Professor Gerard Graham

Professor of Molecular and Structural Immunology (Immunology & Infection)
Dean of Research (MVLS College Senior Management)

telephone: 01413303982
email: Gerard.Graham@glasgow.ac.uk

RB327 Level B3, Iii - Gbrc, University Place, Glasgow G12 8TA

Research interests

Chemokines, Stem Cells and Cancer
We have had a long-standing standing interest in chemokines and their receptors and have been working in this field for 18 years. Currently, we have a number of projects that relate to various aspects of chemokine and chemokine receptor function:Studies into the biological function of the D6-chemokine decoy receptor

In 1997 we reported the cloning of the D6 chemokine receptor. D6 is an atypical receptor and can bind many chemokines with high affinity. Interestingly it does not signal following ligand binding and is thus not a typical chemokine receptor. The chemokines that D6 binds are those that are involved in inflammatory responses. D6 internalises ligand and targets it for intracellular degradation. We have thus proposed a role for D6 as a ‘decoy’ or ‘scavenging’ receptor which is capable of internalising and degrading a range of inflammatory chemokines. We have generated D6-nul mice in collaboration with Dr. Don Cook and Prof Sergio Lira and have shown that these mice display an altered ability to resolve inflammation in both the lung and skin. In the skin, following application of a chemical irritant, these D6-null mice develop a pathology which is similar to human psoriasis. Overall our conclusion is that D6 is an indispensable regulator of the in vivo inflammatory response. We are now undertaking a more detailed investigation of the inflammatory response of the D6 null mice using a range of models. We are also generating D6-GFP reporter mice to help us to detail the key cells that express D6 in the inflamed context and the dynamics of expression of D6 during an inflammatory response.

Studies into the structure of D6
D6, although atypical in the biological sense, is a typical seven transmembrane spanning receptor. There is much interest from the pharmaceutical industry in trying to determine the structure of chemokine receptors to aid rational drug design. Currently the only seven transmembrane spanning receptor structure known is that of Rhodopsin. D6 is curious in that it expresses to extremely high levels in heterologous transfectants and we can purify it to homogeneity in a functional form from transfected mammalian cells. We therefore have a very active interest (in collaboration with Prof Neil Isaacs) in determining the full three dimensional structure of the D6 receptor. It is likely that this structure will provide invaluable information on the structures of the other chemokine receptors and will provide a major boost to attempts to rationally design anti-chemokine receptor drugs.
Therapeutic interference with chemokine receptors

We have developing a number of experimental approaches aimed at examining the ability of chemokine receptors to be used as therapeutic targets. For example we have been ‘shrouding’ adenoviruses with chemokines and have been able to use these altered viruses to specifically infect chemokine receptor expressing cells. Such chemokine-virus conjugates will be of use in introducing a range of gene therapy vectors and even cytotoxic vectors to cells of pathological importance. We are also developing a programme of work in collaboration with ALMAC Sciences which is aimed at producing chemokine variants that will be of therapeutic use in a range of pathologies.
Chemokines and stem cells

We are interested in determining the roles for CXC chemokines in haemopoietic stem cell mobilisation and in the recruitment of neutrophils and neutrophil-derived proteases to the stem cell niche. Embryonic Stem Cell studies: We have a range of interests in murine embryonic stem cells from their use as gene targeting vehicles to the control of the induction of haemopoietic differentiation of ES cells in vitro. We are always keen to talk to researchers interested in working in the above areas or in joining our laboratory to work on related projects.

Publications

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Number of items: 121.

2024

Fukuoka, A., Wilson, G. J., Pitmon, E., Koumbas Foley, L., Johnsson, H., Pingen, M. and Graham, G. J. (2024) Disruption of placental ACKR3 effects embryo, and offspring, growth and hematopoietic development. Development, 151(4), dev202333. (doi: 10.1242/dev.202333) (PMID:38300826)

2023

Gamble, A., Suessmilch, M., Bonestroo, A., Merits, A., Graham, G. J. , Cavanagh, J. , Edgar, J. M. and Pingen, M. (2023) Establishing mixed neuronal and glial cell cultures from embryonic mouse brains to study infection and innate immunity. Journal of Visualized Experiments(196), 65331. (doi: 10.3791/65331) (PMID:37458443)

Cuesta-Gomez, N., Medina-Ruiz, L., Graham, G. J. and Campbell, J. D.M. (2023) IL-6 and TGF-β-secreting adoptively-transferred murine mesenchymal stromal cells accelerate healing of psoriasis-like skin inflammation and upregulate IL-17A and TGF-β. International Journal of Molecular Sciences, 24(12), 10132. (doi: 10.3390/ijms241210132) (PMID:37373278) (PMCID:PMC10298958)

Johnsson, H., Cole, J., McInnes, I. B. , Graham, G. and Siebert, S. (2023) Differences in transcriptional changes in psoriasis and psoriatic arthritis skin with immunoglobulin gene enrichment in psoriatic arthritis. Rheumatology, (doi: 10.1093/rheumatology/kead195) (PMID:37137278) (Early Online Publication)

Johnsson, H., Cole, J., Siebert, S. , McInnes, I. B. and Graham, G. (2023) Cutaneous lesions in psoriatic arthritis are enriched in chemokine transcriptomic pathways. Arthritis Research and Therapy, 25, 73. (doi: 10.1186/s13075-023-03034-6) (PMID:37131254) (PMCID:PMC10152590)

