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    Tracy Handel

    TitleProfessor
    SchoolUniversity of California, San Diego
    DepartmentSchool of Pharmacy and Pharmaceutical Science
    Address9500 Gilman Drive #0684
    CA La Jolla 92093
    Phone858-822-6656
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      Collapse Biography 
      Collapse Education and Training
      Ph.D.California Institute of Technology

      Collapse Overview 

      Collapse Research 
      Collapse Research Activities and Funding
      Chemokine interaction with CXCR4 and ACKR3: structure and activation mechanisms
      NIH/NIGMS R01GM117424Sep 15, 2016 - May 31, 2020
      Role: Principal Investigator
      2016 Chemotactic Cytokines Gordon Research Conference & Gordon Research Seminar
      NIH/NIAID R13AI124469Mar 15, 2016 - Feb 28, 2017
      Role: Principal Investigator
      Dissecting the interactions of gp120 with chemokine receptor CXCR4
      NIH/NIAID R21AI121918Jan 15, 2016 - Dec 31, 2017
      Role: Principal Investigator
      Structure Determination of the Chemokine Receptor CCR2 with Novel Inhibitors
      NIH/NIAID R21AI122211Jan 1, 2016 - Dec 31, 2017
      Role: Principal Investigator
      The structural plasticity of chemokine and gp120 recognition by CCR5
      NIH/NIAID R01AI118985May 11, 2015 - Apr 30, 2020
      Role: Principal Investigator
      Synthetic Fabs for Crystallization of Chemokine:Receptor Complexes
      NIH/NIAID R21AI101687Jul 24, 2012 - Jun 30, 2014
      Role: Principal Investigator
      Structure, Dynamics and Activation Mechanisms of Chemokine Receptors
      NIH/NIGMS U01GM094612Sep 30, 2010 - Jun 30, 2015
      Role: Principal Investigator
      Sensitive Deuterium Exchange MS for Membrane Proteins
      NIH/NIGMS R01GM093325Sep 30, 2010 - Aug 31, 2013
      Role: Principal Investigator
      Engineering Chemokine Receptor Signaling Complexes In Vitro
      NIH/NIGMS R01GM081763Jun 1, 2009 - May 31, 2013
      Role: Principal Investigator
      Hydrogen Deuterium Exchange Mapping of Chemokine Receptor Complex Interfaces
      NIH/NIAID R21AI076961Jun 15, 2008 - May 31, 2011
      Role: Principal Investigator
      Structure-Function Studies &Molecular Interactions of Chemokines
      NIH/NIAID R01AI037113Dec 1, 1994 - Nov 30, 2015
      Role: Principal Investigator

      Collapse ORNG Applications 
      Collapse Websites

      Collapse Bibliographic 
      Collapse Publications
      Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help.
      List All   |   Timeline
      1. Proudfoot AEI, Johnson Z, Bonvin P, Handel T. Glycosaminoglycan Interactions with Chemokines Add Complexity to a Complex System. Pharmaceuticals (Basel). 2017 Aug 09; 10(3). PMID: 28792472.
        View in: PubMed
      2. Zong C, Venot A, Li X, Lu W, Xiao W, Wilkes JL, Salanga CL, Handel T, Wang L, Wolfert MA, Boons GJ. Heparan Sulfate Microarray Reveals That Heparan Sulfate-Protein Binding Exhibits Different Ligand Requirements. J Am Chem Soc. 2017 Jul 07. PMID: 28651046.
        View in: PubMed
      3. Zheng Y, Han GW, Abagyan R, Wu B, Stevens RC, Cherezov V, Kufareva I, Handel T. Structure of CC Chemokine Receptor 5 with a Potent Chemokine Antagonist Reveals Mechanisms of Chemokine Recognition and Molecular Mimicry by HIV. Immunity. 2017 Jun 20; 46(6):1005-1017.e5. PMID: 28636951.
        View in: PubMed
      4. Kufareva I, Gustavsson M, Zheng Y, Stephens BS, Handel T. What Do Structures Tell Us About Chemokine Receptor Function and Antagonism? Annu Rev Biophys. 2017 May 22; 46:175-198. PMID: 28532213.
        View in: PubMed
      5. Gustavsson M, Wang L, van Gils N, Stephens BS, Zhang P, Schall TJ, Yang S, Abagyan R, Chance MR, Kufareva I, Handel T. Structural basis of ligand interaction with atypical chemokine receptor 3. Nat Commun. 2017 Jan 18; 8:14135. PMID: 28098154.
