Usern_member

Jonathan Howard

USERN Advisory Board USERN Policy Making Council

Jonathan Howard is a cell geneticist who has made important contributions through his studies in rats to our understanding of immunogenetics — the interplay between the immune system and genetics. He also identified the transporters required for major histocompatibility complex (MHC) class I assembly, which opened up transport and assembly of membrane proteins as a new and exciting area of research.


His wide-ranging work included breeding congenic and recombinant strains of rat for use in MHC studies, as well as defining the MHC class I and class II regions at the molecular level. More recently, his research has concentrated on the role of immunity related GTPases in facilitating the resistance of mice to the protozoan pathogen, Toxoplasma gondii.


Jonathan has held the membership of and chaired several influential European scientific advisory boards, including the Medical Research Council. He is also the author of the book Darwin: A Very Short Introduction (2001), and has published a significant number of scientific papers.


In the laboratory led by Jonathan Howard, they study the mechanisms of resistance to the intracellular protozoan parasite, Toxoplasma gondii , a relative of malaria, which infects about 40% of the human species. The research group focuses on studying the immunity of mice against T. gondii because the primary hosts of the parasite, in which it produces gametes and makes meiosis, are cats. Therefore, the life cycle of T. gondii  and its abundance in the environment, are caused by an infectious cycle between cat and rat.


The immunity of mice against T. gondii is based on a mechanism absent in humans, the action of GTPases induced by gamma interferon (IRG proteins), which cooperatively destroy the vacuole in which the parasite lives. This mechanism, in turn, is the target of virulent parasites, which have a family of kinases responsible for the inactivation of IRG proteins. Both IRG proteins and kinases are massively polymorphic, consistent with a complex co-evolutionary dynamics.


The work of this research group covers ecological studies in wild mice, biological, biochemical and structural studies.

Education:

University of Oxford: Oxford, Oxfordshire, GB
1966 to 1969 | D. Phil. (Medicine) Oxford  (Cellular Aspects of Antibody Formation“ Supervisor Prof. JL Gowans, MRC Cellular Immunology Unit, Sir William Dunn School of Pathology)

Orissa University of Agriculture and Technology: Bhubaneswar, Orissa, IN
1964 to 1965 | Royal Society Leverhulme Scholarship, Genetics and Biometry Laboratory

University of Oxford: Oxford, Oxfordshire, GB
1961 to 1964 | BA (Zoology)

Employment:


1969-1973 Member of Scientific Staff, MRC Cellular Immunology Unit, Oxford.
1971-1977 Post-Doc, Adjunct Assistant and Adjunct Associate Professor, Department of Pathology, University of Pennsylvania, Philadelphia (Dr DB Wilson)
1974-1994 Member of Staff and from 1986 Head of the Department of Immunology, The Babraham Institute, Cambridge
1994-present Professor of Cell Genetics (C4), Institute for Genetics, University of Cologne
2012-present Managing Director at Instituto Gulbenkian de Ciência (IGC)

Sabbaticals:


1981 Department of Pathology, Stanford University (Dr IL Weissman)
1981 Division of Biology, Cal. Inst. Technology (Dr LE Hood)
1986 Department of Structural Biology, Stanford University (Dr P Parham)
1992 Cell Biology, EMBL Heidelberg (Dr B Dobberstein)
2004 Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge (Dr HT McMahon)

Awards:

1971 Fulbright Scholarship
1970-1973 Weir Junior Research Fellowship, University College, Oxford
1974-1979 Research Fellow, Clare Hall, Cambridge
1993 EMBO member
1995 Fellow of Royal Society (FRS)
2007 Member Academia Europaea
2011 Donald Gordon Fellow, Stellenbosch Institute for Advanced Study (STIAS)

Membership of significant decision-making bodies since moving to Germany in 1994:
1994-1995 Member, Cell and Molecular Biology Board, Medical Research Council, UK
1996-1999 Member, later Chairman, Sectional Committee 7, Royal Society, London
1996-1999 Molecular Biology Grants Committee, Human Frontiers Science Programme (HFSP), Strassburg.
1996-present Member, now Chairman, Scientific Advisory Board, CNRS-INSERM Institut d’Immunologie Marseille-Luminy, France
1996-2004 Member, Scientific Advisory Board, Max Planck Institute for Immunobiology, Freiburg
2002-2005 Member, Courses and Workshops Committee, EMBO, Heidelberg
2004-present Member, Board of Trustees, Max Planck Institute for Plant Breeding, Cologne, Germany
2004-present Member, Scientific Advisory Board, Gulbenkian Institute of Sciences, Lisbon, Portugal
2004 Max Planck Society Research Field Rapporteur (with Prof. Guenther Schütz)
2005-2007 Member, Sectional Committee 7, Royal Society, London
2007-present Member, SNWG selection committee of the MPG
2008-present Member, University Research Fellowships Committee, Royal Society
2009- Member, Acting Chairman, Scientific Advisory Board, Max Planck Institute for Developmental Biology, Tübingen