Ward, E. J. et al. (2023) Placental inflammation leads to abnormal embryonic heart development. Circulation, 147(12), pp. 956-972. (doi: 10.1161/CIRCULATIONAHA.122.061934) (PMID:36484244) (PMCID:PMC10022676)

Gray, A. L. et al. (2023) Chemokine CXCL4 interactions with extracellular matrix proteoglycans mediate widespread immune cell recruitment independent of chemokine receptors. Cell Reports, 42(1), 111930. (doi: 10.1016/j.celrep.2022.111930) (PMID:36640356)

2022

Yu, T., Schuette, F., Christofi, M., Forrester, J. V., Graham, G. J. and Kuffova, L. (2022) The atypical chemokine receptor-2 fine-tunes the immune response in herpes stromal keratitis. Frontiers in Immunology, 13, 1054260. (doi: 10.3389/fimmu.2022.1054260) (PMID:36518752) (PMCID:PMC9742518)

Bartolini, R. , Medina-Ruiz, L., Hayes, A. J., Kelly, C. J., Halawa, H. A. and Graham, G. J. (2022) Inflammatory chemokine receptors support inflammatory macrophage and dendritic cell maturation. ImmunoHorizons, 6(11), pp. 743-759. (doi: 10.4049/immunohorizons.2200069) (PMID:36426967)

Leslie, J. et al. (2022) CXCR2 inhibition enables NASH-HCC immunotherapy. Gut, 71(10), pp. 2093-2106. (doi: 10.1136/gutjnl-2021-326259) (PMID:35477863) (PMCID:PMC9484388)

Medina-Ruiz, L. et al. (2022) Analysis of combinatorial chemokine receptor expression dynamics using multi-receptor reporter mice. eLife, 11, e72418. (doi: 10.7554/eLife.72418) (PMID:35699420) (PMCID:PMC9236609)

Burgoyne, P., Hayes, A. J., Cooper, R. S., Le Brocq, M. L., Hansell, C. A.H., Campbell, J. D.M. and Graham, G. J. (2022) CCR7+ dendritic cells sorted by binding of CCL19 show enhanced Ag-presenting capacity and antitumor potency. Journal of Leukocyte Biology, 111(6), pp. 1243-1251. (doi: 10.1002/JLB.5AB0720-446RR) (PMID:34780080)

Wilson, G. J. , Fukuoka, A. , Vidler, F. and Graham, G. J. (2022) Diverse myeloid cells are recruited to the developing and inflamed mammary gland. Immunology, 165(2), pp. 206-218. (doi: 10.1111/imm.13430) (PMID:34775606)

2021

Mikolajczyk, T. P., Szczepaniak, P., Vidler, F., Maffia, P. , Graham, G. J. and Guzik, T. J. (2021) Role of inflammatory chemokines in hypertension. Pharmacology and Therapeutics, 223, 107799. (doi: 10.1016/j.pharmthera.2020.107799) (PMID:33359600)

Motta, F. et al. (2021) Role of placental inflammatory mediators and growth factors in patients with rheumatic diseases with a focus on systemic sclerosis. Rheumatology, 60(7), pp. 3307-3316. (doi: 10.1093/rheumatology/keaa782) (PMID:33313931) (PMCID:PMC8516508)

2020

Thirlwell, K. L. et al. (2020) Pancreas-derived mesenchymal stromal cells share immune response-modulating and angiogenic potential with bone marrow mesenchymal stromal cells and can be grown to therapeutic scale under Good Manufacturing Practice conditions. Cytotherapy, 22(12), pp. 762-771. (doi: 10.1016/j.jcyt.2020.07.010) (PMID:32828673)

Wilson, G. J. , Fukuoka, A. , Love, S. R., Kim, J., Pingen, M. , Hayes, A. J. and Graham, G. J. (2020) Chemokine receptors coordinately regulate macrophage dynamics and mammary gland development. Development, 147(12), dev187815. (doi: 10.1242/dev.187815) (PMID:32467242) (PMCID:PMC7328164)

Hansell, C. A.H., Love, S., Pingen, M. , Wilson, G. J. , Macleod, M. and Graham, G. (2020) Analysis of lung stromal expression of the atypical chemokine receptor ACKR2 reveals unanticipated expression in blood endothelial cells. European Journal of Immunology, 50(5), pp. 666-675. (doi: 10.1002/eji.201948374) (PMID:32114694)

Nosalski, R. et al. (2020) T cell-derived miRNA-214 mediates perivascular fibrosis in hypertension. Circulation Research, 126, pp. 988-1003. (doi: 10.1161/CIRCRESAHA.119.315428) (PMID:32065054) (PMCID:PMC7147427)

Leung, E. Y.L. et al. (2020) NK cells augment oncolytic adenovirus cytotoxicity in ovarian cancer. Molecular Therapy - Oncolytics, 16, pp. 289-301. (doi: 10.1016/j.omto.2020.02.001) (PMID:32195317) (PMCID:PMC7068056)

Thomson, C., McColl, A., Graham, G. and Cavanagh, J. (2020) Sustained exposure to systemic endotoxin triggers chemokine induction in the brain followed by a rapid influx of leukocytes. Journal of Neuroinflammation, 17, 94. (doi: 10.1186/s12974-020-01759-8) (PMID:32213184) (PMCID:PMC7098135)

