A potent and selective cis-amide inhibitor of ryanodine receptor 2 as a candidate for cardiac arrhythmia treatment

Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the concentration of Ca2+ in the cytosol. RyR2 overactivation causes potentially lethal cardiac arrhythmias, but no specific inhibitor is yet available...

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Published inEuropean journal of medicinal chemistry Vol. 262; p. 115910
Main Authors Ishida, Ryosuke, Kurebayashi, Nagomi, Iinuma, Hiroto, Zeng, Xi, Mori, Shuichi, Kodama, Masami, Murayama, Takashi, Masuno, Hiroyuki, Takeda, Fumi, Kawahata, Masatoshi, Tanatani, Aya, Miura, Aya, Nishio, Hajime, Sakurai, Takashi, Kagechika, Hiroyuki
Format Journal Article
LanguageEnglish
Published ISSY-LES-MOULINEAUX Elsevier Masson SAS 15.12.2023
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Abstract Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the concentration of Ca2+ in the cytosol. RyR2 overactivation causes potentially lethal cardiac arrhythmias, but no specific inhibitor is yet available. Herein we developed the first highly potent and selective RyR2 inhibitor, TMDJ-035, containing 3,5-difluoro substituents on the A ring and a 4-fluoro substituent on the B ring, based on a comprehensive structure-activity relationship (SAR) study of tetrazole compound 1. The SAR study also showed that the amide conformation is critical for inhibitory potency. Single-crystal X-ray diffraction analysis and variable-temperature 1H NMR revealed that TMDJ-035 strongly favors cis-amide configuration, while the inactive analogue TMDJ-011 with a secondary amide takes trans-amide configuration. Examination of the selectivity among RyRs indicated that TMDJ-035 displayed high selectivity for RyR2. TMDJ-035 suppressed abnormal Ca2+ waves and transients in isolated cardiomyocytes from RyR2-mutated mice. It appears to be a promising candidate drug for treating cardiac arrhythmias due to RyR2 overactivation, as well as a tool for studying the mechanism and dynamics of RyR2 channel gating. TMDJ-035 with cis-amide configuration could suppress abnormal Ca2+ signals in cardiomyocytes from RyR2-mutated mice. [Display omitted] •The novel RyR2 selective inhibitor 1 was identified.•Structure-activity relationship discovered quite potent RyR2 inhibitor TMDJ-035.•The amide conformation of TMDJ-035 was verified as cis-amide, which is crucial for the activity expression.•TMDJ-035 showed complete selectivity among RyRs.•TMDJ-035 could suppress the abnormal Ca2+ signals in cardiomyocytes from RyR2-mutated mice.
AbstractList Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the concentration of Ca2+ in the cytosol. RyR2 overactivation causes potentially lethal cardiac arrhythmias, but no specific inhibitor is yet available. Herein we developed the first highly potent and selective RyR2 inhibitor, TMDJ-035, containing 3,5-difluoro substituents on the A ring and a 4-fluoro substituent on the B ring, based on a comprehensive structure-activity relationship (SAR) study of tetrazole compound 1. The SAR study also showed that the amide conformation is critical for inhibitory potency. Single-crystal X-ray diffraction analysis and variable-temperature 1H NMR revealed that TMDJ-035 strongly favors cis-amide configuration, while the inactive analogue TMDJ-011 with a secondary amide takes trans-amide configuration. Examination of the selectivity among RyRs indicated that TMDJ-035 displayed high selectivity for RyR2. TMDJ-035 suppressed abnormal Ca2+ waves and transients in isolated cardiomyocytes from RyR2-mutated mice. It appears to be a promising candidate drug for treating cardiac arrhythmias due to RyR2 overactivation, as well as a tool for studying the mechanism and dynamics of RyR2 channel gating. TMDJ-035 with cis-amide configuration could suppress abnormal Ca2+ signals in cardiomyocytes from RyR2-mutated mice. [Display omitted] •The novel RyR2 selective inhibitor 1 was identified.•Structure-activity relationship discovered quite potent RyR2 inhibitor TMDJ-035.•The amide conformation of TMDJ-035 was verified as cis-amide, which is crucial for the activity expression.•TMDJ-035 showed complete selectivity among RyRs.•TMDJ-035 could suppress the abnormal Ca2+ signals in cardiomyocytes from RyR2-mutated mice.
Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the concentration of Ca2+ in the cytosol. RyR2 overactivation causes potentially lethal cardiac arrhythmias, but no specific inhibitor is yet available. Herein we developed the first highly potent and selective RyR2 inhibitor, TMDJ-035, containing 3,5-difluoro substituents on the A ring and a 4-fluoro substituent on the B ring, based on a comprehensive structure-activity relationship (SAR) study of tetrazole compound 1. The SAR study also showed that the amide conformation is critical for inhibitory potency. Single-crystal X-ray diffraction analysis and variable-temperature 1H NMR revealed that TMDJ-035 strongly favors cis-amide configuration, while the inactive analogue TMDJ-011 with a secondary amide takes trans-amide configuration. Examination of the selectivity among RyRs indicated that TMDJ-035 displayed high selectivity for RyR2. TMDJ-035 suppressed abnormal Ca2+ waves and transients in isolated cardiomyocytes from RyR2-mutated mice. It appears to be a promising candidate drug for treating cardiac arrhythmias due to RyR2 over-activation, as well as a tool for studying the mechanism and dynamics of RyR2 channel gating.
Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the concentration of Ca2+ in the cytosol. RyR2 overactivation causes potentially lethal cardiac arrhythmias, but no specific inhibitor is yet available. Herein we developed the first highly potent and selective RyR2 inhibitor, TMDJ-035, containing 3,5-difluoro substituents on the A ring and a 4-fluoro substituent on the B ring, based on a comprehensive structure-activity relationship (SAR) study of tetrazole compound 1. The SAR study also showed that the amide conformation is critical for inhibitory potency. Single-crystal X-ray diffraction analysis and variable-temperature 1H NMR revealed that TMDJ-035 strongly favors cis-amide configuration, while the inactive analogue TMDJ-011 with a secondary amide takes trans-amide configuration. Examination of the selectivity among RyRs indicated that TMDJ-035 displayed high selectivity for RyR2. TMDJ-035 suppressed abnormal Ca2+ waves and transients in isolated cardiomyocytes from RyR2-mutated mice. It appears to be a promising candidate drug for treating cardiac arrhythmias due to RyR2 overactivation, as well as a tool for studying the mechanism and dynamics of RyR2 channel gating.
ArticleNumber 115910
Author Ishida, Ryosuke
Mori, Shuichi
Kawahata, Masatoshi
Nishio, Hajime
Sakurai, Takashi
Takeda, Fumi
Kagechika, Hiroyuki
Kodama, Masami
Masuno, Hiroyuki
Murayama, Takashi
Kurebayashi, Nagomi
Iinuma, Hiroto
Miura, Aya
Zeng, Xi
Tanatani, Aya
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  surname: Takeda
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  organization: Department of Chemistry, Faculty of Science, Ochanomizu University, 2-1-1 Otsuka, Bunkyo-ku, Tokyo, 112-8610, Japan
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  organization: Faculty of Pharmaceutical Sciences, Showa Pharmaceutical University, 3-3165 Higashi-Tamagawagakuen, Machida, Tokyo, 194-8543, Japan
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  givenname: Aya
  surname: Tanatani
  fullname: Tanatani, Aya
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– sequence: 12
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  surname: Miura
  fullname: Miura, Aya
  organization: Department of Legal Medicine, Hyogo Medical University, Nishinomiya, 663-8501, Japan
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  fullname: Nishio, Hajime
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  givenname: Hiroyuki
  orcidid: 0000-0002-6747-1013
  surname: Kagechika
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Keywords Arrhythmias drug candidate
Ryanodine receptor 2
Ca2+ channel inhibitor
Structure-activity relationship
POLYMORPHIC VENTRICULAR-TACHYCARDIA
TETRAZOLES
DANTROLENE
MALIGNANT HYPERTHERMIA
CONVERSION
SARCOPLASMIC-RETICULUM
RELEASE CHANNEL
PHARMACOLOGY
Ca 2+channel inhibitor
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Snippet Ryanodine receptor 2 (RyR2) is a Ca2+ release channel mainly located on the sarcoplasmic reticulum (SR) membrane of heart muscle cells and regulates the...
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SubjectTerms Arrhythmias drug candidate
Ca2+ channel inhibitor
Chemistry, Medicinal
Life Sciences & Biomedicine
Pharmacology & Pharmacy
Ryanodine receptor 2
Science & Technology
Structure-activity relationship
Title A potent and selective cis-amide inhibitor of ryanodine receptor 2 as a candidate for cardiac arrhythmia treatment
URI https://dx.doi.org/10.1016/j.ejmech.2023.115910
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