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    Lawrence Stern PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentPathology
    AddressUniversity of Massachusetts Medical School
    55 Lake Avenue North
    Worcester MA 01655
    Phone508-856-1831
      Other Positions
      InstitutionUMMS - School of Medicine
      DepartmentBiochemistry and Molecular Pharmacology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentBiochemistry and Molecular Pharmacology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentImmunology and Virology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMD/PhD Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentTranslational Science

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentCenter for AIDS Research

        Overview 
        Narrative

        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.



        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.



        Bibliographic 
        selected publications
        List All   |   Timeline
        1. Parra-López CA, Bernal-Estévez D, 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.
          View in: PubMed
        2. 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.
          View in: PubMed
        3. 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 IC50 determination. J Immunol Methods. 2014 Apr; 406:21-33.
          View in: PubMed
        4. 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 a4ß7 and CCR9. Virology. 2014 Mar; 452-453:191-201.
          View in: PubMed
        5. 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.
          View in: PubMed
        6. Yin L, Stern LJ. HLA-DM Focuses on Conformational Flexibility Around P1 Pocket to Catalyze Peptide Exchange. Front Immunol. 2013; 4:336.
          View in: PubMed
        7. 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.
          View in: PubMed
        8. Santambrogio L, Stern LJ. Carrying yourself: self antigen composition of the lymphatic fluid. Lymphat Res Biol. 2013 Sep; 11(3):149-54.
          View in: PubMed
        9. 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.
          View in: PubMed
        10. 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.
          View in: PubMed
        11. Stratikos E, Stern LJ. Antigenic peptide trimming by ER aminopeptidases--insights from structural studies. Mol Immunol. 2013 Oct; 55(3-4):212-9.
          View in: PubMed
        12. 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.
          View in: PubMed
        13. 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.
          View in: PubMed
        14. 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.
          View in: PubMed
        15. 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.
          View in: PubMed
        16. 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.
          View in: PubMed
        17. 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.
          View in: PubMed
        18. 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.
          View in: PubMed
        19. 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.
          View in: PubMed
        20. 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.
          View in: PubMed
        21. 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.
          View in: PubMed
        22. 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):33144-53.
          View in: PubMed
        23. 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; 5(6):e11355.
          View in: PubMed
        24. 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; 5(3):e9863.
          View in: PubMed
        25. 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.
          View in: PubMed
        26. 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 6; 206(7):1535-47.
          View in: PubMed
        27. Stern LJ, Calvo-Calle JM. HLA-DR: molecular insights and vaccine design. Curr Pharm Des. 2009; 15(28):3249-61.
          View in: PubMed
        28. 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 9; 47(49):12942-4.
          View in: PubMed
        29. 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; 3(6):e2403.
          View in: PubMed
        30. 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.
          View in: PubMed
        31. Vollers SS, Stern LJ. Class II major histocompatibility complex tetramer staining: progress, problems, and prospects. Immunology. 2008 Mar; 123(3):305-13.
          View in: PubMed
        32. 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.
          View in: PubMed
        33. 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.
          View in: PubMed
        34. Stern LJ. Characterizing MHC-associated peptides by mass spectrometry. J Immunol. 2007 Sep 1; 179(5):2667-8.
          View in: PubMed
        35. 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.
          View in: PubMed
        36. 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.
          View in: PubMed
        37. 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 7; 8(7):820-7.
          View in: PubMed
        38. 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.
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        39. 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.
          View in: PubMed
        40. 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.
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        41. 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.
          View in: PubMed
        42. 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.
          View in: PubMed
        43. 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 1; 176(3):1498-505.
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        44. Stern LJ, Potolicchio I, Santambrogio L. MHC class II compartment subtypes: structure and function. Curr Opin Immunol. 2006 Feb; 18(1):64-9.
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        45. 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.
          View in: PubMed
        46. 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.
          View in: PubMed
        47. 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.
          View in: PubMed
        48. 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.
          View in: PubMed
        49. 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 8; 102(10):3744-9.
          View in: PubMed
        50. 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.
          View in: PubMed
        51. 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.
          View in: PubMed
        52. 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 7; 101(36):13279-84.
          View in: PubMed
        53. 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.
          View in: PubMed
        54. 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.
          View in: PubMed
        55. 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.
          View in: PubMed
        56. 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 7; 278(45):44904-12.
          View in: PubMed
        57. 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.
          View in: PubMed
        58. 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.
          View in: PubMed
        59. 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 1; 268(1):51-69.
          View in: PubMed
        60. 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 1; 169(5):2264-73.
          View in: PubMed
        61. 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.
          View in: PubMed
        62. 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 1; 168(9):4287-91.
          View in: PubMed
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