Bryden, S. R. et al. (2020) Pan-viral protection against arboviruses by activating skin macrophages at the inoculation site. Science Translational Medicine, 12(527), eaax2421. (doi: 10.1126/scitranslmed.aax2421) (PMID:31969486)

Forbes, S. et al. (2020) Human umbilical cord perivascular cells improve human pancreatic islet transplant function by increasing vascularization. Science Translational Medicine, 12(526), eaan5907. (doi: 10.1126/scitranslmed.aan5907) (PMID:31941825)

2019

Graham, G. J. , Handel, T. M. and Proudfoot, A. E.I. (2019) Leukocyte adhesion: reconceptualizing chemokine presentation by glycosaminoglycans. Trends in Immunology, 40(6), pp. 472-481. (doi: 10.1016/j.it.2019.03.009) (PMID:31006548)

Lee, K. M., Wilson, G. J. , Pingen, M. , Fukuoka, A. , Hansell, C. A.H., Bartolini, R., Medina-Ruiz, L. and Graham, G. J. (2019) Placental chemokine compartmentalisation: a novel mammalian molecular control mechanism. PLoS Biology, 17(5), e3000287. (doi: 10.1371/journal.pbio.3000287) (PMID:31141500) (PMCID:PMC6557524)

Dyer, D. P. , Nebot, J. B., Kelly, C. J., Medina-Ruiz, L., Schuette, F. and Graham, G. J. (2019) The chemokine receptor CXCR2 contributes to murine adipocyte development. Journal of Leukocyte Biology, 105(3), pp. 497-506. (doi: 10.1002/JLB.1A0618-216RR) (PMID:30517976) (PMCID:PMC6392114)

Dyer, D. P. et al. (2019) Chemokine receptor redundancy and specificity are context dependent. Immunity, 50(2), 378-389.e5. (doi: 10.1016/j.immuni.2019.01.009) (PMID:30784579) (PMCID:PMC6382461)

2018

Girbl, T. et al. (2018) Distinct compartmentalization of the chemokines CXCL1 and CXCL2 and the atypical receptor ACKR1 determine discrete stages of neutrophil diapedesis. Immunity, 49(6), 1062-1076.e6. (doi: 10.1016/j.immuni.2018.09.018) (PMID:30446388) (PMCID:PMC6303217)

Hansell, C. A.H. et al. (2018) The atypical chemokine receptor Ackr2 constrains NK cell migratory activity and promotes metastasis. Journal of Immunology, 201(8), pp. 2510-2519. (doi: 10.4049/jimmunol.1800131) (PMID:30158126) (PMCID:PMC6176105)

Castanheira, F. V. E. S. et al. (2018) The atypical chemokine receptor ACKR2 is protective against sepsis. Shock, 49(6), pp. 682-689. (doi: 10.1097/SHK.0000000000000969) (PMID:29589840)

Shams, K., Kurowska-Stolarska, M. , Schütte, F., Burden, A. D., McKimmie, C. S. and Graham, G. J. (2018) MicroRNA-146 and cell trauma down-regulate expression of the psoriasis-associated atypical chemokine receptor ACKR2. Journal of Biological Chemistry, 293(8), pp. 3003-3012. (doi: 10.1074/jbc.M117.809780) (PMID:29279330) (PMCID:PMC5827444)

Leighton, S.P. , Nerurkar, L., Krishnadas, R. , Johnman, C., Graham, G.J. and Cavanagh, J. (2018) Chemokines in depression in health and in inflammatory illness: a systematic review and meta-analysis. Molecular Psychiatry, 23(1), pp. 48-58. (doi: 10.1038/mp.2017.205) (PMID:29133955) (PMCID:PMC5754468)

2017

Nerurkar, L., McColl, A., Graham, G. and Cavanagh, J. (2017) The systemic response to topical Aldara treatment is mediated through direct TLR7 stimulation as Imiquimod enters the circulation. Scientific Reports, 7, 16570. (doi: 10.1038/s41598-017-16707-5) (PMID:29185473) (PMCID:PMC5707416)

Baldwin, H. M., Singh, M. D., Codullo, V., King, V., Wilson, H., McInnes, I. and Graham, G. J. (2017) Elevated ACKR2 expression is a common feature of inflammatory arthropathies. Rheumatology, 56(9), pp. 1607-1617. (doi: 10.1093/rheumatology/kex176) (PMID:28486662) (PMCID:PMC5850605)

Dyer, D. P. , Pallas, K., Medina Ruiz, L., Schuette, F., Wilson, G. J. and Graham, G. J. (2017) CXCR2 deficient mice display macrophage-dependent exaggerated acute inflammatory responses. Scientific Reports, 7, 42681. (doi: 10.1038/srep42681) (PMID:28205614) (PMCID:PMC5311995)

Graham, G. et al. (2017) Spread of psoriasiform inflammation to remote tissues is restricted by the atypical chemokine receptor ACKR2. Journal of Investigative Dermatology, 137(1), pp. 85-94. (doi: 10.1016/j.jid.2016.07.039) (PMID:27568525) (PMCID:PMC5176004)

Wilson, G. J. , Hewit, K. D., Pallas, K. J., Cairney, C. J., Lee, K. M., Hansell, C. A., Stein, T. and Graham, G. J. (2017) Atypical chemokine receptor ACKR2 controls branching morphogenesis in the developing mammary gland. Development, 144, pp. 74-82. (doi: 10.1242/dev.139733) (PMID:27888192) (PMCID:PMC5278629)

