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Celia A Schiffer PhD

TitleProfessor
InstitutionUniversity of Massachusetts Medical School
DepartmentBiochemistry and Molecular Pharmacology
AddressUniversity of Massachusetts Medical School
364 Plantation Street, LRB
Worcester MA 01605
Phone508-856-8008
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    Other Positions
    InstitutionUMMS - School of Medicine
    DepartmentBiochemistry and Molecular Pharmacology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentBiochemistry and Molecular Pharmacology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentBioinformatics and Computational Biology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentInterdisciplinary Graduate Program

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentMD/PhD Program

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentTranslational Science

    InstitutionUMMS - Programs, Centers and Institutes
    DepartmentBioinformatics and Integrative Biology

    InstitutionUMMS - Programs, Centers and Institutes
    DepartmentCenter for AIDS Research

    InstitutionUMMS - Programs, Centers and Institutes
    DepartmentChemical Biology


    Collapse Biography 
    Collapse education and training
    University of Chicago, Chicago, IL, United StatesBAPhysics
    University of California, San Francisco, San Francisco, CA, United StatesPHDBiophysics

    Collapse Overview 
    Collapse overview

    Academic Background

    B.A., University of Chicago, 1986
    Ph.D., University of California, San Francisco, 1992


    Postdoctoral Fellow, ETH-Zurich, 1992-94
    Postdoctoral Fellow, Genentech, 1994-97

    Director of the Center for AIDS Research (CFAR)

    Structural basis for molecular recognition in HIV Protease

    Photo: Celia A. SchifferMany biological processes involve complex interdependent molecular recognition events, in which molecules recognize each other with high specificity. Such events include an enzyme acting on its substrate in catalysis, a ligand activating a receptor in regulation and a two dimensional peptide chain assembling into a specific three dimensional fold. The specificity of such molecular recognition events can only be thoroughly understood by detailed analyses of the structures, functions and flexibilities of the molecules.

    Investigating molecular recognition of biological macromolecules at the atomic level has been the central objective of my research. In my group we address these questions by using detailed structural and dynamic analyses (both experimental and computational) combined with functional and biophysical assays. This comprehensive approach is essential as molecular recognition is a dynamic event; usually, at least one of the molecular surfaces needs to undergo a conformational change to recognize the other.

    Disruption of the life cycle of HIV, the virus that causes AIDS, is the goal of the drugs used to treat infected pediatric patients. The most successful drugs are the protease inhibitors. As the individual virus particles assemble, a series of their necessary components are attached together. For the virus particles to mature and become infectious these necessary components must be cut apart. The protease is the "scissors" molecule which "knows" where to sever these components. Protease inhibitors block these scissors and prevent the virus from maturing. Unfortunately, the virus changes (mutates) and alters the protease so that the inhibitors no longer block the "scissors" action, and the virus is once again infectious (drug resistant). Our strategy is to examine how the protease "knows" where to cut and how this "knowledge" is changed when the protease becomes drug resistant. By understanding how the protease changes, our data will be complementary to the existing efforts of the pharmaceutical industry.

    Figure

    complex with the peptide that releases the capsid protein

    In the maturation of the human immunodeficiency virus, HIV proteasespecifically recognizes and cleaves nine non-homologous sites in the gag-polpolyproteins. How this symmetric homodimeric protein is able to specificallyrecognize not only a single substrate, but a variety of substrate sequencesposes fascinating questions of molecular recognition. What allowsone molecule to recognize, bind, cleave and release others? To elucidatethis specificity, our laboratory has solved for the first time structuresof substrate complexes of HIV protease with an inactive variant of HIVprotease. The complex with the peptide that releases the capsidprotein is shown above. These structures are then starting pointsfor molecular dynamics simulations to probe the conformational adaptabilityof this protease, its substrates and the solvent environment. Inaddition as drug resistant mutations occur the specificity of the proteasechanges, we are elucidating these changes with phage display, enzyme kineticsand crystal structures of drug resistant proteases bound to inhibitors.




