Abstract
The mechanism conferring resistance to paromomycin in Streptomyces rimosus forma paromomycinus, the producing organism, was studied at the level of both protein synthesis and drug-inactivating enzymes. Ribosomes prepared from this organism grown in either production or nonproduction medium were fully sensitive to paromomycin. A paromomycin acetyltransferase and a paromomycin phosphotransferase, both characteristic of the producer, were highly purified from extracts prepared from two Streptomyces lividans transformants harboring the relevant genes inserted in pIJ702-derived plasmids. In vitro, paromomycin was inactivated by either activity. In vivo, however, S. lividans clones containing the gene for either enzyme inserted in the low-copy-number plasmid pIJ41 were resistant to only low levels of paromomycin. In contrast, an S. lividans transformant containing both genes inserted in the same pIJ41-derived plasmid displayed high levels of resistance to paromomycin. These results indicate that both genes are required to determine the high levels of resistance to this drug in the producing organism. Paromomycin is doubly modified by the enzymes. However, whereas acetylparomomycin was a poorer substrate than paromomycin for the phosphotransferase, phosphorylparomomycin was modified more actively than was the intact drug by the acetyltransferase. These findings are discussed in terms of both a permeability barrier to paromomycin and the possible role(s) of the two enzymes in the biosynthetic pathway of this antibiotic.
MeSH Terms
Acetyltransferases/genetics,isolation & purification,metabolism
Cloning, Molecular
Genes
Genes, Bacterial
Kinetics
Paromomycin/pharmacology
Phosphotransferases/genetics,isolation & purification,metabolism
Phosphotransferases (Alcohol Group Acceptor)
R Factors
Restriction Mapping
Streptomyces/drug effects,enzymology,genetics
Substrate Specificity
Chemicals
Paromomycin
Acetyltransferases
aminoglycoside N1-acetyltransferase
Phosphotransferases
Phosphotransferases (Alcohol Group Acceptor)
paromomycin phosphotransferase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pérez-González J A
Centro de Biología Molecular (CSIC and UAM), Universidad Autónoma, Madrid, Spain.
López-Cabrera M
Pardo J M
Jiménez A
References (26)
26 references, click to expand
-
Genetic analysis and genome structure in Streptomyces coelicolor.
Bacteriol Rev. 1967 Dec;31(4):373-403
PMID: 4866846
-
Enzymatic modification of hygromycin B in Streptomyces hygroscopicus.
J Antibiot (Tokyo). 1982 Apr;35(4):527-8
PMID: 7096208
-
Mechanism of resistance to aminoglycoside antibiotics in nebramycin-producing Streptomyces tenebrarius.
J Antibiot (Tokyo). 1982 Aug;35(8):1020-5
PMID: 7142002
-
Physical analysis of antibiotic-resistance genes from Streptomyces and their use in vector construction.
Gene. 1982 Nov;20(1):51-62
PMID: 6298066
-
Cloning and expression of the tyrosinase gene from Streptomyces antibioticus in Streptomyces lividans.
J Gen Microbiol. 1983 Sep;129(9):2703-14
PMID: 6313861
-
Cloning of the kanamycin resistance gene from a kanamycin-producing Streptomyces species.
J Bacteriol. 1984 Jan;157(1):79-83
PMID: 6690428
-
Molecular cloning and expression in streptomyces lividans of a hygromycin B phosphotransferase gene from Streptomyces hygroscopicus.
Biochem Biophys Res Commun. 1983 Nov 30;117(1):6-12
PMID: 6318753
-
Factors affecting the isolation of CCC DNA from Streptomyces lividans and Escherichia coli.
Plasmid. 1984 Jul;12(1):19-36
PMID: 6387733
-
Self defence in antibiotic-producing organisms.
Br Med Bull. 1984 Jan;40(1):61-7
PMID: 6085482
-
Cloning and expression of a puromycin N-acetyl transferase gene from Streptomyces alboniger in Streptomyces lividans and Escherichia coli.
Gene. 1985;33(2):197-206
PMID: 3888783
-
Nucleotide sequences encoding and promoting expression of three antibiotic resistance genes indigenous to Streptomyces.
Mol Gen Genet. 1985;199(1):26-36
PMID: 2987648
-
Characterization in Micromonospora inyoensis of aminoglycoside acetyltransferase activity not previously encountered among actinomycetes.
J Gen Microbiol. 1985 Mar;131(3):451-7
PMID: 4020339
-
Ribosomal resistance in the gentamicin producer organism Micromonospora purpurea.
Antimicrob Agents Chemother. 1982 Aug;22(2):231-6
PMID: 6927285
-
Biochemical basis of resistance to hygromycin B in Streptomyces hygroscopicus--the producing organism.
J Gen Microbiol. 1985 Jun;131(6):1289-98
PMID: 2995542
-
Methylation of 16S ribosomal RNA and resistance to aminoglycoside antibiotics in clones of Streptomyces lividans carrying DNA from Streptomyces tenjimariensis.
Mol Gen Genet. 1985;200(3):415-21
PMID: 3862930
-
Biosynthesis of puromycin by Streptomyces alboniger: characterization of puromycin N-acetyltransferase.
Biochemistry. 1985 Dec 31;24(27):8074-81
PMID: 4092057
-
The mechanism of resistance to puromycin and to the puromycin-precursor O-demethyl-puromycin in Streptomyces alboniger.
J Gen Microbiol. 1985 Nov;131(11):2877-83
PMID: 4093761
-
Purification and characterization of a hygromycin B phosphotransferase from Streptomyces hygroscopicus.
Eur J Biochem. 1987 Jan 15;162(2):419-22
PMID: 3026811
-
Mechanism of increased kanamycin-resistance generated by protoplast regeneration of Streptomyces griseus. I. Cloning of a gene segment directing a high level of an aminoglycoside 3-N-acetyltransferase activity.
J Antibiot (Tokyo). 1988 Jan;41(1):94-103
PMID: 3126171
-
A second streptomycin resistance gene from Streptomyces griseus codes for streptomycin-3"-phosphotransferase. Relationships between antibiotic and protein kinases.
Arch Microbiol. 1988;150(2):184-92
PMID: 2844130
-
Aminoglycoside-modifying enzymes.
Methods Enzymol. 1975;43:611-28
PMID: 166284
-
Isolation and nucleotide sequencing of an aminocyclitol acetyltransferase gene from Streptomyces rimosus forma paromomycinus.
J Bacteriol. 1989 Jan;171(1):321-8
PMID: 2914849
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Ribosomal resistance of an istamycin producer, Streptomyces tenjimariensis, to aminoglycoside antibiotics.
Biochem Biophys Res Commun. 1981 Jun 16;100(3):1396-401
PMID: 7271807
-
Self-resistance of a Streptomyces which produces istamycins.
J Antibiot (Tokyo). 1981 Jul;34(7):824-9
PMID: 7026523
-
Biochemical characterization of resistance determinants cloned from antibiotic-producing streptomycetes.
J Bacteriol. 1982 Aug;151(2):678-85
PMID: 6284707