Ebolavirus Glycoprotein Fc Fusion Protein Protects Guinea Pigs against Lethal Challenge

Konduru, Krishnamurthy; Shurtleff, Amy C.; Bradfute, Steven B.; Nakamura, Siham; Bavari, Sina; Kaplan, Gerardo; Tsuji, Moriya

doi:10.1371/journal.pone.0162446

Title: Ebolavirus Glycoprotein Fc Fusion Protein Protects Guinea Pigs against Lethal Challenge

Journal Article · Tue Sep 13 00:00:00 EDT 2016 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0162446· OSTI ID:1377872

Konduru, Krishnamurthy ^[1]; Shurtleff, Amy C. ^[2]; Bradfute, Steven B. ^[3]; Nakamura, Siham ^[1]; Bavari, Sina ^[2]; Kaplan, Gerardo ^[1]; Tsuji, Moriya ^[4]

Food and Drug Administration, Silver Spring, MD (United States)
United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD (United States)
United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD (United States); Univ. of New Mexico, Albuquerque, NM (United States)
Rockefeller Univ., New York, NY (United States)

Ebola virus (EBOV), a member of the Filoviridae that can cause severe hemorrhagic fever in humans and nonhuman primates, poses a significant threat to the public health. Currently, there are no licensed vaccines or therapeutics to prevent and treat EBOV infection. Several vaccines based on the EBOV glycoprotein (GP) are under development, including vectored, virus-like particles, and protein-based subunit vaccines. We previously demonstrated that a subunit vaccine containing the extracellular domain of the Ebola ebolavirus (EBOV) GP fused to the Fc fragment of human IgG1 (EBOVgp-Fc) protected mice against EBOV lethal challenge. Here, we show that the EBOVgp-Fc vaccine formulated with QS-21, alum, or polyinosinic-polycytidylic acid-poly-L-lysine carboxymethylcellulose (poly-ICLC) adjuvants induced strong humoral immune responses in guinea pigs. The vaccinated animals developed anti-GP total antibody titers of approximately 10⁵–10⁶ and neutralizing antibody titers of approximately 10³ as assessed by a BSL-2 neutralization assay based on vesicular stomatitis virus (VSV) pseudotypes. The poly-ICLC formulated EBOVgp-Fc vaccine protected all the guinea pigs against EBOV lethal challenge performed under BSL-4 conditions whereas the same vaccine formulated with QS-21 or alum only induced partial protection. Vaccination with a mucin-deletedEBOVgp-Fc construct formulated with QS-21 adjuvant did not have a significant effect in anti-GP antibody levels and protection against EBOV lethal challenge compared to the full-lengthGP construct. The bulk of the humoral response induced by the EBOVgp-Fc vaccine was directed against epitopes outside the EBOV mucin region. Our findings indicate that different adjuvants can eliciting varying levels of protection against lethal EBOV challenge in guinea pigs vaccinated with EBOVgp-Fc,and suggest that levels of total anti-GP antibodies elicit by protein-based GP subunit vaccines do not correlate with protection. In conclusion, our data further support the development of Fc fusions of GP as a candidate vaccine for human use.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Food and Drug Administration, Silver Spring, MD (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: Y1-AI-0664-01; Intramural; DTRA IAA 11005IA-3333-Basic

OSTI ID:: 1377872

Journal Information:: PLoS ONE, Vol. 11, Issue 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 21 works

Citation information provided by
Web of Science

References (64)

