Forty-Five Years of Marburg Virus Research

In 1967, the first reported filovirus hemorrhagic fever outbreak took place in Germany and the former Yugoslavia. The causative agent that was identified during this outbreak, Marburg virus, is one of the most deadly human pathogens. This article provides a comprehensive overview of our current knowledge about Marburg virus disease ranging from ecology to pathogenesis and molecular biology.

[1]  M. Aman,et al.  Advances in virus-like particle vaccines for filoviruses. , 2011, The Journal of infectious diseases.

[2]  M. Katze,et al.  Global Suppression of the Host Antiviral Response by Ebola- and Marburgviruses: Increased Antagonism of the Type I Interferon Response Is Associated with Enhanced Virulence , 2006, Journal of Virology.

[3]  A. Sanchez,et al.  Marburg virus, a filovirus: messenger RNAs, gene order, and regulatory elements of the replication cycle. , 1992, Virus research.

[4]  T. Noda,et al.  Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. , 2008, Cell host & microbe.

[5]  H. Feldmann,et al.  The Ebola Virus Glycoprotein and HIV-1 Vpu Employ Different Strategies to Counteract the Antiviral Factor Tetherin , 2011, The Journal of infectious diseases.

[6]  James L. Riley,et al.  FolateReceptor Alpha and Caveolae Are Not Required for Ebola VirusGlycoprotein-Mediated ViralInfection , 2003, Journal of Virology.

[7]  P. Rollin,et al.  Markedly elevated levels of interferon (IFN)-gamma, IFN-alpha, interleukin (IL)-2, IL-10, and tumor necrosis factor-alpha associated with fatal Ebola virus infection. , 1999, The Journal of infectious diseases.

[8]  R. Ahmed,et al.  Monocyte-Derived Human Macrophages and Peripheral Blood Mononuclear Cells Infected with Ebola Virus Secrete MIP-1α and TNF-α and Inhibit Poly-IC-Induced IFN-α in Vitro , 2001 .

[9]  T. Strecker,et al.  Vacuolar Protein Sorting Pathway Contributes to the Release of Marburg Virus , 2008, Journal of Virology.

[10]  C. Basler,et al.  Filoviral Immune Evasion Mechanisms , 2011, Viruses.

[11]  F. Murphy,et al.  Agent of Disease Contracted from Green Monkeys , 1968, Science.

[12]  Heinz Feldmann,et al.  Single-Injection Vaccine Protects Nonhuman Primates against Infection with Marburg Virus and Three Species of Ebola Virus , 2009, Journal of Virology.

[13]  H. Feldmann,et al.  Ebola virus enters host cells by macropinocytosis and clathrin-mediated endocytosis. , 2011, The Journal of infectious diseases.

[14]  Steven B. Bradfute,et al.  Development and Characterization of a Mouse Model for Marburg Hemorrhagic Fever , 2009, Journal of Virology.

[15]  S. Becker,et al.  Ultrastructural Organization of Recombinant Marburg Virus Nucleoprotein: Comparison with Marburg Virus Inclusions , 2000, Journal of Virology.

[16]  S. Günther,et al.  Response to Imported Case of Marburg Hemorrhagic Fever, the Netherlands , 2009, Emerging infectious diseases.

[17]  M. Raaben,et al.  The Ebola virus glycoprotein mediates entry via a non-classical dynamin-dependent macropinocytic pathway. , 2011, Virology.

[18]  S. Nichol,et al.  Analysis of the role of predicted RNA secondary structures in Ebola virus replication. , 2003, Virology.

[19]  V. Volchkov,et al.  Ectodomain shedding of the glycoprotein GP of Ebola virus , 2004, The EMBO journal.

[20]  W. Weissenhorn,et al.  Crystal structure of the C-terminal domain of Ebola virus VP30 reveals a role in transcription and nucleocapsid association , 2007, Proceedings of the National Academy of Sciences.

[21]  C. Schmaljohn,et al.  Progress in recombinant DNA-derived vaccines for Lassa virus and filoviruses. , 2011, Virus research.

[22]  H. Leirs,et al.  Search for the Ebola virus reservoir in Kikwit, Democratic Republic of the Congo: reflections on a vertebrate collection. , 1999, The Journal of infectious diseases.

[23]  Heinz Feldmann,et al.  Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses , 2005, Nature Medicine.

[24]  H. Klenk,et al.  Forty years of marburg virus. , 2007, The Journal of infectious diseases.

[25]  Stephan Becker,et al.  Comparison of the Transcription and Replication Strategies of Marburg Virus and Ebola Virus by Using Artificial Replication Systems , 1999, Journal of Virology.

[26]  Mark A Olson,et al.  Fold prediction of VP24 protein of Ebola and Marburg viruses using de novo fragment assembly. , 2009, Journal of structural biology.

[27]  P. Jahrling,et al.  Apoptosis Induced In Vitro and In Vivo During Infection by Ebola and Marburg Viruses , 2000, Laboratory Investigation.

[28]  Thomas Hoenen,et al.  Inclusion Bodies Are a Site of Ebolavirus Replication , 2012, Journal of Virology.

[29]  J. Roberts,et al.  Nonhuman Primate Quarantine: Its Evolution and Practice , 2008, ILAR journal.

[30]  H. Klenk,et al.  Intracellular transport and processing of the Marburg virus surface protein in vertebrate and insect cells. , 1996, Virology.

