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Lawrence Stern PhD

TitleProfessor
InstitutionUMass Chan Medical School
DepartmentPathology
AddressUMass Chan Medical School
55 Lake Avenue North
Worcester MA 01655
Phone508-856-1831
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    Other Positions
    InstitutionT.H. Chan School of Medicine
    DepartmentBiochemistry and Molecular Biotechnology

    InstitutionT.H. Chan School of Medicine
    DepartmentPathology
    DivisionAcademic Pathology

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentBiochemistry and Molecular Pharmacology

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentImmunology and Microbiology Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentInterdisciplinary Graduate Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentMD/PhD Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentPostbaccalaureate Research Education Program

    InstitutionMorningside Graduate School of Biomedical Sciences
    DepartmentTranslational Science


    Collapse Biography 
    Collapse education and training
    Cornell University, Ithaca, NY, United StatesBAChemistry
    Massachusetts Institute of Technology, Cambridge, MA, United StatesPHDBiochemistry

    Collapse Overview 
    Collapse overview

    Academic Background

    Education:

      B. A. cum laude Chemistry Cornell University (1983)
      Ph. D. Biochemistry Massachusetts Institute of Technology (1989)

    Professional Experience:

      Assistant (1994-1999 ) and Associate (1999-2002) Professor of Chemistry
      Member, Center for Biomedical Engineering (1997-2002),
      Massachusetts Institute of Technology
      Structure and Function of Immune Receptors

      Postdoctoral Fellow with Don. C. Wiley (1989-1994)
      Harvard University, Department of Biochemistry & Molecular Biology
      Structure of Major Histocompatibility Proteins

      Graduate Research Assistant with H. Gobind Khorana, (1983-1989)
      Massachusetts Institute of Technology, Department of Chemistry
      Structure-Function Studies of Bacteriorhodopsin

      Research Student with Lawrence Que, Jr. (1981-1983)
      Cornell University, Department of Chemistry
      Mechanistic Studies of Catechol Di-oxygenases

    Molecular recognition in the immune system

    Photo: Lawrence J. Stern, PhDMy primary research interest is in the biochemical processes that underlie cellular recognition and signaling. Research in my laboratory has concentrated on the immune system, because of its intrinsic importance to human health and disease, and because of its treasure of biochemical mechanisms by which cells communicate with their environment and with each other. Our approach combines in vitro biophysical and biochemical studies of the proteins involved in these processes, with cellular studies of their functions and intermolecular interactions. We have focus on two related areas: antigen presentation by MHC proteins, and the molecular mechanisms of T cell activation.

    Antigen presentation by MHC proteins

    A key feature of immune recognition is the interaction of proteins encoded by the Major Histocompatibility Complex (MHC) with antibody-like receptors on T cells. MHC proteins bind peptide antigens within the cell, and display them at the cell surface for interaction with T cell receptors. MHC proteins are highly polymorphic, with allelic differences associated with differences in peptide binding preferences and in individual susceptibility to allergy, infection, and autoimmune disease. We study MHC proteins and their interactions with peptides through a combination of biophysical and cellular analysis. The crystal structure of an MHC-peptide complex revealed that peptides of completely different sequence can be accommodated in the site with almost no alteration of the MHC molecule, with binding specificity determined by subtle details of interactions in the side-chain binding pockets. Hydrodynamic, enzymatic, and spectroscopic studies have identified a peptide-dependent conformational change, in which the region ß58-69 of the MHC protein folds over the bound peptide to trap it in the site, in the rate determining step for the overall peptide binding reaction. In continuing studies, we are investigating the mechanism of peptide-exchange catalysis by DM, a major unsolved problem with implications to other systems in which structural homologues function as chaperones or conformational catalysis. In cellular studies, we have discovered a new extracellular pathway for antigen presentation particularly active in immature dendritic cells, in which peptide generation and MHC loading occur entirely outside of the cell. This pathway may help to explain the unique antigen presentation abilities of dendritic cells, particularly their role in maintaining peripheral tolerance to self-antigens. Recently we have observed that this process occurs also in microglia, enigmatic brain cells involved in immune tolerance and response to infection.

    T cell activation

    The interaction of MHC-peptide complexes on the surface of an antigen presenting cell with receptors on T cells induces characteristic T cell effector functions. Once activated, T cells play crucial roles in the initiation and control of the immune response to foreign material in the body, by killing infected cell and activating other immune system cells. The molecular events at the juxtaposed membranes of T cell and antigen presenting cell that trigger these cellular activation processes are unknown, but are believed to involve receptor aggregation or clustering. To approach the mechanism of aggregation-activated signaling in T cells, we developed a novel model system using chemically-defined oligomers of MHC-peptide complexes, and used them to determine the minimal requirements for T cell activation. For a given amount of receptor engagement, the extent of activation was equivalent for MHC dimers, trimers, tetramers, and octamers, but monomers were inactive, showing definitively that TCR dimerization was necessary and sufficient for activation. Using dimers with various topological constraints, we showed that that the activation trigger did not involve a ligand-induced allosteric change, as observed for many other dimerization-activated receptor systems, but rather a ligand-induced oligomerization. To investigate the molecular events by which oligomerization of ligand-binding domains communicates a signal into the cytoplasm, we have begun structure-function studies of TCR cytoplasmic domains implicated in signaling. We have found that the cytoplasmic domain of TCR zeta exhibits a lipid-dependent folding transition, which regulates accessibility to cytoplasmic protein kinases known to interact with engaged receptor. Based on these results we proposed a novel mechanism for coupling receptor clustering to signaling cascades through zeta subunit conformational changes. In addition to helping unravel the activation mechanism, MHC oligomers are proving to be very useful reagents to detect and identify specific CD4+ T cells present at low frequency in mixed populations in blood and other clinical samples. In continuing work we are probing the structure of receptor components, developing new methods to investigate the T cell activation trigger, and using MHC oligomers to detect antigen-specific T cells in malaria, influenza, and HIV infection.

