Tracy Handel

InstitutionUniversity of California San Diego
DepartmentSchool of Pharmacy and Pharmaceutical Science
Address9500 Gilman Drive #0684
La Jolla CA 92093
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    Ph.D.California Institute of Technology

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    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
    Graduate Training in Cellular and Molecular Pharmacology
    NIH/NIGMS T32GM007752Jul 1, 1979 - Jun 30, 2019
    Role: Co-Principal Investigator

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    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.
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    1. Van Hout A, Klarenbeek A, Bobkov V, Doijen J, Arimont M, Zhao C, Heukers R, Rimkunas R, de Graaf C, Verrips T, van der Woning B, de Haard H, Rucker JB, Vermeire K, Handel T, Van Loy T, Smit MJ, Schols D. CXCR4-targeting nanobodies differentially inhibit CXCR4 function and HIV entry. Biochem Pharmacol. 2018 Oct 17. PMID: 30342024.
      View in: PubMed
    2. Grimsey NJ, Narala R, Rada CC, Mehta S, Stephens BS, Kufareva I, Lapek J, Gonzalez DJ, Handel TM, Zhang J, Trejo J. A Tyrosine Switch on NEDD4-2 E3 Ligase Transmits GPCR Inflammatory Signaling. Cell Rep. 2018 Sep 18; 24(12):3312-3323.e5. PMID: 30232011.
      View in: PubMed
    3. Proudfoot AE, Handel TM, Graham G. Editorial: Chemokines - beyond chemotaxis. Cytokine. 2018 Sep; 109:1. PMID: 29861383.
      View in: PubMed
    4. Ortiz Zacarías NV, Lenselink EB, IJzerman AP, Handel TM, Heitman LH. Intracellular Receptor Modulation: Novel Approach to Target GPCRs. Trends Pharmacol Sci. 2018 Apr 10. PMID: 29653834.
      View in: PubMed
    5. Proudfoot AEI, Johnson Z, Bonvin P, Handel TM. Glycosaminoglycan Interactions with Chemokines Add Complexity to a Complex System. Pharmaceuticals (Basel). 2017 Aug 09; 10(3). PMID: 28792472.
      View in: PubMed
    6. Zong C, Venot A, Li X, Lu W, Xiao W, Wilkes JL, Salanga CL, Handel TM, 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 19; 139(28):9534-9543. PMID: 28651046.
      View in: PubMed
    7. Zheng Y, Han GW, Abagyan R, Wu B, Stevens RC, Cherezov V, Kufareva I, Handel TM. Structure of CC Chemokine Receptor 5 with a Potent Chemokine Antagonist Reveals Mechanisms of Chemokine Recognition and Molecular Mimicry by HIV. Immunity. 2017 06 20; 46(6):1005-1017.e5. PMID: 28636951.
      View in: PubMed
    8. Kufareva I, Gustavsson M, Zheng Y, Stephens BS, Handel TM. 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
    9. Gustavsson M, Wang L, van Gils N, Stephens BS, Zhang P, Schall TJ, Yang S, Abagyan R, Chance MR, Kufareva I, Handel TM. Structural basis of ligand interaction with atypical chemokine receptor 3. Nat Commun. 2017 Jan 18; 8:14135. PMID: 28098154.
      View in: PubMed
    10. Dyer DP, Migliorini E, Salanga CL, Thakar D, Handel TM, 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
    11. 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 TM. Structure of CC chemokine receptor 2 with orthosteric and allosteric antagonists. Nature. 2016 12 15; 540(7633):458-461. PMID: 27926736.
      View in: PubMed
    12. Wescott MP, Kufareva I, Paes C, Goodman JR, Thaker Y, Puffer BA, Berdougo E, Rucker JB, Handel TM, Doranz BJ. Signal transmission through the CXC chemokine receptor 4 (CXCR4) transmembrane helices. Proc Natl Acad Sci U S A. 2016 08 30; 113(35):9928-33. PMID: 27543332.
