Cell surface molecules and viral immunomodulation. PI: Ana Angulo Aguado and Pablo Engel Rocamora

Presentation

The research of our group is focused on the study of the structure and function of cell surface receptors involved in the regulation of innate and adaptive immune responses and its modulation during viral infections. More specifically, we are interested in receptors of the immunoglobulin superfamily and, in particular, in the SLAM (Signaling Molecule for the Activation of Lymphocytes) molecules. The SLAM receptors play a crucial role in host-pathogen interactions and also in autoimmunity and cancer. We are analyzing the pathophysiology of these molecules both in vitro and in animal models. We mainly work with cytomegalovirus (CMV), a clinical relevant human pathogen. One of our main objectives is the identification of new molecular targets for the treatment of immune-based pathological processes.

The group is organized into two research teams focused on the following topics:

  1. Functional characterization of leukocyte membrane receptors and development of new immunomodulatory therapeutic strategies (PI: Pablo Engel)
  2. Characterization of the biology and mechanisms of immuno-invasion of cytomegalovirus (PI: Ana Angulo)

Ana Angulo Aguado 
Associate professor
aangulo@ub.edu

 

Pablo Engel Rocamora
Associate professor
pengel@ub.edu

 

Javier Fernández Calles
Laboratory technician
jfernandezc@clinic.cat

 

Pablo Hernández Luis
Predoctoral researcher
pablo_hernandez_luis@ub.edu

 

Rebeca Gutiérrez Cozar
Predoctoral researcher
rebeca.gutierrez@ub.edu

 

Judit Pelegrín Pérez
Predoctoral researcher
juditpelegrinperez@ub.edu

Francesc Poblador Bonet 
Predoctoral researcher
fpoblador@ub.edu

 

Joan Puñet Ortiz
Predoctoral researcher
joan.punet@ub.edu

 

Manuel Eduardo Saez Moya
Predoctoral researcher
msaez@ub.edu

  • Study of the structure and function of the SLAM (Signaling Molecule for the Activation of Lymphocytes) family receptors and SAP (SLAM Associated Protein) adaptor molecule.

  • Analysis of the role of SLAM molecules in autoimmunity and cancer.

  • Study of the modulation of the immune response by CMV and viral immune evasion strategies.

  • Identification and characterization of functions of genes coded by CMV.

  • Repertorio, inmunopatología y terapia dirigida a los linfocitos B en la enfermedad autoinmune, Síndrome de Sjögren

Funding entity: Ministerio de Economia y Competitividad
Project Code: RTI2018-094440-B-I00
Principal investigator: Pablo Engel Rocamora  
Amount: 242.000,00 €
Period: 2019-2021

  • Manipulación de inmunoreceptores de la superfície celular por citomegalovirus

Funding entity: Ministerio de Economia y Competitividad
Project Code: SAF 2017
Principal investigator: Ana Angulo Aguado   
Amount: 181.500 €
Period: 2018-2020

  • Estudio de la homeostasis de las células B de la zona marginal y su papel en la autoinmunidad y linfomagénesis

Funding entity: Ministerio de Economia y Competitividad
Project Code: SAF 2015-69829-R
Principal investigator: Pablo Engel  Rocamora     
Amount: 190.000 €
Peiod: 2016-2018

  • Caracterización funcional de nuevas proteínas del citomegalovirus que interfieren con la respuesta inmune del huésped

Funding entity: Ministerio de Economia y Competitividad
Project Code: SAF 2014-55683-R
Principal investigator: Ana Angulo Aguado
Amount: 190.000 €
Period: 2015-2017

  • SLAM Gene Family Controlled Pathways to SLE

Funding entity: National Institutes of Health
Project Code: 2P01AI065587-06A1
Principal investigator: Cox Terhost/Pablo Engel (co-IP)
Amount: 400.000 $ (direct cost; portion of the group of Pablo Engel)
Period: 2012-2017

For more information for PI publications click in the link:
- PI: Pablo Engel Rocamora
  ORCID: https://orcid.org/0000-0001-8410-252X
- PI: Ana Angulo Aguado
  ORCID: https://orcid.org/0000-0002-5792-1164

Angulo G, Zeleznjak J, Martínez-Vicente P, Puñet-Ortiz J, Hengel H, Messerle M, Oxenius A, Jonjic S, Krmpotic A, Engel P, Angulo A. Cytomegalovirus restricts ICOSL expression on antigen presenting cells disabling T cell co-stimulation and contributing to immune evasion. Elife. 2021 Jan 18;10:e59350. doi: 10.7554/eLife.59350. Epub ahead of print. PMID: 33459589.

van Zelm MC, Ziegler-Heitbrock L, Collins AM, Chan SK, Engel P. Editorial: Nomenclature - Avoiding Babylonian Speech Confusion in Present Day Immunology. Front Immunol. 2020 Dec 14;11:621100. doi: 10.3389/ fimmu. 2020.621100. PMID: 33381126; PMCID: PMC7767845.

