天名精内酯酮抑菌机理初步研究
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摘要
天名精内酯酮是从大花金挖耳(Carpesium macrocephalum)中分离得到的一种倍半萜内酯类化合物。前期研究表明其具有较好的抑菌活性,对小麦白粉病、小麦全蚀病、小麦条锈病等几种病害有较好的防治效果,通过天名精内酯酮对小麦白粉病药效试验结果初步推断出天名精内酯酮具有较优的内吸活性,生理生化研究结果表明,天名精内酯酮可能对病菌的生物氧化及生物合成均存在一定的影响。为进一步明确天名精内酯酮的抑菌作用机理,本文对天名精内酯酮在小麦体内的传导方式进行了研究,并以小麦全蚀病菌(Gaeumannomyces graminis)为测试对象,就天名精内酯酮对小麦全蚀病菌生物氧化过程的影响进行了初步探讨。得出以下主要结果:
1天名精内酯酮对小麦白粉病的控制主要是抑制了菌落的扩展
采用离体叶段法测定了天名精内酯酮对小麦白粉病菌孢子萌发和菌落扩展的影响,结果表明,天名精内酯酮对小麦白粉病菌孢子萌发无明显的抑制作用,但对菌落的扩展存在显著的抑制作用,并呈现明显的浓度依赖性,对小麦白粉病菌菌落扩展的抑制中浓度(EC50)为105.4314mg/L。
2天名精内酯酮在小麦体内存在自下而上的传导方式
小麦白粉病盆栽药效试验结果表明,天名精内酯酮灌根处理对小麦白粉病具有良好的防治效果,在1000mg/L浓度下,保护和治疗作用分别为61.18%和60.77%;采用HPLC法检测小麦植株对土壤和水体中天名精内酯酮的内吸传导活性,结果表明,小麦根系对土壤中天名精内酯酮的内吸传导于24h后达最大,小麦叶片中含量为26.825μg/g;小麦根系对水体中天名精内酯酮的内吸,随时间延长小麦叶片中天名精内酯酮的含量逐渐升高。
综合活性测试和仪器分析结果可见,天名精内酯酮具明显的内吸活性及自下而上的传导方式。
HPLC法检测表明,在试验剂量下,天名精内酯酮在小麦体内无明显的自上而下的内吸传导方式。
3天名精内酯酮对小麦全蚀病菌生物氧化过程存在明显影响
(1)天名精内酯酮与SHAM对小麦全蚀病菌联合毒力测定的研究结果表明,SHAM对天名精内酯酮具明显的增效作用,增效倍数为1.86。由此可见天名精内酯酮可明显影响病菌正常呼吸电子传递链生成ATP的过程。
(2)离体条件下天名精内酯酮对小麦全蚀病菌线粒体呼吸电子传递链复合酶活性存在不同程度的影响。
研究结果表明,随着天名精内酯酮浓度的逐渐升高,复合酶I的活性总体上呈现降低的趋势。在天名精内酯酮浓度为32mg/L时,复合酶II的活性显著增强。当天名精内酯酮浓度为1mg/L时,复合酶III的活性就比空白对照降低了1.4倍。天名精内酯酮对复合酶Ⅳ的活性无明显影响。
(3)活体条件下天名精内酯酮对小麦全蚀病菌线粒体呼吸电子传递链复合酶活性具明显抑制作用,并呈现明显的浓度依赖性。
研究结果表明,在天名精内酯酮溶液浓度较低时,四种复合酶活性与对照相比变化不明显,而随着天名精内酯酮溶液浓度的升高,四种复合酶的活性均表现降低的趋势。
通过天名精内酯酮对离体和活体条件下小麦全蚀病菌复合酶活性测定结果可以看出,天名精内酯酮对小麦全蚀病菌的生物氧化过程存在明显影响,可能是通过对呼吸电子传递链复合酶活性的影响降低了ATP的合成量,致使菌体能量供应不足,最终导致病菌生长缓慢。
Carabrone is a sesquiterpenoid lactone compound from C.macrocephalum. Previous study indicated it has good antifungal activity, and has excellent activity on wheat powdery mildew, wheat take–all, wheat stripe rust, pot culture experiment indicated that Carabrone has a systemic action in wheat, physiological and biochemical test showed that Carabrone may have a certain effect on both biosynthesis and bio-oxidation of pathogen. In order to clear the mode of action and the mechanism of Carabrone to pathogen. In this paper, we study the conduction of Carabrone in wheat and take Gaeumannomyces graminis as test object in order to study the effects of Carabrone on bio-oxidation process of Gaeumannomyces graminis. The main results are as follows:
1 The inhibition of Carabrone on Blumeria graminis mainly by inhibiting the expansion of colony
The results of Carabrone on spore germination and colony expansion of Blumeria graminis by leave fragment method in vitro indicated that there is no significant inhibitory effect on spore germination by Carabrone. But it has significant effect on colony growth and showed some concentration-dependent, EC50 is 105.4314mg/L.