[31]  B. Ligon,et al.  Outbreak of Marburg Hemorrhagic Fever in Angola: A Review of the History of the Disease and its Biological Aspects , 2005, Seminars in Pediatric Infectious Diseases.

[32]  Norman E. Davey,et al.  Cryo-Electron Tomography of Marburg Virus Particles and Their Morphogenesis within Infected Cells , 2011, PLoS biology.

[33]  S. Nichol,et al.  Ebola and marburg hemorrhagic fever. , 2010, Clinics in laboratory medicine.

[34]  A. Kolokoltsov,et al.  The Tyro3 Receptor Kinase Axl Enhances Macropinocytosis of Zaire Ebolavirus , 2010, Journal of Virology.

[35]  Manfred Weidmann,et al.  Rapid detection protocol for filoviruses. , 2004, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[36]  D. Norwood,et al.  Development and evaluation of a fluorogenic 5'-nuclease assay to identify Marburg virus. , 2001, Molecular and cellular probes.

[37]  C. Badger,et al.  A multiagent filovirus DNA vaccine delivered by intramuscular electroporation completely protects mice from ebola and Marburg virus challenge , 2012, Human vaccines & immunotherapeutics.

[38]  P. Rollin,et al.  Markedly elevated levels of interferon (IFN)-γ, IFN-α, interleukin (IL)-2, IL-10, and tumor necrosis factor-α associated with fatal Ebola virus infection , 1999 .

[39]  Andrew Hayhurst,et al.  Rapid assembly of sensitive antigen-capture assays for Marburg virus, using in vitro selection of llama single-domain antibodies, at biosafety level 4. , 2007, The Journal of infectious diseases.

[40]  M. Mavrakis,et al.  Morphology of Marburg virus NP-RNA. , 2002, Virology.

[41]  Lijun Rong,et al.  Comprehensive Analysis of Ebola Virus GP1 in Viral Entry , 2005, Journal of Virology.

[42]  C. Basler,et al.  Marburg Virus VP40 Antagonizes Interferon Signaling in a Species-Specific Manner , 2011, Journal of Virology.

[43]  L. Strelets,et al.  Respiratory Marburg virus infection in guinea pigs , 1996, Archives of Virology.

[44]  J. Casals Marburg Virus Disease , 1972, The Yale Journal of Biology and Medicine.

[45]  Y. Kawaoka,et al.  Human Macrophage C-Type Lectin Specific for Galactose and N-Acetylgalactosamine Promotes Filovirus Entry , 2004, Journal of Virology.

[46]  H. Feldmann,et al.  Recombinant vesicular stomatitis virus-based vaccines against Ebola and Marburg virus infections. , 2011, The Journal of infectious diseases.

[47]  H. Klenk,et al.  VP40, the Matrix Protein of Marburg Virus, Is Associated with Membranes of the Late Endosomal Compartment , 2002, Journal of Virology.

[48]  R. Davey,et al.  The Cytoplasmic Domain of Marburg Virus GP Modulates Early Steps of Viral Infection , 2011, Journal of Virology.

[49]  M. Toribio,et al.  The DC-SIGN-related lectin LSECtin mediates antigen capture and pathogen binding by human myeloid cells. , 2007, Blood.

[50]  H. Klenk,et al.  Phosphorylation of VP30 Impairs Ebola Virus Transcription* , 2002, The Journal of Biological Chemistry.

[51]  Jonathan Y. Richmond,et al.  Biosafety in microbiological and biomedical laboratories , 1999 .

[52]  W. Weissenhorn,et al.  Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. , 1998, Molecular cell.

[53]  H. Klenk,et al.  The Marburg virus surface protein GP is phosphorylated at its ectodomain. , 2002, Virology.

[54]  Yuliang Liu,et al.  Characterization of filovirus protein-protein interactions in mammalian cells using bimolecular complementation. , 2011, The Journal of infectious diseases.

[55]  V. Volchkov,et al.  GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. , 1995, Virology.

[56]  H. Klenk,et al.  VP24 of Marburg Virus Influences Formation of Infectious Particles , 2005, Journal of Virology.

[57]  H. Malherbe,et al.  Marburg virus. , 1970, Lancet.

[58]  O. Dolnik,et al.  Tsg101 Is Recruited by a Late Domain of the Nucleocapsid Protein To Support Budding of Marburg Virus-Like Particles , 2010, Journal of Virology.

[59]  H. Feldmann,et al.  Prospects for immunisation against Marburg and Ebola viruses , 2010, Reviews in medical virology.

[60]  L. Hensley,et al.  Cellular immune response to Marburg virus infection in cynomolgus macaques. , 2008, Viral immunology.

[61]  V. Malashkevich,et al.  Crystal structure of the Marburg virus GP2 core domain in its postfusion conformation. , 2012, Biochemistry.

[62]  H. Klenk,et al.  Interactions of Marburg virus nucleocapsid proteins. , 1998, Virology.

[63]  H. Feldmann,et al.  Breakdown of paraendothelial barrier function during Marburg virus infection is associated with early tyrosine phosphorylation of platelet endothelial cell adhesion molecule-1. , 2007, The Journal of infectious diseases.

[64]  F. Hufert,et al.  Viral load among patients infected with Marburgvirus in Angola. , 2007, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[65]  M. Goldsmith,et al.  Folate Receptor-α Is a Cofactor for Cellular Entry by Marburg and Ebola Viruses , 2001, Cell.