Pathogenesis of Experimental Ebola Virus Infection in Guinea Pigs Connolly, Brett M.; Steele, Keith E.; Davis, Kelly J. The Journal of Infectious Diseases, Vol. 179, Issue s1 https://doi.org/10.1086/514305	journal	February 1999
Nonhuman primates as models for the discovery and development of ebolavirus therapeutics Shurtleff, Amy C.; Warren, Travis K.; Bavari, Sina Expert Opinion on Drug Discovery, Vol. 6, Issue 3 https://doi.org/10.1517/17460441.2011.554815	journal	January 2011
Fc‐fusion proteins: new developments and future perspectives Czajkowsky, Daniel M.; Hu, Jun; Shao, Zhifeng EMBO Molecular Medicine, Vol. 4, Issue 10 https://doi.org/10.1002/emmm.201201379	journal	July 2012
Safety and immunogenicity of a chimpanzee adenovirus-vectored Ebola vaccine in healthy adults: a randomised, double-blind, placebo-controlled, dose-finding, phase 1/2a study De Santis, Olga; Audran, Régine; Pothin, Emilie The Lancet Infectious Diseases, Vol. 16, Issue 3 https://doi.org/10.1016/S1473-3099(15)00486-7	journal	March 2016
Marburg virus-like particles protect guinea pigs from lethal Marburg virus infection Warfield, Kelly L.; Swenson, Dana L.; Negley, Diane L. Vaccine, Vol. 22, Issue 25-26 https://doi.org/10.1016/j.vaccine.2004.01.063	journal	September 2004
Recombinant vesicular stomatitis viruses from DNA. Lawson, N. D.; Stillman, E. A.; Whitt, M. A. Proceedings of the National Academy of Sciences, Vol. 92, Issue 10 https://doi.org/10.1073/pnas.92.10.4477	journal	May 1995
A system for functional analysis of Ebola virus glycoprotein Takada, A.; Robison, C.; Goto, H. Proceedings of the National Academy of Sciences, Vol. 94, Issue 26 https://doi.org/10.1073/pnas.94.26.14764	journal	December 1997
Ebola Virus‐Like Particle–Based Vaccine Protects Nonhuman Primates against Lethal Ebola Virus Challenge Warfield, Kelly L.; Swenson, Dana L.; Olinger, Gene G. The Journal of Infectious Diseases, Vol. 196, Issue s2 https://doi.org/10.1086/520583	journal	November 2007
Antibodies are necessary for rVSV/ZEBOV-GP-mediated protection against lethal Ebola virus challenge in nonhuman primates Marzi, A.; Engelmann, F.; Feldmann, F. Proceedings of the National Academy of Sciences, Vol. 110, Issue 5 https://doi.org/10.1073/pnas.1209591110	journal	January 2013
Fc-receptors and immunity to malaria: from models to vaccines Pleass, R. J. Parasite Immunology, Vol. 31, Issue 9 https://doi.org/10.1111/j.1365-3024.2009.01101.x	journal	September 2009
Immune Parameters Correlate with Protection Against Ebola Virus Infection in Rodents and Nonhuman Primates Wong, G.; Richardson, J. S.; Pillet, S. Science Translational Medicine, Vol. 4, Issue 158 https://doi.org/10.1126/scitranslmed.3004582	journal	October 2012
Cross-reactive HIV-1-neutralizing activity of serum IgG from a rabbit immunized with gp41 fused to IgG1 Fc: Possible role of the prolonged half-life of the immunogen Zhang, Mei-Yun; Wang, Yanping; Mankowski, Marie K. Vaccine, Vol. 27, Issue 6 https://doi.org/10.1016/j.vaccine.2008.11.083	journal	February 2009
Filovirius vaccines Bradfute, Steven B.; Dye, Jr., John M.; Bavari, Sina Human Vaccines, Vol. 7, Issue 6 https://doi.org/10.4161/hv.7.6.15398	journal	June 2011
Correlates of protective immunity for Ebola vaccines: implications for regulatory approval by the animal rule Sullivan, Nancy J.; Martin, Julie E.; Graham, Barney S. Nature Reviews Microbiology, Vol. 7, Issue 5 https://doi.org/10.1038/nrmicro2129	journal	May 2009
Perspectives on West Africa Ebola Virus Disease Outbreak, 2013–2016 Spengler, Jessica R.; Ervin, Elizabeth D.; Towner, Jonathan S. Emerging Infectious Diseases, Vol. 22, Issue 6 https://doi.org/10.3201/eid2206.160021	journal	June 2016
(How) do aluminium adjuvants work? Brewer, J. Immunology Letters, Vol. 102, Issue 1 https://doi.org/10.1016/j.imlet.2005.08.002	journal	January 2006
Immunogenicity of the outer domain of a HIV-1 clade C gp120 Chen, Hongying; Xu, Xiaodong; Jones, Ian M. Retrovirology, Vol. 4, Issue 1 https://doi.org/10.1186/1742-4690-4-33	journal	January 2007
Polymorphism of Filovirus Glycoproteins Volchkov, Viktor E.; Volchkova, Valentina A.; Dolnik, Olga Advances in Virus Research https://doi.org/10.1016/S0065-3527(05)64011-0	book	January 2005
Ebola virus-like particles protect from lethal Ebola virus infection Warfield, K. L.; Bosio, C. M.; Welcher, B. C. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2237038100	journal	December 2003
Biosynthesis and role of filoviral glycoproteins Feldmann, Heinz; Volchkov, Viktor E.; Volchkova, Valentina A. Journal of General Virology, Vol. 82, Issue 12 https://doi.org/10.1099/0022-1317-82-12-2839	journal	December 2001
Natural and synthetic saponin adjuvant QS-21 for vaccines against cancer Ragupathi, Govind; Gardner, Jeffrey R.; Livingston, Philip O. Expert Review of Vaccines, Vol. 10, Issue 4 https://doi.org/10.1586/erv.11.18	journal	April 2011
Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses Jones, Steven M.; Feldmann, Heinz; Ströher, Ute Nature Medicine, Vol. 11, Issue 7 https://doi.org/10.1038/nm1258	journal	June 2005
Ebola Virus Disease 2013-2014 Outbreak in West Africa: An Analysis of the Epidemic Spread and Response Cenciarelli, Orlando; Pietropaoli, Stefano; Malizia, Andrea International Journal of Microbiology, Vol. 2015 https://doi.org/10.1155/2015/769121	journal	January 2015
Postexposure antibody prophylaxis protects nonhuman primates from filovirus disease Dye, J. M.; Herbert, A. S.; Kuehne, A. I. Proceedings of the National Academy of Sciences, Vol. 109, Issue 13 https://doi.org/10.1073/pnas.1200409109	journal	March 2012
Emergence of Zaire Ebola Virus Disease in Guinea Baize, Sylvain; Pannetier, Delphine; Oestereich, Lisa New England Journal of Medicine, Vol. 371, Issue 15 https://doi.org/10.1056/NEJMoa1404505	journal	October 2014
Increased potency of Fc-receptor-targeted antigens Guyre, P. M.; Graziano, Robert F.; Goldstein, Joel Cancer Immunology, Immunotherapy, Vol. 45, Issue 3-4 https://doi.org/10.1007/s002620050418	journal	November 1997
Newly Discovered Ebola Virus Associated with Hemorrhagic Fever Outbreak in Uganda Towner, Jonathan S.; Sealy, Tara K.; Khristova, Marina L. PLoS Pathogens, Vol. 4, Issue 11 https://doi.org/10.1371/journal.ppat.1000212	journal	November 2008
Current perspectives on the phylogeny of Filoviridae Barrette, Roger W.; Xu, Lizhe; Rowland, Jessica M. Infection, Genetics and Evolution, Vol. 11, Issue 7 https://doi.org/10.1016/j.meegid.2011.06.017	journal	October 2011
Synthetic Double-Stranded RNAs Are Adjuvants for the Induction of T Helper 1 and Humoral Immune Responses to Human Papillomavirus in Rhesus Macaques Stahl-Hennig, Christiane; Eisenblätter, Martin; Jasny, Edith PLoS Pathogens, Vol. 5, Issue 4 https://doi.org/10.1371/journal.ppat.1000373	journal	April 2009
Replication-Deficient Ebolavirus as a Vaccine Candidate Halfmann, Peter; Ebihara, Hideki; Marzi, Andrea Journal of Virology, Vol. 83, Issue 8 https://doi.org/10.1128/JVI.00074-09	journal	February 2009
Correlates of Immunity to Filovirus Infection Bradfute, Steven; Bavari, Sina Viruses, Vol. 3, Issue 7 https://doi.org/10.3390/v3070982	journal	June 2011
Development of a preventive vaccine for Ebola virus infection in primates Sullivan, Nancy J.; Sanchez, Anthony; Rollin, Pierre E. Nature, Vol. 408, Issue 6812 https://doi.org/10.1038/35046108	journal	November 2000
Respiratory tract immunization of non-human primates with a Newcastle disease virus-vectored vaccine candidate against Ebola virus elicits a neutralizing antibody response DiNapoli, Joshua M.; Yang, Lijuan; Samal, Siba K. Vaccine, Vol. 29, Issue 1 https://doi.org/10.1016/j.vaccine.2010.10.024	journal	December 2010
Properties of Replication-Competent Vesicular Stomatitis Virus Vectors Expressing Glycoproteins of Filoviruses and Arenaviruses Garbutt, Michael; Liebscher, Ryan; Wahl-Jensen, Victoria Journal of Virology, Vol. 78, Issue 10 https://doi.org/10.1128/JVI.78.10.5458-5465.2004	journal	May 2004
Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates Sullivan, Nancy J.; Geisbert, Thomas W.; Geisbert, Joan B. Nature, Vol. 424, Issue 6949 https://doi.org/10.1038/nature01876	journal	August 2003
Virus nomenclature below the species level: a standardized nomenclature for laboratory animal-adapted strains and variants of viruses assigned to the family Filoviridae Kuhn, Jens H.; Bao, Yiming; Bavari, Sina Archives of Virology, Vol. 158, Issue 6 https://doi.org/10.1007/s00705-012-1594-2	journal	January 2013
Ebola virus glycoprotein Fc fusion protein confers protection against lethal challenge in vaccinated mice Konduru, Krishnamurthy; Bradfute, Steven B.; Jacques, Jerome Vaccine, Vol. 29, Issue 16 https://doi.org/10.1016/j.vaccine.2011.01.113	journal	April 2011
Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations Kuhn, Jens H.; Becker, Stephan; Ebihara, Hideki Archives of Virology, Vol. 155, Issue 12 https://doi.org/10.1007/s00705-010-0814-x	journal	October 2010
Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury Nabel, Gary J.; Yang, Zhi-yong; Duckers, Henricus J. Nature Medicine, Vol. 6, Issue 8, p. 886-889 https://doi.org/10.1038/78645	journal	August 2000
Marburg Virus Vaccines Based upon Alphavirus Replicons Protect Guinea Pigs and Nonhuman Primates Hevey, Michael; Negley, Diane; Pushko, Peter Virology, Vol. 251, Issue 1 https://doi.org/10.1006/viro.1998.9367	journal	November 1998
Hidden reservoirs Heeney, Jonathan L. Nature, Vol. 527, Issue 7579 https://doi.org/10.1038/527453a	journal	November 2015
Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients Baize, Sylvain; Leroy, Eric M.; Georges-Courbot, M. -C. Nature Medicine, Vol. 5, Issue 4 https://doi.org/10.1038/7422	journal	April 1999
