Lewis Lanier, PhD

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Lewis Lanier, PhD

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Professor, School of Medicine
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Natural killer (NK) cells are a type of white blood cell that provides protection against microbial pathogens and tumors. Since the early 1980’s, our lab has investigated how NK cells distinguish between normal healthy cells and cells that are transformed or infected with viruses. NK cells express a diverse array of inhibitory and activating receptors on their cells surface that bind to ligands expressed on the cell surface of potential target cells. When encountering healthy cells, signals transmitted by inhibitory NK receptors dominate and prevent autoimmunity, whereas the loss of ligands for the inhibitory receptors or the upregulation of ligands for the activating NK receptors on infected or transformed cells allows NK cells to kill these abnormal cells and secrete cytokine that influence the subsequent response by T cells and B cells. We have developed mouse models systems in which key signaling molecules such as DAP10 and DAP12 have been ablated to explore the physiological role of these NK receptors in resistance to viral infections (cytomegalovirus, poxviruses, and influenza) and primary tumorigenesis.
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  1. Snyder-Cappione JE, Nixon DF, Chi JC, Nguyen ML, Kirby CK, Milush JM, Koth LL. Invariant natural killer T (iNKT) cell exhaustion in sarcoidosis. Eur J Immunol. 2013 Aug; 43(8):2194-205.
    http://www.ncbi.nlm.nih.gov/pubmed/23278897
  2. Benoist C, Lanier L, Merad M, Mathis D, Immunological Genome Project . Consortium biology in immunology: the perspective from the Immunological Genome Project. Nat Rev Immunol. 2012 10; 12(10):734-40.
    http://www.ncbi.nlm.nih.gov/pubmed/22955842
  3. Bezman NA, Kim CC, Sun JC, Min-Oo G, Hendricks DW, Kamimura Y, Best JA, Goldrath AW, Lanier LL, Immunological Genome Project Consortium . Molecular definition of the identity and activation of natural killer cells. Nat Immunol. 2012 Oct; 13(10):1000-9.
    http://www.ncbi.nlm.nih.gov/pubmed/22902830
  4. Thomas MF, Abdul-Wajid S, Panduro M, Babiarz JE, Rajaram M, Woodruff P, Lanier LL, Heissmeyer V, Ansel KM. Eri1 regulates microRNA homeostasis and mouse lymphocyte development and antiviral function. Blood. 2012 Jul 05; 120(1):130-42.
    http://www.ncbi.nlm.nih.gov/pubmed/22613798
  5. Beilke JN, Meagher CT, Hosiawa K, Champsaur M, Bluestone JA, Lanier LL. NK cells are not required for spontaneous autoimmune diabetes in NOD mice. PLoS One. 2012; 7(4):e36011.
    http://www.ncbi.nlm.nih.gov/pubmed/22558306
  6. Park CY, Jeker LT, Carver-Moore K, Oh A, Liu HJ, Cameron R, Richards H, Li Z, Adler D, Yoshinaga Y, Martinez M, Nefadov M, Abbas AK, Weiss A, Lanier LL, de Jong PJ, Bluestone JA, Srivastava D, McManus MT. A resource for the conditional ablation of microRNAs in the mouse. Cell Rep. 2012 Apr 19; 1(4):385-91.
    http://www.ncbi.nlm.nih.gov/pubmed/22570807
  7. Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J Exp Med. 2012 May 07; 209(5):947-54.
    http://www.ncbi.nlm.nih.gov/pubmed/22493516
  8. Ndhlovu LC, Lopez-Vergès S, Barbour JD, Jones RB, Jha AR, Long BR, Schoeffler EC, Fujita T, Nixon DF, Lanier LL. Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood. 2012 Apr 19; 119(16):3734-43.
    http://www.ncbi.nlm.nih.gov/pubmed/22383801
  9. Nielsen N, Ødum N, Ursø B, Lanier LL, Spee P. Cytotoxicity of CD56(bright) NK cells towards autologous activated CD4+ T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLoS One. 2012; 7(2):e31959.
    http://www.ncbi.nlm.nih.gov/pubmed/22384114
  10. Tietze JK, Wilkins DE, Sckisel GD, Bouchlaka MN, Alderson KL, Weiss JM, Ames E, Bruhn KW, Craft N, Wiltrout RH, Longo DL, Lanier LL, Blazar BR, Redelman D, Murphy WJ. Delineation of antigen-specific and antigen-nonspecific CD8(+) memory T-cell responses after cytokine-based cancer immunotherapy. Blood. 2012 Mar 29; 119(13):3073-83.
    http://www.ncbi.nlm.nih.gov/pubmed/22251483
  11. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, Lopez-Vergès S, Lanier LL, Weisdorf D, Miller JS. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood. 2012 Mar 15; 119(11):2665-74.
    http://www.ncbi.nlm.nih.gov/pubmed/22180440
  12. Chen Z, Chen L, Baker K, Olszak T, Zeissig S, Huang YH, Kuo TT, Mandelboim O, Beauchemin N, Lanier LL, Blumberg RS. CEACAM1 dampens antitumor immunity by down-regulating NKG2D ligand expression on tumor cells. J Exp Med. 2011 Dec 19; 208(13):2633-40.