[66]  Lijun Rong,et al.  Characterization of the receptor-binding domain of Ebola glycoprotein in viral entry , 2011, Virologica Sinica.

[67]  A. Kolokoltsov,et al.  Cellular Entry of Ebola Virus Involves Uptake by a Macropinocytosis-Like Mechanism and Subsequent Trafficking through Early and Late Endosomes , 2010, PLoS pathogens.

[68]  O. Dolnik,et al.  Filoviruses: Interactions with the host cell , 2007, Cellular and Molecular Life Sciences.

[69]  V. Volchkov,et al.  Characterization of Marburg virus glycoprotein in viral entry. , 2007, Virology.

[70]  H. Klenk,et al.  The nucleoprotein of Marburg virus is target for multiple cellular kinases. , 1999, Virology.

[71]  S. Harrison,et al.  Long-COVID Symptoms in Individuals Infected with Different SARS-CoV-2 Variants of Concern: A Systematic Review of the Literature , 2022, Viruses.

[72]  L. Fernando,et al.  Assessment of a vesicular stomatitis virus-based vaccine by use of the mouse model of Ebola virus hemorrhagic fever. , 2007, The Journal of infectious diseases.

[73]  S. Whelan,et al.  Endosomal Proteolysis of the Ebola Virus Glycoprotein Is Necessary for Infection , 2005, Science.

[74]  M. Goldsmith,et al.  Association of the Caveola Vesicular System with Cellular Entry by Filoviruses , 2002, Journal of Virology.

[75]  B. Davidson,et al.  Lentivirus Vectors Pseudotyped with Filoviral Envelope Glycoproteins Transduce Airway Epithelia from the Apical Surface Independently of Folate Receptor Alpha , 2003, Journal of Virology.

[76]  D. Peters,et al.  The aetiology of an unknown human infection transmitted by monkeys (preliminary communication). , 1968, German medical monthly.

[77]  G. Korb,et al.  The morbid anatomy of Marburg virus disease. , 1969, German medical monthly.

[78]  J. Dye,et al.  Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 , 2011, Nature.

[79]  D. Simpson,et al.  Vervet monkey disease. Experiment infection of guinea pigs and monkeys with the causative agent. , 1968, British journal of experimental pathology.

[80]  Nikiforov Vv,et al.  A case of a laboratory infection with Marburg fever , 1994 .

[81]  W. Emmett Barkley,et al.  Biosafety in microbiological and biomedical laboratories , 1984 .

[82]  D. Simpson Marburg agent disease: in monkeys. , 1969, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[83]  J. A. Comer,et al.  Marburgvirus Genomics and Association with a Large Hemorrhagic Fever Outbreak in Angola , 2006, Journal of Virology.

[84]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[85]  S. Harrison,et al.  Structural basis for membrane fusion by enveloped viruses. , 1999, Molecular membrane biology.

[86]  H. Feldmann,et al.  Marburg virus gene 4 encodes the virion membrane protein, a type I transmembrane glycoprotein , 1993, Journal of virology.

[87]  N. I. Gonchar,et al.  [The sensitivity of different experimental animals to the Marburg virus]. , 1991, Voprosy virusologii.

[88]  W. Slenczka The Marburg virus outbreak of 1967 and subsequent episodes. , 1999, Current topics in microbiology and immunology.

[89]  M. Georges-Courbot,et al.  Marburgvirus nucleoprotein-capture enzyme-linked immunosorbent assay using monoclonal antibodies to recombinant nucleoprotein: detection of authentic Marburgvirus. , 2006, Japanese journal of infectious diseases.

[90]  V. Volchkov,et al.  Ebola virus failure to stimulate plasmacytoid dendritic cell interferon responses correlates with impaired cellular entry. , 2011, The Journal of infectious diseases.

[91]  Filoviruses: A Compendium of 40 Years of Epidemiological, Clinical, and Laboratory Studies , 2009, Emerging Infectious Diseases.

[92]  V. Volchkov,et al.  Rescue of Recombinant Marburg Virus from cDNA Is Dependent on Nucleocapsid Protein VP30 , 2006, Journal of Virology.

[93]  H. Klenk,et al.  The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. , 1995, The Journal of general virology.

[94]  D. Swenson,et al.  Monovalent virus-like particle vaccine protects guinea pigs and nonhuman primates against infection with multiple Marburg viruses , 2008, Expert review of vaccines.

[95]  Yuliang Liu,et al.  Conserved Motifs within Ebola and Marburg Virus VP40 Proteins Are Important for Stability, Localization, and Subsequent Budding of Virus-Like Particles , 2009, Journal of Virology.

[96]  P. Jahrling,et al.  Characterization of a new Marburg virus isolated from a 1987 fatal case in Kenya. , 1996, Archives of virology. Supplementum.

[97]  G. Neumann,et al.  Tyro3 Family-Mediated Cell Entry of Ebola and Marburg Viruses , 2006, Journal of Virology.

[98]  P. Formenty,et al.  Outbreak of Marburg hemorrhagic fever among miners in Kamwenge and Ibanda Districts, Uganda, 2007. , 2011, The Journal of infectious diseases.

[99]  K. Johnson,et al.  MARBURG-VIRUS DISEASE IN KENYA , 1982, The Lancet.