    Figure

    Figure 1: Peptide structure

    Figure 1: Structure of an antigenic peptide from influenza virus bound to the class IIMHC protein HLA-DR1. The MHC peptide binding domain is shown as a cyan surface,the influenza peptide as a CPK model. Antigen receptors on T cells bind to thiscomplex as part of the process that triggers an immune response. The structureand function of MHC proteins, and the cellular pathways by which they are loaded,are a focus of study in the Stern laboraotry.

    Figure 2: Interaction model

    Figure 2. Model for the interaction of an MHC-peptide complexon one cell with a T cell receptor on another cell. Recognitionof foreign MHC-peptide complexes activates the T cells to killthe presenting cell or to recruit other immune cells to the vicinity.The triggering process involves clustering or aggregation ofTCR on the T cell surface. Determination of the molecularmechanism of such clustering-induced signaling is anotherfocus of research in the Stern Laboratory.


    Collapse Rotation Projects

    Potential Rotation Projects

    Several rotation projects are available in structural biology of immune receptors, antigen presentation pathways, T-cell activation, and development of novel T-cell detection reagents. Please see Prof. Stern for details.



    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. Arya R, Maben Z, Rane D, Ali A, Stern LJ. Phenylsulfamoyl Benzoic Acid Inhibitor of ERAP2 with a Novel Mode of Inhibition. ACS Chem Biol. 2022 07 15; 17(7):1756-1768. PMID: 35767698.
      Citations:    Fields:    Translation:Cells
    2. Becerra-Artiles A, Calvo-Calle JM, Co MD, Nanaware PP, Cruz J, Weaver GC, Lu L, Forconi C, Finberg RW, Moormann AM, Stern LJ. Broadly recognized, cross-reactive SARS-CoV-2 CD4 T cell epitopes are highly conserved across human coronaviruses and presented by common HLA alleles. Cell Rep. 2022 06 14; 39(11):110952. PMID: 35675811.
      Citations:    Fields:    Translation:HumansCells
    3. Weaver GC, Arya R, Schneider CL, Hudson AW, Stern LJ. Corrigendum: Structural Models for Roseolovirus U20 And U21: Non-Classical MHC-I Like Proteins From HHV-6A, HHV-6B, and HHV-7. Front Immunol. 2022; 13:936968. PMID: 35677042.
      Citations:    Fields:    
    4. Weaver GC, Arya R, Schneider CL, Hudson AW, Stern LJ. Structural Models for Roseolovirus U20 And U21: Non-Classical MHC-I Like Proteins From HHV-6A, HHV-6B, and HHV-7. Front Immunol. 2022; 13:864898. PMID: 35444636.
      Citations:    Fields:    Translation:HumansCells
    5. Ghosh D, Pham TD, Nanaware PP, Sengupta D, Adler LN, Li CG, He X, O'Mara ME, Kantor AB, Nguyen KD, Yang Y, Eisenlohr LC, Jensen PE, Herzenberg LA, Stern LJ, Boyd SD, Ghosn EEB, Mellins ED. Regulation of the BCR signalosome by the class II peptide editor, H2-M, affects the development and repertoire of innate-like B cells. Cell Rep. 2022 01 25; 38(4):110200. PMID: 35081339.
      Citations:    Fields:    Translation:AnimalsCells
    6. Meza-Segura M, Birtley JR, Maldonado-Contreras A, Mueller C, Simin KJ, Stern LJ, McCormick BA. SepA Enhances Shigella Invasion of Epithelial Cells by Degrading Alpha-1 Antitrypsin and Producing a Neutrophil Chemoattractant. mBio. 2021 12 21; 12(6):e0283321. PMID: 34724811.
      Citations: 2     Fields:    Translation:HumansCells
    7. Maben Z, Arya R, Georgiadis D, Stratikos E, Stern LJ. Conformational dynamics linked to domain closure and substrate binding explain the ERAP1 allosteric regulation mechanism. Nat Commun. 2021 09 06; 12(1):5302. PMID: 34489420.
      Citations: 4     Fields:    Translation:HumansCells
    8. Clement CC, Nanaware PP, Stern LJ, Santambrogio L. A protocol for qualitative and quantitative measurement of endosomal processing using hot spot analysis. STAR Protoc. 2021 09 17; 2(3):100648. PMID: 34278334.
      Citations:    Fields:    Translation:AnimalsCells
    9. Nanaware PP, Jurewicz MM, Clement CC, Lu L, Santambrogio L, Stern LJ. Distinguishing Signal From Noise in Immunopeptidome Studies of Limiting-Abundance Biological Samples: Peptides Presented by I-Ab in C57BL/6 Mouse Thymus. Front Immunol. 2021; 12:658601. PMID: 33995376.
      Citations:    Fields:    Translation:HumansAnimalsCells
    10. Clement CC, Nanaware PP, Yamazaki T, Negroni MP, Ramesh K, Morozova K, Thangaswamy S, Graves A, Kim HJ, Li TW, Vigano' M, Soni RK, Gadina M, Tse HY, Galluzzi L, Roche PA, Denzin LK, Stern LJ, Santambrogio L. Pleiotropic consequences of metabolic stress for the major histocompatibility complex class II molecule antigen processing and presentation machinery. Immunity. 2021 04 13; 54(4):721-736.e10. PMID: 33725478.
      Citations: 5     Fields:    Translation:AnimalsCells
    11. Mpakali A, Saridakis E, Giastas P, Maben Z, Stern LJ, Larhed M, Hallberg M, Stratikos E. Structural Basis of Inhibition of Insulin-Regulated Aminopeptidase by a Macrocyclic Peptidic Inhibitor. ACS Med Chem Lett. 2020 Jul 09; 11(7):1429-1434. PMID: 32676150.
