Drug Reaction with Eosinophilia and Systemic Symptoms (DRESS): A Multiorgan Antiviral T Cell Response

A dangerous drug reaction may be caused by a severe immune response to reactivated resident herpes viruses. Drug Sensitivity: Don’t Wake Up the Baby (Virus) The benefits of drugs almost always come with a cost. Anticonvulsants and antibiotics are no exception. Some of these commonly used drugs can cause a skin reaction so severe, appearing several weeks after use, that the patient is treated as a burn victim. Called DRESS (drug reaction with eosinophilia and systemic symptoms), this response results in death 10% of the time. A better understanding of DRESS would be a boon to diagnosis and treatment. Data from 40 DRESS patients gathered by Picard and his colleagues now move us a few steps closer to this goal. They find that the symptoms of DRESS are largely a result of activated immune cells directed at herpes virus–related antigens, which home to the skin and visceral organs. The culprit drugs may reactivate quiescent herpes viruses lurking in the patients’ genomes, triggering expansion of these misguided cells. A careful look at the T lymphocytes from 40 patients with DRESS—induced by carbamazepine, allopurinol, or sulfamethoxazole—revealed excess numbers of activated cytotoxic CD8+ T cells, which had surface proteins directing them to skin and other organs. The cells secreted cytokines such as tumor necrosis factor–α (TNF-α) and interferon-γ (IFN-γ) and expressed genes characteristic of inflammation. To get a better handle on the antigen targets of these activated T cells, the authors tested whether the patients showed viral reactivation, which had been noted before in some patients with DRESS. Not only did 76% of the patients show activation of previously quiescent Epstein-Barr virus (EBV) or human herpes viruses 6 or 7 (HHV-6, HHV-7), but a large proportion of the activated CD8 T cells in blood and affected organs carried T cell receptor sequences known to be specific for antigens from EBV. (Specific sequences for HHV-6 or HHV-7 are not available.) Cellular stimulation by antigenic peptides from EBV confirmed this result. The authors propose that DRESS is caused by an EBV (or other similar virus)–driven selection of CD8+ T lymphocytes, which in turn inappropriately attack multiple organs. They think that the culprit drugs may trigger activation of the patients’ dormant EBV by an as yet undefined mechanism, possibly directly. Indeed, they found that the three culprit drugs induce EBV production in EBV-transformed cells from DRESS patients but not from healthy controls, setting the stage for discovering just what it is that makes some people susceptible to DRESS. Drug reaction with eosinophilia and systemic symptoms (DRESS) is a severe, drug-induced reaction that involves both the skin and the viscera. Evidence for reactivation of herpes family viruses has been seen in some DRESS patients. To understand the immunological components of DRESS and their relationship to viral reactivation, we prospectively assessed 40 patients exhibiting DRESS in response to carbamazepine, allopurinol, or sulfamethoxazole. Peripheral blood T lymphocytes from the patients were evaluated for phenotype, cytokine secretion, and repertoire of CD4+ and CD8+ and for viral reactivation. We found Epstein-Barr virus (EBV), human herpes virus 6 (HHV-6), or HHV-7 reactivation in 76% of the patients. In all patients, circulating CD8+ T lymphocytes were activated, exhibited increased cutaneous homing markers, and secreted large amounts of tumor necrosis factor–α and interferon-γ. The production of these cytokines was particularly high in patients with the most severe visceral involvement. In addition, expanded populations of CD8+ T lymphocytes sharing the same T cell receptor repertoire were detected in the blood, skin, liver, and lungs of patients. Nearly half of these expanded blood CD8+ T lymphocytes specifically recognized one of several EBV epitopes. Finally, we found that the culprit drugs triggered the production of EBV in patients’ EBV-transformed B lymphocytes. Thus, cutaneous and visceral symptoms of DRESS are mediated by activated CD8+ T lymphocytes, which are largely directed against herpes viruses such as EBV.

[1]  R. Lucas,et al.  Epstein-Barr virus infection , 2012, Neurology.

[2]  V. Descamps,et al.  Early effects of drugs responsible for DRESS on HHV-6 replication in vitro. , 2009, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[3]  C. Rouzioux,et al.  HHV‐6 and EBV DNA quantitation in lymph nodes of 86 patients with Hodgkin's lymphoma , 2007, Journal of medical virology.

[4]  Yuan-Tsong Chen,et al.  Human leukocyte antigens and drug hypersensitivity , 2007, Current opinion in allergy and clinical immunology.

[5]  A. Rickinson,et al.  Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. , 2007, Annual review of immunology.

[6]  S. Kenney,et al.  Valproic acid enhances the efficacy of chemotherapy in EBV-positive tumors by increasing lytic viral gene expression. , 2006, Cancer research.

[7]  M. Tohyama,et al.  Reactivation of human herpesvirus (HHV) family members other than HHV‐6 in drug‐induced hypersensitivity syndrome , 2006, The British journal of dermatology.

[8]  T. Shiohara,et al.  Several herpesviruses can reactivate in a severe drug‐induced multiorgan reaction in the same sequential order as in graft‐versus‐host disease , 2006, The British journal of dermatology.

[9]  R. Regal,et al.  Antibiotic allergy [16] , 2006 .

[10]  Y. Le Meur,et al.  Multiplex real-time PCR assay for simultaneous quantitation of human cytomegalovirus and herpesvirus-6 in polymorphonuclear and mononuclear cells of transplant recipients. , 2006, Journal of virological methods.

