Human Endogenous Retrovirus Type W Envelope from Multiple Sclerosis Demyelinating Lesions Shows Unique Solubility and Antigenic Characteristics.

Antigen Brain Demyelination Endogenous retrovirus Envelope Glycolipids HERV-W Hexamer Lipids MSRV-ENV Multiple sclerosis (MS) Oligomer Sulfatides Syncytin

Journal

Virologica Sinica
ISSN: 1995-820X
Titre abrégé: Virol Sin
Pays: Netherlands
ID NLM: 101514185

Informations de publication

Date de publication:
Oct 2021
Historique:
received: 02 02 2021
accepted: 08 02 2021
pubmed: 27 3 2021
medline: 3 11 2021
entrez: 26 3 2021
Statut: ppublish

Résumé

In multiple sclerosis (MS), human endogenous retrovirus W family (HERV-W) envelope protein, pHERV-W ENV, limits remyelination and induces microglia-mediated neurodegeneration. To better understand its role, we examined the soluble pHERV-W antigen from MS brain lesions detected by specific antibodies. Physico-chemical and antigenic characteristics confirmed differences between pHERV-W ENV and syncytin-1. pHERV-W ENV monomers and trimers remained associated with membranes, while hexamers self-assembled from monomers into a soluble macrostructure involving sulfatides in MS brain. Extracellular hexamers are stabilized by internal hydrophobic bonds and external hydrophilic moieties. HERV-W studies in MS also suggest that this diffusible antigen may correspond to a previously described high-molecular-weight neurotoxic factor secreted by MS B-cells and thus represents a major agonist in MS pathogenesis. Adapted methods are now needed to identify encoding HERV provirus(es) in affected cells DNA. The properties and origin of MS brain pHERV-W ENV soluble antigen will allow a better understanding of the role of HERVs in MS pathogenesis. The present results anyhow pave the way to an accurate detection of the different forms of pHERV-W ENV antigen with appropriate conditions that remained unseen until now.

Identifiants

pubmed: 33770381
doi: 10.1007/s12250-021-00372-0
pii: 10.1007/s12250-021-00372-0
pmc: PMC8558138
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1006-1026

Informations de copyright

© 2021. The Author(s).