      Citations:    
    12. Mavridis G, Arya R, Domnick A, Zoidakis J, Makridakis M, Vlahou A, Mpakali A, Lelis A, Georgiadis D, Tampé R, Papakyriakou A, Stern LJ, Stratikos E. A systematic re-examination of processing of MHCI-bound antigenic peptide precursors by endoplasmic reticulum aminopeptidase 1. J Biol Chem. 2020 05 22; 295(21):7193-7210. PMID: 32184355.
      Citations: 9     Fields:    Translation:HumansCells
    13. Jiang W, Birtley JR, Hung SC, Wang W, Chiou SH, Macaubas C, Kornum B, Tian L, Huang H, Adler L, Weaver G, Lu L, Ilstad-Minnihan A, Somasundaram S, Ayyangar S, Davis MM, Stern LJ, Mellins ED. Author Correction: In vivo clonal expansion and phenotypes of hypocretin-specific CD4+ T cells in narcolepsy patients and controls. Nat Commun. 2020 Jan 08; 11(1):242. PMID: 31913263.
      Citations:    Fields:    
    14. Maben Z, Arya R, Rane D, An WF, Metkar S, Hickey M, Bender S, Ali A, Nguyen TT, Evnouchidou I, Schilling R, Stratikos E, Golden J, Stern LJ. Discovery of Selective Inhibitors of Endoplasmic Reticulum Aminopeptidase 1. J Med Chem. 2020 01 09; 63(1):103-121. PMID: 31841350.
      Citations: 9     Fields:    Translation:HumansCells
    15. Kamga L, Gil A, Song I, Brody R, Ghersi D, Aslan N, Stern LJ, Selin LK, Luzuriaga K. CDR3? drives selection of the immunodominant Epstein Barr virus (EBV) BRLF1-specific CD8 T cell receptor repertoire in primary infection. PLoS Pathog. 2019 11; 15(11):e1008122. PMID: 31765434.
      Citations: 10     Fields:    Translation:HumansCells
    16. Jiang W, Birtley JR, Hung SC, Wang W, Chiou SH, Macaubas C, Kornum B, Tian L, Huang H, Adler L, Weaver G, Lu L, Ilstad-Minnihan A, Somasundaram S, Ayyangar S, Davis MM, Stern LJ, Mellins ED. In vivo clonal expansion and phenotypes of hypocretin-specific CD4+ T cells in narcolepsy patients and controls. Nat Commun. 2019 11 20; 10(1):5247. PMID: 31748512.
      Citations: 13     Fields:    Translation:HumansAnimalsCells
    17. Negroni MP, Cho OH, Stern LJ. Recognition of Listeria Infection by Germline Elements of the V?1.1 V?6.3 TCR. Immunohorizons. 2019 07 18; 3(7):341-351. PMID: 31356163.
      Citations: 2     Fields:    Translation:AnimalsCells
    18. Birtley JR, Alomary M, Zanini E, Antony J, Maben Z, Weaver GC, Von Arx C, Mura M, Marinho AT, Lu H, Morecroft EVN, Karali E, Chayen NE, Tate EW, Jurewicz M, Stern LJ, Recchi C, Gabra H. Inactivating mutations and X-ray crystal structure of the tumor suppressor OPCML reveal cancer-associated functions. Nat Commun. 2019 07 17; 10(1):3134. PMID: 31316070.
      Citations: 5     Fields:    Translation:HumansCells
    19. Joshi U, Pearson A, Evans JE, Langlois H, Saltiel N, Ojo J, Klimas N, Sullivan K, Keegan AP, Oberlin S, Darcey T, Cseresznye A, Raya B, Paris D, Hammock B, Vasylieva N, Hongsibsong S, Stern LJ, Crawford F, Mullan M, Abdullah L. A permethrin metabolite is associated with adaptive immune responses in Gulf War Illness. Brain Behav Immun. 2019 10; 81:545-559. PMID: 31325531.
      Citations: 18     Fields:    Translation:HumansAnimals
    20. Koumantou D, Barnea E, Martin-Esteban A, Maben Z, Papakyriakou A, Mpakali A, Kokkala P, Pratsinis H, Georgiadis D, Stern LJ, Admon A, Stratikos E. Editing the immunopeptidome of melanoma cells using a potent inhibitor of endoplasmic reticulum aminopeptidase 1 (ERAP1). Cancer Immunol Immunother. 2019 Aug; 68(8):1245-1261. PMID: 31222486.
      Citations: 12     Fields:    Translation:HumansCells
    21. Stadinski BD, Blevins SJ, Spidale NA, Duke BR, Huseby PG, Stern LJ, Huseby ES. A temporal thymic selection switch and ligand binding kinetics constrain neonatal Foxp3+ Treg cell development. Nat Immunol. 2019 08; 20(8):1046-1058. PMID: 31209405.
      Citations: 13     Fields:    Translation:AnimalsCells
    22. Jurewicz MM, Willis RA, Ramachandiran V, Altman JD, Stern LJ. MHC-I peptide binding activity assessed by exchange after cleavage of peptide covalently linked to ?2-microglobulin. Anal Biochem. 2019 11 01; 584:113328. PMID: 31201791.
      Citations: 3     Fields:    Translation:Cells
    23. Becerra-Artiles A, Cruz J, Leszyk JD, Sidney J, Sette A, Shaffer SA, Stern LJ. Naturally processed HLA-DR3-restricted HHV-6B peptides are recognized broadly with polyfunctional and cytotoxic CD4 T-cell responses. Eur J Immunol. 2019 08; 49(8):1167-1185. PMID: 31020640.
      Citations: 7     Fields:    Translation:HumansCells
    24. Nanaware PP, Jurewicz MM, Leszyk JD, Shaffer SA, Stern LJ. HLA-DO Modulates the Diversity of the MHC-II Self-peptidome. Mol Cell Proteomics. 2019 03; 18(3):490-503. PMID: 30573663.
      Citations: 11     Fields:    Translation:HumansAnimalsCells
    25. Jurewicz MM, Stern LJ. Class II MHC antigen processing in immune tolerance and inflammation. Immunogenetics. 2019 03; 71(3):171-187. PMID: 30421030.
      Citations: 23     Fields:    Translation:HumansAnimalsCells