      View in: PubMed
    13. Dyer DP, Salanga CL, Johns SC, Valdambrini E, Fuster MM, Milner CM, Day AJ, Handel TM. 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; PMCID: PMC4933465.
    14. Fox JC, Tyler RC, Peterson FC, Dyer DP, Zhang F, Linhardt RJ, Handel TM, 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].
    15. Kufareva I, Gustavsson M, Holden LG, Qin L, Zheng Y, Handel TM. Disulfide Trapping for Modeling and Structure Determination of Receptor: Chemokine Complexes. Methods Enzymol. 2016; 570:389-420. PMID: 26921956; PMCID: PMC4782801.
    16. Handel TM. Preface. Methods Enzymol. 2016; 570:xxi-xxii. PMID: 26921963.
      View in: PubMed
    17. Gustavsson M, Zheng Y, Handel TM. Production of Chemokine/Chemokine Receptor Complexes for Structural Biophysical Studies. Methods Enzymol. 2016; 570:233-60. PMID: 26921949; PMCID: PMC4770566 [Available on 01/01/17].
    18. Dyer DP, Salanga CL, Volkman BF, Kawamura T, Handel TM. The dependence of chemokine-glycosaminoglycan interactions on chemokine oligomerization. Glycobiology. 2016 Mar; 26(3):312-26. PMID: 26582609; PMCID: PMC4736540 [Available on 03/01/17].
    19. Yin X, Johns SC, El Ghazal R, Salanga CL, Handel TM, Fuster MM. Examining Roles of Glycans in Chemokine-Mediated Dendritic-Endothelial Cell Interactions. Methods Enzymol. 2016; 570:335-55. PMID: 26921954.
      View in: PubMed
    20. Migliorini E, Thakar D, Kühnle J, Sadir R, Dyer DP, Li Y, Sun C, Volkman BF, Handel TM, 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; PMCID: PMC4554917.
    21. Hanes MS, Salanga CL, Chowdry AB, Comerford I, McColl SR, Kufareva I, Handel TM. 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; PMCID: PMC4566214.
    22. Handel TM. The Structure of a CXCR4:Chemokine Complex. Front Immunol. 2015; 6:282. PMID: 26097480; PMCID: PMC4457019.
    23. Deshauer C, Morgan AM, Ryan EO, Handel TM, Prestegard JH, Wang X. Interactions of the Chemokine CCL5/RANTES with Medium-Sized Chondroitin Sulfate Ligands. Structure. 2015 Jun 02; 23(6):1066-77. PMID: 25982530; PMCID: PMC4456249.
    24. Kufareva I, Salanga CL, Handel TM. Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies. Immunol Cell Biol. 2015 Apr; 93(4):372-83. PMID: 25708536; PMCID: PMC4406842.
    25. 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 TM. Structural biology. Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine. Science. 2015 Mar 06; 347(6226):1117-22. PMID: 25612609; PMCID: PMC4362693.
    26. Kufareva I, Handel TM, Abagyan R. Experiment-Guided Molecular Modeling of Protein-Protein Complexes Involving GPCRs. Methods Mol Biol. 2015; 1335:295-311. PMID: 26260608; PMCID: PMC4551442.
    27. Kufareva I, Stephens BS, Holden LG, Qin L, Zhao C, Kawamura T, Abagyan R, Handel TM. 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; PMCID: PMC4273337.
    28. Bonvin P, Dunn SM, Rousseau F, Dyer DP, Shaw J, Power CA, Handel TM, 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; PMCID: PMC4231662.
    29. Salanga CL, Dyer DP, Kiselar JG, Gupta S, Chance MR, Handel TM. 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; PMCID: PMC4031540.
    30. Verkaar F, van Offenbeek J, van der Lee MMC, van Lith LHCJ, Watts AO, Rops ALWMM, Aguilar DC, Ziarek JJ, van der Vlag J, Handel TM, Volkman BF, Proudfoot AEI, Vischer HF, Zaman GJR, Smit MJ. Chemokine cooperativity is caused by competitive glycosaminoglycan binding. J Immunol. 2014 Apr 15; 192(8):3908-3914. PMID: 24639348; PMCID: PMC4198333.