    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. Matthew AN, Zephyr J, Hill CJ, Jahangir M, Newton A, Petropoulos CJ, Huang W, Kurt Yilmaz N, Schiffer CA, Ali A. Hepatitis C Virus NS3/4A Protease Inhibitors Incorporating Flexible P2 Quinoxalines Target Drug Resistant Viral Variants. J Med Chem. 2017 Jun 08. PMID: 28594175.
      View in: PubMed
    2. Lin KH, Ali A, Rusere L, Soumana DI, Yilmaz NK, Schiffer CA. Dengue Virus NS2B/NS3 Protease Inhibitors Exploiting the Prime Side. J Virol. 2017 Mar 15. PMID: 28298600.
      View in: PubMed
    3. Prachanronarong KL, Özen A, Thayer KM, Yilmaz LS, Zeldovich KB, Bolon DN, Kowalik TF, Jensen JD, Finberg RW, Wang JP, Kurt-Yilmaz N, Schiffer CA. Molecular Basis for Differential Patterns of Drug Resistance in Influenza N1 and N2 Neuraminidase. J Chem Theory Comput. 2016 Dec 13; 12(12):6098-6108. PMID: 27951676.
      View in: PubMed
    4. Shandilya S, Kurt Yilmaz N, Sadowski A, Monir E, Schiller ZA, Thomas WD, Klempner MS, Schiffer CA, Wang Y. Structural and molecular analysis of a protective epitope of Lyme disease antigen OspA and antibody interactions. J Mol Recognit. 2016 Nov 16. PMID: 27859766.
      View in: PubMed
    5. Lin KH, Nalivaika EA, Prachanronarong KL, Yilmaz NK, Schiffer CA. Dengue Protease Substrate Recognition: Binding of the Prime Side. ACS Infect Dis. 2016 Oct 14; 2(10):734-743. PMID: 27657335.
      View in: PubMed
    6. Soumana DI, Kurt Yilmaz N, Ali A, Prachanronarong KL, Schiffer CA. Molecular and Dynamic Mechanism Underlying Drug Resistance in Genotype 3 Hepatitis C NS3/4A Protease. J Am Chem Soc. 2016 Sep 14; 138(36):11850-9. PMID: 27512818.
      View in: PubMed
    7. Kurt Yilmaz N, Swanstrom R, Schiffer CA. Improving Viral Protease Inhibitors to Counter Drug Resistance. Trends Microbiol. 2016 Jul; 24(7):547-57. PMID: 27090931.
      View in: PubMed
    8. Soumana DI, Kurt Yilmaz N, Prachanronarong KL, Aydin C, Ali A, Schiffer CA. Structural and Thermodynamic Effects of Macrocyclization in HCV NS3/4A Inhibitor MK-5172. ACS Chem Biol. 2016 Apr 15; 11(4):900-9. PMID: 26682473.
      View in: PubMed
    9. Jiang L, Liu P, Bank C, Renzette N, Prachanronarong K, Yilmaz LS, Caffrey DR, Zeldovich KB, Schiffer CA, Kowalik TF, Jensen JD, Finberg RW, Wang JP, Bolon DN. A Balance between Inhibitor Binding and Substrate Processing Confers Influenza Drug Resistance. J Mol Biol. 2016 Feb 13; 428(3):538-53. PMID: 26656922.
      View in: PubMed
    10. Prabhu P, Shandilya SM, Britan-Rosich E, Nagler A, Schiffer CA, Kotler M. Inhibition of APOBEC3G activity impedes double-stranded DNA repair. FEBS J. 2016 Jan; 283(1):112-29. PMID: 26460502.
      View in: PubMed
    11. Zhou H, Li S, Badger J, Nalivaika E, Cai Y, Foulkes-Murzycki J, Schiffer C, Makowski L. Modulation of HIV protease flexibility by the T80N mutation. Proteins. 2015 Nov; 83(11):1929-39. PMID: 25488402.
      View in: PubMed
    12. Boopathy S, Silvas TV, Tischbein M, Jansen S, Shandilya SM, Zitzewitz JA, Landers JE, Goode BL, Schiffer CA, Bosco DA. Structural basis for mutation-induced destabilization of profilin 1 in ALS. Proc Natl Acad Sci U S A. 2015 Jun 30; 112(26):7984-9. PMID: 26056300.
      View in: PubMed
    13. Ndjomou J, Corby MJ, Sweeney NL, Hanson AM, Aydin C, Ali A, Schiffer CA, Li K, Frankowski KJ, Schoenen FJ, Frick DN. Simultaneously Targeting the NS3 Protease and Helicase Activities for More Effective Hepatitis C Virus Therapy. ACS Chem Biol. 2015 Aug 21; 10(8):1887-96. PMID: 25961497.
      View in: PubMed
    14. Kouno T, Luengas EM, Shigematsu M, Shandilya SM, Zhang J, Chen L, Hara M, Schiffer CA, Harris RS, Matsuo H. Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G. Nat Struct Mol Biol. 2015 Jun; 22(6):485-91. PMID: 25984970.
      View in: PubMed
    15. Potempa M, Nalivaika E, Ragland D, Lee SK, Schiffer CA, Swanstrom R. A Direct Interaction with RNA Dramatically Enhances the Catalytic Activity of the HIV-1 Protease In Vitro. J Mol Biol. 2015 Jul 17; 427(14):2360-78. PMID: 25986307.
      View in: PubMed
    16. Bohn MF, Schiffer CA. REdiii: a pipeline for automated structure solution. Acta Crystallogr D Biol Crystallogr. 2015 May; 71(Pt 5):1059-67. PMID: 25945571.
      View in: PubMed
    17. Bohn MF, Shandilya SM, Silvas TV, Nalivaika EA, Kouno T, Kelch BA, Ryder SP, Kurt-Yilmaz N, Somasundaran M, Schiffer CA. The ssDNA Mutator APOBEC3A Is Regulated by Cooperative Dimerization. Structure. 2015 May 5; 23(5):903-11. PMID: 25914058.
      View in: PubMed
    18. Zeldovich KB, Liu P, Renzette N, Foll M, Pham ST, Venev SV, Gallagher GR, Bolon DN, Kurt-Jones EA, Jensen JD, Caffrey DR, Schiffer CA, Kowalik TF, Wang JP, Finberg RW. Positive Selection Drives Preferred Segment Combinations during Influenza Virus Reassortment. Mol Biol Evol. 2015 Jun; 32(6):1519-32. PMID: 25713211.
      View in: PubMed
    19. 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.
      View in: PubMed
    20. Özer N, Özen A, Schiffer CA, Haliloglu T. Drug-resistant HIV-1 protease regains functional dynamics through cleavage site coevolution. Evol Appl. 2015 Feb; 8(2):185-98. PMID: 25685193.
      View in: PubMed
    21. Shandilya SM, Bohn MF, Schiffer CA. A computational analysis of the structural determinants of APOBEC3's catalytic activity and vulnerability to HIV-1 Vif. Virology. 2014 Dec; 471-473:105-16. PMID: 25461536.
      View in: PubMed
