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Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO.

Abstract

Like nitric oxide (NO), hydrogen sulfide (H2S) has been recognized as a new gasotransmitter which plays an important role as a signaling molecule in many physiological processes in higher plants. Although fruit ripening is a complex process associated with the metabolism of reactive oxygen species (ROS) and nitrogen oxygen species (RNS), little is known about the potential involvement of endogenous H2S. Using sweet pepper (Capsicum annuum L.) as a model non-climacteric fruit during the green and red ripening stages, we studied endogenous H2S content and cytosolic l-cysteine desulfhydrase (L-DES) activity which increased by 14% and 28%, respectively, in red pepper fruits. NADPH is a redox compound and key cofactor required for cell growth, proliferation and detoxification. We studied the NADPH-regenerating enzyme, NADP-isocitrate dehydrogenase (NADP-ICDH), whose activity decreased by 34% during ripening. To gain a better understanding of its potential regulation by H2S, we obtained a 50-75% ammonium sulfate-enriched protein fraction containing the NADP-ICDH protein; with the aid of in vitro assays in the presence of H2S, we observed that 2 and 10 mM NaHS used as H2S donors resulted in a decrease of up to 36% and 45%, respectively, in NADP-ICDH activity, which was unaffected by reduced glutathione (GSH). On the other hand, peroxynitrite (ONOO-), S-nitrosocyteine (CysNO) and DETA-NONOate, with the last two acting as NO donors, also inhibited NADP-ICDH activity. In silico analysis of the tertiary structure of sweet pepper NADP-ICDH activity (UniProtKB ID A0A2G2Y555) suggests that residues Cys133 and Tyr450 are the most likely potential targets for S-nitrosation and nitration, respectively. Taken together, the data reveal that the increase in the H2S production capacity of red fruits is due to higher L-DES activity during non-climacteric pepper fruit ripening. In vitro assays appear to show that H2S inhibits NADP-ICDH activity, thus suggesting that this enzyme may be regulated by persulfidation, as well as by S-nitrosation and nitration. NO and H2S may therefore regulate NADPH production and consequently cellular redox status during pepper fruit ripening.

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  • Authors+Show Affiliations

    ,

    Group Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, E-18008, Granada, Spain.

    ,

    Group Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, E-18008, Granada, Spain.

    ,

    Group Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, E-18008, Granada, Spain.

    ,

    Institute of Biotechnology, University of Granada, E-18071, Granada, Spain.

    ,

    Group Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, E-18008, Granada, Spain.

    Group Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, E-18008, Granada, Spain. Electronic address: javier.corpas@eez.csic.es.

    Source

    Nitric oxide : biology and chemistry 81: 2018 12 01 pg 36-45

    MeSH

    Capsicum
    Fruit
    Gene Expression Regulation, Plant
    Hydrogen Sulfide
    Isocitrate Dehydrogenase
    Nitric Oxide
    Nitrosation
    Plant Proteins
    Up-Regulation

    Pub Type(s)