2 There is a conduction of Carabrone from down to up in wheat
Pot culture experiment indicated that Carabrone could control Blumeria graminis by irrigation, the protective effect and the curative effect is 61.18% and 60.77% .
Using HPLC method to detect the absorption of Carabrone by wheat roots in soil and in solution. The results showed that after 24h the content is the highest by in soil, reached to 26.825μg/g, and the absorption test of wheat roots in solution showed that the content of Carabrone increased gradually as the time went by.
Comprehensive analysis of the results of activity tests and instrumental analysis can be inferred that Carabrone has apparent systemic action and a conduction from down to up in wheat.
At the test dose, HPLC assay showed that there is not a significant conduction of Carabrone from up to down in wheat.
3 Carabrone has effect on the bio-oxidation process of Gaeumannomyces graminis
(1) The results of Co-toxicity test of Carabrone and SHAM to Gaeumannomyces graminis showed that SHAM has significant synergism to Carabrone. The increment mulliple is 1.86, indicating that Carabrone can affect the generation of ATP by interfere with respiratory electron transport chain process obviously.
(2) Carabrone has different effect on the activity of mitochondrial complexes in Gaeum- annomyces graminis by in vitro.
The results show that as the concentration of Carabrone gradually increased, the activity of complex I showed overall decreasing trend. When the concentration reached to 32mg/L, the activity of complex II were significantly increased. Only when the concentration is 1 mg/L, the activity of complex III were 1.4 times lower than the control.Complex IV have no significant effect by Carabrone.
(3) Carabrone has effect on all the four kinds of mitochondrial complexes in Gaeuman- nomyces graminis by in vivo.
The results showed that when the concentration of Carabrone is low, there is no significant difference compared with the control, with the concentration increased, all the four kinds of complexes decreased.
Through the results we can conclude that Carabrone has certain effect on bio-oxidation of Gaeumannomyces graminis, Carabrone may decreased the synthesis of ATP by interfere with complexes on respiratory electron transport chain , resulting in insufficient supply of biomass energy, leading to slow the growth of mycelium.
1天名精内酯酮对小麦白粉病的控制主要是抑制了菌落的扩展
采用离体叶段法测定了天名精内酯酮对小麦白粉病菌孢子萌发和菌落扩展的影响,结果表明,天名精内酯酮对小麦白粉病菌孢子萌发无明显的抑制作用,但对菌落的扩展存在显著的抑制作用,并呈现明显的浓度依赖性,对小麦白粉病菌菌落扩展的抑制中浓度(EC50)为105.4314mg/L。
2天名精内酯酮在小麦体内存在自下而上的传导方式
小麦白粉病盆栽药效试验结果表明,天名精内酯酮灌根处理对小麦白粉病具有良好的防治效果,在1000mg/L浓度下,保护和治疗作用分别为61.18%和60.77%;采用HPLC法检测小麦植株对土壤和水体中天名精内酯酮的内吸传导活性,结果表明,小麦根系对土壤中天名精内酯酮的内吸传导于24h后达最大,小麦叶片中含量为26.825μg/g;小麦根系对水体中天名精内酯酮的内吸,随时间延长小麦叶片中天名精内酯酮的含量逐渐升高。
综合活性测试和仪器分析结果可见,天名精内酯酮具明显的内吸活性及自下而上的传导方式。
HPLC法检测表明,在试验剂量下,天名精内酯酮在小麦体内无明显的自上而下的内吸传导方式。
3天名精内酯酮对小麦全蚀病菌生物氧化过程存在明显影响
(1)天名精内酯酮与SHAM对小麦全蚀病菌联合毒力测定的研究结果表明,SHAM对天名精内酯酮具明显的增效作用,增效倍数为1.86。由此可见天名精内酯酮可明显影响病菌正常呼吸电子传递链生成ATP的过程。
(2)离体条件下天名精内酯酮对小麦全蚀病菌线粒体呼吸电子传递链复合酶活性存在不同程度的影响。
研究结果表明,随着天名精内酯酮浓度的逐渐升高,复合酶I的活性总体上呈现降低的趋势。在天名精内酯酮浓度为32mg/L时,复合酶II的活性显著增强。当天名精内酯酮浓度为1mg/L时,复合酶III的活性就比空白对照降低了1.4倍。天名精内酯酮对复合酶Ⅳ的活性无明显影响。
(3)活体条件下天名精内酯酮对小麦全蚀病菌线粒体呼吸电子传递链复合酶活性具明显抑制作用,并呈现明显的浓度依赖性。