    22. Özen A, Lin KH, Kurt Yilmaz N, Schiffer CA. Structural basis and distal effects of Gag substrate coevolution in drug resistance to HIV-1 protease. Proc Natl Acad Sci U S A. 2014 Nov 11; 111(45):15993-8. PMID: 25355911.
      View in: PubMed
    23. Soumana DI, Ali A, Schiffer CA. Structural analysis of asunaprevir resistance in HCV NS3/4A protease. ACS Chem Biol. 2014 Nov 21; 9(11):2485-90. PMID: 25243902.
      View in: PubMed
    24. Ragland DA, Nalivaika EA, Nalam MN, Prachanronarong KL, Cao H, Bandaranayake RM, Cai Y, Kurt-Yilmaz N, Schiffer CA. Drug resistance conferred by mutations outside the active site through alterations in the dynamic and structural ensemble of HIV-1 protease. J Am Chem Soc. 2014 Aug 27; 136(34):11956-63. PMID: 25091085.
      View in: PubMed
    25. Cai Y, Myint W, Paulsen JL, Schiffer CA, Ishima R, Kurt Yilmaz N. Drug Resistance Mutations Alter Dynamics of Inhibitor-Bound HIV-1 Protease. J Chem Theory Comput. 2014 Aug 12; 10(8):3438-3448. PMID: 25136270.
      View in: PubMed
    26. Kolli M, Ozen A, Kurt-Yilmaz N, Schiffer CA. HIV-1 protease-substrate coevolution in nelfinavir resistance. J Virol. 2014 Jul; 88(13):7145-54. PMID: 24719428.
      View in: PubMed
    27. 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 2; 588(9):1743-8. PMID: 24657618.
      View in: PubMed
    28. Foll M, Poh YP, Renzette N, Ferrer-Admetlla A, Bank C, Shim H, Malaspinas AS, Ewing G, Liu P, Wegmann D, Caffrey DR, Zeldovich KB, Bolon DN, Wang JP, Kowalik TF, Schiffer CA, Finberg RW, Jensen JD. Influenza virus drug resistance: a time-sampled population genetics perspective. PLoS Genet. 2014 Feb; 10(2):e1004185. PMID: 24586206.
      View in: PubMed
    29. Ozen A, Sherman W, Schiffer CA. Improving the Resistance Profile of Hepatitis C NS3/4A Inhibitors: Dynamic Substrate Envelope Guided Design. J Chem Theory Comput. 2013 Dec 10; 9(12):5693-5705. PMID: 24587770.
      View in: PubMed
    30. Cheng N, Lee SK, Donover PS, Reichman M, Schiffer CA, Hull-Ryde EA, Swanstrom R, Janzen WP. Development of a Novel Screening Strategy Designed to Discover a New Class of HIV Drugs. J Lab Autom. 2014 Jun; 19(3):297-303. PMID: 24305957.
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    31. Renzette N, Caffrey DR, Zeldovich KB, Liu P, Gallagher GR, Aiello D, Porter AJ, Kurt-Jones EA, Bolon DN, Poh YP, Jensen JD, Schiffer CA, Kowalik TF, Finberg RW, Wang JP. Evolution of the influenza A virus genome during development of oseltamivir resistance in vitro. J Virol. 2014 Jan; 88(1):272-81. PMID: 24155392.
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    32. Aydin C, Mukherjee S, Hanson AM, Frick DN, Schiffer CA. The interdomain interface in bifunctional enzyme protein 3/4A (NS3/4A) regulates protease and helicase activities. Protein Sci. 2013 Dec; 22(12):1786-98. PMID: 24123290.
      View in: PubMed
    33. Shen Y, Altman MD, Ali A, Nalam MN, Cao H, Rana TM, Schiffer CA, Tidor B. Testing the substrate-envelope hypothesis with designed pairs of compounds. ACS Chem Biol. 2013 Nov 15; 8(11):2433-41. PMID: 23952265.
      View in: PubMed
    34. Nalam MN, Ali A, Reddy GS, Cao H, Anjum SG, Altman MD, Yilmaz NK, Tidor B, Rana TM, Schiffer CA. Substrate envelope-designed potent HIV-1 protease inhibitors to avoid drug resistance. Chem Biol. 2013 Sep 19; 20(9):1116-24. PMID: 24012370.
      View in: PubMed
    35. Silver NW, King BM, Nalam MN, Cao H, Ali A, Kiran Kumar Reddy GS, Rana TM, Schiffer CA, Tidor B. Efficient Computation of Small-Molecule Configurational Binding Entropy and Free Energy Changes by Ensemble Enumeration. J Chem Theory Comput. 2013 Nov 12; 9(11):5098-5115. PMID: 24250277.
      View in: PubMed
    36. Lee SK, Cheng N, Hull-Ryde E, Potempa M, Schiffer CA, Janzen W, Swanstrom R. A sensitive assay using a native protein substrate for screening HIV-1 maturation inhibitors targeting the protease cleavage site between the matrix and capsid. Biochemistry. 2013 Jul 23; 52(29):4929-40. PMID: 23763575.
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    37. Schiffer C. Interview with Celia Schiffer. Future Med Chem. 2013 Jul; 5(11):1193-7. PMID: 23859201.
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    38. Varghese V, Mitsuya Y, Fessel WJ, Liu TF, Melikian GL, Katzenstein DA, Schiffer CA, Holmes SP, Shafer RW. Prototypical Recombinant Multi-Protease Inhibitor Resistant Infectious Molecular Clones of Human Immunodeficiency Virus Type-1. Antimicrob Agents Chemother. 2013 Sep; 57(9):4290-4299. PMID: 23796938.
      View in: PubMed
    39. Bohn MF, Shandilya SM, Albin JS, Kouno T, Anderson BD, McDougle RM, Carpenter MA, Rathore A, Evans L, Davis AN, Zhang J, Lu Y, Somasundaran M, Matsuo H, Harris RS, Schiffer CA. Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure. 2013 Jun 4; 21(6):1042-50. PMID: 23685212.
      View in: PubMed
    40. Ali A, Aydin C, Gildemeister R, Romano KP, Cao H, Ozen A, Soumana D, Newton A, Petropoulos CJ, Huang W, Schiffer CA. Evaluating the role of macrocycles in the susceptibility of hepatitis C virus NS3/4A protease inhibitors to drug resistance. ACS Chem Biol. 2013 Jul 19; 8(7):1469-78. PMID: 23594083.
      View in: PubMed
    41. Mittal S, Bandaranayake RM, King NM, Prabu-Jeyabalan M, Nalam MN, Nalivaika EA, Yilmaz NK, Schiffer CA. Structural and thermodynamic basis of amprenavir/darunavir and atazanavir resistance in HIV-1 protease with mutations at residue 50. J Virol. 2013 Apr; 87(8):4176-84. PMID: 23365446.
      View in: PubMed