2016

Offiah, I. et al. (2016) The expression of inflammatory mediators in bladder pain syndrome. European Urology, 70(2), pp. 283-290. (doi: 10.1016/j.eururo.2016.02.058) (PMID:26965559) (PMCID:PMC4926725)

Sinclair, A. et al. (2016) CXCR2 and CXCL4 regulate survival and self-renewal of hematopoietic stem/progenitor cells. Blood, 128(3), pp. 371-383. (doi: 10.1182/blood-2015-08-661785) (PMID:27222476) (PMCID:PMC4991087)

Pingen, M. , Bryden, S. R. , Pondeville, E., Schnettler, E., Kohl, A. , Merits, A., Fazakerley, J. K., Graham, G. J. and McKimmie, C. S. (2016) Host inflammatory response to mosquito bites enhances the severity of arbovirus infection. Immunity, 44(6), pp. 1455-1469. (doi: 10.1016/j.immuni.2016.06.002) (PMID:27332734) (PMCID:PMC4920956)

Mccoll, A., Thomson, C. A., Nerurkar, L., Graham, G. J. and Cavanagh, J. (2016) TLR7-mediated skin inflammation remotely triggers chemokine expression and leukocyte accumulation in the brain. Journal of Neuroinflammation, 13, 102. (doi: 10.1186/s12974-016-0562-2) (PMID:27160148)

Bryce, S. A., Wilson, R. A.M., Tiplady, E. M. , Asquith, D. L., Bromley, S. K., Luster, A. D., Graham, G. J. and Nibbs, R. J.B. (2016) ACKR4 on stromal cells scavenges CCL19 to enable CCR7-dependent trafficking of APCs from inflamed skin to lymph nodes. Journal of Immunology, 196(8), pp. 3341-3353. (doi: 10.4049/jimmunol.1501542) (PMID:26976955)

Bonecchi, R. and Graham, G. J. (2016) Atypical chemokine receptors and their roles in the resolution of the inflammatory response. Frontiers in Immunology, 7, 224. (doi: 10.3389/fimmu.2016.00224)

Williams, M. T.S. et al. (2016) The ability to cross the blood-cerebrospinal fluid barrier is a generic property of acute lymphoblastic leukaemia blasts. Blood, 127, 16. (doi: 10.1182/blood-2015-08-665034) (PMID:26869395)

2015

Bachelerie, F., Graham, G.J. , Locati, M., Mantovani, A., Murphy, P.M., Nibbs, R. , Rot, A., Sozzani, S. and Thelen, M. (2015) An atypical addition to the chemokine receptor nomenclature: IUPHAR Review 15. British Journal of Pharmacology, 172(16), pp. 3945-3949. (doi: 10.1111/bph.13182) (PMID:25958743)

Le Brocq, M., Fraser, A. R., Graham, G. J. and Campbell, J. D.M. (2015) CCL19-sorted mature dendritic cells have enhanced lymph node migratory capacity and function. Journal of Inflammation, 12(S1), P2. (doi: 10.1186/1476-9255-12-S1-P2) (PMCID:PMC4416168)

2014

Li, D. et al. (2014) IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. Journal of Allergy and Clinical Immunology, 134(6), 1422-1432.e11. (doi: 10.1016/j.jaci.2014.05.011) (PMID:24985397) (PMCID:PMC4258609)

Elmesmari, A., Gilchrist, D. S., Fraser, A. R., Graham, G. J. , Brewer, J. , Kurowska-Stolarska, M. and McInnes, I. B. (2014) Mir-155 Expression Correlates with Clinical Disease Activity and has Effector Function in Rheumatoid Arthritis. 2014 ACR/ARHP Annual Meeting, Boston, MA, 14-19 Nov 2014. (Unpublished)

Lee, K. M., Danuser, R., Stein, J. V., Graham, D. , Nibbs, R. J.B. and Graham, G. J. (2014) The chemokine receptors ACKR2 and CCR2 reciprocally regulate lymphatic vessel density. EMBO Journal, 33(21), pp. 2564-2580. (doi: 10.15252/embj.201488887)

Michlmayr, D., McKimmie, C.S., Pingen, M. , Haxton, B., Mansfield, K., Johnson, N., Fooks, A.R. and Graham, G.J. (2014) Defining the chemokine basis for leukocyte recruitment during viral encephalitis. Journal of Virology, 88(17), pp. 9553-9567. (doi: 10.1128/JVI.03421-13)

Ford, L. B., Cerovic, V., Milling, S. W.F. , Graham, G. J. , Hansell, C. A.H. and Nibbs, R. J.B. (2014) Characterization of conventional and atypical receptors for the chemokine CCL2 on mouse leukocytes. Journal of Immunology, 193(1), pp. 400-411. (doi: 10.4049/jimmunol.1303236)

Zakrys, L., Ward, R. J., Pediani, J. D. , Godin, A. G., Graham, G. J. and Milligan, G. (2014) Roundabout 1 exists predominantly as a basal dimeric complex and this is unaffected by binding of the ligand Slit2. Biochemical Journal, 461(1), pp. 61-73. (doi: 10.1042/BJ20140190)