[11]  M. Pirmohamed,et al.  Clinical practice. Antibiotic allergy. , 2006, The New England journal of medicine.

[12]  Munir Pirmohamed,et al.  Genetic factors in the predisposition to drug-induced hypersensitivity reactions , 2006, The AAPS Journal.

[13]  R. Nicol,et al.  Carbamazepine is an inhibitor of histone deacetylases. , 2005, Life sciences.

[14]  W. Pichler,et al.  Delayed Drug Hypersensitivity Reactions , 2003, Annals of Internal Medicine.

[15]  J. Carretero-Gómez,et al.  Antiepileptic drug hypersensitivity syndrome in a patient treated with valproate. , 2003, British journal of clinical pharmacology.

[16]  D. Danilenko,et al.  Transgenic overexpression of human IL-17E results in eosinophilia, B-lymphocyte hyperplasia, and altered antibody production. , 2002, Blood.

[17]  S. Alain,et al.  Real-Time PCR for Quantification of Human Herpesvirus 6 DNA from Lymph Nodes and Saliva , 2002, Journal of Clinical Microbiology.

[18]  M. Guenther,et al.  Histone Deacetylase Is a Direct Target of Valproic Acid, a Potent Anticonvulsant, Mood Stabilizer, and Teratogen* , 2001, The Journal of Biological Chemistry.

[19]  P. Dubus,et al.  Sodium valproate‐induced cutaneous pseudolymphoma followed by recurrence with carbamazepine , 2001, The British journal of dermatology.

[20]  N. Shear,et al.  The drug hypersensitivity syndrome: what is the pathogenesis? , 2001, Archives of dermatology.

[21]  B. Crickx,et al.  Association of human herpesvirus 6 infection with drug reaction with eosinophilia and systemic symptoms. , 2001, Archives of dermatology.

[22]  M. Bonneville,et al.  Frequent Contribution of T Cell Clonotypes with Public TCR Features to the Chronic Response Against a Dominant EBV-Derived Epitope: Application to Direct Detection of Their Molecular Imprint on the Human Peripheral T Cell Repertoire1 , 2000, The Journal of Immunology.

[23]  M. Caligiuri,et al.  Endogenous CD8+ T cell expansion during regression of monoclonal EBV-associated posttransplant lymphoproliferative disorder. , 1999, Journal of immunology.

[24]  H. Takada,et al.  Restricted diversification of T‐cells in chronic active Epstein‐Barr virus infection: Potential inclination to T‐lymphoproliferative disease , 1999, American journal of hematology.

[25]  M. Park,et al.  Lamotrigine Monotherapy in Newly Diagnosed Untreated Epilepsy: A Double‐Blind Comparison with Phenytoin , 1999, Epilepsia.

[26]  M. Bonneville,et al.  Frequent enrichment for CD8 T cells reactive against common herpes viruses in chronic inflammatory lesions: towards a reassessment of the physiopathological significance of T cell clonal expansions found in autoimmune inflammatory processes , 1999, European journal of immunology.

[27]  P. Kourilsky,et al.  Immune-mediated destruction of melanocytes in halo nevi is associated with the local expansion of a limited number of T cell clones. , 1999, Journal of immunology.

[28]  J. Roujeau,et al.  Increased levels of interleukin 5 are associated with the generation of eosinophilia in drug‐induced hypersensitivity syndrome , 1998, The British journal of dermatology.

[29]  V. Levitsky,et al.  The clonal composition of a peptide-specific oligoclonal CTL repertoire selected in response to persistent EBV infection is stable over time. , 1998, Journal of immunology.

[30]  S. L. Silins,et al.  Selection of a diverse TCR repertoire in response to an Epstein-Barr virus-encoded transactivator protein BZLF1 by CD8+ cytotoxic T lymphocytes during primary and persistent infection. , 1997, International immunology.

[31]  D. Zehnder,et al.  Comprehensive hospital drug monitoring (CHDM): adverse skin reactions, a 20‐year survey , 1997, Allergy.

[32]  S. L. Silins,et al.  Development of Epstein-Barr virus-specific memory T cell receptor clonotypes in acute infectious mononucleosis , 1996, The Journal of experimental medicine.

[33]  P. Kourilsky,et al.  Expansion of a recurrent V beta 5.3+ T-cell population in newly diagnosed and untreated HLA-DR2 multiple sclerosis patients. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[34]  L. Hughes-Davies,et al.  Severe adverse cutaneous reactions to drugs. , 1995, The New England journal of medicine.

[35]  M. Brodie,et al.  Open multicentre trial of lamotrigine in patients with treatment resistant epilepsy withdrawing from add-on to lamotrigine monotherapy , 1994 .

[36]  V. Paradis,et al.  Twelve-year analysis of severe cases of drug reaction with eosinophilia and systemic symptoms: a cause of unpredictable multiorgan failure. , 2009, Archives of dermatology.

[37]  T. Shiohara,et al.  Drug-induced Hypersensitivity Syndrome(DIHS): A Reaction Induced by a Complex Interplay among Herpesviruses and Antiviral and Antidrug Immune Responses. , 2006, Allergology international : official journal of the Japanese Society of Allergology.

[38]  J. Kolls,et al.  Interleukin-17: an emerging role in lung inflammation. , 2003, American journal of respiratory cell and molecular biology.

[39]  James J. Campbell,et al.  Expression of the chemokine receptors CCR4, CCR5, and CXCR3 by human tissue-infiltrating lymphocytes. , 2002, The American journal of pathology.