Références

Anderson ND, de Borja R, Young MD, Fuligni F, Rosic A, Roberts ND, Hajjar S, Layeghifard M, Novokmet A, Kowalski PE, Anaka M, Davidson S, Zarrei M, Id Said B, Schreiner LC, Marchand R, Sitter J, Gokgoz N, Brunga L, Graham GT, Fullam A, Pillay N, Toretsky JA, Yoshida A, Shibata T, Metzler M, Somers GR, Scherer SW, Flanagan AM, Campbell PJ, Schiffman JD, Shago M, Alexandrov LB, Wunder JS, Andrulis IL, Malkin D, Behjati S, Shlien A (2018) Rearrangement bursts generate canonical gene fusions in bone and soft tissue tumors. Science 361
Antony JM, van Marle G, Opii W, Butterfield DA, Mallet F, Yong VW, Wallace JL, Deacon RM, Warren K, Power C (2004) Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat Neurosci 7:1088–1095
pubmed: 15452578
Ardui S, Ameur A, Vermeesch JR, Hestand MS (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res 46:2159–2168
pubmed: 29401301 pmcid: 5861413
Beimforde N, Hanke K, Ammar I, Kurth R, Bannert N (2008) Molecular cloning and functional characterization of the human endogenous retrovirus K113. Virology 371:216–225
pubmed: 18076964
Blond JL, Beseme F, Duret L, Bouton O, Bedin F, Perron H, Mandrand B, Mallet F (1999) Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family. J Virol 73:1175–1185
pubmed: 9882319 pmcid: 103938
Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL (2000) An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 74:3321–3329
pubmed: 10708449 pmcid: 111833
Bo L, Geurts JJ, Ravid R, Barkhof F (2004) Magnetic resonance imaging as a tool to examine the neuropathology of multiple sclerosis. Neuropathol Appl Neurobiol 30:106–117
pubmed: 15043708
Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, Imbeault M, Izsvak Z, Levin HL, Macfarlan TS, Mager DL, Feschotte C (2018) Ten things you should know about transposable elements. Genome Biol 19:199
pubmed: 30454069 pmcid: 6240941
Charvet B, Reynaud JM, Gourru-Lesimple G, Perron H, Marche PN, Horvat B (2018) Induction of proinflammatory multiple sclerosis-associated retrovirus envelope protein by Human Herpesvirus-6A and CD46 Receptor engagement. Front Immunol 9:2803
pubmed: 30574140 pmcid: 6291489
Cheynet V, Ruggieri A, Oriol G, Blond JL, Boson B, Vachot L, Verrier B, Cosset FL, Mallet F (2005) Synthesis, assembly, and processing of the Env ERVWE1/syncytin human endogenous retroviral envelope. J Virol 79:5585–5593
pubmed: 15827173 pmcid: 1082723
Curtin F, Perron H, Kromminga A, Porchet H, Lang AB (2015) Preclinical and early clinical development of GNbAC1, a humanized IgG4 monoclonal antibody targeting endogenous retroviral MSRV-Env protein. MAbs 7:265–275
pubmed: 25427053
do Olival GS, Faria TS, Nali LH, de Oliveira AC, Casseb J, Vidal JE, Cavenaghi VB, Tilbery CP, Moraes L, Fink MC, Sumita LM, Perron H, Romano CM (2013) Genomic analysis of ERVWE2 locus in patients with multiple sclerosis: absence of genetic association but potential role of human endogenous retrovirus type W elements in molecular mimicry with myelin antigen. Front Microbiol 4:172
pubmed: 23805135 pmcid: 3693062
Dupressoir A, Lavialle C, Heidmann T (2012) From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33:663–671
pubmed: 22695103
Fatima S, Sen P, Sneha P, Priyadoss CG (2017a) Erratum to: hydrophobic interaction between Domain I of albumin and B chain of detemir may support myristate-dependent detemir-albumin binding. Appl Biochem Biotechnol 182:870
pubmed: 27914019
Fatima S, Sen P, Sneha P, Priyadoss CG (2017b) Hydrophobic interaction between Domain I of Albumin and B Chain of detemir may support Myristate-dependent Detemir-Albumin binding. Appl Biochem Biotechnol 182:82–96
pubmed: 27854036
Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283–296
pubmed: 22421730
Firouzi R, Rolland A, Michel M, Jouvin-Marche E, Hauw JJ, Malcus-Vocanson C, Lazarini F, Gebuhrer L, Seigneurin JM, Touraine JL, Sanhadji K, Marche PN, Perron H (2003) Multiple sclerosis-associated retrovirus particles cause T lymphocyte-dependent death with brain hemorrhage in humanized SCID mice model. J Neurovirol 9:79–93
pubmed: 12587071
Garcia-Montojo M, Dominguez-Mozo M, Arias-Leal A, Garcia-Martinez A, De las Heras V, Casanova I, Faucard R, Gehin N, Madeira A, Arroyo R, Curtin F, Alvarez-Lafuente R, Perron H (2013) The DNA copy number of human endogenous retrovirus-W (MSRV-type) is increased in multiple sclerosis patients and is influenced by gender and disease severity. PLoS One 8:e53623.