Le Brocq, M. L., Fraser, A. R., Cotton, G., Woznica, K., McCulloch, C. V., Hewit, K. D., McKimmie, C. S., Nibbs, R. J.B. , Campbell, J. D.M. and Graham, G. J. (2014) Chemokines as novel and versatile reagents for flow cytometry and cell sorting. Journal of Immunology, 192(12), pp. 6120-6130. (doi: 10.4049/jimmunol.1303371) (PMID:24850722)

Elmesmari, A., Gilchrist, D. S., Fraser, A. R., Vaughan, D. , Graham, G. J. , Brewer, J. , Kurowska-Stolarska, M. and McInnes, I. B. (2014) MicroRNA-155 Regulates Chemokines and Chemokine Receptors in Rheumatoid Arthritis Monocytes. Libya Higher Education Forum, London, UK, 5-6 June 2014. (Unpublished)

Hewit, K. D., Fraser, A., Nibbs, R. J.B. and Graham, G. J. (2014) The N-terminal region of the atypical chemokine receptor ACKR2 is a key determinant of ligand binding. Journal of Biological Chemistry, 289(18), pp. 12330-12342. (doi: 10.1074/jbc.M113.534545)

Anselmo, A., Mazzon, C., Borroni, E. M., Bonecchi, R., Graham, G. J. and Locati, M. (2014) Flow cytometry applications for the analysis of chemokine receptor expression and function. Cytometry Part A, 85(4), pp. 292-301. (doi: 10.1002/cyto.a.22439)

Bachelerie, F., Graham, G.J. , Locati, M., Mantovani, A., Murphy, P.M., Nibbs, R. , Rot, A., Sozzani, S. and Thelen, M. (2014) New nomenclature for atypical chemokine receptors. Nature Immunology, 15(3), pp. 207-208. (doi: 10.1038/ni.2812)

Bachelerie, F. et al. (2014) International union of pharmacology. LXXXIX. update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacological Reviews, 66(1), pp. 1-79. (doi: 10.1124/pr.113.007724)

Guabiraba Brito, R. et al. (2014) IL-33 targeting attenuates intestinal mucositis and enhances effective tumor chemotherapy in mice. Mucosal Immunology, 7(5), pp. 1079-1093. (doi: 10.1038/mi.2013.124)

Thomson, C. A., McColl, A., Cavanagh, J. and Graham, G. J. (2014) Peripheral inflammation is associated with remote global gene expression changes in the brain. Journal of Neuroinflammation, 11(73), (doi: 10.1186/1742-2094-11-73)

Williams, M. T.S. et al. (2014) Interleukin-15 enhances cellular proliferation and up-regulates CNS homing molecules in pre-B acute lymphoblastic leukemia. Blood, 123(20), pp. 3116-3127. (doi: 10.1182/blood-2013-05-499970) (PMID:24700781)

2013

Baldwin, H.M., Pallas, K., King, V., Jamieson, T., McKimmie, C.S., Nibbs, R.J.B. , Carballido, J.M., Jaritz, M., Rot, A. and Graham, G.J. (2013) Microarray analyses demonstrate the involvement of type i interferons in psoriasiform pathology development in D6-deficient mice. Journal of Biological Chemistry, 288(51), pp. 36473-36483. (doi: 10.1074/jbc.M113.491563)

Yasar, M. Y. et al. (2013) 3866 An Analysis of Mechanisms of Central Nervous System Infiltration in Acute Lymphoblastic Leukaemia Using Primary Cells Xenografted Into Immunodeficient Mice. 55th ASH Annual Meeting and Exposition, New Orleans, LA, USA, 7-10 Dec 2013.

Rot, A., McKimmie, C., Burt, C.L., Pallas, K.J., Jamieson, T., Pruenster, M., Horuk, R., Nibbs, R.J.B. and Graham, G.J. (2013) Cell-autonomous regulation of neutrophil migration by the D6 chemokine decoy receptor. Journal of Immunology, 190(12), pp. 6450-6456. (doi: 10.4049/jimmunol.1201429)

McKimmie, C.S. et al. (2013) An analysis of the function and expression of D6 on lymphatic endothelial cells. Blood, 121(18), pp. 3768-3777. (doi: 10.1182/blood-2012-04-425314)

Graham, G.J. and Locati, M. (2013) Regulation of the immune and inflammatory responses by the 'atypical' chemokine receptor D6. Journal of Pathology, 229(2), pp. 168-175. (doi: 10.1002/path.4123)

Lee, K., Nibbs, R.J.B. and Graham, G.J. (2013) D6: the 'crowd controller’ at the immune gateway. Trends in Immunology, 34(1), pp. 7-12. (doi: 10.1016/j.it.2012.08.001)

Oleinika, K., Nibbs, R.J. , Graham, G.J. and Fraser, A.R. (2013) Suppression, subversion and escape: the role of regulatory T cells in cancer progression. Clinical and Experimental Immunology, 171(1), pp. 36-45. (doi: 10.1111/j.1365-2249.2012.04657.x)

Mori, M., Andersson, C.K., Graham, G.J. , Löfdahl, C.G. and Erjefält, J.S. (2013) Increased number and altered phenotype of lymphatic vessels in peripheral lung compartments of patients with COPD. Respiratory Research, 14(65), (doi: 10.1186/1465-9921-14-65)