    26. Jardetzky TS, Brown JH, Gorga JC, Stern LJ, Urban RG, Chi YI, Stauffacher C, Strominger JL, Wiley DC. Pillars Article: Three-Dimensional Structure of a Human Class II Histocompatibility Molecule Complexed with Superantigen. Nature. 1994. 368: 711-718. J Immunol. 2018 10 01; 201(7):1819-1826. PMID: 30224361.
      Citations: 1     Fields:    
    27. Clement CC, Wang W, Dzieciatkowska M, Cortese M, Hansen KC, Becerra A, Thangaswamy S, Nizamutdinova I, Moon JY, Stern LJ, Gashev AA, Zawieja D, Santambrogio L. Quantitative Profiling of the Lymph Node Clearance Capacity. Sci Rep. 2018 07 26; 8(1):11253. PMID: 30050160.
      Citations: 18     Fields:    Translation:AnimalsCells
    28. Negroni MP, Stern LJ. The N-terminal region of photocleavable peptides that bind HLA-DR1 determines the kinetics of fragment release. PLoS One. 2018; 13(7):e0199704. PMID: 29965980.
      Citations: 2     Fields:    Translation:HumansCells
    29. Mpakali A, Maben Z, Stern LJ, Stratikos E. Molecular pathways for antigenic peptide generation by ER aminopeptidase 1. Mol Immunol. 2019 09; 113:50-57. PMID: 29678301.
      Citations: 6     Fields:    Translation:HumansAnimalsCells
    30. Becerra-Artiles A, Santoro T, Stern LJ. Evaluation of a method to measure HHV-6B infection in vitro based on cell size. Virol J. 2018 01 05; 15(1):4. PMID: 29304865.
      Citations:    Fields:    Translation:HumansCells
    31. Zimmermann K, Eells R, Heinrich F, Rintoul S, Josey B, Shekhar P, Lösche M, Stern LJ. The cytosolic domain of T-cell receptor ? associates with membranes in a dynamic equilibrium and deeply penetrates the bilayer. J Biol Chem. 2017 10 27; 292(43):17746-17759. PMID: 28893902.
      Citations: 3     Fields:    Translation:HumansCells
    32. Maldonado-Contreras A, Birtley JR, Boll E, Zhao Y, Mumy KL, Toscano J, Ayehunie S, Reinecker HC, Stern LJ, McCormick BA. Shigella depends on SepA to destabilize the intestinal epithelial integrity via cofilin activation. Gut Microbes. 2017 11 02; 8(6):544-560. PMID: 28598765.
      Citations: 17     Fields:    Translation:HumansCells
    33. Stamogiannos A, Maben Z, Papakyriakou A, Mpakali A, Kokkala P, Georgiadis D, Stern LJ, Stratikos E. Critical Role of Interdomain Interactions in the Conformational Change and Catalytic Mechanism of Endoplasmic Reticulum Aminopeptidase 1. Biochemistry. 2017 03 14; 56(10):1546-1558. PMID: 28218509.
      Citations: 17     Fields:    Translation:HumansAnimalsCells
    34. Song I, Gil A, Mishra R, Ghersi D, Selin LK, Stern LJ. Broad TCR repertoire and diverse structural solutions for recognition of an immunodominant CD8+ T cell epitope. Nat Struct Mol Biol. 2017 04; 24(4):395-406. PMID: 28250417.
      Citations: 38     Fields:    Translation:HumansCells
    35. Stern LJ, Santambrogio L. The melting pot of the MHC II peptidome. Curr Opin Immunol. 2016 06; 40:70-7. PMID: 27018930.
      Citations: 17     Fields:    Translation:HumansAnimalsCells
    36. Clement CC, Moncrieffe H, Lele A, Janow G, Becerra A, Bauli F, Saad FA, Perino G, Montagna C, Cobelli N, Hardin J, Stern LJ, Ilowite N, Porcelli SA, Santambrogio L. Autoimmune response to transthyretin in juvenile idiopathic arthritis. JCI Insight. 2016 Feb; 1(2). PMID: 26973882.
      Citations: 11     Fields:    
    37. Hellman LM, Yin L, Wang Y, Blevins SJ, Riley TP, Belden OS, Spear TT, Nishimura MI, Stern LJ, Baker BM. Differential scanning fluorimetry based assessments of the thermal and kinetic stability of peptide-MHC complexes. J Immunol Methods. 2016 May; 432:95-101. PMID: 26906089.
      Citations: 25     Fields:    Translation:HumansCells
    38. Clement CC, Becerra A, Yin L, Zolla V, Huang L, Merlin S, Follenzi A, Shaffer SA, Stern LJ, Santambrogio L. The Dendritic Cell Major Histocompatibility Complex II (MHC II) Peptidome Derives from a Variety of Processing Pathways and Includes Peptides with a Broad Spectrum of HLA-DM Sensitivity. J Biol Chem. 2016 Mar 11; 291(11):5576-5595. PMID: 26740625.
      Citations: 27     Fields:    Translation:HumansAnimalsCells
    39. Becerra-Artiles A, Dominguez-Amorocho O, Stern LJ, Calvo-Calle JM. A Simple Proteomics-Based Approach to Identification of Immunodominant Antigens from a Complex Pathogen: Application to the CD4 T Cell Response against Human Herpesvirus 6B. PLoS One. 2015; 10(11):e0142871. PMID: 26599878.
      Citations: 6     Fields:    Translation:HumansCells
    40. Yin L, Maben ZJ, Becerra A, Stern LJ. Evaluating the Role of HLA-DM in MHC Class II-Peptide Association Reactions. J Immunol. 2015 Jul 15; 195(2):706-16. PMID: 26062997.
      Citations: 14     Fields:    Translation:HumansCells
    41. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. Pillars article: three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 1993. 364: 33-39. J Immunol. 2015 Jan 01; 194(1):5-11. PMID: 25527791.
      Citations: 1     Fields:    Translation:Humans
    42. Becerra A, Gibson L, Stern LJ, Calvo-Calle JM. Immune response to HHV-6 and implications for immunotherapy. Curr Opin Virol. 2014 Dec; 9:154-61. PMID: 25462448.