研究结果表明,在天名精内酯酮溶液浓度较低时,四种复合酶活性与对照相比变化不明显,而随着天名精内酯酮溶液浓度的升高,四种复合酶的活性均表现降低的趋势。
通过天名精内酯酮对离体和活体条件下小麦全蚀病菌复合酶活性测定结果可以看出,天名精内酯酮对小麦全蚀病菌的生物氧化过程存在明显影响,可能是通过对呼吸电子传递链复合酶活性的影响降低了ATP的合成量,致使菌体能量供应不足,最终导致病菌生长缓慢。
Carabrone is a sesquiterpenoid lactone compound from C.macrocephalum. Previous study indicated it has good antifungal activity, and has excellent activity on wheat powdery mildew, wheat take–all, wheat stripe rust, pot culture experiment indicated that Carabrone has a systemic action in wheat, physiological and biochemical test showed that Carabrone may have a certain effect on both biosynthesis and bio-oxidation of pathogen. In order to clear the mode of action and the mechanism of Carabrone to pathogen. In this paper, we study the conduction of Carabrone in wheat and take Gaeumannomyces graminis as test object in order to study the effects of Carabrone on bio-oxidation process of Gaeumannomyces graminis. The main results are as follows:
1 The inhibition of Carabrone on Blumeria graminis mainly by inhibiting the expansion of colony
The results of Carabrone on spore germination and colony expansion of Blumeria graminis by leave fragment method in vitro indicated that there is no significant inhibitory effect on spore germination by Carabrone. But it has significant effect on colony growth and showed some concentration-dependent, EC50 is 105.4314mg/L.
2 There is a conduction of Carabrone from down to up in wheat
Pot culture experiment indicated that Carabrone could control Blumeria graminis by irrigation, the protective effect and the curative effect is 61.18% and 60.77% .
Using HPLC method to detect the absorption of Carabrone by wheat roots in soil and in solution. The results showed that after 24h the content is the highest by in soil, reached to 26.825μg/g, and the absorption test of wheat roots in solution showed that the content of Carabrone increased gradually as the time went by.
Comprehensive analysis of the results of activity tests and instrumental analysis can be inferred that Carabrone has apparent systemic action and a conduction from down to up in wheat.
At the test dose, HPLC assay showed that there is not a significant conduction of Carabrone from up to down in wheat.
3 Carabrone has effect on the bio-oxidation process of Gaeumannomyces graminis
(1) The results of Co-toxicity test of Carabrone and SHAM to Gaeumannomyces graminis showed that SHAM has significant synergism to Carabrone. The increment mulliple is 1.86, indicating that Carabrone can affect the generation of ATP by interfere with respiratory electron transport chain process obviously.
(2) Carabrone has different effect on the activity of mitochondrial complexes in Gaeum- annomyces graminis by in vitro.
The results show that as the concentration of Carabrone gradually increased, the activity of complex I showed overall decreasing trend. When the concentration reached to 32mg/L, the activity of complex II were significantly increased. Only when the concentration is 1 mg/L, the activity of complex III were 1.4 times lower than the control.Complex IV have no significant effect by Carabrone.
(3) Carabrone has effect on all the four kinds of mitochondrial complexes in Gaeuman- nomyces graminis by in vivo.