    42. Foulkes-Murzycki JE, Rosi C, Kurt Yilmaz N, Shafer RW, Schiffer CA. Cooperative effects of drug-resistance mutations in the flap region of HIV-1 protease. ACS Chem Biol. 2013 Mar 15; 8(3):513-8. PMID: 23252515.
      View in: PubMed
    43. Babrzadeh F, Varghese V, Pacold M, Liu TF, Nyrén P, Schiffer C, Fessel WJ, Shafer RW. Collinearity of protease mutations in HIV-1 samples with high-level protease inhibitor class resistance. J Antimicrob Chemother. 2013 Feb; 68(2):414-8. PMID: 23085775.
      View in: PubMed
    44. Carpenter MA, Li M, Rathore A, Lackey L, Law EK, Land AM, Leonard B, Shandilya SM, Bohn MF, Schiffer CA, Brown WL, Harris RS. Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J Biol Chem. 2012 Oct 05; 287(41):34801-8. PMID: 22896697.
      View in: PubMed
    45. Mruk K, Shandilya SM, Blaustein RO, Schiffer CA, Kobertz WR. Structural insights into neuronal K+ channel-calmodulin complexes. Proc Natl Acad Sci U S A. 2012 Aug 21; 109(34):13579-83. PMID: 22869708.
      View in: PubMed
    46. Romano KP, Ali A, Aydin C, Soumana D, Ozen A, Deveau LM, Silver C, Cao H, Newton A, Petropoulos CJ, Huang W, Schiffer CA. The molecular basis of drug resistance against hepatitis C virus NS3/4A protease inhibitors. PLoS Pathog. 2012; 8(7):e1002832. PMID: 22910833.
      View in: PubMed
    47. Parai MK, Huggins DJ, Cao H, Nalam MN, Ali A, Schiffer CA, Tidor B, Rana TM. Design, synthesis, and biological and structural evaluations of novel HIV-1 protease inhibitors to combat drug resistance. J Med Chem. 2012 Jul 26; 55(14):6328-41. PMID: 22708897.
      View in: PubMed
    48. King NM, Prabu-Jeyabalan M, Bandaranayake RM, Nalam MN, Nalivaika EA, Özen A, Haliloglu T, Yilmaz NK, Schiffer CA. Extreme entropy-enthalpy compensation in a drug-resistant variant of HIV-1 protease. ACS Chem Biol. 2012 Sep 21; 7(9):1536-46. PMID: 22712830.
      View in: PubMed
    49. Alvizo O, Mittal S, Mayo SL, Schiffer CA. Structural, kinetic, and thermodynamic studies of specificity designed HIV-1 protease. Protein Sci. 2012 Jul; 21(7):1029-41. PMID: 22549928.
      View in: PubMed
    50. Cai Y, Yilmaz NK, Myint W, Ishima R, Schiffer CA. Differential Flap Dynamics in Wild-type and a Drug Resistant Variant of HIV-1 Protease Revealed by Molecular Dynamics and NMR Relaxation. J Chem Theory Comput. 2012 Oct 9; 8(10):3452-3462. PMID: 23144597.
      View in: PubMed
    51. Myint W, Cai Y, Schiffer CA, Ishima R. Quantitative comparison of errors in 15N transverse relaxation rates measured using various CPMG phasing schemes. J Biomol NMR. 2012 May; 53(1):13-23. PMID: 22466935.
      View in: PubMed
    52. Mittal S, Cai Y, Nalam MN, Bolon DN, Schiffer CA. Hydrophobic core flexibility modulates enzyme activity in HIV-1 protease. J Am Chem Soc. 2012 Mar 7; 134(9):4163-8. PMID: 22295904.
      View in: PubMed
    53. Ozen A, Haliloglu T, Schiffer CA. HIV-1 Protease and Substrate Coevolution Validates the Substrate Envelope As the Substrate Recognition Pattern. J Chem Theory Comput. 2012 Feb 14; 8(2). PMID: 24348205.
      View in: PubMed
    54. Lee SK, Potempa M, Kolli M, Özen A, Schiffer CA, Swanstrom R. Context surrounding processing sites is crucial in determining cleavage rate of a subset of processing sites in HIV-1 Gag and Gag-Pro-Pol polyprotein precursors by viral protease. J Biol Chem. 2012 Apr 13; 287(16):13279-90. PMID: 22334652.
      View in: PubMed
    55. Li M, Shandilya SM, Carpenter MA, Rathore A, Brown WL, Perkins AL, Harki DA, Solberg J, Hook DJ, Pandey KK, Parniak MA, Johnson JR, Krogan NJ, Somasundaran M, Ali A, Schiffer CA, Harris RS. First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem Biol. 2012 Mar 16; 7(3):506-17. PMID: 22181350.
      View in: PubMed
    56. Cai Y, Schiffer C. Decomposing the energetic impact of drug-resistant mutations: the example of HIV-1 protease-DRV binding. Methods Mol Biol. 2012; 819:551-60. PMID: 22183557.
      View in: PubMed
    57. Auclair JR, Somasundaran M, Green KM, Evans JE, Schiffer CA, Ringe D, Petsko GA, Agar JN. Mass spectrometry tools for analysis of intermolecular interactions. Methods Mol Biol. 2012; 896:387-98. PMID: 22821539.
      View in: PubMed
    58. Dierynck I, Van Marck H, Van Ginderen M, Jonckers TH, Nalam MN, Schiffer CA, Raoof A, Kraus G, Picchio G. TMC310911, a novel human immunodeficiency virus type 1 protease inhibitor, shows in vitro an improved resistance profile and higher genetic barrier to resistance compared with current protease inhibitors. Antimicrob Agents Chemother. 2011 Dec; 55(12):5723-31. PMID: 21896904.
      View in: PubMed
    59. Ozen A, Haliloglu T, Schiffer CA. Dynamics of preferential substrate recognition in HIV-1 protease: redefining the substrate envelope. J Mol Biol. 2011 Jul 22; 410(4):726-44. PMID: 21762811.
      View in: PubMed
    60. Anderson AC, Pollastri MP, Schiffer CA, Peet NP. The challenge of developing robust drugs to overcome resistance. Drug Discov Today. 2011 Sep; 16(17-18):755-61. PMID: 21784168.
      View in: PubMed
    61. Romano KP, Laine JM, Deveau LM, Cao H, Massi F, Schiffer CA. Molecular mechanisms of viral and host cell substrate recognition by hepatitis C virus NS3/4A protease. J Virol. 2011 Jul; 85(13):6106-16. PMID: 21507982.
      View in: PubMed
    62. Parry CM, Kolli M, Myers RE, Cane PA, Schiffer C, Pillay D. Three residues in HIV-1 matrix contribute to protease inhibitor susceptibility and replication capacity. Antimicrob Agents Chemother. 2011 Mar; 55(3):1106-13. PMID: 21149628.
      View in: PubMed
    63. 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 7; 107(49):20986-91. PMID: 21084633.