Velasco-Hernandez T, Zanetti SR, Roca-Ho H, Gutierrez-Aguera F, Petazzi P, Sánchez-Martínez D, Molina O, Baroni ML, Fuster JL, Ballerini P, Bueno C, Fernandez-Fuentes N, Engel P, Menendez P. Efficient elimination of primary B-ALL cells in vitro and in vivo using a novel 4-1BB-based CAR targeting a membrane-distal CD22 epitope. J Immunother Cancer. 2020 Aug;8(2):e000896. doi: 10.1136/jitc-2020-000896. PMID: 32788237; PMCID: PMC7422657.

Martínez-Vicente P, Farré D, Engel P, Angulo A. Divergent Traits and Ligand-Binding Properties of the Cytomegalovirus CD48 Gene Family. Viruses. 2020 Jul 28;12(8):813. doi: 10.3390/v12080813. PMID: 32731344; PMCID: PMC7472110.

Huerga Encabo H, Traveset L, Argilaguet J, Angulo A, Nistal-Villán E, Jaiswal  R, Escalante CR, Gekas C, Meyerhans A, Aramburu J, López-Rodríguez C. The transcription factor NFAT5 limits infection-induced type I interferon responses.  J Exp Med. 2020 Mar 2;217 (3). pii: e20190449. doi: 10.1084/ jem.20190449. PMID: 31816635

Strazic Geljic I, Kucan Brlic P, Angulo G, Brizic I, Lisnic B, Jenus T, Juranic Lisnic V, Pietri GP, Engel P, Kaynan N, Zeleznjak J, Schu P, Mandelboim O, Krmpotic A, Angulo A, Jonjic S, Lenac Rovis T. Cytomegalovirus protein m154 perturbs the adaptor protein-1 compartment mediating broad-spectrum immune evasion. Elife. 2020 Jan 13;9. pii: e50803. doi: 10.7554/eLife.50803. PMID: 31928630

Kalina T, Fišer K, Pérez-Andrés M, Kuzílková D, Cuenca M, Bartol SJW, Blanco E, Engel P, van Zelm MC. CD Maps-Dynamic Profiling of CD1-CD100 Surface Expression on Human Leukocyte and Lymphocyte Subsets. Front Immunol. 2019 Oct 23;10:2434. doi: 10.3389/fimmu.2019.02434. PMID: 31708916; PMCID: PMC6820661.

Cossarizza A, Chang HD, Radbruch A, Acs A, Adam D, Adam-Klages S, Agace WW, Aghaeepour N, Akdis M, Allez M, et al. Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur J Immunol. 2019 Oct;49(10):1457-1973. doi: 10.1002/eji.201970107. PMID: 31633216; PMCID: PMC7350392.

Kalina T, Lundsten K, Engel P. Relevance of Antibody Validation for Flow Cytometry. Cytometry A. 2020 Feb;97(2):126-136. doi: 10.1002/cyto.a.23895. Epub 2019 Oct 2. PMID: 31577065.

Wang N, Yigit B, van der Poel CE, Cuenca M, Carroll MC, Herzog RW, Engel P, Terhorst C. The Checkpoint Regulator SLAMF3 Preferentially Prevents Expansion of Auto-Reactive B Cells Generated by Graft-vs.-Host Disease. Front Immunol. 2019 Apr 17;10:831. doi: 10.3389/fimmu.2019.00831. PMID: 31057553; PMCID: PMC6482334.