The results showed that when the concentration of Carabrone is low, there is no significant difference compared with the control, with the concentration increased, all the four kinds of complexes decreased.
Through the results we can conclude that Carabrone has certain effect on bio-oxidation of Gaeumannomyces graminis, Carabrone may decreased the synthesis of ATP by interfere with complexes on respiratory electron transport chain , resulting in insufficient supply of biomass energy, leading to slow the growth of mycelium.
引文
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Calera MR, Soto F, Sanchez P, Bye R, Hernandez-Bautista B, Anaya AL, Lotina-Hennsen B, Mata R. 1995.
Biochemically active sesquiterpene lactones from Ratibida mexicana. Phytochemistry, 40(2):419~425
Chen PK, Leather GR. 1990. Plant growth regulatory activities of artemisinin and its related compounds. Journal of Chemical Ecology, 16(6): 1867~1876
Cowan MM. 1999. Plant products as Antimicrobial Agents. Clinical microbiology reviews, 12(04):564~582 Dong Yunfa, Ding Yunhai. 1988. Sesquiterpene lactones from Carpesium abrotanoides. Journal of integrative plant biology, 30(1): 71~75
Dirsch VM, Stuppner H, Vollmar AM. 2001. Helenalin Triggers a CD95 Death Receptor-independent Apoptosis That Is Not Affected by Overexpression of Bcl-xL or Bcl-2. Cancer Research, 61(15): 5817~5823
Eberhard U. 1985. Control of phytophthora infestans with berberin. CA, (107): 72~74
Feng JT, Ma ZQ, Li JH, He J, Xu H, Zhang X. 2010. Synthesis and Antifungal Activity of Carabrone Derivatives. Molecules, 15(9): 6485~6492
Hsu BD, Lee JY. 1988. Plant Physiol. 87, 116
Hehner SP, Heinrich M, Bork PM, Vogt M, Ratter F, Lehmann V, Schulze-Osthoff K, Droge W, Schmitz ML. 1998. Sesquiterpene lactones specifically inhibit activation of NF-κB by preventing the degradation of IB- and IB-. J Biol Chem, 273: 1288~1297
Hattefi Y, Stiggall DL. 1978. Preparation and properties of succinate:ubiquinone oxidoreductase (complexII). Methods Enzymol, 53: 21~27
Izawa S. 1977. in Encyclopedia of Plant Physiology. New Series, 5: 266~282
Joseph-Horne T, Heppner C, Headrick J, Hollomon DW. 2000. Identification and Characterization of the Mode of Action of MON 65500:A Novel Inhibitor of ATP Export from Mitochondria of the Wheat“Take-All”Fungus, Gaeumannomyces graminis var. tritici. Pesticide Biochemistry and Physiology, 67(3): 168~186
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Koo TH, Lee JH, Park YJ, Hong YS, Kim HS, Kim KW, Lee JJ. 2001. A sesquiterpene lactone, costunolide, from magnolia grandiflora inhibits NF-κB by targeting IκB phosphorylation. Planta Med, 67:103~110
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Lyss G, Knorre A, Schmidt TJ, Pahl HL, Merfort I. 1998. The Anti-inflammatory Sesquiterpene Lactone Helenalin Inhibits the Transcription Factor NF-κB by Directly Targeting p65. The Journal of Biological chemistry, 273(50): 33508~33516
Lotina-Hennsen B, Roque-Reséndiz JL, Jiménez M, Aguilar M. 1991. Naturforsch Z. 46c: 777~780
Maruyama M, OMURA S. 1977. Carpestolin from carpesium abrotanoides. Phytochemistry, 16(04): 782~783
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Parapini S, Basilico N, Mondani M, Olliaro P, Taramelli D, Monti D. 2004. Evidence that hacm iron in the malaria parasite is not needed for the antimalarial effects of artemisinin. FEBS Lett, 575(1): 91~94
Pecci L, Montefoschi G, Fontana M, Cavallini D. 1994. Aminoethylcysteine ketimine decarboxylated dimer inhibits mitochondrial respiration by impairing electron transport at complex I level. Biochem Biophys Res Commun, 199(2): 755~760