Several Publications:

Book:
"Darwin", Oxford University Press, 1st edn 1982, 2nd edn 2001

Papers:
Lilue J, Müller UB, Steinfeldt T, Howard JC. (2013) Reciprocal virulence and resistance polymorphism in the relationship between Toxoplasma gondii and the house mouse. eLife. 2013 Oct 29;2:e01298. doi: 10.7554/eLife.01298.
Springer HM, Schramm M, Taylor GA, Howard JC. (2013) Irgm1 (LRG-47), a regulator of cell-autonomous immunity, does not localize to mycobacterial or listerial phagosomes in IFN-γ-induced mouse cells. J Immunol. Aug 15;191(4):1765-74
Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Könen-Waisman S, Latham SM, Mourier T, Norton R, Quail MA, Sanders M, Shanmugam D, Sohal A, Wasmuth JD, Brunk B, Grigg ME, Howard JC, Parkinson J, Roos DS, Trees AJ, Berriman M, Pain A, Wastling JM. (2012) Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Pathog. 8(3):e1002567
The arginine-rich N-terminal domain of ROP18 is necessary for vacuole targeting and virulence of Toxoplasma gondii. (2012) Fentress SJ, Steinfeldt T, Howard JC, Sibley LD. Cell Microbiol. Dec;14(12):1921-33
Fleckenstein MC, Reese ML, Könen-Waisman S, Boothroyd JC, Howard JC, Steinfeldt T. (2012) A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol. 10(7): e1001358
Howard JC, Hunn JP, Steinfeldt T. (2011) The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr Opin Microbiol. Aug;14(4):414-21
Traver MK, Henry SC, Cantillana V, Oliver T, Hunn JP, Howard JC, Beer S, Pfeffer K, Coers J, Taylor GA. (2011) Immunity-related GTPase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy. J Biol Chem. Sep 2;286(35):30471-80.
Christoph Rohde, Julia P. Hunn, Andreas Meinhardt, Jonathan C. Howard (2011) The conserved Immunity-related GTPase IRGC/Irgc is expressed in haploid spermatids. (Manuscript awaiting submission)
Liesenfeld, O, Parvanova, IA, Zerrahn, J, Han, SJ, Heinrich, F, Munoz, M, Kaiser, F, Aebischer, T, Buch,, T, Waisman, A, Reichmann, G, Utermöhlen, O, von Stebut, E, Bogdan, C, Specht, S, Saeftel, M, Hoerauf, A, Mota, M, Könen-Waisman, S, Kaufmann, SHE, Howard, JC (2011) Irga6/IIGP contributes to in vivo resistance against Toxoplasma gondii infection but not to resistance against other intracellular pathogens including Plasmodium berghei. PLoS One, in press
Nikolaus Pawlowski, Aliaksandr Khaminets, Julia P. Hunn, Natasa Papic, Andreas Schmid, Revathy C. Uthaiah, Rita Lange, Gaby Vopper, Sascha Martens, Eva Wolf, Jonathan C. Howard (2011) The Activation Mechanism of Irga6, an Interferon-Inducible GTPase Contributing to Mouse Resistance against Toxoplasma gondii. BMC Biology 9:7.
Hunn, JP, Feng, CG, Sher, A, Howard, JC. (2011) The Immunity-Related GTPases in Mammals - a fast Evolving Cell-Autonomous Resistance System against Intracellular Pathogens. Mammalian Genome, 22(1-2):43-54. Epub 2010 Oct 30. PMID: 21052678
Zeng, J and Howard, JC (2010) Spontaneous focal activation of iNKT cells in mouse liver and kidney. BMC Biology BMC Biology 2010, 8:142doi:10.1186/1741-7007-8-142
Tobias Steinfeld, Stephanie Könen-Waisman, Lan Tong, Nikolaus Pawlowski, Tobias Lamkemeyer, L. David Sibley, Julia P. Hunn, Jonathan C. Howard (2010) Phosphorylation of IRG resistance proteins is an evasion strategy for virulent T. gondii strains. PLoS Biology 8(12): e1000576. doi:10.1371/journal.pbio.1000576
Melo, M, Kasperowitz, P, Cerny, A, Könen-Waisman, S, Kurt-Jones, E, Lien, E, Beutler, B, Howard, JC, Golenbock, D, Gazzinelli, R. (2010) UNC93B1 mediates host resistance to infection with Toxoplasma gondii. PLoS Pathogens 6(8): e1001071. doi:10.1371/journal.ppat.1001071
Nikolaus Pawlowski (2010) Dynamin self-assembly and the vesicle fission mechanism: structural insights into the large atypical GTPases. BioEssays 32:1033-1039