      Citations: 15     Fields:    Translation:HumansCells
    43. Yin L, Stern LJ. Measurement of Peptide Binding to MHC Class II Molecules by Fluorescence Polarization. Curr Protoc Immunol. 2014 Aug 01; 106:5.10.1-5.10.12. PMID: 25081912.
      Citations: 16     Fields:    Translation:HumansAnimalsCells
    44. Yin L, Trenh P, Guce A, Wieczorek M, Lange S, Sticht J, Jiang W, Bylsma M, Mellins ED, Freund C, Stern LJ. Susceptibility to HLA-DM protein is determined by a dynamic conformation of major histocompatibility complex class II molecule bound with peptide. J Biol Chem. 2014 Aug 22; 289(34):23449-64. PMID: 25002586.
      Citations: 28     Fields:    Translation:HumansCells
    45. Parra-López CA, Bernal-Estévez D, Yin L, Vargas LE, Pulido-Calixto C, Salazar LM, Calvo-Calle JM, Stern LJ. An unstable Th epitope of P. falciparum fosters central memory T cells and anti-CS antibody responses. PLoS One. 2014; 9(7):e100639. PMID: 24983460.
      Citations: 3     Fields:    Translation:HumansAnimalsCells
    46. Stadinski BD, Trenh P, Duke B, Huseby PG, Li G, Stern LJ, Huseby ES. Effect of CDR3 sequences and distal V gene residues in regulating TCR-MHC contacts and ligand specificity. J Immunol. 2014 Jun 15; 192(12):6071-82. PMID: 24813203.
      Citations: 11     Fields:    Translation:AnimalsCells
    47. Yin L, Stern LJ. A novel method to measure HLA-DM-susceptibility of peptides bound to MHC class II molecules based on peptide binding competition assay and differential IC(50) determination. J Immunol Methods. 2014 Apr; 406:21-33. PMID: 24583195.
      Citations: 7     Fields:    Translation:HumansCells
    48. Parra M, Herrera D, Calvo-Calle JM, Stern LJ, Parra-López CA, Butcher E, Franco M, Angel J. Circulating human rotavirus specific CD4 T cells identified with a class II tetramer express the intestinal homing receptors ?4?7 and CCR9. Virology. 2014 Mar; 452-453:191-201. PMID: 24606696.
      Citations: 10     Fields:    Translation:HumansCells
    49. Mellins ED, Stern LJ. HLA-DM and HLA-DO, key regulators of MHC-II processing and presentation. Curr Opin Immunol. 2014 Feb; 26:115-22. PMID: 24463216.
      Citations: 54     Fields:    Translation:HumansAnimalsCells
    50. Yin L, Stern LJ. HLA-DM Focuses on Conformational Flexibility Around P1 Pocket to Catalyze Peptide Exchange. Front Immunol. 2013 Oct 17; 4:336. PMID: 24146666.
      Citations: 8     Fields:    
    51. Shen ZT, Nguyen TT, Daniels KA, Welsh RM, Stern LJ. Disparate epitopes mediating protective heterologous immunity to unrelated viruses share peptide-MHC structural features recognized by cross-reactive T cells. J Immunol. 2013 Nov 15; 191(10):5139-52. PMID: 24127554.
      Citations: 12     Fields:    Translation:AnimalsCells
    52. Santambrogio L, Stern LJ. Carrying yourself: self antigen composition of the lymphatic fluid. Lymphat Res Biol. 2013 Sep; 11(3):149-54. PMID: 24024574.
      Citations: 4     Fields:    Translation:HumansCells
    53. Serra-Moreno R, Zimmermann K, Stern LJ, Evans DT. Tetherin/BST-2 antagonism by Nef depends on a direct physical interaction between Nef and tetherin, and on clathrin-mediated endocytosis. PLoS Pathog. 2013; 9(7):e1003487. PMID: 23853598.
      Citations: 38     Fields:    Translation:HumansAnimalsCells
    54. Yin L, Calvo-Calle JM, Cruz J, Newman FK, Frey SE, Ennis FA, Stern LJ. CD4+ T cells provide intermolecular help to generate robust antibody responses in vaccinia virus-vaccinated humans. J Immunol. 2013 Jun 15; 190(12):6023-33. PMID: 23667112.
      Citations: 12     Fields:    Translation:HumansCellsPHPublic Health
    55. Stratikos E, Stern LJ. Antigenic peptide trimming by ER aminopeptidases--insights from structural studies. Mol Immunol. 2013 Oct; 55(3-4):212-9. PMID: 23545452.
      Citations: 23     Fields:    Translation:HumansAnimalsCells
    56. Guce AI, Mortimer SE, Yoon T, Painter CA, Jiang W, Mellins ED, Stern LJ. HLA-DO acts as a substrate mimic to inhibit HLA-DM by a competitive mechanism. Nat Struct Mol Biol. 2013 Jan; 20(1):90-8. PMID: 23222639.
      Citations: 65     Fields:    Translation:HumansAnimalsCells
    57. Painter CA, Stern LJ. Conformational variation in structures of classical and non-classical MHCII proteins and functional implications. Immunol Rev. 2012 Nov; 250(1):144-57. PMID: 23046127.
      Citations: 36     Fields:    Translation:HumansAnimalsCells
    58. Farfán-Arribas DJ, Stern LJ, Rock KL. Using intein catalysis to probe the origin of major histocompatibility complex class I-presented peptides. Proc Natl Acad Sci U S A. 2012 Oct 16; 109(42):16998-7003. PMID: 23027972.
      Citations: 14     Fields:    Translation:AnimalsCells
    59. Yin L, Calvo-Calle JM, Dominguez-Amorocho O, Stern LJ. HLA-DM constrains epitope selection in the human CD4 T cell response to vaccinia virus by favoring the presentation of peptides with longer HLA-DM-mediated half-lives. J Immunol. 2012 Oct 15; 189(8):3983-94. PMID: 22966084.