        View in: PubMed
      6. Dyer DP, Migliorini E, Salanga CL, Thakar D, Handel T, Richter RP. Differential structural remodelling of heparan sulfate by chemokines: the role of chemokine oligomerization. Open Biol. 2017 Jan; 7(1). PMID: 28123055.
        View in: PubMed
      7. Zheng Y, Qin L, Zacarías NV, de Vries H, Han GW, Gustavsson M, Dabros M, Zhao C, Cherney RJ, Carter P, Stamos D, Abagyan R, Cherezov V, Stevens RC, IJzerman AP, Heitman LH, Tebben A, Kufareva I, Handel T. Structure of CC chemokine receptor 2 with orthosteric and allosteric antagonists. Nature. 2016 Dec 07. PMID: 27926736.
        View in: PubMed
      8. Wescott MP, Kufareva I, Paes C, Goodman JR, Thaker Y, Puffer BA, Berdougo E, Rucker JB, Handel T, Doranz BJ. Signal transmission through the CXC chemokine receptor 4 (CXCR4) transmembrane helices. Proc Natl Acad Sci U S A. 2016 Aug 30; 113(35):9928-33. PMID: 27543332.
        View in: PubMed
      9. Dyer DP, Salanga CL, Johns SC, Valdambrini E, Fuster MM, Milner CM, Day AJ, Handel T. The Anti-inflammatory Protein TSG-6 Regulates Chemokine Function by Inhibiting Chemokine/Glycosaminoglycan Interactions. J Biol Chem. 2016 Jun 10; 291(24):12627-40. PMID: 27044744.
        View in: PubMed
      10. Fox JC, Tyler RC, Peterson FC, Dyer DP, Zhang F, Linhardt RJ, Handel T, Volkman BF. Examination of Glycosaminoglycan Binding Sites on the XCL1 Dimer. Biochemistry. 2016 Mar 01; 55(8):1214-25. PMID: 26836755; PMCID: PMC4775286 [Available on 03/01/17].
      11. Kufareva I, Gustavsson M, Holden LG, Qin L, Zheng Y, Handel T. Disulfide Trapping for Modeling and Structure Determination of Receptor: Chemokine Complexes. Methods Enzymol. 2016; 570:389-420. PMID: 26921956.
        View in: PubMed
      12. Handel T. Preface. Methods Enzymol. 2016; 570:xxi-xxii. PMID: 26921963.
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      13. Gustavsson M, Zheng Y, Handel T. Production of Chemokine/Chemokine Receptor Complexes for Structural Biophysical Studies. Methods Enzymol. 2016; 570:233-60. PMID: 26921949.
        View in: PubMed
      14. Dyer DP, Salanga CL, Volkman BF, Kawamura T, Handel T. The dependence of chemokine-glycosaminoglycan interactions on chemokine oligomerization. Glycobiology. 2016 Mar; 26(3):312-26. PMID: 26582609.
        View in: PubMed
      15. Yin X, Johns SC, El Ghazal R, Salanga CL, Handel T, Fuster MM. Examining Roles of Glycans in Chemokine-Mediated Dendritic-Endothelial Cell Interactions. Methods Enzymol. 2016; 570:335-55. PMID: 26921954.
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      16. Migliorini E, Thakar D, Kühnle J, Sadir R, Dyer DP, Li Y, Sun C, Volkman BF, Handel T, Coche-Guerente L, Fernig DG, Lortat-Jacob H, Richter RP. Cytokines and growth factors cross-link heparan sulfate. Open Biol. 2015 Aug; 5(8). PMID: 26269427.
        View in: PubMed
      17. Hanes MS, Salanga CL, Chowdry AB, Comerford I, McColl SR, Kufareva I, Handel T. Dual Targeting of the Chemokine Receptors CXCR4 and ACKR3 with Novel Engineered Chemokines. J Biol Chem. 2015 Sep 11; 290(37):22385-97. PMID: 26216880.
        View in: PubMed
      18. Handel T. The Structure of a CXCR4:Chemokine Complex. Front Immunol. 2015; 6:282. PMID: 26097480.
        View in: PubMed
      19. Deshauer C, Morgan AM, Ryan EO, Handel T, Prestegard JH, Wang X. Interactions of the Chemokine CCL5/RANTES with Medium-Sized Chondroitin Sulfate Ligands. Structure. 2015 Jun 2; 23(6):1066-77. PMID: 25982530.
        View in: PubMed
      20. Kufareva I, Salanga CL, Handel T. Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies. Immunol Cell Biol. 2015 Apr; 93(4):372-83. PMID: 25708536.