      View in: PubMed
    64. Ali A, Bandaranayake RM, Cai Y, King NM, Kolli M, Mittal S, Murzycki JF, Nalam MN, Nalivaika EA, Ozen A, Prabu-Jeyabalan MM, Thayer K, Schiffer CA. Molecular Basis for Drug Resistance in HIV-1 Protease. Viruses. 2010 Nov; 2(11):2509-35. PMID: 21994628.
      View in: PubMed
    65. Ali A, Reddy GS, Nalam MN, Anjum SG, Cao H, Schiffer CA, Rana TM. Structure-based design, synthesis, and structure-activity relationship studies of HIV-1 protease inhibitors incorporating phenyloxazolidinones. J Med Chem. 2010 Nov 11; 53(21):7699-708. PMID: 20958050.
      View in: PubMed
    66. Straza MW, Paliwal S, Kovi RC, Rajeshkumar B, Trenh P, Parker D, Whalen GF, Lyle S, Schiffer CA, Grossman SR. Therapeutic targeting of C-terminal binding protein in human cancer. Cell Cycle. 2010 Sep 15; 9(18):3740-50. PMID: 20930544.
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    67. Ozer N, Schiffer CA, Haliloglu T. Rationale for more diverse inhibitors in competition with substrates in HIV-1 protease. Biophys J. 2010 Sep 8; 99(5):1650-9. PMID: 20816079.
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    68. Bandaranayake RM, Kolli M, King NM, Nalivaika EA, Heroux A, Kakizawa J, Sugiura W, Schiffer CA. The effect of clade-specific sequence polymorphisms on HIV-1 protease activity and inhibitor resistance pathways. J Virol. 2010 Oct; 84(19):9995-10003. PMID: 20660190.
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    69. Cai Y, Schiffer CA. Decomposing the energetic impact of drug resistant mutations in HIV-1 protease on binding DRV. J Chem Theory Comput. 2010 Apr 13; 6(4):1358-1368. PMID: 20543885.
      View in: PubMed
    70. Nalam MN, Ali A, Altman MD, Reddy GS, Chellappan S, Kairys V, Ozen A, Cao H, Gilson MK, Tidor B, Rana TM, Schiffer CA. Evaluating the substrate-envelope hypothesis: structural analysis of novel HIV-1 protease inhibitors designed to be robust against drug resistance. J Virol. 2010 May; 84(10):5368-78. PMID: 20237088.
      View in: PubMed
    71. 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.
      View in: PubMed
    72. Kairys V, Gilson MK, Lather V, Schiffer CA, Fernandes MX. Toward the design of mutation-resistant enzyme inhibitors: further evaluation of the substrate envelope hypothesis. Chem Biol Drug Des. 2009 Sep; 74(3):234-45. PMID: 19703025.
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    73. Kolli M, Stawiski E, Chappey C, Schiffer CA. Human immunodeficiency virus type 1 protease-correlated cleavage site mutations enhance inhibitor resistance. J Virol. 2009 Nov; 83(21):11027-42. PMID: 19706699.
      View in: PubMed
    74. Jorissen RN, Reddy GS, Ali A, Altman MD, Chellappan S, Anjum SG, Tidor B, Schiffer CA, Rana TM, Gilson MK. Additivity in the analysis and design of HIV protease inhibitors. J Med Chem. 2009 Feb 12; 52(3):737-54. PMID: 19193159.
      View in: PubMed
    75. Anderson J, Schiffer C, Lee SK, Swanstrom R. Viral protease inhibitors. Handb Exp Pharmacol. 2009; (189):85-110. PMID: 19048198.
      View in: PubMed
    76. Nalam MN, Schiffer CA. New approaches to HIV protease inhibitor drug design II: testing the substrate envelope hypothesis to avoid drug resistance and discover robust inhibitors. Curr Opin HIV AIDS. 2008 Nov; 3(6):642-6. PMID: 19373036.
      View in: PubMed
    77. 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.
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    78. Lefebvre E, Schiffer CA. Resilience to resistance of HIV-1 protease inhibitors: profile of darunavir. AIDS Rev. 2008 Jul-Sep; 10(3):131-42. PMID: 18820715.
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    79. Bandaranayake RM, Prabu-Jeyabalan M, Kakizawa J, Sugiura W, Schiffer CA. Structural analysis of human immunodeficiency virus type 1 CRF01_AE protease in complex with the substrate p1-p6. J Virol. 2008 Jul; 82(13):6762-6. PMID: 18434392.
      View in: PubMed
    80. Altman MD, Ali A, Reddy GS, Nalam MN, Anjum SG, Cao H, Chellappan S, Kairys V, Fernandes MX, Gilson MK, Schiffer CA, Rana TM, Tidor B. HIV-1 protease inhibitors from inverse design in the substrate envelope exhibit subnanomolar binding to drug-resistant variants. J Am Chem Soc. 2008 May 14; 130(19):6099-113. PMID: 18412349.
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    81. 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.
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    82. Altman MD, Nalivaika EA, Prabu-Jeyabalan M, Schiffer CA, Tidor B. Computational design and experimental study of tighter binding peptides to an inactivated mutant of HIV-1 protease. Proteins. 2008 Feb 15; 70(3):678-94. PMID: 17729291.
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    83. Auclair JR, Green KM, Shandilya S, Evans JE, Somasundaran M, Schiffer CA. Mass spectrometry analysis of HIV-1 Vif reveals an increase in ordered structure upon oligomerization in regions necessary for viral infectivity. Proteins. 2007 Nov 1; 69(2):270-84. PMID: 17598142.
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    84. Reddy GS, Ali A, Nalam MN, Anjum SG, Cao H, Nathans RS, Schiffer CA, Rana TM. Design and synthesis of HIV-1 protease inhibitors incorporating oxazolidinones as P2/P2' ligands in pseudosymmetric dipeptide isosteres. J Med Chem. 2007 Sep 6; 50(18):4316-28. PMID: 17696512.
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    85. Chellappan S, Kairys V, Fernandes MX, Schiffer C, Gilson MK. Evaluation of the substrate envelope hypothesis for inhibitors of HIV-1 protease. Proteins. 2007 Aug 1; 68(2):561-7. PMID: 17474129.
