Abstract
Two decades after a worldwide vaccination campaign was used to successfully eradicate naturally occurring smallpox, the threat of bioterrorism has led to renewed vaccination programs. In addition, sporadic outbreaks of human monkeypox in Africa and a recent outbreak of human monkeypox in the U.S. have made it clear that naturally occurring zoonotic orthopoxvirus diseases remain a public health concern. Much of the threat posed by orthopoxviruses could be eliminated by vaccination; however, because the smallpox vaccine is a live orthopoxvirus vaccine (vaccinia virus) administered to the skin, the vaccine itself can pose a serious health risk. Here, we demonstrate that rhesus macaques vaccinated with a DNA vaccine consisting of four vaccinia virus genes (L1R, A27L, A33R, and B5R) were protected from severe disease after an otherwise lethal challenge with monkeypox virus. Animals vaccinated with a single gene (L1R) which encodes a target of neutralizing antibodies developed severe disease but survived. This is the first demonstration that a subunit vaccine approach to smallpox-monkeypox immunization is feasible.
MeSH Terms
Animals
Antibodies, Viral/blood
Humans
Macaca mulatta
Membrane Glycoproteins/genetics,immunology
Monkeypox/prevention & control
Monkeypox virus/pathogenicity
Smallpox Vaccine/administration & dosage,immunology
Vaccination
Vaccines, DNA/administration & dosage,immunology
Vaccinia virus/genetics,immunology
Viral Envelope Proteins/genetics,immunology
Viral Proteins/genetics,immunology
Chemicals
A27L protein, Orthopoxvirus
A33R protein, Vaccinia virus
Antibodies, Viral
L1R protein, Vaccinia virus
Membrane Glycoproteins
Smallpox Vaccine
Vaccines, DNA
Viral Envelope Proteins
Viral Proteins
42kDa protein, Vaccinia virus
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Hooper J W
Virology Division, United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, Maryland 21702, USA.
[email protected]
Thompson E
Wilhelmsen C
Zimmerman M
Ichou M Ait
Steffen S E
Schmaljohn C S
Schmaljohn A L
Jahrling P B
References (27)
27 references, click to expand
-
DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge.
Virology. 2000 Jan 20;266(2):329-39
PMID: 10639319
-
Antibody neutralization of the extracellular enveloped form of vaccinia virus.
Virology. 2001 Feb 1;280(1):132-42
PMID: 11162827
-
Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997.
Emerg Infect Dis. 2001 May-Jun;7(3):434-8
PMID: 11384521
-
DNA vaccination with the Hantaan virus M gene protects Hamsters against three of four HFRS hantaviruses and elicits a high-titer neutralizing antibody response in Rhesus monkeys.
J Virol. 2001 Sep;75(18):8469-77
PMID: 11507192
-
Developing new smallpox vaccines.
Emerg Infect Dis. 2001 Nov-Dec;7(6):920-6
PMID: 11747717
-
Administration to mice of a monoclonal antibody that neutralizes the intracellular mature virus form of vaccinia virus limits virus replication efficiently under prophylactic and therapeutic conditions.
J Gen Virol. 2002 May;83(Pt 5):1059-67
PMID: 11961260
-
Analysis of the monkeypox virus genome.
Virology. 2002 Jun 5;297(2):172-94
PMID: 12083817
-
Four-gene-combination DNA vaccine protects mice against a lethal vaccinia virus challenge and elicits appropriate antibody responses in nonhuman primates.
Virology. 2003 Feb 1;306(1):181-95
PMID: 12620810
-
Supplemental recommendations on adverse events following smallpox vaccine in the pre-event vaccination program: recommendations of the Advisory Committee on Immunization Practices.
MMWR Morb Mortal Wkly Rep. 2003 Apr 4;52(13):282-4
PMID: 12729078
-
Multistate outbreak of monkeypox--Illinois, Indiana, and Wisconsin, 2003.
MMWR Morb Mortal Wkly Rep. 2003 Jun 13;52(23):537-40
PMID: 12803191
-
Update: adverse events following civilian smallpox vaccination--United States, 2003.
MMWR Morb Mortal Wkly Rep. 2003 May 9;52(18):419-20
PMID: 12807092
-
Update: multistate outbreak of monkeypox--Illinois, Indiana, Kansas, Missouri, Ohio, and Wisconsin, 2003.
MMWR Morb Mortal Wkly Rep. 2003 Jul 11;52(27):642-6
PMID: 12855947
-
Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses.
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9458-63
PMID: 12869693
-
Real-time PCR assay to detect smallpox virus.
J Clin Microbiol. 2003 Aug;41(8):3835-9
PMID: 12904397
-
Clonal vaccinia virus grown in cell culture as a new smallpox vaccine.
Nat Med. 2003 Sep;9(9):1125-30
PMID: 12925845
-
Duration of antiviral immunity after smallpox vaccination.
Nat Med. 2003 Sep;9(9):1131-7
PMID: 12925846
-
Fatal myocarditis following smallpox vaccination.
Am Heart J. 1957 Jul;54(1):156-7
PMID: 13435214
-
A pox disease of monkeys.
Ann N Y Acad Sci. 1960 May 12;85:951-9
PMID: 13737997
-
PROTECTION OF RHESUS MONKEYS AGAINST MONKEYPOX BY VACCINIA VIRUS IMMUNIZATION.
Am J Vet Res. 1964 Jan;25:192-5
PMID: 14103224
-
Studies smallpox and complications of smallpox vaccination.
Pediatrics. 1960 Aug;26:176-89
PMID: 14408455
-
Vaccinia (smallpox) vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2001.
MMWR Recomm Rep. 2001 Jun 22;50(RR-10):1-25; quiz CE1-7
PMID: 15580803
-
Structural and functional analysis of orthopoxvirus epitopes with neutralizing monoclonal antibodies.
J Gen Virol. 1990 Oct;71 ( Pt 10):2341-52
PMID: 1700065
-
Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein.
J Virol. 1987 Nov;61(11):3550-4
PMID: 2822962
-
Epitope detection in the envelope of intracellular naked orthopox viruses and identification of encoding genes.
Virology. 1994 May 1;200(2):764-77
PMID: 7513922
-
A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies.
Virology. 1995 Aug 1;211(1):53-63
PMID: 7645236
-
Immunologic responses to vaccinia vaccines administered by different parenteral routes.
J Infect Dis. 1997 Apr;175(4):756-63
PMID: 9086127
-
Neutralizing and protective antibodies directed against vaccinia virus envelope antigens.
Virology. 1999 Feb 1;254(1):71-80
PMID: 9927575