[100]  L. Roux,et al.  The Activity of Sendai Virus Genomic and Antigenomic Promoters Requires a Second Element Past the Leader Template Regions: a Motif (GNNNNN)3 Is Essential for Replication , 1998, Journal of Virology.

[101]  S. Becker,et al.  Co- and posttranslational modifications and functions of Marburg virus proteins. , 1999, Current topics in microbiology and immunology.

[102]  J. Gonzalez,et al.  Large serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat populations, and a high seroprevalence of both viruses in Rousettus aegyptiacus , 2009, BMC infectious diseases.

[103]  Lori E Dodd,et al.  Evaluation of perceived threat differences posed by filovirus variants. , 2011, Biosecurity and bioterrorism : biodefense strategy, practice, and science.

[104]  C. Roth,et al.  Risk Factors for Marburg Hemorrhagic Fever, Democratic Republic of the Congo , 2003, Emerging infectious diseases.

[105]  H. Klenk,et al.  Three of the Four Nucleocapsid Proteins of Marburg Virus, NP, VP35, and L, Are Sufficient To Mediate Replication and Transcription of Marburg Virus-Specific Monocistronic Minigenomes , 1998, Journal of Virology.

[106]  J. Briggs,et al.  Electron Tomography Reveals the Steps in Filovirus Budding , 2010, PLoS pathogens.

[107]  A. Schmaljohn,et al.  Genomic differences between guinea pig lethal and nonlethal Marburg virus variants. , 2007, The Journal of infectious diseases.

[108]  W. Stille,et al.  Clinical Course and Prognosis of Marburg Virus (“Green-Monkey”) Disease , 1971 .

[109]  Elliot J. Lefkowitz,et al.  Virus taxonomy: classification and nomenclature of viruses , 2012 .

[110]  S. Günther,et al.  Diagnostic Reverse-Transcription Polymerase Chain Reaction Kit for Filoviruses Based on the Strain Collections of all European Biosafety Level 4 Laboratories , 2007, The Journal of infectious diseases.

[111]  A. Sanchez Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. , 2007, The Journal of infectious diseases.

[112]  Steven J M Jones,et al.  Vesicular stomatitis virus-based vaccines protect nonhuman primates against aerosol challenge with Ebola and Marburg viruses. , 2008, Vaccine.

[113]  D. Simpson,et al.  Fatal human disease from vervet monkeys. , 1967, Lancet.

[114]  S. Whelan,et al.  Transcription and replication of nonsegmented negative-strand RNA viruses. , 2004, Current topics in microbiology and immunology.

[115]  B. Miller,et al.  Field investigations of an outbreak of Ebola hemorrhagic fever, Kikwit, Democratic Republic of the Congo, 1995: arthropod studies. , 1999, The Journal of infectious diseases.

[116]  P. Bates,et al.  Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein , 2009, Proceedings of the National Academy of Sciences.

[117]  H. Feldmann,et al.  The Ebola virus ribonucleoprotein complex: a novel VP30-L interaction identified. , 2009, Virus research.

[118]  Morris Ca,et al.  Letter: Bowie and Dick test for autoclaves. , 1974 .

[119]  G. Ruthel,et al.  Antiviral Activity of a Small-Molecule Inhibitor of Filovirus Infection , 2010, Antimicrobial Agents and Chemotherapy.

[120]  H. Ebihara,et al.  Clinical aspects of Marburg hemorrhagic fever. , 2011, Future virology.

[121]  H. Solcher,et al.  [On the neuropathology of the green monkey (Cercopithecus aethiops) transmitted infectious diseases in Marburg]. , 1968, Deutsche medizinische Wochenschrift.

[122]  Mike Bray,et al.  Basic clinical and laboratory features of filoviral hemorrhagic fever. , 2011, The Journal of infectious diseases.

[123]  H. Klenk,et al.  Acylation of the Marburg virus glycoprotein. , 1995, Virology.

[124]  P. Jahrling,et al.  Treatment of Ebola virus infection with a recombinant inhibitor of factor VIIa/tissue factor: a study in rhesus monkeys , 2003, The Lancet.

[125]  K. Mansfield,et al.  A small nonhuman primate model for filovirus-induced disease , 2011, Virology.

[126]  J. Modrof,et al.  Ebola Virus Transcription Activator VP30 Is a Zinc-Binding Protein , 2003, Journal of Virology.

[127]  J. Yasuda,et al.  Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. , 2010, The Journal of general virology.

[128]  M. Aman,et al.  Virus-like particles exhibit potential as a pan-filovirus vaccine for both Ebola and Marburg viral infections. , 2005, Vaccine.

[129]  G. Ruthel,et al.  Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. , 2003, The Journal of infectious diseases.

[130]  G. Ignatyev,et al.  Inactivated Marburg virus elicits a nonprotective immune response in Rhesus monkeys. , 1996, Journal of biotechnology.

[131]  Stephan Becker,et al.  Ebola Virus VP30-Mediated Transcription Is Regulated by RNA Secondary Structure Formation , 2002, Journal of Virology.

[132]  E. Ryabchikova,et al.  Ebola and Marburg Viruses: A View of Infection Using Electron Microscopy , 2002 .

[133]  D. Swenson,et al.  Vaccine To Confer to Nonhuman Primates Complete Protection against Multistrain Ebola and Marburg Virus Infections , 2008, Clinical and Vaccine Immunology.