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    86. Nalam MN, Peeters A, Jonckers TH, Dierynck I, Schiffer CA. Crystal structure of lysine sulfonamide inhibitor reveals the displacement of the conserved flap water molecule in human immunodeficiency virus type 1 protease. J Virol. 2007 Sep; 81(17):9512-8. PMID: 17596316.
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    87. Chellappan S, Kiran Kumar Reddy GS, Ali A, Nalam MN, Anjum SG, Cao H, Kairys V, Fernandes MX, Altman MD, Tidor B, Rana TM, Schiffer CA, Gilson MK. Design of mutation-resistant HIV protease inhibitors with the substrate envelope hypothesis. Chem Biol Drug Des. 2007 May; 69(5):298-313. PMID: 17539822.
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    88. 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.
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    89. Foulkes-Murzycki JE, Scott WR, Schiffer CA. Hydrophobic sliding: a possible mechanism for drug resistance in human immunodeficiency virus type 1 protease. Structure. 2007 Feb; 15(2):225-33. PMID: 17292840.
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    90. Ali A, Reddy GS, Cao H, Anjum SG, Nalam MN, Schiffer CA, Rana TM. Discovery of HIV-1 protease inhibitors with picomolar affinities incorporating N-aryl-oxazolidinone-5-carboxamides as novel P2 ligands. J Med Chem. 2006 Dec 14; 49(25):7342-56. PMID: 17149864.
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    91. Mitsuya Y, Winters MA, Fessel WJ, Rhee SY, Hurley L, Horberg M, Schiffer CA, Zolopa AR, Shafer RW. N88D facilitates the co-occurrence of D30N and L90M and the development of multidrug resistance in HIV type 1 protease following nelfinavir treatment failure. AIDS Res Hum Retroviruses. 2006 Dec; 22(12):1300-5. PMID: 17209774.
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    92. Forget AL, Kudron MM, McGrew DA, Calmann MA, Schiffer CA, Knight KL. RecA dimers serve as a functional unit for assembly of active nucleoprotein filaments. Biochemistry. 2006 Nov 14; 45(45):13537-42. PMID: 17087507.
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    93. Ozer N, Haliloglu T, Schiffer CA. Substrate specificity in HIV-1 protease by a biased sequence search method. Proteins. 2006 Aug 1; 64(2):444-56. PMID: 16741993.
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    94. Foulkes JE, Prabu-Jeyabalan M, Cooper D, Henderson GJ, Harris J, Swanstrom R, Schiffer CA. Role of invariant Thr80 in human immunodeficiency virus type 1 protease structure, function, and viral infectivity. J Virol. 2006 Jul; 80(14):6906-16. PMID: 16809296.
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    95. Prabu-Jeyabalan M, Nalivaika EA, Romano K, Schiffer CA. Mechanism of substrate recognition by drug-resistant human immunodeficiency virus type 1 protease variants revealed by a novel structural intermediate. J Virol. 2006 Apr; 80(7):3607-16. PMID: 16537628.
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    96. Prabu-Jeyabalan M, King NM, Nalivaika EA, Heilek-Snyder G, Cammack N, Schiffer CA. Substrate envelope and drug resistance: crystal structure of RO1 in complex with wild-type human immunodeficiency virus type 1 protease. Antimicrob Agents Chemother. 2006 Apr; 50(4):1518-21. PMID: 16569872.
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    97. Kolli M, Lastere S, Schiffer CA. Co-evolution of nelfinavir-resistant HIV-1 protease and the p1-p6 substrate. Virology. 2006 Apr 10; 347(2):405-9. PMID: 16430939.
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    98. Liu F, Wagner S, Campbell RB, Nickerson JA, Schiffer CA, Ross AH. PTEN enters the nucleus by diffusion. J Cell Biochem. 2005 Oct 1; 96(2):221-34. PMID: 16088943.
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    99. Afkar E, Reguera G, Schiffer M, Lovley DR. A novel Geobacteraceae-specific outer membrane protein J (OmpJ) is essential for electron transport to Fe(III) and Mn(IV) oxides in Geobacter sulfurreducens. BMC Microbiol. 2005 Jul 06; 5:41. PMID: 16000176.
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    100. Surleraux DL, de Kock HA, Verschueren WG, Pille GM, Maes LJ, Peeters A, Vendeville S, De Meyer S, Azijn H, Pauwels R, de Bethune MP, King NM, Prabu-Jeyabalan M, Schiffer CA, Wigerinck PB. Design of HIV-1 protease inhibitors active on multidrug-resistant virus. J Med Chem. 2005 Mar 24; 48(6):1965-73. PMID: 15771440.
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    101. Surleraux DL, Tahri A, Verschueren WG, Pille GM, de Kock HA, Jonckers TH, Peeters A, De Meyer S, Azijn H, Pauwels R, de Bethune MP, King NM, Prabu-Jeyabalan M, Schiffer CA, Wigerinck PB. Discovery and selection of TMC114, a next generation HIV-1 protease inhibitor. J Med Chem. 2005 Mar 24; 48(6):1813-22. PMID: 15771427.
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    102. Johnston E, Winters MA, Rhee SY, Merigan TC, Schiffer CA, Shafer RW. Association of a novel human immunodeficiency virus type 1 protease substrate cleft mutation, L23I, with protease inhibitor therapy and in vitro drug resistance. Antimicrob Agents Chemother. 2004 Dec; 48(12):4864-8. PMID: 15561868.
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    103. King NM, Prabu-Jeyabalan M, Nalivaika EA, Wigerinck P, de Béthune MP, Schiffer CA. Structural and thermodynamic basis for the binding of TMC114, a next-generation human immunodeficiency virus type 1 protease inhibitor. J Virol. 2004 Nov; 78(21):12012-21. PMID: 15479840.