Nibbs, R.J.B. and Graham, G.J. (2013) Immune regulation by atypical chemokine receptors. Nature Reviews Immunology, 13(11), pp. 815-829. (doi: 10.1038/nri3544)

2012

Singh, M.D. et al. (2012) Elevated expression of the chemokine-scavenging receptor D6 is associated with impaired lesion development in psoriasis. American Journal of Pathology, 181(4), pp. 1158-1164. (doi: 10.1016/j.ajpath.2012.06.042) (PMID:22867710) (PMCID:PMC3532592)

Akbar, M., Fraser, A. R., Graham, G. J. , Brewer, J. M. and Grant, M. H. (2012) Acute inflammatory response to cobalt chromium orthopaedic wear debris in a rodent air-pouch model. Journal of the Royal Society: Interface, 9(74), pp. 2109-2119. (doi: 10.1098/rsif.2012.0006)

Graham, G.J. , Locati, M., Mantovani, A., Rot, A. and Thelen, M. (2012) The biochemistry and biology of the atypical chemokine receptors. Immunology Letters, 145(1-2), pp. 30-38. (doi: 10.1016/j.imlet.2012.04.004)

Elmesmari, A., Gilchrist, D. S., Fraser, A. D., Vaughan, D. , McQueenie, R., Graham, G. , Brewer, J. , McInnes, I. B. and Kurowska-Stolarska, M. (2012) Microrna-155 regulates chemokines and chemokine receptors in Rheumatoid Arthritis monocyte. In: American College of Rheumatology & Association of Rheumatology Health Professionals, Annual Scientific Meeting, Washington DC, USA, 9-14 Nov 2012, S384. (doi: 10.1002/art.37735)

Halsey, C. , Docherty, M., McNeill, M., Gilchrist, D., Le Brocq, M., Gibson, B. and Graham, G. (2012) The GATA1s isoform is normally down-regulated during terminal haematopoietic differentiation and over-expression leads to failure to repress MYB, CCND2 and SKI during erythroid differentiation of K562 cells. Journal of Hematology and Oncology, 5, p. 45. (doi: 10.1186/1756-8722-5-45)

2011

Lee, K. M. et al. (2011) D6 facilitates cellular migration and fluid flow to lymph nodes by suppressing lymphatic congestion. Blood, 118(23), pp. 6220-6229. (doi: 10.1182/blood-2011-03-344044)

Hueber, A. J., Alves-Filho, J. C., Asquith, D. L., Michels, C., Millar, N. L. , Reilly, J. H., Graham, G. J. , Liew, F. Y., Miller, A. M. and McInnes, I. B. (2011) IL-33 induces skin inflammation with mast cell and neutrophil activation. European Journal of Immunology, 41(8), pp. 2229-2237. (doi: 10.1002/eji.201041360) (PMID:21674479)

Williams, M.T., Graham, G. , Gibson, B. and Halsey, C. (2011) Homing to the central nervous system is associated with differential expression of selectins, integrins and chemokine receptors in pre-B acute lymphoblastic leukaemia cell lines. In: 51st Annual Scientific Meeting of the British Society for Haematology, Brighton, UK, 4-6 April 2011, pp. 1-88. (doi: 10.1111/j.1365-2141.2011.08609.x)

Williams, M.T., Graham, G. , Gibson, B. and Halsey, C. (2011) An investigation into the role of interleukin-15 on the growth and survival of pre-B acute lymphoblastic leukaemia cell lines. In: 51st Annual Scientific Meeting of the British Society for Haematology, Brighton, UK, 4-6 April 2011, pp. 1-88. (doi: 10.1111/j.1365-2141.2011.08609.x)

Codullo, V. et al. (2011) An investigation of the inflammatory cytokine and chemokine network in systemic sclerosis. Annals of the Rheumatic Diseases, 70(6), pp. 1115-1121. (doi: 10.1136/ard.2010.137349) (PMID:21285114)

2010

Singh, M., Nibbs, R.J. and Graham, G.J. (2010) The atypical chemokine receptors. In: Smit, M.J., Lira, S.A. and Leurs, R. (eds.) Chemokine Receptors as Drug Targets. Wiley-VCH: Weinheim, Germany. ISBN 9783527632008

Bradford, L., Marshall, H., Robertson, H., Kirby, J. A., Graham, G. , Ali, S. and O'Boyle, G. (2010) Cardiac Allograft Rejection: Examination of the Expression and Function of the Decoy Chemokine Receptor D6. Transplantation, 89(11), pp. 1411-1416. (doi: 10.1097/TP.0b013e3181da604b)

Halsey, C. , Tunstall, O., Gibson, B., Roberts, I. and Graham, G. (2010) Role of GATA-1s in early hematopoiesis and differences between alternative splicing in human and murine GATA-1. Blood, 115(16), pp. 3415-3416. (doi: 10.1182/blood-2010-02-267930)

Henriques, C. M., Rino, J., Nibbs, R. J. , Graham, G. J. and Barata, J. T. (2010) IL-7 induces rapid clathrin-mediated internalization and JAK3-dependent degradation of IL-7R alpha in T cells. Blood, 115(16), pp. 3269-3277. (doi: 10.1182/blood-2009-10-246876)

Madigan, J. et al. (2010) Chemokine Scavenger D6 Is Expressed by Trophoblasts and Aids the Survival of Mouse Embryos Transferred into Allogeneic Recipients. Journal of Immunology, 184(6), pp. 3202-3212. (doi: 10.4049/jimmunol.0902118)