    31. Dyer DP, Thomson JM, Hermant A, Jowitt TA, Handel TM, Proudfoot AE, Day AJ, Milner CM. TSG-6 inhibits neutrophil migration via direct interaction with the chemokine CXCL8. J Immunol. 2014 Mar 01; 192(5):2177-85. PMID: 24501198; PMCID: PMC3988464.
    32. Yin X, Johns SC, Kim D, Mikulski Z, Salanga CL, Handel TM, 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 01; 192(5):2133-42. PMID: 24493818; PMCID: PMC3960083.
    33. 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 TM. A general method for site specific fluorescent labeling of recombinant chemokines. PLoS One. 2014; 9(1):e81454. PMID: 24489642; PMCID: PMC3904831.
    34. Gilliland CT, Salanga CL, Kawamura T, Trejo J, Handel TM. The chemokine receptor CCR1 is constitutively active, which leads to G protein-independent, ß-arrestin-mediated internalization. J Biol Chem. 2013 Nov 08; 288(45):32194-210. PMID: 24056371; PMCID: PMC3820859.
    35. Ziarek JJ, Getschman AE, Butler SJ, Taleski D, Stephens B, Kufareva I, Handel TM, 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; PMCID: PMC3783652.
    36. Kara EE, Comerford I, Bastow CR, Fenix KA, Litchfield W, Handel TM, McColl SR. Distinct chemokine receptor axes regulate Th9 cell trafficking to allergic and autoimmune inflammatory sites. J Immunol. 2013 Aug 01; 191(3):1110-7. PMID: 23797668; PMCID: PMC3721028.
    37. 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 TM, 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; PMCID: PMC3679389.
    38. O'Hayre M, Vázquez-Prado J, Kufareva I, Stawiski EW, Handel TM, Seshagiri S, Gutkind JS. The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer. Nat Rev Cancer. 2013 06; 13(6):412-24. PMID: 23640210; PMCID: PMC4068741.
    39. Kufareva I, Stephens B, Gilliland CT, Wu B, Fenalti G, Hamel D, Stevens RC, Abagyan R, Handel TM. 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; PMCID: PMC4091634.
    40. Wang X, Sharp JS, Handel TM, Prestegard JH. Chemokine oligomerization in cell signaling and migration. Prog Mol Biol Transl Sci. 2013; 117:531-78. PMID: 23663982; PMCID: PMC3937849.
    41. Stephens B, Handel TM. Chemokine receptor oligomerization and allostery. Prog Mol Biol Transl Sci. 2013; 115:375-420. PMID: 23415099; PMCID: PMC4072031.
    42. Webb DR, Handel TM, Kretz-Rommel A, Stevens RC. Opportunities for functional selectivity in GPCR antibodies. Biochem Pharmacol. 2013 Jan 15; 85(2):147-52. PMID: 22975405; PMCID: PMC3729224.
    43. Axelsson J, Xu D, Kang BN, Nussbacher JK, Handel TM, 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; PMCID: PMC3429312.
    44. Fecteau JF, Bharati IS, O'Hayre M, Handel TM, 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 Feb 10; 18:19-28. PMID: 21979753; PMCID: PMC3269641.
    45. O'Hayre M, Niederst M, Fecteau JF, Nguyen VM, Kipps TJ, Messmer D, Newton AC, Handel TM. Mechanisms and consequences of the loss of PHLPP1 phosphatase in chronic lymphocytic leukemia (CLL). Leukemia. 2012 Jul; 26(7):1689-92. PMID: 22237780; PMCID: PMC3395972.
    46. 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; PMCID: PMC3285330.
    47. Wang X, Watson C, Sharp JS, Handel TM, 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; PMCID: PMC3159919.
    48. Kulig P, Kantyka T, Zabel BA, Banas M, Chyra A, Stefanska A, Tu H, Allen SJ, Handel TM, Kozik A, Potempa J, Butcher EC, Cichy J. Regulation of chemerin chemoattractant and antibacterial activity by human cysteine cathepsins. J Immunol. 2011 Aug 01; 187(3):1403-10. PMID: 21715684; PMCID: PMC3140563.