Martínez-Vicente P, Farré D, Sánchez C, Alcamí A, Engel P, Angulo A. Subversion of natural killer cell responses by a cytomegalovirus-encoded soluble CD48 decoy receptor. PLoS Pathog. 2019 Apr 4;15(4):e1007658. doi: 10.1371/journal.ppat.1007658. eCollection 2019 Apr. PMID: 30947296

Sanchez LR, Godoy GJ, Gorosito Serrán M, Breser ML, Fiocca Vernengo F, Engel P, Motrich RD, Gruppi A, Rivero VE. IL-10 Producing B Cells Dampen Protective T Cell Response and Allow Chlamydia muridarumInfection of the Male Genital Tract. Front Immunol. 2019 Mar 1;10:356. doi: 10.3389/fimmu.2019.00356. eCollection 2019. PMID: 30881362

Angulo A, Cuenca M, Martínez-Vicente P, Engel P. Viral CD229 (Ly9) homologs as new manipulators of host immunity. J Leukoc Biol. 2019 Feb 21. doi: 10.1002/JLB.2MR1018-413R. [Epub ahead of print]. Review. PMID: 30791129

Castella M, Boronat A, Martín-Ibáñez R, Rodríguez V, Suñé G, Caballero M, Marzal B, Pérez-Amill L, Martín-Antonio B, Castaño J, Bueno C, Balagué O, González-Navarro EA, Serra-Pages C, Engel P, Vilella R, Benitez-Ribas D, Ortiz-Maldonado V, Cid J, Tabera J, Canals JM, Lozano M, Baumann T, Vilarrodona A, Trias E, Campo E, Menendez P, Urbano-Ispizua Á, Yagüe J, Pérez-Galán P, Rives S, Delgado J, Juan M. Development of a Novel Anti-CD19 Chimeric Antigen Receptor: A Paradigm for an Affordable CAR T Cell Production at Academic Institutions. Mol Ther Methods Clin Dev. 2018 Dec 6;12:134-144. doi: 10.1016/j.omtm.2018.11.010. eCollection 2019 Mar 15. PMID: 30623002

Cuenca M, Sintes J, Lányi Á, Engel P. CD84 cell surface signaling molecule: An emerging biomarker and target for cancer and autoimmune disorders. Clin Immunol. 2018 Oct 26. pii: S1521-6616(18)30567-9. doi: 10.1016/j.clim.2018.10.017. [Epub ahead of print] Review. PMID: 30522694

Pérez-Carmona N, Martínez-Vicente P, Farré D, Gabaev I, Messerle M, Engel P, Angulo A.. A Prominent Role of the Human Cytomegalovirus UL8 Glycoprotein in Restraining Proinflammatory Cytokine Production by Myeloid Cells at Late Times during Infection.J Virol. 2018 Apr 13;92(9). pii: e02229-17. doi: 10.1128/JVI.02229-17. Print 2018 May 1. PMID: 29467314

Agod Z, Pazmandi K, Bencze D, Vereb G, Biro T, Szabo A, Rajnavolgyi E, Bacsi A, Engel P, Lanyi A.. Signaling Lymphocyte Activation Molecule Family 5 Enhances Autophagy and Fine-Tunes Cytokine Response in Monocyte-Derived Dendritic Cells via Stabilization of Interferon Regulatory Factor 8.Front Immunol. 2018 Jan 26;9:62. doi: 10.3389/fimmu.2018.00062. eCollection 2018. PMID: 29434592

Cuenca M, Puñet-Ortiz J, Ruart M, Terhorst C, Engel P.. Ly9 (SLAMF3) receptor differentially regulates iNKT cell development and activation in mice. Eur J Immunol. 2018 Jan;48(1):99-105. doi: 10.1002/eji.201746925. Epub 2017 Nov 7. PMID: 28980301

Pupuleku A, Costa-García M, Farré D, Hengel H, Angulo A, Muntasell A, López-Botet M.. Elusive Role of the CD94/NKG2C NK Cell Receptor in the Response to Cytomegalovirus: Novel Experimental Observations in a Reporter Cell System. Front Immunol. 2017 Oct 24;8:1317. doi: 10.3389/fimmu.2017.01317. eCollection 2017. PMID: 29114247 

Dantoft W, Martínez-Vicente P, Jafali J, Pérez-Martínez L, Martin K, Kotzamanis K, Craigon M, Auer M, Young NT, Walsh P, Marchant A, Angulo A, Forster T, Ghazal P. Genomic Programming of Human Neonatal Dendritic Cells in Congenital Systemic and In Vitro Cytomegalovirus Infection Reveal Plastic and Robust Immune Pathway Biology Responses. Front Immunol. 2017 Sep 25;8:1146. doi: 10.3389/fimmu.2017.01146. eCollection 2017. PMID: 28993767