McKimmie, C. S. and Graham, G. J. (2010) Astrocytes modulate the chemokine network in a pathogen-specific manner. Biochemical and Biophysical Research Communications, 394(4), pp. 1006-1011. (doi: 10.1016/j.bbrc.2010.03.111)

2009

Singh, M.D., Kreiner, M., McKimmie, C.S., Holt, S., van der Walle, C.F. and Graham, G.J. (2009) Dimeric integrin alpha 5 beta 1 ligands confer morphological and differentiation responses to murine embryonic stem cells. Biochemical and Biophysical Research Communications, 390(3), pp. 716-721. (doi: 10.1016/j.bbrc.2009.10.035)

Asquith, D., Miller, A., Hueber, A., McKinnon, H., Sattar, N., Graham, G. and McInnes, I. (2009) Liver X receptor agonism promotes articular inflammation in murine collagen-induced arthritis. Arthritis and Rheumatism, 60(9), pp. 2655-2665. (doi: 10.1002/art.24717) (PMID:19714646)

McKimmie, C. S. et al. (2009) A TLR2 ligand suppresses inflammation by modulation of chemokine receptors and redirection of leukocyte migration. Blood, 113(18), pp. 4224-4231. (doi: 10.1182/blood-2008-08-174698) (PMID:19202130)

Graham, G. (2009) D6 and the atypical chemokine receptor family: Novel regulators of immune and inflammatory processes. European Journal of Immunology, 39(2), pp. 342-351. (doi: 10.1002/eji.200838858)

Nibbs, R. J.B. , McLean, P., McCulloch, C., Riboldi‐Tunnicliffe, A., Blair, E., Zhu, Y., Isaacs, N. and Graham, G. J. (2009) Structure–function dissection of D6, an atypical scavenger receptor. In: Abelson, J. N. and Simon, M. I. (eds.) Chemokines, Part A. Series: Methods in enzymology (460). Academic Press: Amsterdam, pp. 245-261. ISBN 9780123749086 (doi: 10.1016/S0076-6879(09)05212-4)

Patel, M., McInnes, I. and Graham, G. (2009) Atypical Chemokine Receptors in Inflammatory Disease. Current Molecular Medicine, 9(1), pp. 86-93. (doi: 10.2174/156652409787314480) (PMID:19199944)

Pruenster, M. et al. (2009) The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nature Immunology, 10(1), pp. 101-108. (doi: 10.1038/ni.1675)

2008

McKimmie, C. S. et al. (2008) Hemopoietic cell expression of the chemokine decoy receptor D6 is dynamic and regulated by GATA1. Journal of Immunology, 181(5), pp. 3353-3363. (doi: 10.4049/jimmunol.181.11.8170-a) (PMID:19039854)

Deruaz, M. et al. (2008) Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. Journal of Experimental Medicine, 205(9), pp. 2019-2031. (doi: 10.1084/jem.20072689)

McCulloch, C., Morrow, V., Milasta, S., Comerford, I., Milligan, G. , Graham, G. , Isaacs, N. and Nibbs, R. (2008) Multiple roles for the C-terminal tail of the chemokine scavenger D6. Journal of Biological Chemistry, 283(12), pp. 7972-7982. (doi: 10.1074/jbc.M710128200)

Truman, L. et al. (2008) CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood, 112(13), pp. 5026-5036. (doi: 10.1182/blood-2008-06-162404)

2007

Nibbs, R. J.B. , Gilchrist, D. S., King, V., Ferra, A., Forrow, S., Hunter, K. D. and Graham, G. J. (2007) The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors. Journal of Clinical Investigation, 117(7), pp. 1884-1892. (doi: 10.1172/JCI30068)

Halsey, C. , Fisher, C., Strathdee, G., Gibson, B., Holyoake, T., Vyas, P. and Graham, G. (2007) GATA1 mutational analysis in chronic myeloid leukaemia. British Journal of Haematology, 137(4), pp. 375-376. (doi: 10.1111/j.1365-2141.2007.06563.x) (PMID:17408401)

Card, J. W., Cook, D. N., DeGraff, L. M., Graham, G. J. , Lira, S. A., Wang, T. and Whitehead, G. S. (2007) The chemokine receptor D6 has opposing effects on allergic inflammation and airway reactivity. American Journal of Respiratory and Critical Care Medicine, 175(3), pp. 243-249. (doi: 10.1164/rccm.200606-839OC)

Graham, G.J. and Nibbs, R.J. (2007) Chemokine receptors: a structural overview. In: Harrison, J.K. and Lukacs, N.W. (eds.) The Chemokine Receptors. Series: Receptors. Humana Press: Totowa, NJ, pp. 31-54. ISBN 978-1-58829-773-0

Graham, S., Vass, J., Holyoake, T. and Graham, G. (2007) Transcriptional analysis of quiescent and proliferating CD34+human hemopoietic cells from normal and chronic myeloid leukemia sources. Stem Cells, 25(12), pp. 3111-3120. (doi: 10.1634/stemcells.2007-0250)

2006

Graham, G.J. and McKimmie, C.S. (2006) Leucocyte expression of the chemokine scavenger D6. Biochemical Society Transactions, 34(6), pp. 1002-1004. (doi: 10.1042/BST0341002)