        View in: PubMed
      21. Qin L, Kufareva I, Holden LG, Wang C, Zheng Y, Zhao C, Fenalti G, Wu H, Han GW, Cherezov V, Abagyan R, Stevens RC, Handel T. Structural biology. Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine. Science. 2015 Mar 6; 347(6226):1117-22. PMID: 25612609.
        View in: PubMed
      22. Kufareva I, Handel T, Abagyan R. Experiment-Guided Molecular Modeling of Protein-Protein Complexes Involving GPCRs. Methods Mol Biol. 2015; 1335:295-311. PMID: 26260608.
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      23. Kufareva I, Stephens BS, Holden LG, Qin L, Zhao C, Kawamura T, Abagyan R, Handel T. Stoichiometry and geometry of the CXC chemokine receptor 4 complex with CXC ligand 12: Molecular modeling and experimental validation. Proc Natl Acad Sci U S A. 2014 Dec 16; 111(50):E5363-72. PMID: 25468967.
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      24. Bonvin P, Dunn SM, Rousseau F, Dyer DP, Shaw J, Power CA, Handel T, Proudfoot AE. Identification of the Pharmacophore of the CC Chemokine-binding Proteins Evasin-1 and -4 Using Phage Display. J Biol Chem. 2014 Nov 14; 289(46):31846-55. PMID: 25266725.
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      25. Salanga CL, Dyer DP, Kiselar JG, Gupta S, Chance MR, Handel T. Multiple Glycosaminoglycan-binding Epitopes of Monocyte Chemoattractant Protein-3/CCL7 Enable It to Function as a Non-oligomerizing Chemokine. J Biol Chem. 2014 May 23; 289(21):14896-912. PMID: 24727473.
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      26. Verkaar F, van Offenbeek J, van der Lee MM, van Lith LH, Watts AO, Rops AL, Aguilar DC, Ziarek JJ, van der Vlag J, Handel T, Volkman BF, Proudfoot AE, Vischer HF, Zaman GJ, Smit MJ. Chemokine cooperativity is caused by competitive glycosaminoglycan binding. J Immunol. 2014 Apr 15; 192(8):3908-14. PMID: 24639348.
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      27. Dyer DP, Thomson JM, Hermant A, Jowitt TA, Handel T, Proudfoot AE, Day AJ, Milner CM. TSG-6 Inhibits Neutrophil Migration via Direct Interaction with the Chemokine CXCL8. J Immunol. 2014 Mar 1; 192(5):2177-85. PMID: 24501198.
        View in: PubMed
      28. Yin X, Johns SC, Kim D, Mikulski Z, Salanga CL, Handel T, Macal M, Zúñiga EI, Fuster MM. Lymphatic specific disruption in the fine structure of heparan sulfate inhibits dendritic cell traffic and functional T cell responses in the lymph node. J Immunol. 2014 Mar 1; 192(5):2133-42. PMID: 24493818.
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      29. Kawamura T, Stephens B, Qin L, Yin X, Dores MR, Smith TH, Grimsey N, Abagyan R, Trejo J, Kufareva I, Fuster MM, Salanga CL, Handel T. A general method for site specific fluorescent labeling of recombinant chemokines. PLoS One. 2014; 9(1):e81454. PMID: 24489642.
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      30. Gilliland CT, Salanga CL, Kawamura T, Trejo J, Handel T. The Chemokine Receptor CCR1 Is Constitutively Active, Which Leads to G Protein-independent, ß-Arrestin-mediated Internalization. J Biol Chem. 2013 Nov 8; 288(45):32194-210. PMID: 24056371.
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      31. Ziarek JJ, Getschman AE, Butler SJ, Taleski D, Stephens B, Kufareva I, Handel T, Payne RJ, Volkman BF. Sulfopeptide probes of the CXCR4/CXCL12 interface reveal oligomer-specific contacts and chemokine allostery. ACS Chem Biol. 2013 Sep 20; 8(9):1955-63. PMID: 23802178.
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      32. Kara EE, Comerford I, Bastow CR, Fenix KA, Litchfield W, Handel T, McColl SR. Distinct chemokine receptor axes regulate Th9 cell trafficking to allergic and autoimmune inflammatory sites. J Immunol. 2013 Aug 1; 191(3):1110-7. PMID: 23797668.
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      33. Wiesner P, Tafelmeier M, Chittka D, Choi SH, Zhang L, Byun YS, Almazan F, Yang X, Iqbal N, Chowdhury P, Maisel A, Witztum JL, Handel T, Tsimikas S, Miller YI. MCP-1 binds to oxidized LDL and is carried by lipoprotein(a) in human plasma. J Lipid Res. 2013 Jul; 54(7):1877-83. PMID: 23667177.