[134]  V. Krähling,et al.  The Marburg Virus 3′ Noncoding Region Structurally and Functionally Differs from That of Ebola Virus , 2009, Journal of Virology.

[135]  A. MacNeil,et al.  Serology and cytokine profiles in patients infected with the newly discovered Bundibugyo ebolavirus. , 2012, Virology.

[136]  S. Bavari,et al.  Key Genomic Changes Necessary for an In Vivo Lethal Mouse Marburgvirus Variant Selection Process , 2011, Journal of Virology.

[137]  C. Kunz,et al.  [Biological and morphological characteristics of the "hemorrhagic fever" virus occurring in Germany]. , 1968, Wiener klinische Wochenschrift.

[138]  P. Formenty,et al.  Studies of Reservoir Hosts for Marburg Virus , 2007, Emerging infectious diseases.

[139]  Christian Drosten,et al.  Rapid Detection and Quantification of RNA of Ebola and Marburg Viruses, Lassa Virus, Crimean-Congo Hemorrhagic Fever Virus, Rift Valley Fever Virus, Dengue Virus, and Yellow Fever Virus by Real-Time Reverse Transcription-PCR , 2002, Journal of Clinical Microbiology.

[140]  H. Feldmann,et al.  The nucleotide sequence of the L gene of Marburg virus, a filovirus: homologies with paramyxoviruses and rhabdoviruses. , 1992, Virology.

[141]  T. Hope,et al.  Differential requirements for clathrin endocytic pathway components in cellular entry by Ebola and Marburg glycoprotein pseudovirions. , 2011, Virology.

[142]  S. Nichol,et al.  A C-terminal basic amino acid motif of Zaire ebolavirus VP35 is essential for type I interferon antagonism and displays high identity with the RNA-binding domain of another interferon antagonist, the NS1 protein of influenza A virus. , 2004, Virology.

[143]  T. Meyer,et al.  Inhibition of Marburg virus protein expression and viral release by RNA interference. , 2005, The Journal of general virology.

[144]  L. Fernando,et al.  Postexposure protection against Marburg haemorrhagic fever with recombinant vesicular stomatitis virus vectors in non-human primates: an efficacy assessment , 2006, The Lancet.

[145]  Augustine Goba,et al.  Comprehensive panel of real-time TaqMan polymerase chain reaction assays for detection and absolute quantification of filoviruses, arenaviruses, and New World hantaviruses. , 2010, The American journal of tropical medicine and hygiene.

[146]  M. Goldsmith,et al.  Folate receptor-alpha is a cofactor for cellular entry by Marburg and Ebola viruses. , 2001, Cell.

[147]  E. Lefkowitz,et al.  Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2014) , 2014, Archives of Virology.

[148]  H. Feldmann,et al.  Marburg and Ebola hemorrhagic fevers: does the primary course of infection depend on the accessibility of organ-specific macrophages? , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[149]  T. Noda,et al.  Identification of amino acids in Marburg virus VP40 that are important for virus-like particle budding. , 2011, The Journal of infectious diseases.

[150]  H. Feldmann,et al.  Cross-Protection against Marburg Virus Strains by Using a Live, Attenuated Recombinant Vaccine , 2006, Journal of Virology.

[151]  W. Weissenhorn,et al.  Oligomerization and polymerization of the filovirus matrix protein VP40. , 2003, Virology.

[152]  W. Garten,et al.  Role of the Transmembrane Domain of Marburg Virus Surface Protein GP in Assembly of the Viral Envelope , 2007, Journal of Virology.

[153]  A. K. Hansen,et al.  Marburg and Ebola virus infections in laboratory non-human primates: a literature review. , 2000, Comparative medicine.

[154]  A. Sanchez,et al.  Covalent Modifications of the Ebola Virus Glycoprotein , 2002, Journal of Virology.

[155]  Y. Kawaoka,et al.  Different Potential of C-Type Lectin-Mediated Entry between Marburg Virus Strains , 2010, Journal of Virology.

[156]  M. Aman,et al.  Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. , 2004, FEMS immunology and medical microbiology.

[157]  C. Möritz,et al.  Phosphorylation of Marburg virus VP30 at serines 40 and 42 is critical for its interaction with NP inclusions. , 2001, Virology.

[158]  C. Rupprecht,et al.  Marburg Virus in Fruit Bat, Kenya , 2010, Emerging infectious diseases.

[159]  M. Bray The role of the Type I interferon response in the resistance of mice to filovirus infection. , 2001, The Journal of general virology.

[160]  H. Feldmann,et al.  The nucleoprotein of Marburg virus is phosphorylated. , 1994, The Journal of general virology.

[161]  S. Becker,et al.  Phosphorylation of Marburg virus NP region II modulates viral RNA synthesis. , 2011, The Journal of infectious diseases.

[162]  M. Aman,et al.  Marburg virus-like particles protect guinea pigs from lethal Marburg virus infection. , 2004, Vaccine.

[163]  A. Peterson,et al.  Geographic potential for outbreaks of Marburg hemorrhagic fever. , 2006, The American journal of tropical medicine and hygiene.

[164]  M. E. Miranda,et al.  Reston ebolavirus in humans and animals in the Philippines: a review. , 2011, The Journal of infectious diseases.

[165]  C. B. Robbins,et al.  A search for Ebola virus in animals in the Democratic Republic of the Congo and Cameroon: ecologic, virologic, and serologic surveys, 1979-1980. Ebola Virus Study Teams. , 1999, The Journal of infectious diseases.