Rungeler P, Castro V, Mora G, G?ren N, Vichnewski W, Pahl HL, Merfort I, Schmidt TJ. 1999. Inhibition of Transcription Factor NF-κB by Sesquiterpene Lactones:a Proposed Molecular Mechanism of Action. Bioorganic & Medicinal Chemistry, 7 (11): 2343~2352
Richards EL. 1968. A monograph of the genus Ratibida. Rhodora, 70: 348~393
Rutherford AW, Zimmerman JL, Mathis P. 1984. FEBS Letters. 165: 156~162
Singer TP. 1974. Determination of the activity of succinate, NADH, choline, and alpha-glycerophosphate dehydrogenases. Methods Biochem Anal, 22: 123~175
Samson G, Morissette JC, Popovic R. 1988. Photochem Photobiol. 48: 329~332
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Tahara H. 1988. a fungitocin inducibly Produced by Dandelion Leaves Treated with Cupric Chloride. Agric Biol Chem, 52(1): 2947~2948
Woerdenbag H J. 1986. Evaluation of the invitro cytotoxicity of some sesquiterpene lactones on human lung carcinoma cell line using the fast green dye exclusion assay. Planta Medica1, 52(2): 112~114
Wei N, Sadrzadeh SMH. 1994. Enhancement of hemin-induced membrane damage by artemisinin. Biochem Pharmaco1, 48(4): 737~74l
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Bonizzi G, Karin M. 2004. The two NFκB activation pathways and their role in innate and adaptive immunity. Trends Immunol, 25(6): 280~288
Calera MR, Soto F, Sanchez P, Bye R, Hernandez-Bautista B, Anaya AL, Lotina-Hennsen B, Mata R. 1995.
Biochemically active sesquiterpene lactones from Ratibida mexicana. Phytochemistry, 40(2):419~425
Chen PK, Leather GR. 1990. Plant growth regulatory activities of artemisinin and its related compounds. Journal of Chemical Ecology, 16(6): 1867~1876
Cowan MM. 1999. Plant products as Antimicrobial Agents. Clinical microbiology reviews, 12(04):564~582 Dong Yunfa, Ding Yunhai. 1988. Sesquiterpene lactones from Carpesium abrotanoides. Journal of integrative plant biology, 30(1): 71~75
Dirsch VM, Stuppner H, Vollmar AM. 2001. Helenalin Triggers a CD95 Death Receptor-independent Apoptosis That Is Not Affected by Overexpression of Bcl-xL or Bcl-2. Cancer Research, 61(15): 5817~5823
Eberhard U. 1985. Control of phytophthora infestans with berberin. CA, (107): 72~74
Feng JT, Ma ZQ, Li JH, He J, Xu H, Zhang X. 2010. Synthesis and Antifungal Activity of Carabrone Derivatives. Molecules, 15(9): 6485~6492
Hsu BD, Lee JY. 1988. Plant Physiol. 87, 116
Hehner SP, Heinrich M, Bork PM, Vogt M, Ratter F, Lehmann V, Schulze-Osthoff K, Droge W, Schmitz ML. 1998. Sesquiterpene lactones specifically inhibit activation of NF-κB by preventing the degradation of IB- and IB-. J Biol Chem, 273: 1288~1297
Hattefi Y, Stiggall DL. 1978. Preparation and properties of succinate:ubiquinone oxidoreductase (complexII). Methods Enzymol, 53: 21~27
Izawa S. 1977. in Encyclopedia of Plant Physiology. New Series, 5: 266~282
Joseph-Horne T, Heppner C, Headrick J, Hollomon DW. 2000. Identification and Characterization of the Mode of Action of MON 65500:A Novel Inhibitor of ATP Export from Mitochondria of the Wheat“Take-All”Fungus, Gaeumannomyces graminis var. tritici. Pesticide Biochemistry and Physiology, 67(3): 168~186
Krahenbühl S, Chang M, Brass EP. 1991. Decreased activities of ubiquinol: ferricytochrome c oxidoreductase (complex III) and ferrocytochromec: oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin (c-lactam)-induced methylmalonic aciduria. J Biol Chem, 266(31): 20998~21003