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

    Language

    eng

    PubMed ID

    30326260

    Citation

    Muñoz-Vargas, María A., et al. "Endogenous Hydrogen Sulfide (H2S) Is Up-regulated During Sweet Pepper (Capsicum Annuum L.) Fruit Ripening. in Vitro Analysis Shows That NADP-dependent Isocitrate Dehydrogenase (ICDH) Activity Is Inhibited By H2S and NO." Nitric Oxide : Biology and Chemistry, vol. 81, 2018, pp. 36-45.
    Muñoz-Vargas MA, González-Gordo S, Cañas A, et al. Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO. Nitric Oxide. 2018;81:36-45.
    Muñoz-Vargas, M. A., González-Gordo, S., Cañas, A., López-Jaramillo, J., Palma, J. M., & Corpas, F. J. (2018). Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO. Nitric Oxide : Biology and Chemistry, 81, pp. 36-45. doi:10.1016/j.niox.2018.10.002.
    Muñoz-Vargas MA, et al. Endogenous Hydrogen Sulfide (H2S) Is Up-regulated During Sweet Pepper (Capsicum Annuum L.) Fruit Ripening. in Vitro Analysis Shows That NADP-dependent Isocitrate Dehydrogenase (ICDH) Activity Is Inhibited By H2S and NO. Nitric Oxide. 2018 12 1;81:36-45. PubMed PMID: 30326260.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO. AU - Muñoz-Vargas,María A, AU - González-Gordo,Salvador, AU - Cañas,Amanda, AU - López-Jaramillo,Javier, AU - Palma,José M, AU - Corpas,Francisco J, Y1 - 2018/10/13/ PY - 2018/06/15/received PY - 2018/10/04/revised PY - 2018/10/07/accepted PY - 2018/10/17/pubmed PY - 2019/2/23/medline PY - 2018/10/17/entrez KW - Fruit ripening KW - Hydrogen sulfide KW - NADP-isocitrate dehydrogenase KW - Nitration KW - Nitric oxide KW - Pepper KW - Persulfidation KW - S-nitrosation KW - S-nitrosocyteine KW - S-nitrosylation KW - S-sulfhydration SP - 36 EP - 45 JF - Nitric oxide : biology and chemistry JO - Nitric Oxide VL - 81 N2 - Like nitric oxide (NO), hydrogen sulfide (H2S) has been recognized as a new gasotransmitter which plays an important role as a signaling molecule in many physiological processes in higher plants. Although fruit ripening is a complex process associated with the metabolism of reactive oxygen species (ROS) and nitrogen oxygen species (RNS), little is known about the potential involvement of endogenous H2S. Using sweet pepper (Capsicum annuum L.) as a model non-climacteric fruit during the green and red ripening stages, we studied endogenous H2S content and cytosolic l-cysteine desulfhydrase (L-DES) activity which increased by 14% and 28%, respectively, in red pepper fruits. NADPH is a redox compound and key cofactor required for cell growth, proliferation and detoxification. We studied the NADPH-regenerating enzyme, NADP-isocitrate dehydrogenase (NADP-ICDH), whose activity decreased by 34% during ripening. To gain a better understanding of its potential regulation by H2S, we obtained a 50-75% ammonium sulfate-enriched protein fraction containing the NADP-ICDH protein; with the aid of in vitro assays in the presence of H2S, we observed that 2 and 10 mM NaHS used as H2S donors resulted in a decrease of up to 36% and 45%, respectively, in NADP-ICDH activity, which was unaffected by reduced glutathione (GSH). On the other hand, peroxynitrite (ONOO-), S-nitrosocyteine (CysNO) and DETA-NONOate, with the last two acting as NO donors, also inhibited NADP-ICDH activity. In silico analysis of the tertiary structure of sweet pepper NADP-ICDH activity (UniProtKB ID A0A2G2Y555) suggests that residues Cys133 and Tyr450 are the most likely potential targets for S-nitrosation and nitration, respectively. Taken together, the data reveal that the increase in the H2S production capacity of red fruits is due to higher L-DES activity during non-climacteric pepper fruit ripening. In vitro assays appear to show that H2S inhibits NADP-ICDH activity, thus suggesting that this enzyme may be regulated by persulfidation, as well as by S-nitrosation and nitration. NO and H2S may therefore regulate NADPH production and consequently cellular redox status during pepper fruit ripening. SN - 1089-8611 UR - https://www.unboundmedicine.com/medline/citation/30326260/Endogenous_hydrogen_sulfide_(H2S)_is_up-regulated_during_sweet_pepper_(Capsicum_annuum_L.)_fruit_ripening._In_vitro_analysis_shows_that_NADP-dependent_isocitrate_dehydrogenase_(ICDH)_activity_is_inhibited_by_H2S_and_NO L2 - https://linkinghub.elsevier.com/retrieve/pii/S1089-8603(18)30168-X DB - PRIME DP - Unbound Medicine ER -