Hunn, JP, Howard, JC (2010) The mouse resistance protein, Irgm1 (LRG-47): a regulator or an effector of pathogen defense PLOS Pathogens P6(7): e1001008. doi:10.1371/journal.ppat.1001008
Khaminets, A, Könen-Waisman, S, Hunn JP, Zhao, YO, Preukschat, D, Coers J, Boyle, JP, Ong YC, Boothroyd JC, Reichmann G, Howard, JC (2010) Coordinated loading of multiple IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cellular Microbiology 12(7):939-61, PMID: 20109161
Zhao, YO, Könen-Waisman, S, Taylor, GA, Martens, S, Howard, JC (2010) Localisation and mis-localisation of the interferon-inducible immunity-related GTPase, Irgm1 (LRG-47) in mouse cells. PLoS One Jan 13;5(1):e8648
Lapaque, N, Muller, A, Alexopolou, L, Howard, JC, Gorvel, JP (2009) Brucella abortus induces Irgm3 and Irga6 expression via Type-I IFN by a MyD88-dependent pathway, without the requirement of TLR2, TLR4, TLR5 and TLR9. Microbial Pathogenesis, ePub 09 Sept 09. doi:10.1016/j.micpath.2009.09.005
Zeng, J, Parvanova, IA, Howard, JC (2009) A dedicated promoter drives constitutive expression of the cell-autonomous immune resistance GTPase, Irga6 (IIGP1) in mouse liver. PLOS One, 4(8): e6787. doi:10.1371/journal.pone.0006787
Howard JC 2009 Why didn’t Darwin discover Mendel’s Laws? J. Biol. 8:15
Henry SC, Daniell XG, Burroughs AR, Indaram M, Howell DN, Coers J, Starnbach MN, Hunn JP, Howard JC, Feng CG, Sher A, Taylor GA. 2009 Balance of Irgm protein activities determines IFN-{gamma}-induced host defense. J Leukoc Biol. Jan 27 PMID: 19176402 (5)
Bekpen C, Marques-Bonet T, Alkan C, Antonacci F, Leogrande MB, Ventura M, Kidd JM, Siswara P, Howard JC, Eichler EE 2009 Death and Resurrection of the Human IRGM Gene. PLOS Genetics PLoS Genet 5(3): e1000403. doi:10.1371/journal.pgen.1000403 (11)
Zhao, YO, Khaminets, A, Howard, JC 2009 Disruption of the Toxoplasma gondii Parasitophorous Vacuole by Immunity-related GTPases (IRG proteins) Causes Necrotic Death in IFN?-induced Cells. PLoS Pathog 5(2): e1000288. doi:10.1371 (13)
Zhao YO, Rohde C, Lilue JT, Könen-Waisman S, Khaminets A, Hunn JP, Howard JC. 2009 Toxoplasma gondii and the IRG (Immunity-Related GTPase) resistance system in mice: a review. Memorias do Instituto Oswaldo Cruz. 104(2):234-40.
Zhao Y, Ferguson DJ, Wilson DC, Howard JC, Sibley LD, Yap GS. 2009 . Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. J Immunol. Mar 15;182(6):3775-81.
Coers J, Starnbach MN, Howard, JC. 2009 Modeling infectious disease in mice: co-adaptation and the role of host-specific IFNg responses. PLOS Pathogens. 5(5): e1000333. doi:10.1371/journal.ppat.1000333 (1)
Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC. 2008 . Inactive and active states of the interferon-inducible resistance GTPase, Irga6, In Vivo. J Biol Chem. 2008 Nov 14;283(46):32143-51 (5)
Hunn, J, Koenen-Waisman, S, Papic, N, Schroeder, N, Pawlowski, N, Lange, R, Kaiser, F, Zerrahn, J, Martens, S and Howard JC. 2008 Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO Journal, 27(19):2495-509 (11)
Howard, JC. 2008 . The IRG proteins: A function in search of a mechanism. Immunobiology 213:367-375 (9)
Coers J, Bernstein-Hanley I, Grotsky D, Parvanova I, Howard JC, Taylor GA, Dietrich WF, Starnbach MN. 2008 Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J Immunol. 180(9):6237-45. (18)
Deverson EV, Gow IR, Coadwell WJ, Monaco JJ, Butcher GW, Howard JC. 2008 Pillars Article: MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters. 1990. Nature 348: 738-41. Classical article. J Immunol 180(5):2729-32
Howard, JC (2007) Cell-autonomous immunity. Microbes and Infection 9(14-15):1633-5
Könen-Waisman, S and Howard, JC (2007) Cell-autonomous immunity to Toxoplasma gondii in mouse and man. Microbes and Infection 9(14-15):1652-61 (9)
Howard JC, Jack RS. (2007) Evolution of immunity and pathogens Eur J Immunol. 37(7):1721-3.
Martens S and Howard JC (2006) The interferon-inducible GTPases. Annu. Rev. Cell Dev. Biol. 22:559-590 (37)