    49. Allen SJ, Hamel DJ, Handel TM. A rapid and efficient way to obtain modified chemokines for functional and biophysical studies. Cytokine. 2011 Aug; 55(2):168-73. PMID: 21632261; PMCID: PMC3126891.
    50. 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 TM, 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; PMCID: PMC3229226.
    51. Hanes MS, Reynolds KA, McNamara C, Ghosh P, Bonomo RA, Kirsch JF, Handel TM. 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; PMCID: PMC3417816.
    52. Salanga CL, Handel TM. 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; PMCID: PMC3089961.
    53. Yin X, Truty J, Lawrence R, Johns SC, Srinivasan RS, Handel TM, Fuster MM. A critical role for lymphatic endothelial heparan sulfate in lymph node metastasis. Mol Cancer. 2010 Dec 20; 9:316. PMID: 21172016; PMCID: PMC3019167.
    54. Messmer D, Fecteau JF, O'Hayre M, Bharati IS, Handel TM, 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; PMCID: PMC3035080.
    55. O'Hayre M, Salanga CL, Handel TM, 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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    56. 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 TM, 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; PMCID: PMC3074590.
    57. Hanes MS, Ratcliff K, Marqusee S, Handel TM. Protein-protein binding affinities by pulse proteolysis: application to TEM-1/BLIP protein complexes. Protein Sci. 2010 Oct; 19(10):1996-2000. PMID: 20669180; PMCID: PMC2998734.
    58. O'Hayre M, Salanga CL, Kipps TJ, Messmer D, Dorrestein PC, Handel TM. Elucidating the CXCL12/CXCR4 signaling network in chronic lymphocytic leukemia through phosphoproteomics analysis. PLoS One. 2010 Jul 22; 5(7):e11716. PMID: 20661426; PMCID: PMC2908618.
    59. Handel TM, Horuk R. Duffy antigen inhibitors: useful therapeutics for malaria? Trends Parasitol. 2010 Jul; 26(7):329-33. PMID: 20382562.
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    60. 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 04; 285(23):17713-24. PMID: 20363748; PMCID: PMC2878535.
    61. Guttman M, Prieto JH, Handel TM, 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; PMCID: PMC2880916.
    62. Jansma AL, Kirkpatrick JP, Hsu AR, Handel TM, Nietlispach D. NMR analysis of the structure, dynamics, and unique oligomerization properties of the chemokine CCL27. J Biol Chem. 2010 May 07; 285(19):14424-37. PMID: 20200157; PMCID: PMC2863231.
    63. Hanes MS, Jude KM, Berger JM, Bonomo RA, Handel TM. Structural and biochemical characterization of the interaction between KPC-2 beta-lactamase and beta-lactamase inhibitor protein. Biochemistry. 2009 Oct 06; 48(39):9185-93. PMID: 19731932; PMCID: PMC2769493.
    64. 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; PMCID: PMC2738873.
    65. Allen SJ, Ribeiro S, Horuk R, Handel TM. Expression, purification and in vitro functional reconstitution of the chemokine receptor CCR1. Protein Expr Purif. 2009 Jul; 66(1):73-81. PMID: 19275940; PMCID: PMC2706832.
    66. O'Hayre M, Salanga CL, Dorrestein PC, Handel TM. Phosphoproteomic analysis of chemokine signaling networks. Methods Enzymol. 2009; 460:331-46. PMID: 19446733.
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    67. Jansma A, Handel TM, Hamel DJ. Chapter 2. Homo- and hetero-oligomerization of chemokines. Methods Enzymol. 2009; 461:31-50. PMID: 19480913.
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    68. Hamel DJ, Sielaff I, Proudfoot AE, Handel TM. Chapter 4. Interactions of chemokines with glycosaminoglycans. Methods Enzymol. 2009; 461:71-102. PMID: 19480915.
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    69. Hamel DJ, Handel TM. Methods to probe the physical characteristics, dynamics, modifications, and interactions of chemokines and chemokine receptors. Preface. Methods Enzymol. 2009; 461:xv. PMID: 19480911.