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    104. Prabu-Jeyabalan M, Nalivaika EA, King NM, Schiffer CA. Structural basis for coevolution of a human immunodeficiency virus type 1 nucleocapsid-p1 cleavage site with a V82A drug-resistant mutation in viral protease. J Virol. 2004 Nov; 78(22):12446-54. PMID: 15507631.
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    105. King NM, Prabu-Jeyabalan M, Nalivaika EA, Schiffer CA. Combating susceptibility to drug resistance: lessons from HIV-1 protease. Chem Biol. 2004 Oct; 11(10):1333-8. PMID: 15489160.
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    106. Hoffman NG, Schiffer CA, Swanstrom R. Covariation of amino acid positions in HIV-1 protease. Virology. 2003 Sep 30; 314(2):536-48. PMID: 14554082.
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    107. Kurt N, Haliloglu T, Schiffer CA. Structure-based prediction of potential binding and nonbinding peptides to HIV-1 protease. Biophys J. 2003 Aug; 85(2):853-63. PMID: 12885633.
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    108. Kurt N, Scott WR, Schiffer CA, Haliloglu T. Cooperative fluctuations of unliganded and substrate-bound HIV-1 protease: a structure-based analysis on a variety of conformations from crystallography and molecular dynamics simulations. Proteins. 2003 May 15; 51(3):409-22. PMID: 12696052.
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    109. Wu TD, Schiffer CA, Gonzales MJ, Taylor J, Kantor R, Chou S, Israelski D, Zolopa AR, Fessel WJ, Shafer RW. Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J Virol. 2003 Apr; 77(8):4836-47. PMID: 12663790.
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    110. Prabu-Jeyabalan M, Nalivaika EA, King NM, Schiffer CA. Viability of a drug-resistant human immunodeficiency virus type 1 protease variant: structural insights for better antiviral therapy. J Virol. 2003 Jan; 77(2):1306-15. PMID: 12502847.
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    111. Schiffer C, Hermans J. Promise of advances in simulation methods for protein crystallography: implicit solvent models, time-averaging refinement, and quantum mechanical modeling. Methods Enzymol. 2003; 374:412-61. PMID: 14696384.
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    112. Schonhoff CM, Daou MC, Jones SN, Schiffer CA, Ross AH. Nitric oxide-mediated inhibition of Hdm2-p53 binding. Biochemistry. 2002 Nov 19; 41(46):13570-4. PMID: 12427017.
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    113. Pettit SC, Henderson GJ, Schiffer CA, Swanstrom R. Replacement of the P1 amino acid of human immunodeficiency virus type 1 Gag processing sites can inhibit or enhance the rate of cleavage by the viral protease. J Virol. 2002 Oct; 76(20):10226-33. PMID: 12239298.
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    114. Liu H, Radhakrishnan P, Magoun L, Prabu M, Campellone KG, Savage P, He F, Schiffer CA, Leong JM. Point mutants of EHEC intimin that diminish Tir recognition and actin pedestal formation highlight a putative Tir binding pocket. Mol Microbiol. 2002 Sep; 45(6):1557-73. PMID: 12354225.
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    115. Prabu-Jeyabalan M, Nalivaika E, Schiffer CA. Substrate shape determines specificity of recognition for HIV-1 protease: analysis of crystal structures of six substrate complexes. Structure. 2002 Mar; 10(3):369-81. PMID: 12005435.
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    116. Schiffer C, Ultsch M, Walsh S, Somers W, de Vos AM, Kossiakoff A. Structure of a phage display-derived variant of human growth hormone complexed to two copies of the extracellular domain of its receptor: evidence for strong structural coupling between receptor binding sites. J Mol Biol. 2002 Feb 15; 316(2):277-89. PMID: 11851338.
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    117. King NM, Melnick L, Prabu-Jeyabalan M, Nalivaika EA, Yang SS, Gao Y, Nie X, Zepp C, Heefner DL, Schiffer CA. Lack of synergy for inhibitors targeting a multi-drug-resistant HIV-1 protease. Protein Sci. 2002 Feb; 11(2):418-29. PMID: 11790852.
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    118. Bakri Y, Schiffer C, Zennou V, Charneau P, Kahn E, Benjouad A, Gluckman JC, Canque B. The maturation of dendritic cells results in postintegration inhibition of HIV-1 replication. J Immunol. 2001 Mar 15; 166(6):3780-8. PMID: 11238620.
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    119. Scott WR, Schiffer CA. Curling of flap tips in HIV-1 protease as a mechanism for substrate entry and tolerance of drug resistance. Structure. 2000 Dec 15; 8(12):1259-65. PMID: 11188690.
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    120. Prabu-Jeyabalan M, Nalivaika E, Schiffer CA. How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J Mol Biol. 2000 Sep 1; 301(5):1207-20. PMID: 10966816.
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    121. Hensley ML, Peterson B, Silver RT, Larson RA, Schiffer CA, Szatrowski TP. Risk factors for severe neuropsychiatric toxicity in patients receiving interferon alfa-2b and low-dose cytarabine for chronic myelogenous leukemia: analysis of Cancer and Leukemia Group B 9013. J Clin Oncol. 2000 Mar; 18(6):1301-8. PMID: 10715301.
