Precursor genes of Bowman-Birk-type serine proteinase inhibitors comprise multiple inhibitory domains to promote diversity.

Alternative splicing Asparagaceae Monocots Plant serine protease inhibitor Precursor gene Processing mechanism

Journal

Biochimica et biophysica acta. General subjects
ISSN: 1872-8006
Titre abrégé: Biochim Biophys Acta Gen Subj
Pays: Netherlands
ID NLM: 101731726

Informations de publication

Date de publication:
01 2023
Historique:
received: 07 07 2022
revised: 13 09 2022
accepted: 26 09 2022
pubmed: 4 10 2022
medline: 18 11 2022
entrez: 3 10 2022
Statut: ppublish

Résumé

Proteinase inhibitors are important for the regulation of the activity of enzymes essential for the survival and maintenance of all organisms, and they may hold medicinal and agricultural value. Hyacinthus orientalis L. serine protease inhibitors (HOSPIs), belonging to the Bowman-Birk type inhibitor (BBI) family, have strong inhibitory activities against mammalian serine proteinases. This study explored the relationship between gene structure and multiple isoinhibitor production of these diversified BBIs by analyzing sequences of HOSPI precursor genes. Genomic DNA of H. orientalis roots was obtained and fragmented using 13 specific restriction enzymes, which were amplified by inverse and nested polymerase chain reactions, cloned into the pBluescript II SK (+) vector, and directly sequenced using specific primers. HOSPI gene and protein expression were assessed by quantitative real-time PCR and western blot, respectively. Proteinase inhibitory activity of hyacinth bulb extracts was evaluated by fluorescein isothiocyanate-labeled casein. Four distinct HOSPI precursor genes were identified, encoding 2-4 different HOSPI domains that were surrounded by additional sequences (named head, linker, and tail sequences) and some introns. Moreover, 3' splicing of the linker sequence may occur through introns inserted between linker sequences. HOSPI gene and protein expression was higher during the stem elongation and the flowering periods. These results indicate that gene duplication of the HOSPI precursor as a single set, including tandem repeated HOSPI domains, leads to diversity and effective production of mature HOSPIs by posttranslational processing. These findings shed light on the diversity of proteinase inhibitors.

Sections du résumé

BACKGROUND
Proteinase inhibitors are important for the regulation of the activity of enzymes essential for the survival and maintenance of all organisms, and they may hold medicinal and agricultural value. Hyacinthus orientalis L. serine protease inhibitors (HOSPIs), belonging to the Bowman-Birk type inhibitor (BBI) family, have strong inhibitory activities against mammalian serine proteinases. This study explored the relationship between gene structure and multiple isoinhibitor production of these diversified BBIs by analyzing sequences of HOSPI precursor genes.
METHODS
Genomic DNA of H. orientalis roots was obtained and fragmented using 13 specific restriction enzymes, which were amplified by inverse and nested polymerase chain reactions, cloned into the pBluescript II SK (+) vector, and directly sequenced using specific primers. HOSPI gene and protein expression were assessed by quantitative real-time PCR and western blot, respectively. Proteinase inhibitory activity of hyacinth bulb extracts was evaluated by fluorescein isothiocyanate-labeled casein.
RESULTS
Four distinct HOSPI precursor genes were identified, encoding 2-4 different HOSPI domains that were surrounded by additional sequences (named head, linker, and tail sequences) and some introns. Moreover, 3' splicing of the linker sequence may occur through introns inserted between linker sequences. HOSPI gene and protein expression was higher during the stem elongation and the flowering periods.
CONCLUSIONS
These results indicate that gene duplication of the HOSPI precursor as a single set, including tandem repeated HOSPI domains, leads to diversity and effective production of mature HOSPIs by posttranslational processing.
GENERAL SIGNIFICANCE
These findings shed light on the diversity of proteinase inhibitors.

Identifiants

pubmed: 36191739
pii: S0304-4165(22)00166-0
doi: 10.1016/j.bbagen.2022.130248
pii:
doi:

Substances chimiques

Serine Proteinase Inhibitors 0
Peptide Hydrolases EC 3.4.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

130248

Informations de copyright

Copyright © 2022 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors have no conflicting financial interests.

Auteurs

Narumi Aoki-Shioi (N)

Department of Chemistry, Faculty of Science, Fukuoka University, 19-1, 8-chome Nanakuma, Jonan-ku, Fukuoka 814-0180, Japan. Electronic address: anarumi@fukuoka-u.ac.jp.

Yuki Nagai (Y)

Department of Chemistry, Faculty of Science, Fukuoka University, 19-1, 8-chome Nanakuma, Jonan-ku, Fukuoka 814-0180, Japan.

Masanobu Deshimaru (M)

Department of Chemistry, Faculty of Science, Fukuoka University, 19-1, 8-chome Nanakuma, Jonan-ku, Fukuoka 814-0180, Japan. Electronic address: deshi@adm.fukuoka-u.ac.jp.

Shigeyuki Terada (S)

Department of Chemistry, Faculty of Science, Fukuoka University, 19-1, 8-chome Nanakuma, Jonan-ku, Fukuoka 814-0180, Japan. Electronic address: sterada@fukuoka-u.ac.jp.

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Classifications MeSH