Cossarizza A, Chang HD, Radbruch A, Akdis M, Andrä I, Annunziato F, Bacher P, Barnaba V, Battistini L, Bauer WM, Baumgart S, Becher B, Beisker W, Berek C, Blanco A, Borsellino G, Boulais PE, Brinkman RR, Büscher M, Busch DH, Bushnell TP, Cao X, Cavani A, Chattopadhyay PK, Cheng Q, Chow S, Clerici M, Cooke A, Cosma A, Cosmi L, Cumano A, Dang VD, Davies D, De Biasi S, Del Zotto G, Della Bella S, Dellabona P, Deniz G, Dessing M, Diefenbach A, Di Santo J, Dieli F, Dolf A, Donnenberg VS, Dörner T, Ehrhardt GRA, Endl E, Engel P, Engelhardt B, Esser C, Everts B, Dreher A, Falk CS, Fehniger TA, Filby A, Fillatreau S, Follo M, Förster I, Foster J, Foulds GA, Frenette PS, Galbraith D, Garbi N, García-Godoy MD, Geginat J, Ghoreschi K, Gibellini L, Goettlinger C, Goodyear CS, Gori A, Grogan J, Gross M, Grützkau A, Grummitt D, Hahn J, Hammer Q, Hauser AE, Haviland DL, Hedley D, Herrera G, Herrmann M, Hiepe F, Holland T, Hombrink P, Houston JP, Hoyer BF, Huang B, Hunter CA, Iannone A, Jäck HM, Jávega B, Jonjic S, Juelke K, Jung S, Kaiser T, Kalina T, Keller B, Khan S, Kienhöfer D, Kroneis T, Kunkel D, Kurts C, Kvistborg P, Lannigan J, Lantz O, Larbi A, LeibundGut-Landmann S, Leipold MD, Levings MK, Litwin V, Liu Y, Lohoff M, Lombardi G, Lopez L, Lovett-Racke A, Lubberts E, Ludewig B, Lugli E, Maecker HT, Martrus G, Matarese G, Maueröder C, McGrath M, McInnes I, Mei HE, Melchers F, Melzer S, Mielenz D, Mills K, Mirrer D, Mjösberg J, Moore J, Moran B, Moretta A, Moretta L, Mosmann TR, Müller S, Müller W, Münz C, Multhoff G, Munoz LE, Murphy KM, Nakayama T, Nasi M, Neudörfl C, Nolan J, Nourshargh S, O'Connor JE, Ouyang W, Oxenius A, Palankar R, Panse I, Peterson P, Peth C, Petriz J, Philips D, Pickl W, Piconese S, Pinti M, Pockley AG, Podolska MJ, Pucillo C, Quataert SA, Radstake TRDJ, Rajwa B, Rebhahn JA, Recktenwald D, Remmerswaal EBM, Rezvani K, Rico LG, Robinson JP, Romagnani C, Rubartelli A, Ruckert B, Ruland J, Sakaguchi S, Sala-de-Oyanguren F, Samstag Y, Sanderson S, Sawitzki B, Scheffold A, Schiemann M, Schildberg F, Schimisky E, Schmid SA, Schmitt S, Schober K, Schüler T, Schulz AR, Schumacher T, Scotta C, Shankey TV, Shemer A, Simon AK, Spidlen J, Stall AM, Stark R, Stehle C, Stein M, Steinmetz T, Stockinger H, Takahama Y, Tarnok A, Tian Z, Toldi G, Tornack J, Traggiai E, Trotter J, Ulrich H, van der Braber M, van Lier RAW, Veldhoen M, Vento-Asturias S, Vieira P, Voehringer D, Volk HD, von Volkmann K, Waisman A, Walker R, Ward MD, Warnatz K, Warth S, Watson JV, Watzl C, Wegener L, Wiedemann A, Wienands J, Willimsky G, Wing J, Wurst P, Yu L, Yue A, Zhang Q, Zhao Y, Ziegler S, Zimmermann J. Guidelines for the use of flow cytometry and cell sorting in immunological studies. Eur J Immunol. 2017 Oct;47(10):1584-1797. doi: 10.1002/eji.201646632. No abstract available