      View in: PubMed
    70. Winter JM, Jansma AL, Handel TM, 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; PMCID: PMC3517086.
    71. Du XY, Zabel BA, Myles T, Allen SJ, Handel TM, 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 09; 284(2):751-8. PMID: 19010784; PMCID: PMC2613638.
    72. Zabel BA, Nakae S, Zúñiga L, Kim JY, Ohyama T, Alt C, Pan J, Suto H, Soler D, Allen SJ, Handel TM, 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; PMCID: PMC2556791.
    73. Handel TM, 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; PMCID: PMC2538597.
    74. Reynolds KA, Hanes MS, Thomson JM, Antczak AJ, Berger JM, Bonomo RA, Kirsch JF, Handel TM. 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; PMCID: PMC4085744.
    75. Shahrara S, Proudfoot AE, Park CC, Volin MV, Haines GK, Woods JM, Aikens CH, Handel TM, Pope RM. Inhibition of monocyte chemoattractant protein-1 ameliorates rat adjuvant-induced arthritis. J Immunol. 2008 Mar 01; 180(5):3447-56. PMID: 18292571.
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    76. O'Hayre M, Salanga CL, Handel TM, Allen SJ. Chemokines and cancer: migration, intracellular signalling and intercellular communication in the microenvironment. Biochem J. 2008 Feb 01; 409(3):635-49. PMID: 18177271.
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    77. Zhang X, DeChancie J, Gunaydin H, Chowdry AB, Clemente FR, Smith AJ, Handel TM, Houk KN. Quantum mechanical design of enzyme active sites. J Org Chem. 2008 Feb 01; 73(3):889-99. PMID: 18179229.
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    78. Chowdry AB, Reynolds KA, Hanes MS, Voorhies M, Pokala N, Handel TM. An object-oriented library for computational protein design. J Comput Chem. 2007 Nov 15; 28(14):2378-88. PMID: 17471459.
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    79. Allen SJ, Zabel BA, Kirkpatrick J, Butcher EC, Nietlispach D, Handel TM. NMR assignment of human chemerin, a novel chemoattractant. Biomol NMR Assign. 2007 Dec; 1(2):171-3. PMID: 19636857.
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    80. Douglas AE, Corbett KD, Berger JM, McFadden G, Handel TM. Structure of M11L: A myxoma virus structural homolog of the apoptosis inhibitor, Bcl-2. Protein Sci. 2007 Apr; 16(4):695-703. PMID: 17384234; PMCID: PMC2203349.
    81. Kulig P, Zabel BA, Dubin G, Allen SJ, Ohyama T, Potempa J, Handel TM, 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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    82. Allen SJ, Crown SE, Handel TM. Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol. 2007; 25:787-820. PMID: 17291188.
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    83. Zabel BA, Zuniga L, Ohyama T, Allen SJ, Cichy J, Handel TM, 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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    84. Zabel BA, Ohyama T, Zuniga L, Kim JY, Johnston B, Allen SJ, Guido DG, Handel TM, 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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    85. Reynolds KA, Thomson JM, Corbett KD, Bethel CR, Berger JM, Kirsch JF, Bonomo RA, Handel TM. Structural and computational characterization of the SHV-1 beta-lactamase-beta-lactamase inhibitor protein interface. J Biol Chem. 2006 Sep 08; 281(36):26745-53. PMID: 16809340.
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    86. Crown SE, Yu Y, Sweeney MD, Leary JA, Handel TM. Heterodimerization of CCR2 chemokines and regulation by glycosaminoglycan binding. J Biol Chem. 2006 Sep 01; 281(35):25438-46. PMID: 16803905.