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      34. O'Hayre M, Vázquez-Prado J, Kufareva I, Stawiski EW, Handel T, Seshagiri S, Gutkind JS. The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer. Nat Rev Cancer. 2013 Jun; 13(6):412-24. PMID: 23640210.
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      35. Kufareva I, Stephens B, Gilliland CT, Wu B, Fenalti G, Hamel D, Stevens RC, Abagyan R, Handel T. A novel approach to quantify G-protein-coupled receptor dimerization equilibrium using bioluminescence resonance energy transfer. Methods Mol Biol. 2013; 1013:93-127. PMID: 23625495.
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      36. Stephens B, Handel T. Chemokine receptor oligomerization and allostery. Prog Mol Biol Transl Sci. 2013; 115:375-420. PMID: 23415099.
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      37. Wang X, Sharp JS, Handel T, Prestegard JH. Chemokine oligomerization in cell signaling and migration. Prog Mol Biol Transl Sci. 2013; 117:531-78. PMID: 23663982.
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      38. Webb DR, Handel T, Kretz-Rommel A, Stevens RC. Opportunities for functional selectivity in GPCR antibodies. Biochem Pharmacol. 2013 Jan 15; 85(2):147-52. PMID: 22975405.
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      39. Axelsson J, Xu D, Kang BN, Nussbacher JK, Handel T, Ley K, Sriramarao P, Esko JD. Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood. 2012 Aug 23; 120(8):1742-51. PMID: 22791291.
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      40. Fecteau JF, Bharati IS, O'Hayre M, Handel T, Kipps TJ, Messmer D. Sorafenib-induced apoptosis of chronic lymphocytic leukemia cells is associated with downregulation of RAF and myeloid cell leukemia sequence 1 (Mcl-1). Mol Med. 2012; 18:19-28. PMID: 21979753.
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      41. O'Hayre M, Niederst M, Fecteau JF, Nguyen VM, Kipps TJ, Messmer D, Newton AC, Handel T. Mechanisms and consequences of the loss of PHLPP1 phosphatase in chronic lymphocytic leukemia (CLL). Leukemia. 2012 Jul; 26(7):1689-92. PMID: 22237780.
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      42. Zhang S, Condac E, Qiu H, Jiang J, Gutierrez-Sanchez G, Bergmann C, Handel T, Wang L. Heparin-induced leukocytosis requires 6-O-sulfation and is caused by blockade of selectin- and CXCL12 protein-mediated leukocyte trafficking in mice. J Biol Chem. 2012 Feb 17; 287(8):5542-53. PMID: 22194593.
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      43. Wang X, Watson C, Sharp JS, Handel T, Prestegard JH. Oligomeric structure of the chemokine CCL5/RANTES from NMR, MS, and SAXS data. Structure. 2011 Aug 10; 19(8):1138-48. PMID: 21827949.
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      44. Kulig P, Kantyka T, Zabel BA, Banas M, Chyra A, Stefanska A, Tu H, Allen SJ, Handel T, Kozik A, Potempa J, Butcher EC, Cichy J. Regulation of chemerin chemoattractant and antibacterial activity by human cysteine cathepsins. J Immunol. 2011 Aug 1; 187(3):1403-10. PMID: 21715684.
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      45. Allen SJ, Hamel DJ, Handel T. A rapid and efficient way to obtain modified chemokines for functional and biophysical studies. Cytokine. 2011 Aug; 55(2):168-73. PMID: 21632261.
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      46. Laborde E, Macsata RW, Meng F, Peterson BT, Robinson L, Schow SR, Simon RJ, Xu H, Baba K, Inagaki H, Ishiwata Y, Jomori T, Matsumoto Y, Miyachi A, Nakamura T, Okamoto M, Handel T, Bernard CC. Discovery, optimization, and pharmacological characterization of novel heteroaroylphenylureas antagonists of C-C chemokine ligand 2 function. J Med Chem. 2011 Mar 24; 54(6):1667-81. PMID: 21341682.
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      47. Hanes MS, Reynolds KA, McNamara C, Ghosh P, Bonomo RA, Kirsch JF, Handel T. Specificity and cooperativity at ß-lactamase position 104 in TEM-1/BLIP and SHV-1/BLIP interactions. Proteins. 2011 Apr; 79(4):1267-76. PMID: 21294157.
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      48. Salanga CL, Handel T. Chemokine oligomerization and interactions with receptors and glycosaminoglycans: the role of structural dynamics in function. Exp Cell Res. 2011 Mar 10; 317(5):590-601. PMID: 21223963.
