Binding Protein Inhibitors, Mediates Inhibitor Disruption of CtBP Oligomerization and Transcription Coregulatory Activities. Mol Pharmacol. 2019 07; 96(1):99-108. PMID: 31036695.
      Citations: 4     Fields:    Translation:HumansAnimalsCells
    6. Bellesis AG, Jecrois AM, Hayes JA, Schiffer CA, Royer WE. Assembly of human C-terminal binding protein (CtBP) into tetramers. J Biol Chem. 2018 06 08; 293(23):9101-9112. PMID: 29700119.
      Citations: 23     Fields:    Translation:HumansCells
    7. Kouno T, Silvas TV, Hilbert BJ, Shandilya SMD, Bohn MF, Kelch BA, Royer WE, Somasundaran M, Kurt Yilmaz N, Matsuo H, Schiffer CA. Crystal structure of APOBEC3A bound to single-stranded DNA reveals structural basis for cytidine deamination and specificity. Nat Commun. 2017 04 28; 8:15024. PMID: 28452355.
      Citations: 81     Fields:    Translation:HumansCells
    8. Korwar S, Morris BL, Parikh HI, Coover RA, Doughty TW, Love IM, Hilbert BJ, Royer WE, Kellogg GE, Grossman SR, Ellis KC. Design, synthesis, and biological evaluation of substrate-competitive inhibitors of C-terminal Binding Protein (CtBP). Bioorg Med Chem. 2016 06 15; 24(12):2707-15. PMID: 27156192.
      Citations: 14     Fields:    Translation:HumansCells
    9. Hilbert BJ, Morris BL, Ellis KC, Paulsen JL, Schiffer CA, Grossman SR, Royer WE. Structure-guided design of a high affinity inhibitor to human CtBP. ACS Chem Biol. 2015 Apr 17; 10(4):1118-27. PMID: 25636004.
      Citations: 17     Fields:    Translation:HumansCells
    10. Laine JM, Amat M, Morgan BR, Royer WE, Massi F. Insight into the allosteric mechanism of Scapharca dimeric hemoglobin. Biochemistry. 2014 Nov 25; 53(46):7199-210. PMID: 25356908.
      Citations: 9     Fields:    Translation:AnimalsCells
    11. Hilbert BJ, Grossman SR, Schiffer CA, Royer WE. Crystal structures of human CtBP in complex with substrate MTOB reveal active site features useful for inhibitor design. FEBS Lett. 2014 May 02; 588(9):1743-8. PMID: 24657618.
      Citations: 22     Fields:    Translation:HumansCells
    12. Ren Z, Chan PW, Moffat K, Pai EF, Royer WE, ?rajer V, Yang X. Resolution of structural heterogeneity in dynamic crystallography. Acta Crystallogr D Biol Crystallogr. 2013 Jun; 69(Pt 6):946-59. PMID: 23695239.
      Citations: 21     Fields:    
    13. Ronda L, Bettati S, Henry ER, Kashav T, Sanders JM, Royer WE, Mozzarelli A. Tertiary and quaternary allostery in tetrameric hemoglobin from Scapharca inaequivalvis. Biochemistry. 2013 Mar 26; 52(12):2108-17. PMID: 23458680.
      Citations: 4     Fields:    Translation:HumansAnimalsCells
    14. Ren Z, Srajer V, Knapp JE, Royer WE. Cooperative macromolecular device revealed by meta-analysis of static and time-resolved structures. Proc Natl Acad Sci U S A. 2012 Jan 03; 109(1):107-12. PMID: 22171006.
      Citations: 25     Fields:    Translation:AnimalsCells
    15. Romano KP, Ali A, Royer WE, Schiffer CA. Drug resistance against HCV NS3/4A inhibitors is defined by the balance of substrate recognition versus inhibitor binding. Proc Natl Acad Sci U S A. 2010 Dec 07; 107(49):20986-91. PMID: 21084633.
      Citations: 89     Fields:    Translation:HumansCells
    16. Choi J, Muniyappan S, Wallis JT, Royer WE, Ihee H. Protein conformational dynamics of homodimeric hemoglobin revealed by combined time-resolved spectroscopic probes. Chemphyschem. 2010 Jan 18; 11(1):109-14. PMID: 19924759.
      Citations: 6     Fields:    Translation:AnimalsCells
    17. Shandilya SM, Nalam MN, Nalivaika EA, Gross PJ, Valesano JC, Shindo K, Li M, Munson M, Royer WE, Harjes E, Kono T, Matsuo H, Harris RS, Somasundaran M, Schiffer CA. Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure. 2010 Jan 13; 18(1):28-38. PMID: 20152150.