      Citations: 36     Fields:    Translation:HumansCells
    60. Holland CJ, Rizkallah PJ, Vollers S, Calvo-Calle JM, Madura F, Fuller A, Sewell AK, Stern LJ, Godkin A, Cole DK. Minimal conformational plasticity enables TCR cross-reactivity to different MHC class II heterodimers. Sci Rep. 2012; 2:629. PMID: 22953050.
      Citations: 18     Fields:    Translation:HumansCells
    61. Yoon T, Macmillan H, Mortimer SE, Jiang W, Rinderknecht CH, Stern LJ, Mellins ED. Mapping the HLA-DO/HLA-DM complex by FRET and mutagenesis. Proc Natl Acad Sci U S A. 2012 Jul 10; 109(28):11276-81. PMID: 22733780.
      Citations: 27     Fields:    Translation:HumansAnimalsCells
    62. Huseby ES, Stadinski BD, Trenh P, Stern LJ. Response to Garcia et al. Immunity. 2012 Jun 29; 36(6):889-90. PMID: 22705102.
      Citations:    Fields:    Translation:Animals
    63. Nastke MD, Becerra A, Yin L, Dominguez-Amorocho O, Gibson L, Stern LJ, Calvo-Calle JM. Human CD4+ T cell response to human herpesvirus 6. J Virol. 2012 May; 86(9):4776-92. PMID: 22357271.
      Citations: 30     Fields:    Translation:HumansCells
    64. Stadinski BD, Trenh P, Smith RL, Bautista B, Huseby PG, Li G, Stern LJ, Huseby ES. A role for differential variable gene pairing in creating T cell receptors specific for unique major histocompatibility ligands. Immunity. 2011 Nov 23; 35(5):694-704. PMID: 22101158.
      Citations: 45     Fields:    Translation:AnimalsCells
    65. Painter CA, Negroni MP, Kellersberger KA, Zavala-Ruiz Z, Evans JE, Stern LJ. Conformational lability in the class II MHC 310 helix and adjacent extended strand dictate HLA-DM susceptibility and peptide exchange. Proc Natl Acad Sci U S A. 2011 Nov 29; 108(48):19329-34. PMID: 22084083.
      Citations: 45     Fields:    Translation:AnimalsCells
    66. Nguyen TT, Chang SC, Evnouchidou I, York IA, Zikos C, Rock KL, Goldberg AL, Stratikos E, Stern LJ. Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat Struct Mol Biol. 2011 May; 18(5):604-13. PMID: 21478864.
      Citations: 85     Fields:    Translation:HumansCells
    67. Painter CA, Stern LJ. Structural Insights Into HLA-DM Mediated MHC II Peptide Exchange. Curr Top Biochem Res. 2011; 13(2):39-55. PMID: 25264402.
      Citations:    
    68. Shen ZT, Brehm MA, Daniels KA, Sigalov AB, Selin LK, Welsh RM, Stern LJ. Bi-specific MHC heterodimers for characterization of cross-reactive T cells. J Biol Chem. 2010 Oct 22; 285(43):33144-33153. PMID: 20729210.
      Citations: 7     Fields:    Translation:HumansAnimalsCells
    69. Ge X, Gebe JA, Bollyky PL, James EA, Yang J, Stern LJ, Kwok WW. Peptide-MHC cellular microarray with innovative data analysis system for simultaneously detecting multiple CD4 T-cell responses. PLoS One. 2010 Jun 28; 5(6):e11355. PMID: 20634998.
      Citations: 11     Fields:    Translation:HumansCells
    70. Clement CC, Cannizzo ES, Nastke MD, Sahu R, Olszewski W, Miller NE, Stern LJ, Santambrogio L. An expanded self-antigen peptidome is carried by the human lymph as compared to the plasma. PLoS One. 2010 Mar 26; 5(3):e9863. PMID: 20360855.
      Citations: 42     Fields:    Translation:Humans
    71. Kim WM, Sigalov AB, Stern LJ. Pseudo-merohedral twinning and noncrystallographic symmetry in orthorhombic crystals of SIVmac239 Nef core domain bound to different-length TCRzeta fragments. Acta Crystallogr D Biol Crystallogr. 2010 Feb; 66(Pt 2):163-75. PMID: 20124696.
      Citations: 12     Fields:    Translation:Cells
    72. Campbell JD, Buckland KF, McMillan SJ, Kearley J, Oldfield WL, Stern LJ, Grönlund H, van Hage M, Reynolds CJ, Boyton RJ, Cobbold SP, Kay AB, Altmann DM, Lloyd CM, Larché M. Peptide immunotherapy in allergic asthma generates IL-10-dependent immunological tolerance associated with linked epitope suppression. J Exp Med. 2009 Jul 06; 206(7):1535-47. PMID: 19528258.
      Citations: 86     Fields:    Translation:HumansAnimalsCells
    73. Stern LJ, Calvo-Calle JM. HLA-DR: molecular insights and vaccine design. Curr Pharm Des. 2009; 15(28):3249-61. PMID: 19860674.
      Citations: 31     Fields:    Translation:HumansAnimalsCells
    74. Sigalov AB, Kim WM, Saline M, Stern LJ. The intrinsically disordered cytoplasmic domain of the T cell receptor zeta chain binds to the nef protein of simian immunodeficiency virus without a disorder-to-order transition. Biochemistry. 2008 Dec 09; 47(49):12942-4. PMID: 19012413.
      Citations: 25     Fields:    Translation:Cells
    75. Painter CA, Cruz A, López GE, Stern LJ, Zavala-Ruiz Z. Model for the peptide-free conformation of class II MHC proteins. PLoS One. 2008 Jun 11; 3(6):e2403. PMID: 18545669.
      Citations: 38     Fields:    Translation:Cells
    76. Strug I, Calvo-Calle JM, Green KM, Cruz J, Ennis FA, Evans JE, Stern LJ. Vaccinia peptides eluted from HLA-DR1 isolated from virus-infected cells are recognized by CD4+ T cells from a vaccinated donor. J Proteome Res. 2008 Jul; 7(7):2703-11. PMID: 18507432.