Immune Protection of Nonhuman Primates against Ebola Virus with Single Low-Dose Adenovirus Vectors Encoding Modified GPs Sullivan, Nancy J.; Geisbert, Thomas W.; Geisbert, Joan B. PLoS Medicine, Vol. 3, Issue 6 https://doi.org/10.1371/journal.pmed.0030177	journal	May 2006
Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor Lee, Jeffrey E.; Fusco, Marnie L.; Hessell, Ann J. Nature, Vol. 454, Issue 7201 https://doi.org/10.1038/nature07082	journal	July 2008
Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans Caskey, Marina; Lefebvre, François; Filali-Mouhim, Abdelali Journal of Experimental Medicine, Vol. 208, Issue 12 https://doi.org/10.1084/jem.20111171	journal	November 2011
Mucosal Immunization of Cynomolgus Macaques with the VSVΔG/ZEBOVGP Vaccine Stimulates Strong Ebola GP-Specific Immune Responses Qiu, Xiangguo; Fernando, Lisa; Alimonti, Judie B. PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005547	journal	May 2009
Effective Post-Exposure Treatment of Ebola Infection Feldmann, Heinz; Jones, Steven M.; Daddario-DiCaprio, Kathleen M. PLoS Pathogens, Vol. 3, Issue 1 https://doi.org/10.1371/journal.ppat.0030002	journal	January 2007
Ebola and Marburg Hemorrhagic Fever Hartman, Amy L.; Towner, Jonathan S.; Nichol, Stuart T. Clinics in Laboratory Medicine, Vol. 30, Issue 1 https://doi.org/10.1016/j.cll.2009.12.001	journal	March 2010
Ebola virus vaccines: an overview of current approaches Marzi, Andrea; Feldmann, Heinz Expert Review of Vaccines, Vol. 13, Issue 4 https://doi.org/10.1586/14760584.2014.885841	journal	February 2014
Ebola virus: from discovery to vaccine Feldmann, Heinz; Jones, Steven; Klenk, Hans-Dieter Nature Reviews Immunology, Vol. 3, Issue 8 https://doi.org/10.1038/nri1154	journal	August 2003
Action of Saponin on Biological Cell Membranes Bangham, A. D.; Horne, R. W. Nature, Vol. 196, Issue 4858 https://doi.org/10.1038/196952a0	journal	December 1962
Generation of Bovine Respiratory Syncytial Virus (BRSV) from cDNA: BRSV NS2 Is Not Essential for Virus Replication in Tissue Culture, and the Human RSV Leader Region Acts as a Functional BRSV Genome Promoter Buchholz, Ursula J.; Finke, Stefan; Conzelmann, Karl-Klaus Journal of Virology, Vol. 73, Issue 1 https://doi.org/10.1128/JVI.73.1.251-259.1999	journal	January 1999
The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. Schnell, M. J.; Buonocore, L.; Whitt, M. A. Journal of virology, Vol. 70, Issue 4 https://doi.org/10.1128/JVI.70.4.2318-2323.1996	journal	January 1996
Aluminum compounds as vaccine adjuvants Gupta, R. Advanced Drug Delivery Reviews, Vol. 32, Issue 3 https://doi.org/10.1016/s0169-409x(98)00008-8	journal	July 1998
Ebola vaccines: we have options Falzarano, Darryl The Lancet Infectious Diseases, Vol. 16, Issue 3 https://doi.org/10.1016/s1473-3099(15)00534-4	journal	March 2016
Phase 1 Trials of rVSV Ebola Vaccine in Africa and Europe Agnandji, Selidji T.; Huttner, Angela; Zinser, Madeleine E. New England Journal of Medicine, Vol. 374, Issue 17 https://doi.org/10.1056/nejmoa1502924	journal	April 2016
Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques Olinger, G. G.; Pettitt, J.; Kim, D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1213709109	journal	October 2012
Successful Treatment of Ebola Virus-Infected Cynomolgus Macaques with Monoclonal Antibodies Qiu, X.; Audet, J.; Wong, G. Science Translational Medicine, Vol. 4, Issue 138 https://doi.org/10.1126/scitranslmed.3003876	journal	June 2012
A New Ebola Virus Nonstructural Glycoprotein Expressed through RNA Editing Mehedi, M.; Falzarano, D.; Seebach, J. Journal of Virology, Vol. 85, Issue 11 https://doi.org/10.1128/jvi.02190-10	journal	March 2011
Ebola Virus Can Be Effectively Neutralized by Antibody Produced in Natural Human Infection Maruyama, Toshiaki; Rodriguez, Luis L.; Jahrling, Peter B. Journal of Virology, Vol. 73, Issue 7 https://doi.org/10.1128/jvi.73.7.6024-6030.1999	journal	July 1999
Analysis of Human Peripheral Blood Samples from Fatal and Nonfatal Cases of Ebola (Sudan) Hemorrhagic Fever: Cellular Responses, Virus Load, and Nitric Oxide Levels Sanchez, A.; Lukwiya, M.; Bausch, D. Journal of Virology, Vol. 78, Issue 19 https://doi.org/10.1128/jvi.78.19.10370-10377.2004	journal	September 2004
Transmission of Ebola Viruses: What We Know and What We Do Not Know Osterholm, Michael T.; Moore, Kristine A.; Kelley, Nicholas S. mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mbio.00137-15	journal	February 2015
Dead or alive: animal sampling during Ebola hemorrhagic fever outbreaks in humans Olson, Sarah H.; Reed, Patricia; Cameron, Kenneth N. Emerging Health Threats Journal, Vol. 5, Issue 1 https://doi.org/10.3402/ehtj.v5i0.9134	journal	January 2012
Newly discovered Ebola virus associated with hemorrhagic fever outbreak in Uganda Towner, Jonathan S.; Sealy, Tara K.; Khristova, Marina L. Columbia University https://doi.org/10.7916/d8vq37gb	text	January 2008