Lapaque, N, Takeuchi, O, Corrales, F, Akira, S, Moriyon, I, Howard, JC, Gorvel, JP. 2006 . Differential inductions of TNF and IGTP, IIGP by structurally diverse classic and non-classiclipopolysaccharides. Cellular Microbiology 8:401-413 (20)
Bekpen, C, Hunn, JP, Rohde, C, Parvanova, I, Guethlein, L, Dunn, DM, Glowalla, E, Leptin, M, Howard, JC. 2005 The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell-autonomous resistance mechanism in the human lineage. Genome Biology, 6(11):R92 (66)
Martens, S, Parvanova, I, Zerrahn, J, Griffiths, G, Schell, G, Reichman, G, Howard, JC. 2005 Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47 resistance GTPases. PLOS Pathogens, 1(3):e24 (73)
Ghosh A, Uthaiah R, Howard JC, Herrmann C, and Wolf E. 2004 Crystal Structure of IIGP1: A Paradigm for Interferon-Inducible p47 Resistance GTPases. Molecular Cell 15:727-739 (21)
Martens S, Sabel K, Lange R, Uthaiah R, Wolf E, Howard JC. 2004 Mechanisms regulating the positioning of mouse p47 resistance GTPases LRG-47 and IIGP1 on cellular membranes: retargeting to plasma membrane induced by phagocytosis. J Immunol. 173(4):2594-606. (42)
Klamp T, Boehm U, Schenk D, Pfeffer K, Howard JC. 2003 A giant GTPase, very large inducible GTPase-1, is inducible by IFNs.J Immunol. 171(3):1255-65. (16)
Uthaiah RC, Praefcke GJ, Howard JC, Herrmann C. 2003 IIGP1, an interferon-gamma-inducible 47-kDa GTPase of the mouse, showing cooperative enzymatic activity and GTP-dependent multimerization. J Biol Chem. 278(31):29336-43. (32)
Wettey FR, Hawkins SF, Stewart A, Luzio JP, Howard JC, Jackson AP. 2002 . Controlled elimination of clathrin heavy-chain expression in DT40 lymphocytes. Science. 297(5586):1521-5. (50)
Alberts P, Daumke O, Deverson EV, Howard JC, Knittler MR. 2001 Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr Biol. 11(4):242-51. (41)
Guethlein LA, Howard JC. 2000 Is a mutator analogous to the Ig hypermutator of the sheep ileal Peyer's patch active on MHC class I genes in the germ line? Immunogenetics. 51(6):462-72.
Martinsohn JT, Sousa AB, Guethlein LA, Howard JC. 1999 The gene conversion hypothesis of MHC evolution: a review. Immunogenetics. 50(3-4):168-200. Review. Erratum in: Immunogenetics 2000 Jun;51(7):613. (67)
Knittler MR, Alberts P, Deverson EV, Howard JC. 1999 Nucleotide binding by TAP mediates association with peptide and release of assembled MHC class I molecules. Curr Biol. 9(18):999-1008. (55)
Boehm U, Guethlein L, Klamp T, Ozbek K, Schaub A, Futterer A, Pfeffer K, Howard JC. 1998 Two families of GTPases dominate the complex cellular response to IFN-gamma. J Immunol. 161(12):6715-23. (130)
Knittler MR, Gulow K, Seelig A, Howard JC. 1998 MHC class I molecules compete in the endoplasmic reticulum for access to transporter associated with antigen processing. J Immunol. 161(11):5967-77. (30)
Joly E, Le Rolle AF, Gonzalez AL, Mehling B, Stevens J, Coadwell WJ, Hunig T, Howard JC, Butcher GW. 1998 Co-evolution of rat TAP transporters and MHC class I RT1-A molecules.Curr Biol. 8(3):169-72. (47)
Deverson EV, Leong L, Seelig A, Coadwell WJ, Tredgett EM, Butcher GW, Howard JC. 1998 Functional analysis by site-directed mutagenesis of the complex polymorphism in rat transporter associated with antigen processing. J Immunol. 160(6):2767-79. (28)
Lambracht D, Wonigeit K, Howard JC, Fischer Lindahl K. Markers for interspecies relationship in the RT1 complex.Transplant Proc. 1997 May;29(3):1665-7.
Cresswell P, Howard JC. Antigen recognition. Curr Opin Immunol. 1997 Feb;9(1):71-4. Review. (23)
Howard JC. Contemplations on the evolution of pro- and eukaryotic mono(ADP-ribosyl) transferases in the context of the immune system. Adv Exp Med Biol. 1997 ;419:453-8. Review. (3)
Boehm U, Klamp T, Groot M, Howard JC. 1997 Cellular responses to interferon-gamma. Annu Rev Immunol.;15:749-95. (1753)