      Citations: 94     Fields:    Translation:HumansCells
    18. Chen W, Royer WE. Structural insights into interferon regulatory factor activation. Cell Signal. 2010 Jun; 22(6):883-7. PMID: 20043992.
      Citations: 36     Fields:    Translation:Cells
    19. Knapp JE, Pahl R, Cohen J, Nichols JC, Schulten K, Gibson QH, Srajer V, Royer WE. Ligand migration and cavities within Scapharca Dimeric HbI: studies by time-resolved crystallo-graphy, Xe binding, and computational analysis. Structure. 2009 Nov 11; 17(11):1494-504. PMID: 19913484.
      Citations: 32     Fields:    Translation:AnimalsCells
    20. Chen W, Lam SS, Srinath H, Jiang Z, Correia JJ, Schiffer CA, Fitzgerald KA, Lin K, Royer WE. Insights into interferon regulatory factor activation from the crystal structure of dimeric IRF5. Nat Struct Mol Biol. 2008 Nov; 15(11):1213-20. PMID: 18836453.
      Citations: 66     Fields:    Translation:HumansCells
    21. Chen W, Srinath H, Lam SS, Schiffer CA, Royer WE, Lin K. Contribution of Ser386 and Ser396 to activation of interferon regulatory factor 3. J Mol Biol. 2008 May 30; 379(2):251-60. PMID: 18440553.
      Citations: 40     Fields:    Translation:HumansCells
    22. Srajer V, Royer WE. Time-resolved x-ray crystallography of heme proteins. Methods Enzymol. 2008; 437:379-95. PMID: 18433638.
      Citations: 9     Fields:    Translation:AnimalsCells
    23. Nienhaus K, Knapp JE, Palladino P, Royer WE, Nienhaus GU. Ligand migration and binding in the dimeric hemoglobin of Scapharca inaequivalvis. Biochemistry. 2007 Dec 11; 46(49):14018-31. PMID: 18001141.
      Citations: 22     Fields:    Translation:AnimalsCells
    24. Chen W, Lam SS, Srinath H, Schiffer CA, Royer WE, Lin K. Competition between Ski and CREB-binding protein for binding to Smad proteins in transforming growth factor-beta signaling. J Biol Chem. 2007 Apr 13; 282(15):11365-76. PMID: 17283070.
      Citations: 20     Fields:    Translation:HumansCells
    25. Nichols JC, Royer WE, Gibson QH. An optical signal correlated with the allosteric transition in Scapharca inaequivalvis HbI. Biochemistry. 2006 Dec 26; 45(51):15748-55. PMID: 17176097.
      Citations: 7     Fields:    Translation:AnimalsCells
    26. Royer WE, Omartian MN, Knapp JE. Low resolution crystal structure of Arenicola erythrocruorin: influence of coiled coils on the architecture of a megadalton respiratory protein. J Mol Biol. 2007 Jan 05; 365(1):226-36. PMID: 17084861.
      Citations: 5     Fields:    Translation:AnimalsCells
    27. Royer WE, Sharma H, Strand K, Knapp JE, Bhyravbhatla B. Lumbricus erythrocruorin at 3.5 A resolution: architecture of a megadalton respiratory complex. Structure. 2006 Jul; 14(7):1167-77. PMID: 16843898.
      Citations: 32     Fields:    Translation:AnimalsCells
    28. Knapp JE, Pahl R, Srajer V, Royer WE. Allosteric action in real time: time-resolved crystallographic studies of a cooperative dimeric hemoglobin. Proc Natl Acad Sci U S A. 2006 May 16; 103(20):7649-54. PMID: 16684887.
      Citations: 40     Fields:    Translation:HumansAnimalsCells
    29. Knapp JE, Bonham MA, Gibson QH, Nichols JC, Royer WE. Residue F4 plays a key role in modulating oxygen affinity and cooperativity in Scapharca dimeric hemoglobin. Biochemistry. 2005 Nov 08; 44(44):14419-30. PMID: 16262242.
      Citations: 19     Fields:    Translation:AnimalsCells
    30. Royer WE, Zhu H, Gorr TA, Flores JF, Knapp JE. Allosteric hemoglobin assembly: diversity and similarity. J Biol Chem. 2005 Jul 29; 280(30):27477-80. PMID: 15932877.
      Citations: 23     Fields:    Translation:HumansAnimalsCells
    31. Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW, Royer WE. Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Natl Acad Sci U S A. 2005 Feb 22; 102(8):2713-8. PMID: 15710902.