Cited By (5)

Ebola and Marburg virus vaccines Reynolds, Pierce; Marzi, Andrea Virus Genes, Vol. 53, Issue 4 https://doi.org/10.1007/s11262-017-1455-x	journal	April 2017
Vaccines against Ebola virus and Marburg virus: recent advances and promising candidates Suschak, John J.; Schmaljohn, Connie S. Human Vaccines & Immunotherapeutics, Vol. 15, Issue 10 https://doi.org/10.1080/21645515.2019.1651140	journal	May 2019
Advances in Designing and Developing Vaccines, Drugs, and Therapies to Counter Ebola Virus Dhama, Kuldeep; Karthik, Kumaragurubaran; Khandia, Rekha Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.01803	journal	August 2018
Saponins from Quillaja saponaria and Quillaja brasiliensis: Particular Chemical Characteristics and Biological Activities Fleck, Juliane Deise; Betti, Andresa Heemann; Da Silva, Francini Pereira Molecules, Vol. 24, Issue 1 https://doi.org/10.3390/molecules24010171	journal	January 2019
A Novel Bacterium-Like Particle-Based Vaccine Displaying the SUDV Glycoprotein Induces Potent Humoral and Cellular Immune Responses in Mice Xu, Shengnan; Jiao, Cuicui; Jin, Hongli Viruses, Vol. 11, Issue 12 https://doi.org/10.3390/v11121149	journal	December 2019