[166]  H. Feldmann,et al.  Infection and Activation of Monocytes by Marburg and Ebola Viruses , 2001, Journal of Virology.

[167]  V. Blinov,et al.  Characterization of the L gene and 5' trailer region of Ebola virus. , 1999, The Journal of general virology.

[168]  N. Gallagher,et al.  Imported case of Marburg hemorrhagic fever - Colorado, 2008. , 2009, MMWR. Morbidity and mortality weekly report.

[169]  Kathryn L. Schornberg,et al.  Role of Endosomal Cathepsins in Entry Mediated by the Ebola Virus Glycoprotein , 2006, Journal of Virology.

[170]  Hong-gang Yu,et al.  De novo syntheses of Marburg virus antigens from adenovirus vectors induce potent humoral and cellular immune responses. , 2006, Vaccine.

[171]  P. Formenty,et al.  Marburg Virus Angola Infection of Rhesus Macaques: Pathogenesis and Treatment with Recombinant Nematode Anticoagulant Protein c2 , 2007, The Journal of infectious diseases.

[172]  A. N. Sergeev,et al.  [Certain pathogenetic characteristics of a disease in monkeys in infected with the Marburg virus by an airborne route]. , 1995, Voprosy virusologii.

[173]  T. Monath Ecology of Marburg and Ebola viruses: speculations and directions for future research. , 1999, The Journal of infectious diseases.

[174]  P. Geldenhuys,et al.  Epidemiologic investigation of Marburg virus disease, Southern Africa, 1975. , 1978, The American journal of tropical medicine and hygiene.

[175]  V. Volchkov,et al.  Role of VP30 phosphorylation in the Ebola virus replication cycle. , 2011, The Journal of infectious diseases.

[176]  H. Feldmann,et al.  Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages , 1996, Journal of virology.

[177]  S. Becker,et al.  Both matrix proteins of Ebola virus contribute to the regulation of viral genome replication and transcription. , 2010, Virology.

[178]  Sinroku Otatume,et al.  Ebola haemorrhagic fever in Zaire , 1996 .

[179]  S. Becker,et al.  Establishment and application of an infectious virus-like particle system for Marburg virus. , 2010, The Journal of general virology.

[180]  T. Geisbert,et al.  Marburg hemorrhagic fever: report of a case studied by immunohistochemistry and electron microscopy. , 1998, Ultrastructural pathology.

[181]  Gabriele Neumann,et al.  Ebolavirus Is Internalized into Host Cells via Macropinocytosis in a Viral Glycoprotein-Dependent Manner , 2010, PLoS pathogens.

[182]  P. Iversen,et al.  Advanced antisense therapies for postexposure protection against lethal filovirus infections , 2010, Nature Medicine.

[183]  H. Feldmann,et al.  Carbohydrate structure of Marburg virus glycoprotein , 1992, Glycobiology.

[184]  A. Sanchez,et al.  The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[185]  V. Blinov,et al.  The GP‐protein of Marburg virus contains the region similar to the ‘immunosuppressive domain’ of oncogenic retrovirus P15E proteins , 1993, FEBS letters.

[186]  D. Peters,et al.  The Marburg agent and structures associated with leptospira. , 1969, Lancet.

[187]  I. Zlotnik Marburg agent disease: pathology. , 1969, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[188]  E. Mühlberger Filovirus replication and transcription. , 2007, Future virology.

[189]  P. Jahrling,et al.  Marburg virus vaccines: comparing classical and new approaches. , 2001, Vaccine.

[190]  M. Borchert,et al.  The Medecins Sans Frontieres intervention in the Marburg hemorrhagic fever epidemic, Uige, Angola, 2005. I. Lessons learned in the hospital. , 2007, The Journal of infectious diseases.

[191]  P. Bieniasz,et al.  Broad-Spectrum Inhibition of Retroviral and Filoviral Particle Release by Tetherin , 2008, Journal of Virology.

[192]  H. Klenk,et al.  Homo-Oligomerization of Marburgvirus VP35 Is Essential for Its Function in Replication and Transcription , 2005, Journal of Virology.

[193]  D. Peters,et al.  Morphology, Development, and Classification of the Marburg Virus , 1971 .

[194]  S. Becker,et al.  The Matrix Protein of Marburg Virus Is Transported to the Plasma Membrane along Cellular Membranes: Exploiting the Retrograde Late Endosomal Pathway , 2004, Journal of Virology.

[195]  A. Sanchez,et al.  Characterization of filoviruses based on differences in structure and antigenicity of the virion glycoprotein. , 1994, Virology.

[196]  J. Smith,et al.  Marburg virus vaccines based upon alphavirus replicons protect guinea pigs and nonhuman primates. , 1998, Virology.

[197]  Heinz Feldmann,et al.  Disease modeling for Ebola and Marburg viruses , 2009, Disease Models & Mechanisms.

[198]  W. Sundquist,et al.  An interferon-alpha-induced tethering mechanism inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. , 2007, Cell host & microbe.

[199]  H. Feldmann,et al.  The nonstructural small glycoprotein sGP of Ebola virus is secreted as an antiparallel-orientated homodimer. , 1998, Virology.

[200]  T. Noda,et al.  Ebola virus (EBOV) VP24 inhibits transcription and replication of the EBOV genome. , 2007, The Journal of infectious diseases.