Powis SJ, Young LL, Joly E, Barker PJ, Richardson L, Brandt RP, Melief CJ, Howard JC, Butcher GW. The rat cim effect: TAP allele-dependent changes in a class I MHC anchor motif and evidence against C-terminal trimming of peptides in the ER.Immunity. 1996 Feb;4(2):159-65. (89)
Howard JC. Supply and transport of peptides presented by class I MHC molecules.Curr Opin Immunol. 1995 Feb;7(1):69-76. Review. (81)
Wang CR, Lambracht D, Wonigeit K, Howard JC, Lindahl KF. Rat RT1 orthologs of mouse H2-M class Ib genes. Immunogenetics. 1995 ;42(1):63-7. (24)
Thorpe CJ, Moss DS, Powis SJ, Howard JC, Butcher GW, Travers PJ. An analysis of the antigen binding site of RT1.Aa suggests an allele-specific motif. Immunogenetics. 1995 ;41(5):329-31. (8)
Joly E, Clarkson C, Howard JC, Butcher GW. Isolation of a functional cDNA encoding the RT1.Au MHC class I heavy chain by a novel PCR-based method. Immunogenetics. 1995 ;41(5):326-8. (36)
Momburg F, Roelse J, Howard JC, Butcher GW, Hammerling GJ, Neefjes JJ. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature. 1994 Feb 17;367(6464):648-51. (244)
Joly E, Deverson EV, Coadwell JW, Gunther E, Howard JC, Butcher GW. The distribution of Tap2 alleles among laboratory rat RT1 haplotypes. Immunogenetics. 1994 ;40(1):45-53. (39)
Ossevoort MA, Sijts AJ, van Veen KJ, Momburg F, Hammerling GJ, Seelig A, Butcher GW, Howard JC, Kast WM, Melief CJ. Differential effect of transporter Tap 2 gene introduction into RMA-S cells on viral antigen processing. Eur J Immunol. 1993 Dec;23(12):3082-8. (70)
Powis SJ, Young LL, Barker PJ, Richardson L, Howard JC, Butcher GW. Major histocompatibility complex-encoded ABC transporters and rat class I peptide motifs. Transplant Proc. 1993 Oct;25(5):2752-3. (15)
Howard JC, Seelig A. Antigen processing. Peptides and the proteasome. Nature. 1993 Sep 16;365(6443):211-2. (9)
Howard JC. Restrictions on the use of antigenic peptides by the immune system. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3777-9. Review. 22)
Yousaf N, Howard JC, Williams BD. Complement-dependent synergistic effects of rat monoclonal IgG antibodies in vivo. Eur J Immunol. 1993 Feb;23(2):369-75.
Ahmad I, Howard JC, Ng YK, Iannaccone PM. Chimeric drift in blood cell populations of chimeric rats constructed between congenic strains. Pathobiology. 1993 ;61(2):117-22.
Momburg F, Ortiz-Navarrete V, Neefjes J, Goulmy E, van de Wal Y, Spits H, Powis SJ, Butcher GW, Howard JC, Walden P, et al. Proteasome subunits encoded by the major histocompatibility complex are not essential for antigen presentation. Nature. 1992 Nov 12;360(6400):174-7.(179)
Jameson SC, Tope WD, Tredgett EM, Windle JM, Diamond AG, Howard JC. Cloning and expression of class I major histocompatibility complex genes of the rat. J Exp Med. 1992 Jun 1;175(6):1749-57. (39)
Powis SJ, Deverson EV, Coadwell WJ, Ciruela A, Huskisson NS, Smith H, Butcher GW, Howard JC. Effect of polymorphism of an MHC-linked transporter on the peptides assembled in a class I molecule. Nature. 1992 May 21;357(6375):211-5. (285)
Ballingall KT, Wright H, Redmond J, Dutia BM, Hopkins J, Lang J, Deverson EV, Howard JC, Puri N, Haig D. Expression and characterization of ovine major histocompatibility complex class II (OLA-DR) genes. Anim Genet. 1992 ;23(4):347-59. (28)
Powis SJ, Townsend AR, Deverson EV, Bastin J, Butcher GW, Howard JC. Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature. 1991 Dec 19-26;354(6354):528-31. (259)
Howard JC. Immunology. Disease and evolution. Nature. 1991 Aug 15;352(6336):565-7. (41) .
Yousaf N, Howard JC, Williams BD. Targeting behavior of rat monoclonal IgG antibodies in vivo: role of antibody isotype, specificity and the target cell antigen density. Eur J Immunol. 1991 Apr;21(4):943-50. (9)