Consuegra-Fernández M, Martínez-Florensa M, Aranda F, de Salort J, Armiger-Borràs N, Lozano T, Casares N, Lasarte JJ, Engel P, Lozano F. Relevance of CD6-Mediated Interactions in the Regulation of Peripheral T-Cell Responses and Tolerance. Front Immunol. 2017 May 30;8:594. doi: 10.3389/fimmu.2017.00594. eCollection 2017. PMID: 28611770

Robertson KA, Hsieh WY, Forster T, Blanc M, Lu H, Crick PJ, Yutuc E, Watterson S, Martin K, Griffiths SJ, Enright AJ, Yamamoto M, Pradeepa MM, Lennox KA, Behlke MA, Talbot S, Haas J, Dölken L, Griffiths WJ, Wang Y, Angulo A, Ghazal P. An Interferon Regulated MicroRNA Provides Broad Cell-Intrinsic Antiviral Immunity through Multihit Host-Directed Targeting of the Sterol Pathway. PLoS Biol. 2016 Mar 3;14(3):e1002364. doi: 10.1371 /journal. pbio.1002364. eCollection 2016 Mar. PMID: 26938778

Wang N, Keszei M, Halibozek P, Yigit B, Engel P, Terhorst C. Slamf6 negatively regulates autoimmunity. Clin Immunol. 2016 Dec;173:19-26. doi: 10.1016/j.clim.2016.06.009. Epub 2016 Jun 29. PMID: 27368806

Yigit B, Halibozek PJ, Chen SS, O'Keeffe MS, Arnason J, Avigan D, Gattei V, Bhan A, Cen O, Longnecker R, Chiorazzi N, Wang N, Engel P, Terhorst C. A combination of an anti-SLAMF6 antibody and ibrutinib efficiently abrogates expansion of chronic lymphocytic leukemia cells.Oncotarget. 2016 May 3;7(18):26346-60. doi: 10.18632/oncotarget.8378. PMID: 27029059.

Clark G, Stockinger H, Balderas R, van Zelm MC, Zola H, Hart D, Engel P. Nomenclature of CD molecules from the Tenth Human Leucocyte Differentiation Antigen Workshop. Clin Transl Immunology. 2016 Jan 22;5(1):e57. doi: 10.1038/cti.2015.38. eCollection 2016 Jan. No abstract available. PMID: 26900471

van Driel BJ, Liao G, Engel P, Terhorst C. Responses to Microbial Challenges by SLAMF Receptors. Front Immunol. 2016 Jan 20;7:4. doi: 10.3389/fimmu.2016.00004. eCollection 2016. Review. PMID: 26834746

Cuenca M, Romero X, Sintes J, Terhorst C, Engel P. Targeting of Ly9 (CD229) Disrupts Marginal Zone and B1 B Cell Homeostasis and Antibody Responses. J Immunol. 2016 Jan 15;196(2):726-37. doi: 10.4049/jimmunol.1501266. Epub 2015 Dec 14. PMID: 26667173

Engel P, Boumsell L, Balderas R, Bensussan A, Gattei V, Horejsi V, Jin BQ, Malavasi F, Mortari F, Schwartz-Albiez R, Stockinger H, van Zelm MC, Zola H, Clark G. CD Nomenclature 2015: Human Leukocyte Differentiation Antigen Workshops as a Driving Force in Immunology. J Immunol. 2015 Nov 15;195(10):4555-63. doi: 10.4049/ jimmunol.1502033. PMID: 26546687

Roncador G, Engel P, Maestre L, Anderson AP, Cordell JL, Cragg MS, Šerbec VČ, Jones M, Lisnic VJ, Kremer L, Li D, Koch-Nolte F, Pascual N, Rodríguez-Barbosa JI, Torensma R, Turley H, Pulford K, Banham AH. The European antibody network's practical guide to finding and validating suitable antibodies for research. MAbs. 2016;8(1):27-36. doi: 10.1080/19420862.2015.1100787. Epub 2015 Sep 29. PMID: 26418356

Pérez-Carmona N, Farré D, Martínez-Vicente P, Terhorst C, Engel P, Angulo A. Signaling Lymphocytic Activation Molecule Family Receptor Homologs in New World Monkey Cytomegaloviruses. J Virol. 2015 Nov;89(22):11323-36. doi: 10.1128/JVI.01296-15. Epub 2015 Sep 2. PMID: 26339044

