Abstract
We used the mammalian reoviruses to determine the molecular basis of the clearance of a virus from the bloodstream by specific organs. Reovirus serotypes 1 (T1) and 3 (T3) were radiolabeled with [35S]methionine or 125I, and the viruses were injected intravenously into weanling rats. The distribution of radioactivity within the animals was determined at various times after the injection. Both viruses were cleared rapidly from the bloodstream and concentrated in different organs. Reovirus T1 was found predominantly in the lungs and liver, whereas T3 was found predominantly in the liver, with very little virus in the lungs. Using intertypic reassortants, we determined that the T1 S1 gene, which encodes the viral hemagglutinin (sigma 1 protein), is responsible for the difference in uptake of T1 and T3 by the lungs. The genetic mapping was extended by using several approaches. (i) T1 subjected to limited proteolytic digestion with chymotrypsin was cleared efficiently by the lungs despite the removal of sigma 3 and digestion of mu 1C to delta. (ii) Uptake of T1 by the lungs was totally inhibited by incubation of T1 with an anti-sigma 1 monoclonal antibody or its Fab fragment before injection. (iii) A reovirus T1 variant in the sigma 1 protein was poorly taken up by the lungs. These data indicate that clearance of reovirus from the bloodstream by the lungs is dependent on the presence of the T1 sigma 1 protein.
MeSH Terms
Animals
Genes, Viral
Hemagglutinins, Viral/genetics
Liver/microbiology
Lung/microbiology
Male
Rats
Rats, Inbred Strains
Reoviridae/genetics,immunology,physiology
Spleen/microbiology
Viremia
Chemicals
Hemagglutinins, Viral
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Verdin E M
Elliot P. Joslin Research Laboratory, Joslin Diabetes Center, Boston, Massachusetts.
Lynn S P
Fields B N
Maratos-Flier E
References (28)
28 references, click to expand
-
Biosynthesis of reovirus-specified polypeptides. Molecular cDNA cloning and nucleotide sequence of the reovirus serotype 1 Lang strain bicistronic s1 mRNA which encodes the minor capsid polypeptide sigma 1a and the nonstructural polypeptide sigma 1bNS.
Biochem Biophys Res Commun. 1986 Oct 30;140(2):508-14
PMID: 2430568
-
Distinct pathways of viral spread in the host determined by reovirus S1 gene segment.
Science. 1986 Aug 15;233(4765):770-4
PMID: 3016895
-
Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle.
J Virol. 1987 Aug;61(8):2351-61
PMID: 2885424
-
Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles.
J Virol. 1988 Jan;62(1):246-56
PMID: 3275434
-
Serologic grouping of reoviruses by hemagglutination-inhibition.
Am J Hyg. 1960 Mar;71:242-9
PMID: 14438891
-
Tissue weights of the rat. I. Normal values determined by dissection and chemical methods.
Proc Soc Exp Biol Med. 1956 Jan;91(1):122-6
PMID: 13297726
-
Two variants of Sindbis virus which differ in interferon induction and serum clearance. I. The phenomenon.
J Infect Dis. 1969 Sep;120(3):339-47
PMID: 5822615
-
Two variants of Sindbis virus which differ in interferon induction and serum clearance. II. Virological characterizations.
J Infect Dis. 1969 Sep;120(3):348-55
PMID: 5822616
-
Polypeptide components of virions, top component and cores of reovirus type 3.
Virology. 1969 Dec;39(4):791-810
PMID: 4311639
-
Vascular clearance of venezuelan equine encephalomyelitis viruses as a correlate to virulence for rhesus monkeys.
Arch Virol. 1977;55(1-2):161-4
PMID: 411457
-
Identification of the gene coding for the hemagglutinin of reovirus.
Virology. 1978 May 15;86(2):581-4
PMID: 566483
-
Genetics of reovirus: identification of the ds RNA segments encoding the polypeptides of the mu and sigma size classes.
Virology. 1978 Sep;89(2):594-604
PMID: 716219
-
Absolute linkage of virulence and central nervous system cell tropism of reoviruses to viral hemagglutinin.
J Infect Dis. 1980 May;141(5):609-16
PMID: 6989930
-
Protein sigma 1 is the reovirus cell attachment protein.
Virology. 1981 Jan 15;108(1):156-63
PMID: 7269235
-
Evidence for functional domains on the reovirus type 3 hemagglutinin.
Virology. 1982 Feb;117(1):146-55
PMID: 6175082
-
Biochemical studies on the mechanism of chemical and physical inactivation of reovirus.
J Gen Virol. 1982 Nov;63 (Pt 1):161-70
PMID: 7175501
-
The sigma 1 protein determines the extent of spread of reovirus from the gastrointestinal tract of mice.
Virology. 1983 Jan 30;124(2):403-10
PMID: 6823749
-
Topological analysis of the reovirus type 3 hemagglutinin.
Virology. 1983 May;127(1):220-4
PMID: 6858002
-
Specific plasma membrane receptors for reovirus on rat pituitary cells in culture.
J Clin Invest. 1983 Aug;72(2):617-21
PMID: 6308058
-
The ultrastructure of various cell types in the lung of the rat: a survey.
Exp Pathol. 1983;24(1):15-33
PMID: 6685053
-
Molecular basis of viral neurotropism: experimental reovirus infection.
Neurology. 1985 Jan;35(1):88-92
PMID: 2981418
-
Pathogenesis of viral infections. Basic concepts derived from the reovirus model.
N Engl J Med. 1985 Feb 21;312(8):486-97
PMID: 2982096
-
Sequences of the S1 genes of the three serotypes of reovirus.
Proc Natl Acad Sci U S A. 1985 Jan;82(1):24-8
PMID: 3855545
-
Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames.
Proc Natl Acad Sci U S A. 1985 Jan;82(1):48-52
PMID: 3855548
-
Identification of a new polypeptide coded by reovirus gene S1.
J Virol. 1985 Jun;54(3):720-5
PMID: 3999193
-
Biosynthesis of reovirus-specified polypeptides: the reovirus s1 mRNA encodes two primary translation products.
Virology. 1985 May;143(1):63-74
PMID: 4060584
-
Biosynthesis of reovirus-specified polypeptides. The s1 mRNA synthesized in vivo is structurally and functionally indistinguishable from in vitro-synthesized s1 mRNA and encodes two polypeptides, sigma 1a and sigma 1bNS.
Virology. 1985 Nov;147(1):9-18
PMID: 2998074
-
Visualization of viral clearance in the living animal.
Science. 1987 Apr 24;236(4800):439-42
PMID: 3031817