Powis SJ, Howard JC, Butcher GW. The major histocompatibility complex class II-linked cim locus controls the kinetics of intracellular transport of a classical class I molecule. J Exp Med. 1991 Apr 1;173(4):913-21. (35)
Deverson EV, Wright H, Watson S, Ballingall K, Huskisson N, Diamond AG, Howard JC. Class II major histocompatibility complex genes of the sheep. Anim Genet. 1991 ;22(3):211-25. (20)
Livingstone AM, Powis SJ, Gunther E, Cramer DV, Howard JC, Butcher GW. Cim: an MHC class II-linked allelism affecting the antigenicity of a classical class I molecule for T lymphocytes. Immunogenetics. 1991 ;34(3):157-63. (31)
van den Bogaerde J, Howard JC. Xenogeneic responses in vitro in the Syrian hamster, Mesocricetus auratus. I. Evidence for a normal T cell repertoire. Int Immunol. 1991 Jan;3(1):49-56.
Deverson EV, Gow IR, Coadwell WJ, Monaco JJ, Butcher GW, Howard JC. MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters. Nature. 1990 Dec 20-27;348(6303):738-41. (323)
Powis CJ, Howard JC, Butcher GW. Variation in the biosynthesis of the rat RT1.Aa classical class I antigen due to the cim system. Transplant Proc. 1990 Dec;22(6):2517-8. .
Jameson SC, Rada C, Lorenzi R, Diamond AG, Butcher GW, Howard JC. Cloning, expression, and evolution of rat classical and nonclassical class I genes. Transplant Proc. 1990 Dec;22(6):2510-1.(3)
Rada C, Lorenzi R, Powis SJ, van den Bogaerde J, Parham P, Howard JC. Concerted evolution of class I genes in the major histocompatibility complex of murine rodents. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2167-71. (105)
Livingstone AM, Powis SJ, Diamond AG, Butcher GW, Howard JC. A trans-acting major histocompatibility complex-linked gene whose alleles determine gain and loss changes in the antigenic structure of a classical class I molecule. J Exp Med. 1989 Sep 1;170(3):777-95. (70)
Diamond AG, Hood LE, Howard JC, Windle M, Winoto A. The class II genes of the rat MHC. J Immunol. 1989 May 1;142(9):3268-74. (28)
Howard JC. The new pragmatics of immunology. Cold Spring Harb Symp Quant Biol. 1989 ;54 Pt 2:947-57. (1)
Iannaccone PM, Howard JC, Berkwits L. Mosaic pattern and lineage analysis in chimeras. Cell Differ Dev. 1988 Nov;25 Suppl:77-90. Review. (3)
Yousaf N, Howard JC, Williams BD. Studies in the rat of antibody-sensitized and N-ethylmaleimide-treatederythrocyte clearance by the liver: effects of immune complex infusion and complement activation. Immunology. 1988 Jun;64(2):193-9.
Howard JC. Molecular evolution. How old is a polymorphism? Nature. 1988 Apr 14;332(6165):588-90.
Yousaf N, Howard JC, Williams BD. Studies in cobra venom factor treated rats of antibody coated erythrocyte clearance by the spleen: differential influence of red blood cell antigen number on the inhibitory effects of immune complexes on Fc dependent clearance. Clin Exp Immunol. 1986 Dec;66(3):654-60.
Yousaf N, Howard JC, Williams BD. Studies in the rat of antibody-coated and N-ethylmaleimide-treated erythrocyte clearance by the spleen. II. Effects of immune complex infusion. Immunology. 1986 Sep;59(1):81-5.
Yousaf N, Howard JC, Williams BD. Studies in the rat of antibody-coated and N-ethylmaleimide-treated erythrocyte clearance by the spleen. I. Effects of in vivo complement activation. Immunology. 1986 Sep;59(1):75-9. (5)
Watts C, Howard JC. Membrane recycling and antigen presentation. Bioessays. 1986 Jun;4(6):265-7.
Hughes-Jones NC, Gorick BD, Howard JC, Feinstein A. Antibody density on rat red cells determines the rate of activation of the complement component C1. Eur J Immunol. 1985 Oct;15(10):976-80. (9)
Howard JC. Immunological help at last. Nature. 1985 Apr 11-17;314(6011):494-5. .
Weinberg WC, Howard JC, Iannaccone PM. Histological demonstration of mosaicism in a series of chimeric rats produced between congenic strains. Science. 1985 Feb 1;227(4686):524-7.(37)