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      49. Yin X, Truty J, Lawrence R, Johns SC, Srinivasan RS, Handel T, Fuster MM. A critical role for lymphatic endothelial heparan sulfate in lymph node metastasis. Mol Cancer. 2010; 9:316. PMID: 21172016.
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      50. Messmer D, Fecteau JF, O'Hayre M, Bharati IS, Handel T, Kipps TJ. Chronic lymphocytic leukemia cells receive RAF-dependent survival signals in response to CXCL12 that are sensitive to inhibition by sorafenib. Blood. 2011 Jan 20; 117(3):882-9. PMID: 21079155.
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      51. O'Hayre M, Salanga CL, Handel T, Hamel DJ. Emerging concepts and approaches for chemokine-receptor drug discovery. Expert Opin Drug Discov. 2010 Nov; 5(11):1109-22. PMID: 21132095.
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      52. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V, Abagyan R, Brooun A, Wells P, Bi FC, Hamel DJ, Kuhn P, Handel T, Cherezov V, Stevens RC. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science. 2010 Nov 19; 330(6007):1066-71. PMID: 20929726.
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      53. Hanes MS, Ratcliff K, Marqusee S, Handel T. Protein-protein binding affinities by pulse proteolysis: application to TEM-1/BLIP protein complexes. Protein Sci. 2010 Oct; 19(10):1996-2000. PMID: 20669180.
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      54. O'Hayre M, Salanga CL, Kipps TJ, Messmer D, Dorrestein PC, Handel T. Elucidating the CXCL12/CXCR4 signaling network in chronic lymphocytic leukemia through phosphoproteomics analysis. PLoS One. 2010; 5(7):e11716. PMID: 20661426.
        View in: PubMed
      55. Handel T, Horuk R. Duffy antigen inhibitors: useful therapeutics for malaria? Trends Parasitol. 2010 Jul; 26(7):329-33. PMID: 20382562.
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      56. Severin IC, Gaudry JP, Johnson Z, Kungl A, Jansma A, Gesslbauer B, Mulloy B, Power C, Proudfoot AE, Handel T. Characterization of the chemokine CXCL11-heparin interaction suggests two different affinities for glycosaminoglycans. J Biol Chem. 2010 Jun 4; 285(23):17713-24. PMID: 20363748.
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      57. Guttman M, Prieto JH, Handel T, Domaille PJ, Komives EA. Structure of the minimal interface between ApoE and LRP. J Mol Biol. 2010 Apr 30; 398(2):306-19. PMID: 20303980.
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      58. Jansma AL, Kirkpatrick JP, Hsu AR, Handel T, Nietlispach D. NMR analysis of the structure, dynamics, and unique oligomerization properties of the chemokine CCL27. J Biol Chem. 2010 May 7; 285(19):14424-37. PMID: 20200157.
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      59. Hanes MS, Jude KM, Berger JM, Bonomo RA, Handel T. Structural and biochemical characterization of the interaction between KPC-2 beta-lactamase and beta-lactamase inhibitor protein. Biochemistry. 2009 Oct 6; 48(39):9185-93. PMID: 19731932.
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      60. Salanga CL, O'Hayre M, Handel T. Modulation of chemokine receptor activity through dimerization and crosstalk. Cell Mol Life Sci. 2009 Apr; 66(8):1370-86. PMID: 19099182.
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      61. Allen SJ, Ribeiro S, Horuk R, Handel T. Expression, purification and in vitro functional reconstitution of the chemokine receptor CCR1. Protein Expr Purif. 2009 Jul; 66(1):73-81. PMID: 19275940.
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      62. O'Hayre M, Salanga CL, Dorrestein PC, Handel T. Phosphoproteomic analysis of chemokine signaling networks. Methods Enzymol. 2009; 460:331-46. PMID: 19446733.
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      63. Winter JM, Jansma AL, Handel T, Moore BS. Formation of the pyridazine natural product azamerone by biosynthetic rearrangement of an aryl diazoketone. Angew Chem Int Ed Engl. 2009; 48(4):767-70. PMID: 19072974.
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      64. Hamel DJ, Sielaff I, Proudfoot AE, Handel T. Chapter 4. Interactions of chemokines with glycosaminoglycans. Methods Enzymol. 2009; 461:71-102. PMID: 19480915.
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      65. Jansma A, Handel T, Hamel DJ. Chapter 2. Homo- and hetero-oligomerization of chemokines. Methods Enzymol. 2009; 461:31-50. PMID: 19480913.
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      66. Hamel DJ, Handel T. Methods to probe the physical characteristics, dynamics, modifications, and interactions of chemokines and chemokine receptors. Preface. Methods Enzymol. 2009; 461:xv. PMID: 19480911.