[201]  Sergeev An,et al.  Certain pathogenetic characteristics of a disease in monkeys in infected with the Marburg virus by an airborne route , 1995 .

[202]  V. Volchkov,et al.  Role of Ebola Virus VP30 in Transcription Reinitiation , 2008, Journal of Virology.

[203]  H. Feldmann,et al.  Development and Evaluation of a Simple Assay for Marburg Virus Detection Using a Reverse Transcription-Loop-Mediated Isothermal Amplification Method , 2010, Journal of Clinical Microbiology.

[204]  M. Lackemeyer,et al.  Aerosol Exposure to the Angola Strain of Marburg Virus Causes Lethal Viral Hemorrhagic Fever in Cynomolgus Macaques , 2010, Veterinary pathology.

[205]  Basolateral budding of Marburg virus: VP40 retargets viral glycoprotein GP to the basolateral surface. , 2007, The Journal of infectious diseases.

[206]  Joshua C. Johnson,et al.  Postexposure Treatment of Marburg Virus Infection , 2010, Emerging infectious diseases.

[207]  E. Mühlberger,et al.  The Ebola Virus Genomic Replication Promoter Is Bipartite and Follows the Rule of Six , 2005, Journal of Virology.

[208]  K. Mansfield,et al.  Recombinant Vesicular Stomatitis Virus Vaccine Vectors Expressing Filovirus Glycoproteins Lack Neurovirulence in Nonhuman Primates , 2012, PLoS neglected tropical diseases.

[209]  Laurent Roux,et al.  Paramyxovirus mRNA editing, the "rule of six" and error catastrophe: a hypothesis. , 2005, The Journal of general virology.

[210]  H. Feldmann,et al.  Proteolytic processing of Marburg virus glycoprotein. , 2000, Virology.

[211]  Alan Kemp,et al.  Isolation of Genetically Diverse Marburg Viruses from Egyptian Fruit Bats , 2009, PLoS pathogens.

[212]  F. Salguero,et al.  Lethality and pathogenesis of airborne infection with filoviruses in A129 α/β -/- interferon receptor-deficient mice. , 2012, Journal of medical microbiology.

[213]  B. Ivins,et al.  Comparison of individual and combination DNA vaccines for B. anthracis, Ebola virus, Marburg virus and Venezuelan equine encephalitis virus. , 2003, Vaccine.

[214]  J. Stoker,et al.  The Department of Health and Human Services. , 1999, Home healthcare nurse.

[215]  H. Feldmann,et al.  Replication of Marburg virus in human endothelial cells. A possible mechanism for the development of viral hemorrhagic disease. , 1993, The Journal of clinical investigation.

[216]  H. Feldmann,et al.  Glycosylation and oligomerization of the spike protein of marburg virus , 1991, Virology.

[217]  M. V. Regenmortel,et al.  Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. , 2000 .

[218]  Alan Kemp,et al.  Marburg hemorrhagic fever associated with multiple genetic lineages of virus. , 2006, The New England journal of medicine.

[219]  R. Ahmed,et al.  Monocyte-derived human macrophages and peripheral blood mononuclear cells infected with ebola virus secrete MIP-1alpha and TNF-alpha and inhibit poly-IC-induced IFN-alpha in vitro. , 2001, Virology.

[220]  M. Saijo,et al.  Enzyme-Linked Immunosorbent Assays for Detection of Antibodies to Ebola and Marburg Viruses Using Recombinant Nucleoproteins , 2001, Journal of Clinical Microbiology.

[221]  S. Becker,et al.  Multivesicular Bodies as a Platform for Formation of the Marburg Virus Envelope , 2004, Journal of Virology.

[222]  G. Grard,et al.  Marburg Virus Infection Detected in a Common African Bat , 2007, PloS one.

[223]  Steven J M Jones,et al.  Vesicular Stomatitis Virus-Based Ebola Vaccine Is Well-Tolerated and Protects Immunocompromised Nonhuman Primates , 2008, PLoS pathogens.

[224]  J. Gonzalez,et al.  Is Marburg virus enzootic in Gabon? , 2011, The Journal of infectious diseases.

[225]  Heinz Feldmann,et al.  A New Ebola Virus Nonstructural Glycoprotein Expressed through RNA Editing , 2011, Journal of Virology.

[226]  N. Tordo,et al.  Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. , 1990, The Journal of general virology.

[227]  Kimihito Ito,et al.  Enzyme-Linked Immunosorbent Assay for Detection of Filovirus Species-Specific Antibodies , 2010, Clinical and Vaccine Immunology.

[228]  S. Pöhlmann,et al.  Cathepsins B and L activate Ebola but not Marburg virus glycoproteins for efficient entry into cell lines and macrophages independent of TMPRSS2 expression , 2012, Virology.

[229]  R. Salt,et al.  PERCUTANEOUS LUNG BIOPSY , 1976, The Lancet.

[230]  M. Goldsmith,et al.  Distinct Mechanisms of Entry by Envelope Glycoproteins of Marburg and Ebola (Zaire) Viruses , 2000, Journal of virology.

[231]  Steven B. Bradfute,et al.  Development of a model for marburgvirus based on severe-combined immunodeficiency mice , 2007, Virology Journal.

[232]  R. Koup,et al.  Vector Choice Determines Immunogenicity and Potency of Genetic Vaccines against Angola Marburg Virus in Nonhuman Primates , 2010, Journal of Virology.