      Citations: 19     Fields:    Translation:AnimalsCells
    32. Strand K, Knapp JE, Bhyravbhatla B, Royer WE. Crystal structure of the hemoglobin dodecamer from Lumbricus erythrocruorin: allosteric core of giant annelid respiratory complexes. J Mol Biol. 2004 Nov 12; 344(1):119-34. PMID: 15504406.
      Citations: 16     Fields:    Translation:AnimalsCells
    33. Knapp JE, Srajer V, Pahl R, Royer WE. Immobilization of Scapharca HbI crystals improves data quality in time-resolved crystallographic experiments. Micron. 2004; 35(1-2):107-8. PMID: 15036308.
      Citations: 3     Fields:    Translation:Animals
    34. Bennett EJ, Bjerregaard J, Knapp JE, Chavous DA, Friedman AM, Royer WE, O'Connor CM. Catalytic implications from the Drosophila protein L-isoaspartyl methyltransferase structure and site-directed mutagenesis. Biochemistry. 2003 Nov 11; 42(44):12844-53. PMID: 14596598.
      Citations: 5     Fields:    Translation:HumansAnimalsCells
    35. Knapp JE, Royer WE. Ligand-linked structural transitions in crystals of a cooperative dimeric hemoglobin. Biochemistry. 2003 Apr 29; 42(16):4640-7. PMID: 12705827.
      Citations: 11     Fields:    Translation:Cells
    36. Knapp JE, Gibson QH, Cushing L, Royer WE. Restricting the ligand-linked heme movement in Scapharca dimeric hemoglobin reveals tight coupling between distal and proximal contributions to cooperativity. Biochemistry. 2001 Dec 11; 40(49):14795-805. PMID: 11732898.
      Citations: 11     Fields:    Translation:AnimalsCells
    37. Heaslet HA, Royer WE. Crystalline ligand transitions in lamprey hemoglobin. Structural evidence for the regulation of oxygen affinity. J Biol Chem. 2001 Jul 13; 276(28):26230-6. PMID: 11340069.
      Citations: 2     Fields:    Translation:AnimalsCells
    38. Royer WE, Knapp JE, Strand K, Heaslet HA. Cooperative hemoglobins: conserved fold, diverse quaternary assemblies and allosteric mechanisms. Trends Biochem Sci. 2001 May; 26(5):297-304. PMID: 11343922.
      Citations: 32     Fields:    Translation:HumansAnimalsCells
    39. Royer WE, Strand K, van Heel M, Hendrickson WA. Structural hierarchy in erythrocruorin, the giant respiratory assemblage of annelids. Proc Natl Acad Sci U S A. 2000 Jun 20; 97(13):7107-11. PMID: 10860978.
      Citations: 21     Fields:    Translation:AnimalsCells
    40. Richardson RC, King NM, Harrington DJ, Sun H, Royer WE, Nelson DJ. X-Ray crystal structure and molecular dynamics simulations of silver hake parvalbumin (Isoform B). Protein Sci. 2000 Jan; 9(1):73-82. PMID: 10739249.
      Citations: 2     Fields:    Translation:AnimalsCells
    41. Heaslet HA, Royer WE. The 2.7 A crystal structure of deoxygenated hemoglobin from the sea lamprey (Petromyzon marinus): structural basis for a lowered oxygen affinity and Bohr effect. Structure. 1999 May; 7(5):517-26. PMID: 10378271.
      Citations: 3     Fields:    Translation:AnimalsCells
    42. Pardanani A, Gambacurta A, Ascoli F, Royer WE. Mutational destabilization of the critical interface water cluster in Scapharca dimeric hemoglobin: structural basis for altered allosteric activity. J Mol Biol. 1998 Dec 04; 284(3):729-39. PMID: 9826511.
      Citations: 10     Fields:    Translation:AnimalsCells
    43. Harrington DJ, Adachi K, Royer WE. Crystal structure of deoxy-human hemoglobin beta6 Glu --> Trp. Implications for the structure and formation of the sickle cell fiber. J Biol Chem. 1998 Dec 04; 273(49):32690-6. PMID: 9830011.
      Citations: 6     Fields:    Translation:HumansCells
    44. Harrington DJ, Adachi K, Royer WE. The high resolution crystal structure of deoxyhemoglobin S. J Mol Biol. 1997 Sep 26; 272(3):398-407. PMID: 9325099.
      Citations: 53     Fields:    Translation:HumansCells
    45. Pardanani A, Gibson QH, Colotti G, Royer WE. Mutation of residue Phe97 to Leu disrupts the central allosteric pathway in Scapharca dimeric hemoglobin. J Biol Chem. 1997 May 16; 272(20):13171-9. PMID: 9148933.