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      67. Du XY, Zabel BA, Myles T, Allen SJ, Handel T, Lee PP, Butcher EC, Leung LL. Regulation of chemerin bioactivity by plasma carboxypeptidase N, carboxypeptidase B (activated thrombin-activable fibrinolysis inhibitor), and platelets. J Biol Chem. 2009 Jan 9; 284(2):751-8. PMID: 19010784.
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      68. Zabel BA, Nakae S, Zúñiga L, Kim JY, Ohyama T, Alt C, Pan J, Suto H, Soler D, Allen SJ, Handel T, Song CH, Galli SJ, Butcher EC. Mast cell-expressed orphan receptor CCRL2 binds chemerin and is required for optimal induction of IgE-mediated passive cutaneous anaphylaxis. J Exp Med. 2008 Sep 29; 205(10):2207-20. PMID: 18794339.
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      69. Handel T, Johnson Z, Rodrigues DH, Dos Santos AC, Cirillo R, Muzio V, Riva S, Mack M, Déruaz M, Borlat F, Vitte PA, Wells TN, Teixeira MM, Proudfoot AE. An engineered monomer of CCL2 has anti-inflammatory properties emphasizing the importance of oligomerization for chemokine activity in vivo. J Leukoc Biol. 2008 Oct; 84(4):1101-8. PMID: 18662971.
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      70. Reynolds KA, Hanes MS, Thomson JM, Antczak AJ, Berger JM, Bonomo RA, Kirsch JF, Handel T. Computational redesign of the SHV-1 beta-lactamase/beta-lactamase inhibitor protein interface. J Mol Biol. 2008 Oct 24; 382(5):1265-75. PMID: 18775544.
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      71. Shahrara S, Proudfoot AE, Park CC, Volin MV, Haines GK, Woods JM, Aikens CH, Handel T, Pope RM. Inhibition of monocyte chemoattractant protein-1 ameliorates rat adjuvant-induced arthritis. J Immunol. 2008 Mar 1; 180(5):3447-56. PMID: 18292571.
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      72. O'Hayre M, Salanga CL, Handel T, Allen SJ. Chemokines and cancer: migration, intracellular signalling and intercellular communication in the microenvironment. Biochem J. 2008 Feb 1; 409(3):635-49. PMID: 18177271.
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      73. Zhang X, DeChancie J, Gunaydin H, Chowdry AB, Clemente FR, Smith AJ, Handel T, Houk KN. Quantum mechanical design of enzyme active sites. J Org Chem. 2008 Feb 1; 73(3):889-99. PMID: 18179229.
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      74. Chowdry AB, Reynolds KA, Hanes MS, Voorhies M, Pokala N, Handel T. An object-oriented library for computational protein design. J Comput Chem. 2007 Nov 15; 28(14):2378-88. PMID: 17471459.
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      75. Allen SJ, Zabel BA, Kirkpatrick J, Butcher EC, Nietlispach D, Handel T. NMR assignment of human chemerin, a novel chemoattractant. Biomol NMR Assign. 2007 Dec; 1(2):171-3. PMID: 19636857.
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      76. Douglas AE, Corbett KD, Berger JM, McFadden G, Handel T. Structure of M11L: A myxoma virus structural homolog of the apoptosis inhibitor, Bcl-2. Protein Sci. 2007 Apr; 16(4):695-703. PMID: 17384234.
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      77. Kulig P, Zabel BA, Dubin G, Allen SJ, Ohyama T, Potempa J, Handel T, Butcher EC, Cichy J. Staphylococcus aureus-derived staphopain B, a potent cysteine protease activator of plasma chemerin. J Immunol. 2007 Mar 15; 178(6):3713-20. PMID: 17339469.
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      78. Allen SJ, Crown SE, Handel T. Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol. 2007; 25:787-820. PMID: 17291188.
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      79. Zabel BA, Ohyama T, Zuniga L, Kim JY, Johnston B, Allen SJ, Guido DG, Handel T, Butcher EC. Chemokine-like receptor 1 expression by macrophages in vivo: regulation by TGF-beta and TLR ligands. Exp Hematol. 2006 Aug; 34(8):1106-14. PMID: 16863918.
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      80. Zabel BA, Zuniga L, Ohyama T, Allen SJ, Cichy J, Handel T, Butcher EC. Chemoattractants, extracellular proteases, and the integrated host defense response. Exp Hematol. 2006 Aug; 34(8):1021-32. PMID: 16863908.
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      81. Reynolds KA, Thomson JM, Corbett KD, Bethel CR, Berger JM, Kirsch JF, Bonomo RA, Handel T. Structural and computational characterization of the SHV-1 beta-lactamase-beta-lactamase inhibitor protein interface. J Biol Chem. 2006 Sep 8; 281(36):26745-53. PMID: 16809340.