    http://www.ncbi.nlm.nih.gov/pubmed/22143889
  13. Bezman NA, Chakraborty T, Bender T, Lanier LL. miR-150 regulates the development of NK and iNKT cells. J Exp Med. 2011 Dec 19; 208(13):2717-31.
    http://www.ncbi.nlm.nih.gov/pubmed/22124110
  14. Sun JC, Lanier LL. NK cell development, homeostasis and function: parallels with CD8⁺ T cells. Nat Rev Immunol. 2011 Aug 26; 11(10):645-57.
    http://www.ncbi.nlm.nih.gov/pubmed/21869816
  15. ina Höhne, Hildegard Pfister, Tanja Brückl, Petra Zimmermann, Manfred Uhr, Florian Holsboer, Marcus Ising, Sandra Cornelisse, Vanessa A. van Ast, Marian Joëls, Merel Kindt, Nadine Skoluda, Johanna Marie Doerr, Urs Markus Nater, Myriam V. Thoma, Ulrike Ehlert, Barbara Vanaelst, Inge Huybrechts, Karin Bammann, Nathalie Michels, Tineke de Vriendt, Krishna Vyncke, Isabelle Sioen, Licia Iacoviello, Kathrin Gunther, Denes Molnar, Lauren Lissner, Noellie Rivet, Jean-Sebastien Raul, Stefaan de Henauw, Stefanie Eva Mayer, James L. Abelson, Thane Erickson, Hedieh Briggs, Jennifer Crocker, Israel Liberzon, Ingibjörg H. Jonsdottir, Kristina Glise, Gunnar Ahlborg, Anna Sjörs, Magdalena Buckert, Christiane Schwieren, Brigitte M. Kudielka, Christian J. Fiebach, Blake Gurfein, Andrew Stamm, Peter Bacchetti, Mary Dallman, Nachiket Nadkarni, Jeffrey Milush, Chadi Touma, Rupert Palme, Jan Pieter Konsman, Michael Acree, Mary Premenko-Lanier, Nicolas Darcel, Frederick Hecht, Douglas Nixon, Laura Ortega, Rosa Monseny, Itziar Montalvo, Núria Manzanares, Joan Franch, Brian R. Walker, Alfonso Gutiérrez-Zotes, Rebecca M. Reynolds, Javier Labad, Andrea Amaro Quesada, Rosana M. Tristão, Fernanda B. Vianna, Lucas B.D. Barbosa, Igor C. Carneiro, Caroline N. Minchillo, Riccardo Pratesi, Oliver T. Wolf, Nitsan Kozlovsky, Joseph Zohar, Zeev Kaplan, Hagit Cohen, Marcia J. Slattery, Adam J. Grieve, Elliott M. Paletz, Ned H. Kalin, Charissa Andreotti, Paige Garrard, Sneha Venkatraman, Linda Luecken, Bruce Compas, Katri Savolainen, Johan G. Eriksson, Laura Kananen, Eero Kajantie, Iiris Hovatta, Marius Lahti, Jari Lahti, Anu-Katriina Pesonen, Kati Heinonen, Katri Räikkönen, Nagisa Sugaya, Shuhei Izawa, Keisuke Saito, Kentaro Shirotsuki, Shinobu Nomura, Hironori Shimada, Kazutaka Ikeda, Tobias Stalder, Clemens Kirschbaum, Robert Miller, Joachim Fischer, Anne Marita Milde, Tove Saga Nordling, Dag Øystein Nordanger, Kristin J. Ziegler, Jan-Felix Kersten, Schulamith Krüger, Karl-Heinz Schulz, Christoph Heesen, Stefan M. Gold, Jeffrey Milush, Vanessa York, Aric Prather, Douglas Nixon, Hecht Frederick, Elissa S. Epel, Nina Alexander, Franziska Rosenlöcher, Tobias Stalder, Julia Linke, Wolfgang Distler, Joachim Morgner, Clemens Kirschbaum, Mary Eileen Saczawa, Julia. A. Graber, Jeanne Brooks-Gunn, Malak Abu Shakra, Jens C. Pruessner, Alain Dagher, Marco Leyton, Robert Pihl, Owen M. Wolkowitz, Synthia H. Mellon, Yali Su, Victor I. Reus, Scott Mackin, Heather M. Burke, Rebecca Rosser, John Coetzee, Elissa S. Epel, Steven P. Hamilton, Craig J. Nelson, Laura Mahan, Michelle Coy, Michael W. Weiner, Susanne Mueller, Hannah Bruehl, Peter N.C. Mohr, Alex Hatri, Hauke R. Heekeren, Owen M. Wolkowitz, Jodie Bryk, Synthia H. Mellon, Elissa S. Epel, Elizabeth H. Blackburn, Jue Lin, Robert H. Lustig, Peter J. Havel, Victor I. Reus, Heather M. Burke, Rebecca Rosser, John Coetzee, Laura Mahan, Michelle Coy, Steven P. Hamilton, Craig J. Nelson, Agorastos Agorastos, Oliver Stiedl, Judith A. Boel, Pia S. Heppner, Torben