Gimenez JMF (2007) ERVWE1 ( endogenous retroviral family W, Env(C7), member 1). Atlas Genet Cytogenet OncolHaematol 12:14
Gong R, Peng X, Kang S, Feng H, Huang J, Zhang W, Lin D, Tien P, Xiao G (2005) Structural characterization of the fusion core in syncytin, envelope protein of human endogenous retrovirus family W. Biochem Biophys Res Commun 331:1193–1200
pubmed: 15883002 pmcid: 7092852
Gottle P, Forster M, Gruchot J, Kremer D, Hartung HP, Perron H, Kury P (2019) Rescuing the negative impact of human endogenous retrovirus envelope protein on oligodendroglial differentiation and myelination. Glia 67:160–170
pubmed: 30430656
Grandi N, Tramontano E (2018a) HERV envelope proteins: physiological role and pathogenic potential in cancer and autoimmunity. Front Microbiol 9:462
pubmed: 29593697 pmcid: 5861771
Grandi N, Tramontano E (2018b) Human endogenous retroviruses are ancient acquired elements still shaping innate immune responses. Front Immunol 9:2039
pubmed: 30250470 pmcid: 6139349
Haahr S, Sommerlund M, Moller-Larsen A, Nielsen R, Hansen HJ (1991) Just another dubious virus in cells from a patient with multiple sclerosis? Lancet 337:863–864
pubmed: 1672959
Hancks DC, Kazazian HH Jr (2016) Roles for retrotransposon insertions in human disease. Mob DNA 7:9
pubmed: 27158268 pmcid: 4859970
Hanke K, Kramer P, Seeher S, Beimforde N, Kurth R, Bannert N (2009) Reconstitution of the ancestral glycoprotein of human endogenous retrovirus k and modulation of its functional activity by truncation of the cytoplasmic domain. J Virol 83:12790–12800
pubmed: 19812154 pmcid: 2786854
Huddleston J, Chaisson MJP, Steinberg KM, Warren W, Hoekzema K, Gordon D, Graves-Lindsay TA, Munson KM, Kronenberg ZN, Vives L, Peluso P, Boitano M, Chin CS, Korlach J, Wilson RK, Eichler EE (2017) Discovery and genotyping of structural variation from long-read haploid genome sequence data. Genome Res 27:677–685
pubmed: 27895111 pmcid: 5411763
Iourov IY, Vorsanova SG, Yurov YB (2010) Somatic genome variations in health and disease. Curr Genomics 11:387–396
pubmed: 21358982 pmcid: 3018718
Ironside JW, Head MW (2004) Neuropathology and molecular biology of variant Creutzfeldt-Jakob disease. Curr Top Microbiol Immunol 284:133–159
pubmed: 15148991
Jacques PE, Jeyakani J, Bourque G (2013) The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9:e1003504.
Kazazian HH Jr, Moran JV (2017) Mobile DNA in health and disease. N Engl J Med 377:361–370
pubmed: 28745987 pmcid: 5980640
Kipp M, van der Valk P, Amor S (2012) Pathology of multiple sclerosis. CNS Neurol Disord Drug Targets 11:506–517
pubmed: 22583433
Komurian-Pradel F, Paranhos-Baccala G, Bedin F, Ounanian-Paraz A, Sodoyer M, Ott C, Rajoharison A, Garcia E, Mallet F, Mandrand B, Perron H (1999) Molecular cloning and characterization of MSRV-related sequences associated with retrovirus-like particles. Virology 260:1–9
pubmed: 10405350
Kremer D, Forster M, Schichel T, Gottle P, Hartung HP, Perron H, Kury P (2015) The neutralizing antibody GNbAC1 abrogates HERV-W envelope protein-mediated oligodendroglial maturation blockade. Mult Scler 21:1200–1203
pubmed: 25480862
Kremer D, Gruchot J, Weyers V, Oldemeier L, Gottle P, Healy L, Ho Jang J, Kang TXY, Volsko C, Dutta R, Trapp BD, Perron H, Hartung HP, Kury P (2019a) pHERV-W envelope protein fuels microglial cell-dependent damage of myelinated axons in multiple sclerosis. Proc Natl Acad Sci U S A 116:15216–15225
pubmed: 31213545 pmcid: 6660731
Kremer D, Perron H, Kury P (2019b) Reply to Ruprecht and Mayer: Unearthing genomic fossils in the pathogenesis of multiple sclerosis. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1912315116
doi: 10.1073/pnas.1912315116 pubmed: 31455745 pmcid: 6778245
Kremer D, Schichel T, Forster M, Tzekova N, Bernard C, van der Valk P, van Horssen J, Hartung HP, Perron H, Kury P (2013) Human endogenous retrovirus type W envelope protein inhibits oligodendroglial precursor cell differentiation. Ann Neurol 74:721–732
pubmed: 23836485
Kury P, Nath A, Creange A, Dolei A, Marche P, Gold J, Giovannoni G, Hartung HP, Perron H (2018) Human endogenous retroviruses in neurological diseases. Trends Mol Med 24:379–394
pubmed: 29551251 pmcid: 7185488