Kropp KA, Hsieh WY, Isern E, Forster T, Krause E, Brune W, Angulo A, Ghazal P. A temporal gate for viral enhancers to co-opt Toll-like-receptor transcriptional activation pathways upon acute infection. PLoS Pathog. 2015 Apr 9;11(4):e1004737. doi: 10.1371/journal.ppat.1004737. eCollection 2015 Apr. PMID: 25856589

Kotzamanis K, Angulo A, Ghazal P. Infection homeostasis: implications for therapeutic and immune programming of metabolism in controlling infection. Med Microbiol Immunol. 2015 Jun;204(3):395-407. doi: 10.1007/ s00430-015-0402-5. Epub 2015 Mar 24. Review. PMID: 25800350

Romero X, Sintes J, Engel P. Role of SLAM family receptors and specific adapter SAP in innate-like lymphocytes. Crit Rev Immunol. 2014;34(4):263-99. Review. PMID: 24941157

De Calisto J, Wang N, Wang G, Yigit B, Engel P, Terhorst C. SAP-Dependent and -Independent Regulation of Innate T Cell Development Involving SLAMF Receptors. Front Immunol. 2014 Apr 23;5:186. doi:  10.3389/ fimmu.2014. 00186. eCollection 2014. PMID: 24795728

Romero X, Cañete JD, Engel P. Determination of soluble tumor necrosis factor receptor 2 produced by alternative splicing.Methods Mol Biol. 2014;1155:187-99. doi: 10.1007/978-1-4939-0669-7_16. PMID: 24788183

Zarama A, Pérez-Carmona N, Farré D, Tomic A, Borst EM, Messerle M, Jonjic S, Engel P, Angulo A. Cytomegalovirus m154 hinders CD48 cell-surface expression and promotes viral escape from host natural killer cell control. PLoS Pathog. 2014 Mar 13;10(3):e1004000. doi: 10.1371/journal.ppat.1004000. eCollection 2014 Mar. Erratum in: PLoS Pathog. 2014 Apr;10(4):e1004121. PMID: 24626474

Fenutría R, Martinez VG, Simões I, Postigo J, Gil V, Martínez-Florensa M, Sintes J, Naves R, Cashman KS, Alberola-Ila J, Ramos-Casals M, Soldevila G, Raman C, Merino J, Merino R, Engel P, Lozano F. Transgenic expression of soluble human CD5 enhances experimentally-induced autoimmune and anti-tumoral immune responses. PLoS One. 2014 Jan 15;9(1):e84895. doi: 10.1371/journal.pone.0084895. eCollection 2014. PMID: 24454761

Liao G, van Driel B, Magelky E, O'Keeffe MS, de Waal Malefyt R, Engel P, Herzog RW, Mizoguchi E, Bhan AK, Terhorst C. Glucocorticoid-induced TNF receptor family-related protein ligand regulates the migration of monocytes to the inflamed intestine. FASEB J. 2014 Jan;28(1):474-84. doi: 10.1096/fj.13-236505. Epub 2013 Oct 9. PMID: 24107315.

Kropp KA, Angulo A, Ghazal P. Viral enhancer mimicry of host innate-immune promoters. PLoS Pathog. 2014 Feb 6;10(2):e1003804. doi: 10.1371/journal.ppat.1003804. eCollection 2014 Feb. Review. No abstract available. PMID: 24516378

Garcia-Recio S, Fuster G, Fernandez-Nogueira P, Pastor-Arroyo EM, Park SY, Mayordomo C, Ametller E, Mancino M, Gonzalez-Farre X, Russnes HG, Engel P, Costamagna D, Fernandez PL, Gascón P, Almendro V. Substance P autocrine signaling contributes to persistent HER2 activation that drives malignant progression and drug resistance in breast cancer. Cancer Res. 2013 Nov 1;73(21):6424-34. doi: 10.1158/0008-5472.CAN-12-4573. Epub 2013 Sep 12. PMID: 24030979

de Salort J, Cuenca M, Terhorst C, Engel P, Romero X. Ly9 (CD229) Cell-Surface Receptor is Crucial for the Development of Spontaneous Autoantibody Production to Nuclear Antigens. Front Immunol. 2013 Jul 31;4:225. doi: 10.3389/fimmu.2013.00225. eCollection 2013. PMID: 23914190