[233]  Kimihito Ito,et al.  Detection of all known filovirus species by reverse transcription-polymerase chain reaction using a primer set specific for the viral nucleoprotein gene. , 2011, Journal of virological methods.

[234]  H. Klenk,et al.  Sorting of Marburg Virus Surface Protein and Virus Release Take Place at Opposite Surfaces of Infected Polarized Epithelial Cells , 2001, Journal of Virology.

[235]  P. Collins,et al.  Transcription elongation factor of respiratory syncytial virus, a nonsegmented negative-strand RNA virus. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[236]  Claire Marie Filone,et al.  Filoviruses Require Endosomal Cysteine Proteases for Entry but Exhibit Distinct Protease Preferences , 2012, Journal of Virology.

[237]  S. Longhi,et al.  Ebola Virus VP30 Is an RNA Binding Protein , 2007, Journal of Virology.

[238]  G. Ruthel,et al.  Ebola and Marburg virus-like particles activate human myeloid dendritic cells. , 2004, Virology.

[239]  A. Steinkasserer,et al.  DC-SIGN and DC-SIGNR Interact with the Glycoprotein of Marburg Virus and the S Protein of Severe Acute Respiratory Syndrome Coronavirus , 2004, Journal of Virology.

[240]  J. Gonzalez,et al.  Fruit bats as reservoirs of Ebola virus , 2005, Nature.

[241]  S. Becker,et al.  Phosphorylation of Marburg virus matrix protein VP40 triggers assembly of nucleocapsids with the viral envelope at the plasma membrane , 2012, Cellular microbiology.

[242]  H. Klenk,et al.  Oligomerization of Ebola Virus VP30 Is Essential for Viral Transcription and Can Be Inhibited by a Synthetic Peptide* , 2003, Journal of Biological Chemistry.

[243]  V. Krähling,et al.  Recombinant Marburg virus expressing EGFP allows rapid screening of virus growth and real-time visualization of virus spread. , 2011, The Journal of infectious diseases.

[244]  G. Palacios,et al.  Implication of a retrovirus‐like glycoprotein peptide in the immunopathogenesis of Ebola and Marburg viruses , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[245]  N. Wauquier,et al.  Human Fatal Zaire Ebola Virus Infection Is Associated with an Aberrant Innate Immunity and with Massive Lymphocyte Apoptosis , 2010, PLoS neglected tropical diseases.

[246]  C. Basler,et al.  Marburg Virus Evades Interferon Responses by a Mechanism Distinct from Ebola Virus , 2010, PLoS pathogens.

[247]  A. Peterson,et al.  Potential Mammalian Filovirus Reservoirs , 2004, Emerging infectious diseases.

[248]  G. Martini Marburg agent disease: in man. , 1969, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[249]  V. V. Nikiforov,et al.  [A case of a laboratory infection with Marburg fever]. , 1994, Zhurnal mikrobiologii, epidemiologii, i immunobiologii.

[250]  R. Davey,et al.  T-cell immunoglobulin and mucin domain 1 (TIM-1) is a receptor for Zaire Ebolavirus and Lake Victoria Marburgvirus , 2011, Proceedings of the National Academy of Sciences.

[251]  H. Feldmann,et al.  Viral hemorrhagic fever – a vascular disease? , 2003, Thrombosis and Haemostasis.

[252]  Ari Helenius,et al.  Virus entry by macropinocytosis , 2009, Nature Cell Biology.

[253]  T. Bothwell,et al.  Outbreake of Marburg virus disease in Johannesburg. , 1975, British medical journal.

[254]  Slenczka Wg The Marburg virus outbreak of 1967 and subsequent episodes. , 1999 .

[255]  L. Pereboeva,et al.  Ebola virus infection in guinea pigs: presumable role of granulomatous inflammation in pathogenesis , 1996, Archives of Virology.

[256]  H. Feldmann Marburg hemorrhagic fever--the forgotten cousin strikes. , 2006, The New England journal of medicine.

[257]  F. Kirchhoff,et al.  LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus , 2005, Virology.

[258]  J. Kuhn,et al.  Conserved Receptor-binding Domains of Lake Victoria Marburgvirus and Zaire Ebolavirus Bind a Common Receptor* , 2006, Journal of Biological Chemistry.

[259]  Steven B. Bradfute,et al.  Filovirus infection of STAT-1 knockout mice. , 2011, The Journal of infectious diseases.

[260]  L. Hensley,et al.  Pathogenesis of Marburg hemorrhagic fever in cynomolgus macaques. , 2011, The Journal of infectious diseases.

[261]  S. Becker,et al.  Budding of Marburgvirus is associated with filopodia , 2007, Cellular microbiology.

[262]  T. Ksiazek,et al.  High-throughput molecular detection of hemorrhagic fever virus threats with applications for outbreak settings. , 2007, The Journal of infectious diseases.

[263]  S. Becker,et al.  Nucleocapsid formation and RNA synthesis of Marburg virus is dependent on two coiled coil motifs in the nucleoprotein , 2007, Virology Journal.

[264]  P. Jahrling,et al.  Antigenicity and vaccine potential of Marburg virus glycoprotein expressed by baculovirus recombinants. , 1997, Virology.

[265]  P. Jahrling,et al.  Differentiation of filoviruses by electron microscopy. , 1995, Virus research.