      Citations: 10     Fields:    Translation:AnimalsCells
    46. Royer WE, Fox RA, Smith FR, Zhu D, Braswell EH. Ligand linked assembly of Scapharca dimeric hemoglobin. J Biol Chem. 1997 Feb 28; 272(9):5689-94. PMID: 9038179.
      Citations: 4     Fields:    Translation:AnimalsCells
    47. Royer WE, Pardanani A, Gibson QH, Peterson ES, Friedman JM. Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin. Proc Natl Acad Sci U S A. 1996 Dec 10; 93(25):14526-31. PMID: 8962085.
      Citations: 43     Fields:    Translation:AnimalsCells
    48. Royer WE, Heard KS, Harrington DJ, Chiancone E. The 2.0 A crystal structure of Scapharca tetrameric hemoglobin: cooperative dimers within an allosteric tetramer. J Mol Biol. 1995 Oct 13; 253(1):168-86. PMID: 7473710.
      Citations: 10     Fields:    Translation:HumansAnimalsCells
    49. Summerford CM, Pardanani A, Betts AH, Poteete AR, Colotti G, Royer WE. Bacterial expression of Scapharca dimeric hemoglobin: a simple model system for investigating protein cooperatively. Protein Eng. 1995 Jun; 8(6):593-9. PMID: 8532684.
      Citations: 11     Fields:    Translation:AnimalsCells
    50. Condon PJ, Royer WE. Crystal structure of oxygenated Scapharca dimeric hemoglobin at 1.7-A resolution. J Biol Chem. 1994 Oct 14; 269(41):25259-67. PMID: 7929217.
      Citations: 14     Fields:    Translation:AnimalsCells
    51. Aronson HE, Royer WE, Hendrickson WA. Quantification of tertiary structural conservation despite primary sequence drift in the globin fold. Protein Sci. 1994 Oct; 3(10):1706-11. PMID: 7849587.
      Citations: 20     Fields:    Translation:HumansAnimalsCells
    52. Royer WE. High-resolution crystallographic analysis of a co-operative dimeric hemoglobin. J Mol Biol. 1994 Jan 14; 235(2):657-81. PMID: 8289287.
      Citations: 31     Fields:    Translation:AnimalsCells
    53. Chiancone E, Elber R, Royer WE, Regan R, Gibson QH. Ligand binding and conformation change in the dimeric hemoglobin of the clam Scapharca inaequivalvis. J Biol Chem. 1993 Mar 15; 268(8):5711-8. PMID: 8449933.
      Citations: 16     Fields:    Translation:AnimalsCells
    54. Chiancone E, Verzili D, Boffi A, Royer WE, Hendrickson WA. A cooperative hemoglobin with directly communicating hemes. The Scapharca inaequivalvis homodimer. Biophys Chem. 1990 Aug 31; 37(1-3):287-92. PMID: 2285790.
      Citations: 7     Fields:    Translation:AnimalsCells
    55. Royer WE, Hendrickson WA, Chiancone E. Structural transitions upon ligand binding in a cooperative dimeric hemoglobin. Science. 1990 Aug 03; 249(4968):518-21. PMID: 2382132.
      Citations: 19     Fields:    Translation:AnimalsCells
    56. Royer WE, Hendrickson WA, Chiancone E. The 2.4-A crystal structure of Scapharca dimeric hemoglobin. Cooperativity based on directly communicating hemes at a novel subunit interface. J Biol Chem. 1989 Dec 15; 264(35):21052-61. PMID: 2592366.
      Citations: 13     Fields:    Translation:AnimalsCells
    57. Royer WE, Hendrickson WA. Molecular symmetry of Lumbricus erythrocruorin. J Biol Chem. 1988 Sep 25; 263(27):13762-5. PMID: 3417678.
      Citations: 2     Fields:    Translation:AnimalsCells
    58. Royer WE, Hendrickson WA, Love WE. Crystals of Lumbricus erythrocruorin. J Mol Biol. 1987 Sep 05; 197(1):149-53. PMID: 3681992.
      Citations: 3     Fields:    Translation:AnimalsCells
    59. Hendrickson WA, Royer WE. Principles in the assembly of annelid erythrocruorins. Biophys J. 1986 Jan; 49(1):177-89. PMID: 3955169.
      Citations: 2     Fields:    Translation:AnimalsCells
    60. Royer WE, Love WE, Fenderson FF. Cooperative dimeric and tetrameric clam haemoglobins are novel assemblages of myoglobin folds. Nature. 1985 Jul 18-24; 316(6025):277-80. PMID: 4022123.
      Citations: 24     Fields:    Translation:AnimalsCells
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