Sintes J, Cuenca M, Romero X, Bastos R, Terhorst C, Angulo A, Engel P. Cutting edge: Ly9 (CD229), a SLAM family receptor, negatively regulates the development of thymic innate memory-like CD8+ T and invariant NKT cells. J Immunol. 2013 Jan 1;190(1):21-6. doi: 10.4049/jimmunol.1202435. Epub 2012 Dec 7. PMID: 23225888

Muntasell A, Vilches C, Angulo A, López-Botet M. Adaptive reconfiguration of the human NK-cell compartment in response to cytomegalovirus: a different perspective of the host-pathogen interaction. Eur J Immunol. 2013 May;43(5):1133-41. doi: 10.1002/eji.201243117. Review. PMID: 23552990

Engel P, Angulo A. Viral immunomodulatory proteins: usurping host genes as a  survival strategy. Adv Exp Med Biol. 2012;738:256-76. doi: 10.1007/978-1-4614-1680-7_15.

Liao G, Detre C, Berger SB, Engel P, de Waal Malefyt R, Herzog RW, Bhan AK, Terhorst C. Glucocorticoid-induced tumor necrosis factor receptor family-related protein regulates CD4(+)T cell-mediated colitis in mice. Gastroenterology. 2012 Mar;142(3):582-591.e8. doi: 10.1053/j.gastro.2011.11.031. Epub 2011 Dec 6. PMID: 22155173

Rodríguez-Martín S, Kropp KA, Wilhelmi V, Lisnic VJ, Hsieh WY, Blanc M, Livingston A, Busche A, Tekotte H, Messerle M, Auer M, Fraser I, Jonjic S, Angulo A, Reddehase MJ, Ghazal P. Ablation of the regulatory IE1 protein of murine cytomegalovirus alters in vivo pro-inflammatory TNF-alpha production during acute infection. PLoS Pathog. 2012;8(8):e1002901. doi: 10.1371/journal.ppat.1002901. Epub 2012 Aug 30. PMID: 22952450

Shikhagaie M, Mercé-Maldonado E, Isern E, Muntasell A, Albà MM, López-Botet M, Hengel H, Angulo A. The human cytomegalovirus-specific UL1 gene encodes a late-phase glycoprotein incorporated in the virion envelope. J Virol. 2012 Apr;86(8):4091-101. doi: 10.1128/JVI.06291-11. Epub 2012 Feb 15. PMID:22345456

Blanc M, Hsieh WY, Robertson KA, Kropp KA, Forster T, Shui G, Lacaze P, Watterson S, Griffiths SJ, Spann NJ, Meljon A, Talbot S, Krishnan K, Covey DF, Wenk MR, Craigon M, Ruzsics Z, Haas J, Angulo A, Griffiths WJ, Glass CK, Wang Y, Ghazal P. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity. 2013 Jan 24;38(1):106-18. doi: 10.1016/j.immuni.2012.11.004. Epub 2012 Dec 27. PMID: 23273843

Engel P, Pérez-Carmona N, Albà MM, Robertson K, Ghazal P, Angulo A. Human cytomegalovirus UL7, a homologue of the SLAM-family receptor CD229, impairs cytokine production. Immunol Cell Biol. 2011 Oct;89(7):753-66. doi: 10.1038/icb.2011.55. Epub 2011 Jun 14. PMID: 21670740

Keszei M, Detre C, Rietdijk ST, Muñoz P, Romero X, Berger SB, Calpe S, Liao G, Castro W, Julien A, Wu YY, Shin DM, Sancho J, Zubiaur M, Morse HC 3rd, Morel L, Engel P, Wang N, Terhorst C. A novel isoform of the Ly108 gene ameliorates murine lupus. J Exp Med. 2011 Apr 11;208(4):811-22. doi: 10.1084/jem.20101653. Epub 2011 Mar 21. PMID: 21422172

Engel P, Gómez-Puerta JA, Ramos-Casals M, Lozano F, Bosch X. Therapeutic targeting of B cells for rheumatic autoimmune diseases. Pharmacol Rev. 2011 Mar;63(1):127-56. doi: 10.1124/pr.109.002006. Epub 2011 Jan 18. Review. PMID: 21245206