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      82. Crown SE, Yu Y, Sweeney MD, Leary JA, Handel T. Heterodimerization of CCR2 chemokines and regulation by glycosaminoglycan binding. J Biol Chem. 2006 Sep 1; 281(35):25438-46. PMID: 16803905.
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      83. Zabel BA, Allen SJ, Kulig P, Allen JA, Cichy J, Handel T, Butcher EC. Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. J Biol Chem. 2005 Oct 14; 280(41):34661-6. PMID: 16096270.
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      84. Yu Y, Sweeney MD, Saad OM, Crown SE, Hsu AR, Handel T, Leary JA. Chemokine-glycosaminoglycan binding: specificity for CCR2 ligand binding to highly sulfated oligosaccharides using FTICR mass spectrometry. J Biol Chem. 2005 Sep 16; 280(37):32200-8. PMID: 16033763.
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      85. Johnson Z, Proudfoot AE, Handel T. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 2005 Dec; 16(6):625-36. PMID: 15990353.
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      86. Huang D, Wujek J, Kidd G, He TT, Cardona A, Sasse ME, Stein EJ, Kish J, Tani M, Charo IF, Proudfoot AE, Rollins BJ, Handel T, Ransohoff RM. Chronic expression of monocyte chemoattractant protein-1 in the central nervous system causes delayed encephalopathy and impaired microglial function in mice. FASEB J. 2005 May; 19(7):761-72. PMID: 15857890.
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      87. Sandhoff R, Grieshaber H, Djafarzadeh R, Sijmonsma TP, Proudfoot AE, Handel T, Wiegandt H, Nelson PJ, Gröne HJ. Chemokines bind to sulfatides as revealed by surface plasmon resonance. Biochim Biophys Acta. 2005 Feb 21; 1687(1-3):52-63. PMID: 15708353.
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      88. Pokala N, Handel T. Energy functions for protein design: adjustment with protein-protein complex affinities, models for the unfolded state, and negative design of solubility and specificity. J Mol Biol. 2005 Mar 18; 347(1):203-27. PMID: 15733929.
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      89. Handel T, Johnson Z, Crown SE, Lau EK, Proudfoot AE. Regulation of protein function by glycosaminoglycans--as exemplified by chemokines. Annu Rev Biochem. 2005; 74:385-410. PMID: 15952892.
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      90. Lau EK, Paavola CD, Johnson Z, Gaudry JP, Geretti E, Borlat F, Kungl AJ, Proudfoot AE, Handel T. Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1: implications for structure and function in vivo. J Biol Chem. 2004 May 21; 279(21):22294-305. PMID: 15033992.
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      91. Pokala N, Handel T. Energy functions for protein design I: efficient and accurate continuum electrostatics and solvation. Protein Sci. 2004 Apr; 13(4):925-36. PMID: 15010542.
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      92. Lau EK, Allen S, Hsu AR, Handel T. Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv Protein Chem. 2004; 68:351-91. PMID: 15500866.
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      93. Hardy LA, Booth TA, Lau EK, Handel T, Ali S, Kirby JA. Examination of MCP-1 (CCL2) partitioning and presentation during transendothelial leukocyte migration. Lab Invest. 2004 Jan; 84(1):81-90. PMID: 14647401.
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      94. Handel T, Lau EK. Chemokine structure and receptor interactions. Ernst Schering Res Found Workshop. 2004; (45):101-24. PMID: 14699797.
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      95. Seet BT, McCaughan CA, Handel T, Mercer A, Brunetti C, McFadden G, Fleming SB. Analysis of an orf virus chemokine-binding protein: Shifting ligand specificities among a family of poxvirus viroceptors. Proc Natl Acad Sci U S A. 2003 Dec 9; 100(25):15137-42. PMID: 14657392.
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      96. Proudfoot AE, Handel T, Johnson Z, Lau EK, LiWang P, Clark-Lewis I, Borlat F, Wells TN, Kosco-Vilbois MH. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A. 2003 Feb 18; 100(4):1885-90. PMID: 12571364.
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      97. Alexander JM, Nelson CA, van Berkel V, Lau EK, Studts JM, Brett TJ, Speck SH, Handel T, Virgin HW, Fremont DH. Structural basis of chemokine sequestration by a herpesvirus decoy receptor. Cell. 2002 Nov 1; 111(3):343-56. PMID: 12419245.