Hager, Tobias Moeller-Bertram, Uzair Haji, Arame Motazedi, Dewleen G. Baker, Danielle Gianferante, Myriam V. Thoma, Juliette Saltz, Brian Dahlben, Holly Beaulac, Nicolas Rohleder, Chia-Ying Chou, Roberto La Marca, Andrew Steptoe, Chris R. Brewin, Jessie Frijling, Mirjam van Zuiden, Saskia Koch, Laura Nawijn, Dick Veltman, Miranda Olff, Anna Sjörs, Per-Anders Jansson, Jan W. Eriksson, Ingibjörg H. Jonsdottir, Tony W. Buchanan, Christina N. White, Mary Kralemann, Stephanie D. Preston, Victor L. Kallen, Jan-Willem Mark, Luc Bischoff, Ben van Ommen, Nico van Meeteren, Marie-France Marin, Catherine Raymond, Julie-Katia Morin-Major, Anne Hand, Robert-Paul Juster, Shireen Sindi, Sonia J. Lupien, Jinshia Ly, Sivan Rotenberg, Jennifer J. McGrath, Yrsa Bergmann Sverrisdóttir, Anna-Karin Lennartsson, Ingibjörg H. Jonsdottir, Pelle de Koning, Robert-Paul Juster, Nathan G. Smith, Philip J. Johnson, Jean-Philippe Lefebvre-Louis, Marie-France Marin, Shireen Sindi, Jens C. Pruessner, Sonia. POSTERS. European Journal of Psychotraumatology. 2012 Dec 1; 3(1):19557.
    http://www.ncbi.nlm.nih.gov/pubmed/21825173
  16. Nakano-Yokomizo T, Tahara-Hanaoka S, Nakahashi-Oda C, Nabekura T, Tchao NK, Kadosaki M, Totsuka N, Kurita N, Nakamagoe K, Tamaoka A, Takai T, Yasui T, Kikutani H, Honda S, Shibuya K, Lanier LL, Shibuya A. The immunoreceptor adapter protein DAP12 suppresses B lymphocyte-driven adaptive immune responses. J Exp Med. 2011 Aug 01; 208(8):1661-71.
    http://www.ncbi.nlm.nih.gov/pubmed/21727189
  17. Fang M, Orr MT, Spee P, Egebjerg T, Lanier LL, Sigal LJ. CD94 is essential for NK cell-mediated resistance to a lethal viral disease. Immunity. 2011 Apr 22; 34(4):579-89.
    http://www.ncbi.nlm.nih.gov/pubmed/21439856
  18. Barao I, Alvarez M, Ames E, Orr MT, Stefanski HE, Blazar BR, Lanier LL, Anderson SK, Redelman D, Murphy WJ. Mouse Ly49G2+ NK cells dominate early responses during both immune reconstitution and activation independently of MHC. Blood. 2011 Jun 30; 117(26):7032-41.
    http://www.ncbi.nlm.nih.gov/pubmed/21498673
  19. Sun JC, Lopez-Verges S, Kim CC, DeRisi JL, Lanier LL. NK cells and immune "memory". J Immunol. 2011 Feb 15; 186(4):1891-7.
    http://www.ncbi.nlm.nih.gov/pubmed/21289313
  20. Sun JC, Beilke JN, Bezman NA, Lanier LL. Homeostatic proliferation generates long-lived natural killer cells that respond against viral infection. J Exp Med. 2011 Feb 14; 208(2):357-68.
    http://www.ncbi.nlm.nih.gov/pubmed/21262959
  21. Hesslein DG, Palacios EH, Sun JC, Beilke JN, Watson SR, Weiss A, Lanier LL. Differential requirements for CD45 in NK-cell function reveal distinct roles for Syk-family kinases. Blood. 2011 Mar 17; 117(11):3087-95.
    http://www.ncbi.nlm.nih.gov/pubmed/21245479
  22. Kogure A, Shiratori I, Wang J, Lanier LL, Arase H. PANP is a novel O-glycosylated PILRα ligand expressed in neural tissues. Biochem Biophys Res Commun. 2011 Feb 18; 405(3):428-33.
    http://www.ncbi.nlm.nih.gov/pubmed/21241660
  23. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science. 2011 Jan 07; 331(6013):44-9.
    http://www.ncbi.nlm.nih.gov/pubmed/21212348
  24. Orr MT, Lanier LL. Inhibitory Ly49 receptors on mouse natural killer cells. Curr Top Microbiol Immunol. 2011; 350:67-87.
    http://www.ncbi.nlm.nih.gov/pubmed/20680808
  25. Orr MT, Lanier LL. Natural killer cell licensing during viral infection. Adv Exp Med Biol. 2011; 780:37-44.
    http://www.ncbi.nlm.nih.gov/pubmed/21842363