Graham, G. J. and McKimmie, C. S. (2006) Chemokine scavenging by D6: a movable feast? Trends in Immunology, 27, pp. 381-386. (doi: 10.1016/j.it.2006.06.006)

Awadalla, P., Driehaus, J., Forrester, L.M., Gautier, P., Gilchrist, D., Graham, G.J. , Jackson, M., Keebler, J., Prugnolle, F. and Watt, A.J. (2006) A murine specific expansion of the Rhox cluster involved in embryonic stem cell biology is under natural selection. BMC Genomics, 7, (doi: 10.1186/1471-2164-7-212)

Canasto-Chibuque, C., Cook, D., Damodaran, A., Graham, G. , Hu, T., Lira, S., Liu, L., Ransohoff, R. and Sasse, M. (2006) Cutting edge: The silent chemokine receptor D6 is required for generating T cell responses that mediate experimental autoimmune encephalomyelitis. Journal of Immunology, 177, pp. 17-21.

2005

Jamieson, T., Cook, D. N., Nibbs, R. J.B. , Rot, A., Nixon, C., Mclean, P., Alcami, A., Lira, S. A., Wiekowski, M. and Graham, G. J. (2005) The chemokine receptor D6 limits the inflammatory response in vivo. Nature Immunology, 6, pp. 403-411. (doi: 10.1038/ni1182)

2004

Weber, M., Blair, E., Simpson, C. V., O'Hara, M., Blackburn, P. E., Rot, A., Graham, G. J. and Nibbs, R. J.B. (2004) The chemokine receptor D6 constitutively traffics to and from the cell surface to internalize and degrade chemokine. Molecular Biology of the Cell, 15(5), pp. 2492-2508. (doi: 10.1091/mbc.E03-09-0634)

2003

Chvatchko, Y. et al. (2003) Inhibition of airway inflammation by amino-terminally modified RANTES/CC chemokine ligand 5 analogues is not mediated through CCR3. Journal of Immunology, 171(10), pp. 5498-5506.

Graham, G. and Nibbs, R. (2003) CCL27/PESKY: a novel paradigm for chemokine function. Expert Opinion on Biological Therapy, 3(1), pp. 15-22.

Nibbs, R. , Graham, G. and Rot, A. (2003) Chemokines on the move: control by the chemokine 'interceptors' Duffy blood group antigen and D6. Seminars in Immunology, 15(5), pp. 287-294.

2002

Gortz, A., Nibbs, R. J.B. , McLean, P., Jarmin, D., Lambie, W., Baird, J. W. and Graham, G. J. (2002) The chemokine ESkine/CCL27 displays novel modes of intracrine and paracrine function. Journal of Immunology, 169(3), pp. 1387-1394.

Jackson, M., Baird, J., Cambray, N., Ansell, J., Forrester, L. and Graham, G. (2002) Cloning and characterization of Ehox, a novel homeobox gene essential for embryonic stem cell differentiation. Journal of Biological Chemistry, 277(41), pp. 38683-38692.

Stringer, S., Forster, M., Mulloy, B., Bishop, C., Graham, G. and Gallagher, J. (2002) Characterization of the binding site on heparan sulfate for macrophage inflammatory protein 1 alpha. Blood, 100(5), pp. 1543-1550.

2001

Holyoake, T., Freshney, M., Samuel, K., Ansell, J., Watson, G., Wright, E., Graham, G. and Pragnell, I. (2001) In vivo expansion of the endogenous B-cell compartment stimulated by radiation and serial bone marrow transplantation induces B-cell leukaemia in mice. British Journal of Haematology, 114(1), pp. 49-56. (doi: 10.1046/j.1365-2141.2001.02903.x)

Baird, J. et al. (2001) Differentiating embryonal stem cells are a rich source of haemopoietic gene products and suggest erythroid preconditioning of primitive haemopoietic stem cells. Journal of Biological Chemistry, 276(12), pp. 9189-9198. (doi: 10.1074/jbc.M008354200)

Nibbs, R. et al. (2001) The beta-chemokine receptor D6 is expressed by lymphatic endothelium and a subset of vascular tumors. American Journal of Pathology, 158, pp. 867-877.

Ottersbach, K., Cook, D., Kuziel, W., Humbles, A., Lu, B., Gerard, C., Proudfoot, A. and Graham, G. (2001) Macrophage inflammatory protein-1 alpha uses a novel receptor for primitive hemopoietic cell inhibition. Blood, 98(12), pp. 3476-3478.

Ottersbach, K. and Graham, G. (2001) Aggregation-independent modulation of proteoglycan binding by neutralization of C-terminal acidic residues in the chemokine macrophage inflammatory protein 1 alpha. Biochemical Journal, 354, pp. 447-453.

2000

Townson, J. R., Graham, G. J. , Landau, N. R., Rasala, B. and Nibbs, R. J.B. (2000) Aminooxypentane addition to the chemokine macrophage inflammatory Protein-1 alpha P increases receptor affinities and HIV inhibition. Journal of Biological Chemistry, 275(50), pp. 39254-39261. (doi: 10.1074/jbc.M006768200)

Nibbs, R. J.B. et al. (2000) C-C chemokine receptor 3 antagonism by the beta-chemokine macrophage inflammatory protein 4, a property strongly enhanced by an amino-terminal alanine-methionine swap. Journal of Immunology, 164(3), pp. 1488-97.

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