Cañete JD, Albaladejo C, Hernández MV, Laínez B, Pinto JA, Ramírez J, López-Armada MJ, Rodríguez-Cros JR, Engel P, Blanco FJ, Sanmartí R. Clinical significance of high levels of soluble tumour necrosis factor-α receptor-2 produced by alternative splicing in rheumatoid arthritis: a longitudinal prospective cohort study. Rheumatology (Oxford). 2011 Apr;50(4):721-8. doi: 10.1093/rheumatology/keq381. Epub 2010 Dec 6. PMID: 21134963

Sintes J, Engel P. SLAM (CD150) is a multitasking immunoreceptor: from cosignalling to bacterial recognition. Immunol Cell Biol. 2011 Feb;89(2):161-3. doi: 10.1038/icb.2010.145. Epub 2010 Nov 23. No abstract available. PMID:21102539

Wang N, Calpe S, Westcott J, Castro W, Ma C, Engel P, Schatzle JD, Terhorst C. Cutting edge: The adapters EAT-2A and -2B are positive regulators of CD244- and CD84-dependent NK cell functions in the C57BL/6 mouse. J Immunol. 2010 Nov 15;185(10):5683-7. doi: 10.4049/jimmunol.1001974. Epub 2010 Oct 20. PMID: 20962259

Llinàs L, Lázaro A, de Salort J, Matesanz-Isabel J, Sintes J, Engel P. Expression profiles of novel cell surface molecules on B-cell subsets and plasma cells as analyzed by flow cytometry. Immunol Lett. 2011 Jan 30;134(2):113-21. doi: 10.1016/j.imlet.2010.10.009. Epub 2010 Oct 15. PMID: 20951740

De Salort J, Sintes J, Llinàs L, Matesanz-Isabel J, Engel P. Expression of SLAM (CD150) cell-surface receptors on human B-cell subsets: from pro-B to plasma cells. Immunol Lett. 2011 Jan 30;134(2):129-36. doi: 10.1016 /j.imlet. 2010.09.021. Epub 2010 Oct 7. PMID: 20933013

Matesanz-Isabel J, Sintes J, Llinàs L, de Salort J, Lázaro A, Engel P. New B-cell CD molecules. Immunol Lett. 2011 Jan 30;134(2):104-12. doi: 10.1016/j.imlet.2010.09.019. Epub 2010 Oct 7. PMID: 20933010

Díaz-Ramos MC, Engel P, Bastos R. Towards a comprehensive human cell-surface immunome database. Immunol Lett. 2011 Jan 30;134(2):183-7. doi: 10.1016/j.imlet.2010.09.016. Epub 2010 Nov 3. PMID: 20932860

Kropp KA, Robertson KA, Sing G, Rodriguez-Martin S, Blanc M, Lacaze P, Hassim MF, Khondoker MR, Busche A, Dickinson P, Forster T, Strobl B, Mueller M, Jonjic S, Angulo A, Ghazal P. Reversible inhibition of murine cytomegalovirus replication by gamma interferon (IFN-γ) in primary macrophages involves a primed type I IFN-signaling subnetwork for full establishment of an immediate-early antiviral state. J Virol. 2011 Oct;85(19):10286-99. doi: 10.1128/JVI.00373-11. Epub 2011 Jul 20. PMID: 21775459

Romo N, Magri G, Muntasell A, Heredia G, Baía D, Angulo A, Guma M, López-Botet M. Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J Leukoc Biol. 2011 Oct;90(4):717-26. doi: 10.1189/jlb.0311171. Epub 2011 Jul 8. PMID: 21742939

Lacaze P, Forster T, Ross A, Kerr LE, Salvo-Chirnside E, Lisnic VJ, López-Campos GH, García-Ramírez JJ, Messerle M, Trgovcich J, Angulo A, Ghazal P. Temporal profiling of the coding and noncoding murine cytomegalovirus transcriptomes. J Virol. 2011 Jun;85(12):6065-76. doi: 10.1128/JVI.02341-10. Epub 2011 Apr 6. PMID: 21471238

Blanc M, Hsieh WY, Robertson KA, Watterson S, Shui G, Lacaze P, Khondoker M, Dickinson P, Sing G, Rodríguez-Martín S, Phelan P, Forster T, Strobl B, Müller M, Riemersma R, Osborne T, Wenk MR, Angulo A, Ghazal P. Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLoS Biol. 2011 Mar;9(3):e1000598. doi: 10.1371/journal.pbio.1000598. Epub 2011 Mar 8. PMID: 21408089

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