      Citations: 18     Fields:    Translation:HumansCellsPHPublic Health
    77. Vollers SS, Stern LJ. Class II major histocompatibility complex tetramer staining: progress, problems, and prospects. Immunology. 2008 Mar; 123(3):305-13. PMID: 18251991.
      Citations: 57     Fields:    Translation:HumansCells
    78. Chitta S, Santambrogio L, Stern LJ. GMCSF in the absence of other cytokines sustains human dendritic cell precursors with T cell regulatory activity and capacity to differentiate into functional dendritic cells. Immunol Lett. 2008 Feb 15; 116(1):41-54. PMID: 18166231.
      Citations: 16     Fields:    Translation:HumansCells
    79. Calvo-Calle JM, Strug I, Nastke MD, Baker SP, Stern LJ. Human CD4+ T cell epitopes from vaccinia virus induced by vaccination or infection. PLoS Pathog. 2007 Oct 12; 3(10):1511-29. PMID: 17937498.
      Citations: 39     Fields:    Translation:HumansCells
    80. Stern LJ. Characterizing MHC-associated peptides by mass spectrometry. J Immunol. 2007 Sep 01; 179(5):2667-8. PMID: 17709475.
      Citations: 3     Fields:    Translation:Humans
    81. Mitra-Kaushik S, Cruz J, Stern LJ, Ennis FA, Terajima M. Human cytotoxic CD4+ T cells recognize HLA-DR1-restricted epitopes on vaccinia virus proteins A24R and D1R conserved among poxviruses. J Immunol. 2007 Jul 15; 179(2):1303-12. PMID: 17617623.
      Citations: 16     Fields:    Translation:HumansCells
    82. Parry CS, Gorski J, Stern LJ. Crystallographic structure of the human leukocyte antigen DRA, DRB3*0101: models of a directional alloimmune response and autoimmunity. J Mol Biol. 2007 Aug 10; 371(2):435-46. PMID: 17583734.
      Citations: 19     Fields:    Translation:HumansCells
    83. Duchardt E, Sigalov AB, Aivazian D, Stern LJ, Schwalbe H. Structure induction of the T-cell receptor zeta-chain upon lipid binding investigated by NMR spectroscopy. Chembiochem. 2007 May 07; 8(7):820-7. PMID: 17410622.
      Citations: 19     Fields:    Translation:Cells
    84. Venkatraman P, Nguyen TT, Sainlos M, Bilsel O, Chitta S, Imperiali B, Stern LJ. Fluorogenic probes for monitoring peptide binding to class II MHC proteins in living cells. Nat Chem Biol. 2007 Apr; 3(4):222-8. PMID: 17351628.
      Citations: 38     Fields:    Translation:HumansAnimalsCells
    85. Younes SA, Trautmann L, Yassine-Diab B, Kalfayan LH, Kernaleguen AE, Cameron TO, Boulassel R, Stern LJ, Routy JP, Grossman Z, Dumont AR, Sekaly RP. The duration of exposure to HIV modulates the breadth and the magnitude of HIV-specific memory CD4+ T cells. J Immunol. 2007 Jan 15; 178(2):788-97. PMID: 17202340.
      Citations: 15     Fields:    Translation:HumansCells
    86. Sigalov AB, Aivazian DA, Uversky VN, Stern LJ. Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits. Biochemistry. 2006 Dec 26; 45(51):15731-9. PMID: 17176095.
      Citations: 60     Fields:    Translation:HumansCells
    87. Parra-López C, Calvo-Calle JM, Cameron TO, Vargas LE, Salazar LM, Patarroyo ME, Nardin E, Stern LJ. Major histocompatibility complex and T cell interactions of a universal T cell epitope from Plasmodium falciparum circumsporozoite protein. J Biol Chem. 2006 May 26; 281(21):14907-17. PMID: 16565072.
      Citations: 15     Fields:    Translation:HumansAnimalsCells
    88. De Wall SL, Painter C, Stone JD, Bandaranayake R, Wiley DC, Mitchison TJ, Stern LJ, DeDecker BS. Noble metals strip peptides from class II MHC proteins. Nat Chem Biol. 2006 Apr; 2(4):197-201. PMID: 16505807.
      Citations: 10     Fields:    Translation:HumansAnimalsCells
    89. Stone JD, Stern LJ. CD8 T cells, like CD4 T cells, are triggered by multivalent engagement of TCRs by MHC-peptide ligands but not by monovalent engagement. J Immunol. 2006 Feb 01; 176(3):1498-505. PMID: 16424178.
      Citations: 17     Fields:    Translation:HumansAnimalsCells
    90. Stern LJ, Potolicchio I, Santambrogio L. MHC class II compartment subtypes: structure and function. Curr Opin Immunol. 2006 Feb; 18(1):64-9. PMID: 16337363.
      Citations: 28     Fields:    Translation:HumansAnimalsCells
    91. Carven GJ, Stern LJ. Probing the ligand-induced conformational change in HLA-DR1 by selective chemical modification and mass spectrometric mapping. Biochemistry. 2005 Oct 25; 44(42):13625-37. PMID: 16229453.
      Citations: 28     Fields:    Translation:Cells
    92. Potolicchio I, Chitta S, Xu X, Fonseca D, Crisi G, Horejsi V, Strominger JL, Stern LJ, Raposo G, Santambrogio L. Conformational variation of surface class II MHC proteins during myeloid dendritic cell differentiation accompanies structural changes in lysosomal MIIC. J Immunol. 2005 Oct 15; 175(8):4935-47. PMID: 16210595.
      Citations: 23     Fields:    Translation:HumansCells
    93. Norris PJ, Stone JD, Anikeeva N, Heitman JW, Wilson IC, Hirschkorn DF, Clark MJ, Moffett HF, Cameron TO, Sykulev Y, Stern LJ, Walker BD. Antagonism of HIV-specific CD4+ T cells by C-terminal truncation of a minimum epitope. Mol Immunol. 2006 Mar; 43(9):1349-57. PMID: 16216327.