Lassmann H (2014) Multiple sclerosis: lessons from molecular neuropathology. Exp Neurol 262 Pt A:2–7.
Levet S, Medina J, Joanou J, Demolder A, Queruel N, Reant K, Normand M, Seffals M, Dimier J, Germi R, Piofczyk T, Portoukalian J, Touraine JL, Perron H (2017) An ancestral retroviral protein identified as a therapeutic target in type-1 diabetes. JCI Insight 2
Lisak RP, Nedelkoska L, Benjamins JA, Schalk D, Bealmear B, Touil H, Li R, Muirhead G, Bar-Or A (2017) B cells from patients with multiple sclerosis induce cell death via apoptosis in neurons in vitro. J Neuroimmunol 309:88–99
pubmed: 28601295
Malone MJ, Conole J (1969) Sulfatides and demyelination. Subcellular localization in metachromatic leukodystrophy. Arch Neurol 21:32–43
pubmed: 5772549
Mantere T, Kersten S, Hoischen A (2019) Long-read sequencing emerging in medical genetics. Front Genet 10:426
pubmed: 31134132 pmcid: 6514244
Marks P, Garcia S, Barrio AM, Belhocine K, Bernate J, Bharadwaj R, Bjornson K, Catalanotti C, Delaney J, Fehr A, Fiddes IT, Galvin B, Heaton H, Herschleb J, Hindson C, Holt E, Jabara CB, Jett S, Keivanfar N, Kyriazopoulou-Panagiotopoulou S, Lek M, Lin B, Lowe A, Mahamdallie S, Maheshwari S, Makarewicz T, Marshall J, Meschi F, O’Keefe CJ, Ordonez H, Patel P, Price A, Royall A, Ruark E, Seal S, Schnall-Levin M, Shah P, Stafford D, Williams S, Wu I, Xu AW, Rahman N, MacArthur D, Church DM (2019) Resolving the full spectrum of human genome variation using Linked-Reads. Genome Res 29:635–645
pubmed: 30894395 pmcid: 6442396
Medina J, Perron H (2017) DNA sequences from mobile genetic elements, a hidden half of the human genome. Med Sci (Paris) 33:151–158
Morandi E, Tanasescu R, Tarlinton RE, Constantinescu CS, Zhang W, Tench C, Gran B (2017) The association between human endogenous retroviruses and multiple sclerosis: A systematic review and meta-analysis. PLoS ONE 12. https://doi.org/10.1371/journal.pone.0172415
Moyano AL, Pituch K, Li G, van Breemen R, Mansson JE, Givogri MI (2013) Levels of plasma sulfatides C18: 0 and C24: 1 correlate with disease status in relapsing-remitting multiple sclerosis. J Neurochem 127:600–604
pubmed: 23777394
Naudi A, Cabre R, Jove M, Ayala V, Gonzalo H, Portero-Otin M, Ferrer I, Pamplona R (2015) Lipidomics of human brain aging and Alzheimer’s disease pathology. Int Rev Neurobiol 122:133–189
pubmed: 26358893
Noorali S, Rotar IC, Lewis C, Pestaner JP, Pace DG, Sison A, Bagasra O (2009) Role of HERV-W syncytin-1 in placentation and maintenance of human pregnancy. Appl Immunohistochem Mol Morphol 17:319–328
pubmed: 19407656
Pace JK 2nd, Feschotte C (2007) The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res 17:422–432
pubmed: 17339369 pmcid: 1832089
Payer LM, Burns KH (2019) Transposable elements in human genetic disease. Nat Rev Genet 20:760–772
pubmed: 31515540
Perron H, Dougier-Reynaud HL, Lomparski C, Popa I, Firouzi R, Bertrand JB, Marusic S, Portoukalian J, Jouvin-Marche E, Villiers CL, Touraine JL, Marche PN (2013) Human endogenous retrovirus protein activates innate immunity and promotes experimental allergic encephalomyelitis in mice. PLoS One 8:e80128
Perron H, Firouzi R, Tuke P, Garson JA, Michel M, Beseme F, Bedin F, Mallet F, Marcel E, Seigneurin JM, Mandrand B (1997a) Cell cultures and associated retroviruses in multiple sclerosis. Collaborative Research Group on MS. Acta Neurol Scand Suppl 169:22–31
pubmed: 9174637
Perron H, Garson JA, Bedin F, Beseme F, Paranhos-Baccala G, Komurian-Pradel F, Mallet F, Tuke PW, Voisset C, Blond JL, Lalande B, Seigneurin JM, Mandrand B (1997b) Molecular identification of a novel retrovirus repeatedly isolated from patients with multiple sclerosis. The Collaborative Research Group on Multiple Sclerosis. Proc Natl Acad Sci U S A 94:7583–7588
pubmed: 9207135 pmcid: 23865
Perron H, Germi R, Bernard C, Garcia-Montojo M, Deluen C, Farinelli L, Faucard R, Veas F, Stefas I, Fabriek BO, Van-Horssen J, Van-der-Valk P, Gerdil C, Mancuso R, Saresella M, Clerici M, Marcel S, Creange A, Cavaretta R, Caputo D, Arru G, Morand P, Lang AB, Sotgiu S, Ruprecht K, Rieckmann P, Villoslada P, Chofflon M, Boucraut J, Pelletier J, Hartung HP (2012) Human endogenous retrovirus type W envelope expression in blood and brain cells provides new insights into multiple sclerosis disease. Mult Scler 18:1721–1736