Hughes-Jones NC, Gorick BD, Miller NG, Howard JC. IgG pair formation on one antigenic molecule is the main mechanism of synergy between antibodies in complement-mediated lysis. Eur J Immunol. 1984 Nov;14(11):974-8.
Hughes-Jones NC, Feinstein A, Richardson NE, Gorick BD, Howard JC. C1 activation by immunoglobulin and immunoglobulin antibodies. Biochem Soc Trans. 1984 Oct;12(5):738-9.
Diamond AG, Larkins AP, Wright B, Ellis ST, Butcher GW, Howard JC. The alloantigenic organization of RT1Aa, a class I major histocompatibility complex molecule of the rat. Eur J Immunol. 1984 May;14(5):405-12. (33)
Diamond AG, Butcher GW, Howard JC. Localized conformational changes induced in a class I major histocompatibility antigen by the binding of monoclonal antibodies. J Immunol. 1984 Mar;132(3):1169-75.(19)
Feeney AJ, Corvalan JR, Matzinger P, Howard JC. T helper cells required for the in vitro primary antibody response to SRBC are neither SRBC-specific nor MHC-restricted. J Mol Cell Immunol. 1984 ;1(4):211-22.
Hughes-Jones NC, Gorick BD, Howard JC. The mechanism of synergistic complement-mediated lysis of rat red cells by monoclonal IgG antibodies. Eur J Immunol. 1983 Aug;13(8):635-41. (48)
Howard JC. The major histocompatibility complex of the rat: a partial review. Metabolism. 1983 Jul;32(7 Suppl 1):41-50. Review. (26)
Butcher GW, Howard JC. Genetic control of transplant rejection. Transplantation. 1982 Oct;34(4):161-6. Review. (74)
Butcher GW, Corvalan JR, Licence DR, Howard JC. Immune response genes controlling responsiveness to major transplantation antigens. Specific major histocompatibility complex-linked defect for antibody responses to class I alloantigens. J Exp Med. 1982 Jan 1;155(1):303-20.
Howard JC, Butcher GW. The mechanism of graft rejection and the concept of antigenic strength. Scand J Immunol. 1981 Dec;14(6):687-91.(24) .
Howard JC A tropical volute shell and the Icarus syndrome. 1981 Nature 290: 441–442
Smith RN, Howard JC. Heterogeneity of the tolerant state in rats with long established skin grafts. J Immunol. 1980 Nov;125(5):2289-94.(15)
Howard JC, Butcher GW, Licence DR, Galfre G, Wright B, Milstein C. Isolation of six monoclonal alloantibodies against rat histocompatibility antigens: clonal competition. Immunology. 1980 Sep;41(1):131-41. (20)
Galfre G, Butcher GW, Howard JC, Wilde CD, Milstein C. Clonal competition and stability of hybrid myelomas of mouse and rat origin. Transplant Proc. 1980 Sep;12(3):371-5.
Antczak DF, Howard JC. Analysis of lymphocytes reactive to histocompatibility antigens. IV. Detection of inclusion among allo-reactive lymphocyte populations by specific enrichment for reactive cells. Cell Immunol. 1979 Aug;46(1):127-37.
Antczak DF, Howard JC. Analysis of lymphocytes reactive to histocompatibility antigens. III. Detection of inclusion among allo-reactive lymphocyte populations by specific depletion of reactive cells. Cell Immunol. 1979 Aug;46(1):119-26.
Howard JC, Corvalan JR. Demonstration of MHC-specific haemolytic plaque-forming cells. Nature. 1979 Mar 29;278(5703):449-51.
Antczak DF, Howard JC. Analysis of lymphocytes reactive to histocompatibility antigens. II. Exponential alloantigen-dependent lymphocyte growth in vitro. Cell Immunol. 1979 Mar 15;43(2):317-25. (3)
Antczak DF, Brown D, Howard JC. Analysis of lymphocytes reactive to histocompatibility antigens. I. A quantitative titration assay for mixed lymphocyte interactions in the rat. Cell Immunol. 1979 Mar 15;43(2):304-16. (14)
Howard JC, Butcher GW, Galfre G, Milstein C, Milstein CP. Monoclonal antibodies as tools to analyze the serological and genetic complexities of major transplantation antigens. Immunol Rev. 1979 ;47:139-74. Review. (97)
Gallico GG, Butcher GW, Howard JC. The role of subregions of the rat major histocompatibility complex in the rejection and passive enhancement of renal allografts. J Exp Med. 1979 Jan 1;149(1):244-53.(30)