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      98. Lougheed JC, Domaille PJ, Handel T. Solution structure and dynamics of melanoma inhibitory activity protein. J Biomol NMR. 2002 Mar; 22(3):211-23. PMID: 11991352.
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      99. Seet BT, Singh R, Paavola C, Lau EK, Handel T, McFadden G. Molecular determinants for CC-chemokine recognition by a poxvirus CC-chemokine inhibitor. Proc Natl Acad Sci U S A. 2001 Jul 31; 98(16):9008-13. PMID: 11470923.
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      100. Mizoue LS, Sullivan SK, King DS, Kledal TN, Schwartz TW, Bacon KB, Handel T. Molecular determinants of receptor binding and signaling by the CX3C chemokine fractalkine. J Biol Chem. 2001 Sep 7; 276(36):33906-14. PMID: 11432858.
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      101. Lougheed JC, Holton JM, Alber T, Bazan JF, Handel T. Structure of melanoma inhibitory activity protein, a member of a recently identified family of secreted proteins. Proc Natl Acad Sci U S A. 2001 May 8; 98(10):5515-20. PMID: 11331761.
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      102. Pokala N, Handel T. Review: protein design--where we were, where we are, where we're going. J Struct Biol. 2001 May-Jun; 134(2-3):269-81. PMID: 11551185.
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      103. Marcaurelle LA, Mizoue LS, Wilken J, Oldham L, Kent SB, Handel T, Bertozzi CR. Chemical synthesis of lymphotactin: a glycosylated chemokine with a C-terminal mucin-like domain. Chemistry. 2001 Mar 2; 7(5):1129-32. PMID: 11303872.
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      104. Hoover DM, Mizoue LS, Handel T, Lubkowski J. The crystal structure of the chemokine domain of fractalkine shows a novel quaternary arrangement. J Biol Chem. 2000 Jul 28; 275(30):23187-93. PMID: 10770945.
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      105. Jarnagin K, Grunberger D, Mulkins M, Wong B, Hemmerich S, Paavola C, Bloom A, Bhakta S, Diehl F, Freedman R, McCarley D, Polsky I, Ping-Tsou A, Kosaka A, Handel T. Identification of surface residues of the monocyte chemotactic protein 1 that affect signaling through the receptor CCR2. Biochemistry. 1999 Dec 7; 38(49):16167-77. PMID: 10587439.
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      106. Lazar GA, Johnson EC, Desjarlais JR, Handel T. Rotamer strain as a determinant of protein structural specificity. Protein Sci. 1999 Dec; 8(12):2598-610. PMID: 10631975.
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      107. Hemmerich S, Paavola C, Bloom A, Bhakta S, Freedman R, Grunberger D, Krstenansky J, Lee S, McCarley D, Mulkins M, Wong B, Pease J, Mizoue L, Mirzadegan T, Polsky I, Thompson K, Handel T, Jarnagin K. Identification of residues in the monocyte chemotactic protein-1 that contact the MCP-1 receptor, CCR2. Biochemistry. 1999 Oct 5; 38(40):13013-25. PMID: 10529171.
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      108. Mizoue LS, Bazan JF, Johnson EC, Handel T. Solution structure and dynamics of the CX3C chemokine domain of fractalkine and its interaction with an N-terminal fragment of CX3CR1. Biochemistry. 1999 Feb 2; 38(5):1402-14. PMID: 9931005.
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      109. Paavola CD, Hemmerich S, Grunberger D, Polsky I, Bloom A, Freedman R, Mulkins M, Bhakta S, McCarley D, Wiesent L, Wong B, Jarnagin K, Handel T. Monomeric monocyte chemoattractant protein-1 (MCP-1) binds and activates the MCP-1 receptor CCR2B. J Biol Chem. 1998 Dec 11; 273(50):33157-65. PMID: 9837883.
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      110. Hedrick JA, Saylor V, Figueroa D, Mizoue L, Xu Y, Menon S, Abrams J, Handel T, Zlotnik A. Lymphotactin is produced by NK cells and attracts both NK cells and T cells in vivo. J Immunol. 1997 Feb 15; 158(4):1533-40. PMID: 9029087.
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      111. Lubkowski J, Bujacz G, Boqué L, Domaille PJ, Handel T, Wlodawer A. The structure of MCP-1 in two crystal forms provides a rare example of variable quaternary interactions. Nat Struct Biol. 1997 Jan; 4(1):64-9. PMID: 8989326.
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      112. Handel T, Domaille PJ. Heteronuclear (1H, 13C, 15N) NMR assignments and solution structure of the monocyte chemoattractant protein-1 (MCP-1) dimer. Biochemistry. 1996 May 28; 35(21):6569-84. PMID: 8639605.
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