      Citations: 10     Fields:    Translation:HumansCells
    94. Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ, Santambrogio L. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol. 2005 Aug 15; 175(4):2237-43. PMID: 16081791.
      Citations: 166     Fields:    Translation:AnimalsCells
    95. Stone JD, Demkowicz WE, Stern LJ. HLA-restricted epitope identification and detection of functional T cell responses by using MHC-peptide and costimulatory microarrays. Proc Natl Acad Sci U S A. 2005 Mar 08; 102(10):3744-9. PMID: 15728728.
      Citations: 27     Fields:    Translation:HumansCells
    96. Baggio R, Carven GJ, Chiulli A, Palmer M, Stern LJ, Arenas JE. Induced fit of an epitope peptide to a monoclonal antibody probed with a novel parallel surface plasmon resonance assay. J Biol Chem. 2005 Feb 11; 280(6):4188-94. PMID: 15556932.
      Citations: 3     Fields:    Translation:AnimalsCells
    97. Zavala-Ruiz Z, Strug I, Anderson MW, Gorski J, Stern LJ. A polymorphic pocket at the P10 position contributes to peptide binding specificity in class II MHC proteins. Chem Biol. 2004 Oct; 11(10):1395-402. PMID: 15489166.
      Citations: 23     Fields:    Translation:Cells
    98. Zavala-Ruiz Z, Strug I, Walker BD, Norris PJ, Stern LJ. A hairpin turn in a class II MHC-bound peptide orients residues outside the binding groove for T cell recognition. Proc Natl Acad Sci U S A. 2004 Sep 07; 101(36):13279-84. PMID: 15331779.
      Citations: 26     Fields:    Translation:HumansCells
    99. Sigalov A, Aivazian D, Stern L. Homooligomerization of the cytoplasmic domain of the T cell receptor zeta chain and of other proteins containing the immunoreceptor tyrosine-based activation motif. Biochemistry. 2004 Feb 24; 43(7):2049-61. PMID: 14967045.
      Citations: 55     Fields:    Translation:HumansCells
    100. Carven GJ, Chitta S, Hilgert I, Rushe MM, Baggio RF, Palmer M, Arenas JE, Strominger JL, Horejsi V, Santambrogio L, Stern LJ. Monoclonal antibodies specific for the empty conformation of HLA-DR1 reveal aspects of the conformational change associated with peptide binding. J Biol Chem. 2004 Apr 16; 279(16):16561-70. PMID: 14757758.
      Citations: 22     Fields:    Translation:HumansCells
    101. Stratikos E, Wiley DC, Stern LJ. Enhanced catalytic action of HLA-DM on the exchange of peptides lacking backbone hydrogen bonds between their N-terminal region and the MHC class II alpha-chain. J Immunol. 2004 Jan 15; 172(2):1109-17. PMID: 14707085.
      Citations: 33     Fields:    Translation:HumansCells
    102. Zavala-Ruiz Z, Sundberg EJ, Stone JD, DeOliveira DB, Chan IC, Svendsen J, Mariuzza RA, Stern LJ. Exploration of the P6/P7 region of the peptide-binding site of the human class II major histocompatability complex protein HLA-DR1. J Biol Chem. 2003 Nov 07; 278(45):44904-12. PMID: 12952957.
      Citations: 8     Fields:    Translation:HumansCells
    103. Cameron TO, Cohen GB, Islam SA, Stern LJ. Examination of the highly diverse CD4(+) T-cell repertoire directed against an influenza peptide: a step towards TCR proteomics. Immunogenetics. 2002 Dec; 54(9):611-20. PMID: 12466894.
      Citations: 10     Fields:    Translation:HumansCells
    104. Ge Q, Stone JD, Thompson MT, Cochran JR, Rushe M, Eisen HN, Chen J, Stern LJ. Soluble peptide-MHC monomers cause activation of CD8+ T cells through transfer of the peptide to T cell MHC molecules. Proc Natl Acad Sci U S A. 2002 Oct 15; 99(21):13729-34. PMID: 12374859.
      Citations: 29     Fields:    Translation:AnimalsCells
    105. Cameron TO, Norris PJ, Patel A, Moulon C, Rosenberg ES, Mellins ED, Wedderburn LR, Stern LJ. Labeling antigen-specific CD4(+) T cells with class II MHC oligomers. J Immunol Methods. 2002 Oct 01; 268(1):51-69. PMID: 12213343.
      Citations: 22     Fields:    Translation:HumansAnimalsCells
    106. Re F, Belyanskaya SL, Riese RJ, Cipriani B, Fischer FR, Granucci F, Ricciardi-Castagnoli P, Brosnan C, Stern LJ, Strominger JL, Santambrogio L. Granulocyte-macrophage colony-stimulating factor induces an expression program in neonatal microglia that primes them for antigen presentation. J Immunol. 2002 Sep 01; 169(5):2264-73. PMID: 12193691.
      Citations: 27     Fields:    Translation:AnimalsCells
    107. Sigalov AB, Stern LJ. Dihydrolipoic acid as an effective cofactor for peptide methionine sulfoxide reductase in enzymatic repair of oxidative damage to both lipid-free and lipid-bound apolipoprotein a-I. Antioxid Redox Signal. 2002 Jun; 4(3):553-7. PMID: 12215223.
      Citations: 1     Fields:    Translation:Cells
    108. Zaru R, Cameron TO, Stern LJ, Müller S, Valitutti S. Cutting edge: TCR engagement and triggering in the absence of large-scale molecular segregation at the T cell-APC contact site. J Immunol. 2002 May 01; 168(9):4287-91. PMID: 11970969.
      Citations: 14     Fields:    Translation:Cells
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