Similar Records

Chimeric human parainfluenza virus bearing the Ebola virus glycoprotein as the sole surface protein is immunogenic and highly protective against Ebola virus challenge

Journal Article · Tue Jan 20 00:00:00 EST 2009 · Virology · OSTI ID:1377872

Bukreyev, Alexander; Marzi, Andrea; Feldmann, Friederike; +8 more

The efficacy of poly-ICLC against Ebola-Zaire virus (EBOV) infection in mice and cynomolgus monkeys

Journal Article · Thu Jan 03 00:00:00 EST 2019 · Antiviral Research · OSTI ID:1377872

Kende, Meir; Paragas, Jason; Salazar, Andres M.

Candidate mosaic proteins for a pan-filoviral cytotoxic T-Cell lymphocyte vaccine

Journal Article · Tue Jan 01 00:00:00 EST 2008 · Journal of Virology · OSTI ID:1377872

Fenimore, Paul W; Fischer, William M; Kuiken, Carla; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
vaccines
guinea pigs
antibodies
immunologic adjuvants
enzyme-linked immunoassays
alumni
vesicular stomatitis virus
immune response

Title: Ebolavirus Glycoprotein Fc Fusion Protein Protects Guinea Pigs against Lethal Challenge

Citation Formats

References (64)

Cited By (5)

Similar Records

Related Subjects