Kurita N, Miyaji M. 1979. Antifungal activity and molecular orbital energies aldehyde compounds from oils if higher plants. Agric Biol Chem, 43(11): 2365~2371
Kim MR, Lee SK, Kim CS, Kim KS, Moon DC. 2004. Phytochemical Constitunts of Carpesium macrocephalum FR. Et S(AV). Arch Pharm Res, 27(10): 1029~1033
Koo TH, Lee JH, Park YJ, Hong YS, Kim HS, Kim KW, Lee JJ. 2001. A sesquiterpene lactone, costunolide, from magnolia grandiflora inhibits NF-κB by targeting IκB phosphorylation. Planta Med, 67:103~110
Lee KH, Huang ES, Piantadosi C, Pagano JS, Geissman TA. 1971. Cytotoxicity of Sesquiterpene Lactones. Cancer Research, 31(11): 1649~1654
Lyss G, Knorre A, Schmidt TJ, Pahl HL, Merfort I. 1998. The Anti-inflammatory Sesquiterpene Lactone Helenalin Inhibits the Transcription Factor NF-κB by Directly Targeting p65. The Journal of Biological chemistry, 273(50): 33508~33516
Lotina-Hennsen B, Roque-Reséndiz JL, Jiménez M, Aguilar M. 1991. Naturforsch Z. 46c: 777~780
Maruyama M, OMURA S. 1977. Carpestolin from carpesium abrotanoides. Phytochemistry, 16(04): 782~783
Mohanty N, Vass I, Demeter, S. 1989. Plant Physiol. 90, 175
Nakagawa M, Ohno T, Maruyama R, Okubo M, Nagatsu A, Inoue M, Tanabe H, Takemura G, Minatoguchi S, Fujiwara H. 2007. Sesquiterpene Lactone Suppresses Vascular Smooth Muscle Cell Proliferation and Migration via Inhibition of Cell Cycle Progression. Biol Pharm Bull, 30(9): 1754~1757
Picman AK, Schneider IEF. 1993. Biochem Syst Ecol, 21, 307
Parapini S, Basilico N, Mondani M, Olliaro P, Taramelli D, Monti D. 2004. Evidence that hacm iron in the malaria parasite is not needed for the antimalarial effects of artemisinin. FEBS Lett, 575(1): 91~94
Pecci L, Montefoschi G, Fontana M, Cavallini D. 1994. Aminoethylcysteine ketimine decarboxylated dimer inhibits mitochondrial respiration by impairing electron transport at complex I level. Biochem Biophys Res Commun, 199(2): 755~760
Rungeler P, Castro V, Mora G, G?ren N, Vichnewski W, Pahl HL, Merfort I, Schmidt TJ. 1999. Inhibition of Transcription Factor NF-κB by Sesquiterpene Lactones:a Proposed Molecular Mechanism of Action. Bioorganic & Medicinal Chemistry, 7 (11): 2343~2352
Richards EL. 1968. A monograph of the genus Ratibida. Rhodora, 70: 348~393
Rutherford AW, Zimmerman JL, Mathis P. 1984. FEBS Letters. 165: 156~162
Singer TP. 1974. Determination of the activity of succinate, NADH, choline, and alpha-glycerophosphate dehydrogenases. Methods Biochem Anal, 22: 123~175
Samson G, Morissette JC, Popovic R. 1988. Photochem Photobiol. 48: 329~332
Singh D, Singh S. 1987. Plant Physiol. 83: 12~14
Tahara H. 1988. a fungitocin inducibly Produced by Dandelion Leaves Treated with Cupric Chloride. Agric Biol Chem, 52(1): 2947~2948
Woerdenbag H J. 1986. Evaluation of the invitro cytotoxicity of some sesquiterpene lactones on human lung carcinoma cell line using the fast green dye exclusion assay. Planta Medica1, 52(2): 112~114
Wei N, Sadrzadeh SMH. 1994. Enhancement of hemin-induced membrane damage by artemisinin. Biochem Pharmaco1, 48(4): 737~74l
Xie QW, Whisnant R, Nathan C. 1993. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. Journal of Experimental Medicine, 177(6): 1779~1784
Xie QW, Kashiwabara Y, Nathan C. 1994. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. Journal of Biological Chemistry, 269(7): 4705~4708
Yruela I, Montoya G, Alonso PJ, Picorel R. 1991. Identification of the pheophytin-QA-Fe domain of the reducing side of the photosystem II as the Cu(II)-inhibitory binding site. J Bio Chem, 266(34): 22847~22850