Antczak DF, Howard JC. Allo-antigen specific lymphocyte growth in vitro [proceedings J Physiol. 1978 Nov;284:6P-7P.
Corvalan JR, Howard JC. Primary in vitro antibody formation in the rat: partial characterization and properties of an inhibitor cell present in normal spleen. Eur J Immunol. 1978 May;8(5):331-5. (11)
Howard JC, Butcher GW, Galfre G, Milstein C. Monoclonal anti-rat MHC (H-1) alloantibodies. Curr Top Microbiol Immunol. 1978 ;81:54-60. (25)
Galfre G, Howe SC, Milstein C, Butcher GW, Howard JC. Antibodies to major histocompatibility antigens produced by hybrid cell lines. Nature. 1977 Apr 7;266(5602):550-2. (1224)
Butcher GW, Howard JC. A recombinant in the major histocompatibility complex of the rat. Nature. 1977 Mar 24;266(5600):362-4. (74)
Wilson DB, Heber-Katz E, Sprent J, Howard JC. On the possibility of multiple T-cell receptors. Cold Spring Harb Symp Quant Biol. 1977 ;41 Pt 2:559-61.(9)
Howard, JC, 1977. H-2 and mating preference. Nature 266:406-8 (20)
Wilson DB, Marshak A, Razzino-Pierson G, Howard JC. Specific selection of cytotoxic effector cells: the generation of cytotoxic T cells in rat thoracic duct lymphocyte populations positively or negatively selected for reactivity to specific strong histocompatibility alloantigens. J Immunol. 1976 Jun;116(6):1624-8. (7)
Howard JC. The genetic basis for responses to major transplantation antigens. Transplant Proc. 1976 Jun;8(2):157-60.
Wilson DB, Marshak A, Howard JC. Specific positive and negative selection of rat lymphocytes reactive to strong histocompatibility antigens: activation with alloantigens in vitro and in vivo. J Immunol. 1976 Apr;116(4):1030-40. (24)
Gonatas NK, Howard JC. Inhibition of experimental allergic encephalomyelitis in rats severely depleted of T cells. Science. 1974 Nov 29;186(4166):839-41.(99)
Howard JC, Scott DW. The identification of sera distinguishing marrow-derived and thymus-derived lymphocytes in the rat thoracic duct. Immunology. 1974 Nov;27(5):903-22. (55)
Howard JC, Wilson DB. Specific positive selection of lymphocytes reactive to strong histocompatibility antigens. J Exp Med. 1974 Sep 1;140(3):660-72. (57)
Howard JC. On the relationship between initiator and effector cells in the response to major tansplantation antigens. Transplant Proc. 1973 Dec;5(4):1451-6. (7) .
Howard JC, Gowans JL. The role of lymphocytes in antibody formation. 3. The origin from small lymphocytes of cells forming direct and indirect haemolytic plaques to sheep erythrocytes in the rat. Proc R Soc Lond B Biol Sci. 1972 Sep 19;182(67):193-209. ( 12)
Howard JC, Scott DW. The role of recirculating lymphocytes in the immunological competence of rat bone marrow cells. Cell Immunol. 1972 Mar;3(3):421-9. (55)
Scott DW, Howard JC. Collaboration between thymus-derived and marrow-derived thoracic duct lymphocytes in the hemolysin response of the rat. Cell Immunol. 1972 Mar;3(3):430-41. (55)
Howard JC, Hunt SV, Gowans JL. Identification of marrow-derived and thymus-derived small lymphocytes in the lymphoid tissue and thoracic duct lymph of normal rats. J Exp Med. 1972 Feb 1;135(2):200-19. (214)
Howard JC. The life-span and recirculation of marrow-derived small lymphocytes from the rat thoracic duct. J Exp Med. 1972 Feb 1;135(2):185-99. (163)
Wilson DB, Howard JC, Nowell PC. Some biological aspects of lymphocytes reactive to strong histocompatibility alloantigens. Transplant Rev. 1972 ;12:3-29. Review. (43)
Howard JC. A histocompatible chromosome marker system in the laboratory rat Rattus norvegicus. Transplantation. 1971 Jul;12(1):95-7.
Ellis ST, Gowans JL, Howard JC. The origin of antibody forming cells from lymphocytes. Antibiot Chemother. 1969 ;15:40-55. (32)

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