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    87. Zabel BA, Allen SJ, Kulig P, Allen JA, Cichy J, Handel TM, 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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    88. Yu Y, Sweeney MD, Saad OM, Crown SE, Hsu AR, Handel TM, 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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    89. Johnson Z, Proudfoot AE, Handel TM. 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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    90. 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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    91. Sandhoff R, Grieshaber H, Djafarzadeh R, Sijmonsma TP, Proudfoot AE, Handel TM, 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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    92. Pokala N, Handel TM. 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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    93. Handel TM, 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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    94. Lau EK, Paavola CD, Johnson Z, Gaudry JP, Geretti E, Borlat F, Kungl AJ, Proudfoot AE, Handel TM. 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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    95. Pokala N, Handel TM. Energy functions for protein design I: efficient and accurate continuum electrostatics and solvation. Protein Sci. 2004 Apr; 13(4):925-36. PMID: 15010542; PMCID: PMC2280065.
    96. Handel TM, Lau EK. Chemokine structure and receptor interactions. Ernst Schering Res Found Workshop. 2004; (45):101-24. PMID: 14699797.
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    97. Lau EK, Allen S, Hsu AR, Handel TM. Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv Protein Chem. 2004; 68:351-91. PMID: 15500866.
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    98. Hardy LA, Booth TA, Lau EK, Handel TM, 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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    99. Seet BT, McCaughan CA, Handel TM, 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 09; 100(25):15137-42. PMID: 14657392; PMCID: PMC299921.
    100. Proudfoot AE, Handel TM, 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; PMCID: PMC149928.
    101. Alexander JM, Nelson CA, van Berkel V, Lau EK, Studts JM, Brett TJ, Speck SH, Handel TM, Virgin HW, Fremont DH. Structural basis of chemokine sequestration by a herpesvirus decoy receptor. Cell. 2002 Nov 01; 111(3):343-56. PMID: 12419245.
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    102. Lougheed JC, Domaille PJ, Handel TM. Solution structure and dynamics of melanoma inhibitory activity protein. J Biomol NMR. 2002 Mar; 22(3):211-23. PMID: 11991352.
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    103. Seet BT, Singh R, Paavola C, Lau EK, Handel TM, 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; PMCID: PMC55364.
    104. Mizoue LS, Sullivan SK, King DS, Kledal TN, Schwartz TW, Bacon KB, Handel TM. Molecular determinants of receptor binding and signaling by the CX3C chemokine fractalkine. J Biol Chem. 2001 Sep 07; 276(36):33906-14. PMID: 11432858.
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    105. Lougheed JC, Holton JM, Alber T, Bazan JF, Handel TM. 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 08; 98(10):5515-20. PMID: 11331761; PMCID: PMC33244.
    106. Pokala N, Handel TM. 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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    107. Marcaurelle LA, Mizoue LS, Wilken J, Oldham L, Kent SB, Handel TM, Bertozzi CR. Chemical synthesis of lymphotactin: a glycosylated chemokine with a C-terminal mucin-like domain. Chemistry. 2001 Mar 02; 7(5):1129-32. PMID: 11303872.
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    108. Hoover DM, Mizoue LS, Handel TM, 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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    109. 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 TM. Identification of surface residues of the monocyte chemotactic protein 1 that affect signaling through the receptor CCR2. Biochemistry. 1999 Dec 07; 38(49):16167-77. PMID: 10587439.
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    110. Lazar GA, Johnson EC, Desjarlais JR, Handel TM. Rotamer strain as a determinant of protein structural specificity. Protein Sci. 1999 Dec; 8(12):2598-610. PMID: 10631975; PMCID: PMC2144231.
    111. 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 TM, Jarnagin K. Identification of residues in the monocyte chemotactic protein-1 that contact the MCP-1 receptor, CCR2. Biochemistry. 1999 Oct 05; 38(40):13013-25. PMID: 10529171.
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    112. Mizoue LS, Bazan JF, Johnson EC, Handel TM. Solution structure and dynamics of the CX3C chemokine domain of fractalkine and its interaction with an N-terminal fragment of CX3CR1. Biochemistry. 1999 Feb 02; 38(5):1402-14. PMID: 9931005.
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    113. 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 TM. 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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    114. 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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    115. Lubkowski J, Bujacz G, Boqué L, Domaille PJ, Handel TM, 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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    116. Handel TM, 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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