pubmed: 22457345 pmcid: 3573672
Perron H, Jouvin-Marche E, Michel M, Ounanian-Paraz A, Camelo S, Dumon A, Jolivet-Reynaud C, Marcel F, Souillet Y, Borel E, Gebuhrer L, Santoro L, Marcel S, Seigneurin JM, Marche PN, Lafon M (2001) Multiple sclerosis retrovirus particles and recombinant envelope trigger an abnormal immune response in vitro, by inducing polyclonal Vbeta16 T-lymphocyte activation. Virology 287:321–332
pubmed: 11531410
Perron H, Lang A (2010) The human endogenous retrovirus link between genes and environment in multiple sclerosis and in multifactorial diseases associating neuroinflammation. Clin Rev Allergy Immunol 39:51–61
pubmed: 19697163
Perron H, Lazarini F, Ruprecht K, Pechoux-Longin C, Seilhean D, Sazdovitch V, Creange A, Battail-Poirot N, Sibai G, Santoro L, Jolivet M, Darlix JL, Rieckmann P, Arzberger T, Hauw JJ, Lassmann H (2005) Human endogenous retrovirus (HERV)-W ENV and GAG proteins: physiological expression in human brain and pathophysiological modulation in multiple sclerosis lesions. J Neurovirol 11:23–33
pubmed: 15804956
Roebke C, Wahl S, Laufer G, Stadelmann C, Sauter M, Mueller-Lantzsch N, Mayer J, Ruprecht K (2010) An N-terminally truncated envelope protein encoded by a human endogenous retrovirus W locus on chromosome Xq22.3. Retrovirology 7:69
Ruigrok K, Vaney MC, Buchrieser J, Baquero E, Hellert J, Baron B, England P, Schwartz O, Rey FA, Backovic M (2019) X-ray Structures of the Post-fusion 6-Helix Bundle of the Human Syncytins and their Functional Implications. J Mol Biol 431:4922–4940
pubmed: 31711961 pmcid: 7094397
Ruprecht K, Mayer J (2019) On the origin of a pathogenic HERV-W envelope protein present in multiple sclerosis lesions. Proc Natl Acad Sci U S A 116:19791–19792
pubmed: 31455746 pmcid: 6778242
Schupbach J, Tomasik Z, Nadal D, Ledergerber B, Flepp M, Opravil M, Boni J (2000) Use of HIV-1 p24 as a sensitive, precise and inexpensive marker for infection, disease progression and treatment failure. Int J Antimicrob Agents 16:441–445
pubmed: 11118855
Sedlazeck FJ, Rescheneder P, Smolka M, Fang H, Nattestad M, von Haeseler A, Schatz MC (2018) Accurate detection of complex structural variations using single-molecule sequencing. Nat Methods 15:461–468
pubmed: 29713083 pmcid: 5990442
Soe K, Andersen TL, Hobolt-Pedersen AS, Bjerregaard B, Larsson LI, Delaisse JM (2011) Involvement of human endogenous retroviral syncytin-1 in human osteoclast fusion. Bone 48:837–846
pubmed: 21111077
Strick R, Ackermann S, Langbein M, Swiatek J, Schubert SW, Hashemolhosseini S, Koscheck T, Fasching PA, Schild RL, Beckmann MW, Strissel PL (2007) Proliferation and cell-cell fusion of endometrial carcinoma are induced by the human endogenous retroviral Syncytin-1 and regulated by TGF-beta. J Mol Med (Berl) 85:23–38
Suchanski J, Ugorski M (2016) The biological role of sulfatides. Postepy Hig Med Dosw (Online) 70:489–504
Thomas J, Perron H, Feschotte C (2018) Variation in proviral content among human genomes mediated by LTR recombination. Mob DNA 9:36
pubmed: 30568734 pmcid: 6298018
van Horssen J, van der Pol S, Nijland P, Amor S, Perron H (2016) Human endogenous retrovirus W in brain lesions: rationale for targeted therapy in multiple sclerosis. Mult Scler Relat Disord 8:11–18
pubmed: 27456869
Wildschutte JH, Williams ZH, Montesion M, Subramanian RP, Kidd JM, Coffin JM (2016) Discovery of unfixed endogenous retrovirus insertions in diverse human populations. Proc Natl Acad Sci U S A 113:E2326-2334
pubmed: 27001843 pmcid: 4843416
Wilson R, Tocher DR (1991) Lipid and fatty acid composition is altered in plaque tissue from multiple sclerosis brain compared with normal brain white matter. Lipids 26:9–15
pubmed: 2051890
Xanthopoulos K, Polymenidou M, Bellworthy SJ, Benestad SL, Sklaviadis T (2009) Species and strain glycosylation patterns of PrPSc. PLoS One 4:e5633
Zhang H, Pandey S, Travers M, Sun H, Morton G, Madzo J, Chung W, Khowsathit J, Perez-Leal O, Barrero CA, Merali C, Okamoto Y, Sato T, Pan J, Garriga J, Bhanu NV, Simithy J, Patel B, Huang J, Raynal NJ, Garcia BA, Jacobson MA, Kadoch C, Merali S, Zhang Y, Childers W, Abou-Gharbia M, Karanicolas J, Baylin SB, Zahnow CA, Jelinek J, Grana X, Issa JJ (2018) Targeting CDK9 reactivates epigenetically silenced genes in cancer. Cell 175:1244-1258.e26
pubmed: 30454645 pmcid: 6247954