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    122. Schiffer CA, van Gunsteren WF. Accessibility and order of water sites in and around proteins: A crystallographic time-averaging study. Proteins. 1999 Sep 1; 36(4):501-11. PMID: 10450092.
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    123. Kornblith AB, Herndon JE, Zuckerman E, Cella DF, Cherin E, Wolchok S, Weiss RB, Diehl LF, Henderson E, Cooper MR, Schiffer C, Canellos GP, Mayer RJ, Silver RT, Schilling A, Peterson BA, Greenberg D, Holland JC. Comparison of psychosocial adaptation of advanced stage Hodgkin's disease and acute leukemia survivors. Cancer and Leukemia Group B. Ann Oncol. 1998 Mar; 9(3):297-306. PMID: 9602264.
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    124. Peng JW, Schiffer CA, Xu P, van Gunsteren WF, Ernst RR. Investigations of peptide hydration using NMR and molecular dynamics simulations: A study of effects of water on the conformation and dynamics of antamanide. J Biomol NMR. 1996 Dec; 8(4):453-76. PMID: 20859779.
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    125. Schiffer CA, van Gunsteren WF. Structural stability of disulfide mutants of basic pancreatic trypsin inhibitor: a molecular dynamics study. Proteins. 1996 Sep; 26(1):66-71. PMID: 8880930.
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    126. Schiffer CA, Dötsch V. The role of protein-solvent interactions in protein unfolding. Curr Opin Biotechnol. 1996 Aug; 7(4):428-32. PMID: 8768902.
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    127. Schiffer CA, Clifton IJ, Davisson VJ, Santi DV, Stroud RM. Crystal structure of human thymidylate synthase: a structural mechanism for guiding substrates into the active site. Biochemistry. 1995 Dec 19; 34(50):16279-87. PMID: 8845352.
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    128. Schiffer CA, Dötsch V, Wüthrich K, van Gunsteren WF. Exploring the role of the solvent in the denaturation of a protein: a molecular dynamics study of the DNA binding domain of the 434 repressor. Biochemistry. 1995 Nov 21; 34(46):15057-67. PMID: 7578118.
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    129. Van Gunsteren WF, Hünenberger PH, Kovacs H, Mark AE, Schiffer CA. Investigation of protein unfolding and stability by computer simulation. Philos Trans R Soc Lond B Biol Sci. 1995 Apr 29; 348(1323):49-59. PMID: 7770486.
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    130. Schiffer CA, Gros P, van Gunsteren WF. Time-averaging crystallographic refinement: possibilities and limitations using alpha-cyclodextrin as a test system. Acta Crystallogr D Biol Crystallogr. 1995 Jan 1; 51(Pt 1):85-92. PMID: 15299339.
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    131. Schiffer CA, Huber R, Wüthrich K, van Gunsteren WF. Simultaneous refinement of the structure of BPTI against NMR data measured in solution and X-ray diffraction data measured in single crystals. J Mol Biol. 1994 Aug 26; 241(4):588-99. PMID: 7520085.
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    132. Greene PJ, Yu PL, Zhao J, Schiffer CA, Santi D. Expression, purification, and characterization of thymidylate synthase from Lactococcus lactis. Protein Sci. 1994 Jul; 3(7):1114-6. PMID: 7920258.
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    133. Neubauer A, Dodge RK, George SL, Davey FR, Silver RT, Schiffer CA, Mayer RJ, Ball ED, Wurster-Hill D, Bloomfield CD, et al. Prognostic importance of mutations in the ras proto-oncogenes in de novo acute myeloid leukemia. Blood. 1994 Mar 15; 83(6):1603-11. PMID: 8123851.
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    134. van Gunsteren WF, Brunne RM, Gros P, van Schaik RC, Schiffer CA, Torda AE. Accounting for molecular mobility in structure determination based on nuclear magnetic resonance spectroscopic and X-ray diffraction data. Methods Enzymol. 1994; 239:619-54. PMID: 7530320.
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    135. Sandler DP, Shore DL, Anderson JR, Davey FR, Arthur D, Mayer RJ, Silver RT, Weiss RB, Moore JO, Schiffer CA, et al. Cigarette smoking and risk of acute leukemia: associations with morphology and cytogenetic abnormalities in bone marrow. J Natl Cancer Inst. 1993 Dec 15; 85(24):1994-2003. PMID: 8246285.
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    136. Ozer H, George SL, Schiffer CA, Rao K, Rao PN, Wurster-Hill DH, Arthur DD, Powell B, Gottlieb A, Peterson BA, Rai K, Testa JR, LeBeau M, Tantravahi R, Bloomfield CD. Prolonged subcutaneous administration of recombinant alpha 2b interferon in patients with previously untreated Philadelphia chromosome-positive chronic-phase chronic myelogenous leukemia: effect on remission duration and survival: Cancer and Leukemia Group B study 8583. Blood. 1993 Nov 15; 82(10):2975-84. PMID: 8219189.
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    137. Schiffer CA, Caldwell JW, Stroud RM, Kollman PA. Inclusion of solvation free energy with molecular mechanics energy: alanyl dipeptide as a test case. Protein Sci. 1992 Mar; 1(3):396-400. PMID: 1304346.
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    138. Schiffer CA, Davisson VJ, Santi DV, Stroud RM. Crystallization of human thymidylate synthase. J Mol Biol. 1991 May 20; 219(2):161-3. PMID: 2038053.
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    139. Schiffer CA, Caldwell JW, Kollman PA, Stroud RM. Prediction of homologous protein structures based on conformational searches and energetics. Proteins. 1990; 8(1):30-43. PMID: 2217162.
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