Auteurs

Benjamin Charvet (B)

GeNeuro Innovation, Lyon, 69008, France. bc@geneuro.com.
CIRI, International Center for Infectiology Research, INSERM U1111, CNRS UMR5308, University of Lyon, ENS Lyon, France. bc@geneuro.com.
Université Claude Bernard Lyon 1, Lyon, 69000, France. bc@geneuro.com.

Justine Pierquin (J)

GeNeuro Innovation, Lyon, 69008, France.

Joanna Brunel (J)

GeNeuro Innovation, Lyon, 69008, France.
CIRI, International Center for Infectiology Research, INSERM U1111, CNRS UMR5308, University of Lyon, ENS Lyon, France.
Université Claude Bernard Lyon 1, Lyon, 69000, France.

Rianne Gorter (R)

Department of Pathology, Amsterdam UMC, Location VUMC, 1007 MB, Amsterdam, The Netherlands.

Christophe Quétard (C)

ProteinSimple, Abingdon, OX14 3NB, UK.

Branka Horvat (B)

CIRI, International Center for Infectiology Research, INSERM U1111, CNRS UMR5308, University of Lyon, ENS Lyon, France.
Université Claude Bernard Lyon 1, Lyon, 69000, France.

Sandra Amor (S)

Department of Pathology, Amsterdam UMC, Location VUMC, 1007 MB, Amsterdam, The Netherlands.
Centre for Neuroscience and Trauma, Blizard Institute, Barts and London School of Medicine and Dentistry, Queen Mary University of London, London, E1 2AT, UK.

Jacques Portoukalian (J)

Université Claude Bernard Lyon 1, Lyon, 69000, France.

Hervé Perron (H)

GeNeuro Innovation, Lyon, 69008, France. hp@geneuro.com.
Université Claude Bernard Lyon 1, Lyon, 69000, France. hp@geneuro.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH