Literature DB >> 24812278

Tubulin polymerization disrupts cardiac β-adrenergic regulation of late INa.

Nataliya Dybkova1, Stefan Wagner2, Johannes Backs3, Thomas J Hund4, Peter J Mohler4, Thomas Sowa1, Viacheslav O Nikolaev1, Lars S Maier5.   

Abstract

AIMS: The anticancer drug paclitaxel (TXL) that polymerizes microtubules is associated with arrhythmias and sinus node dysfunction. TXL can alter membrane expression of Na channels (NaV1.5) and Na current (INa), but the mechanisms are unknown. Calcium/calmodulin-dependent protein kinase II (CaMKII) can be activated by β-adrenergic stimulation and regulates INa gating. We tested whether TXL interferes with isoproterenol (ISO)-induced activation of CaMKII and consequent INa regulation. METHODS AND
RESULTS: In wild-type mouse myocytes, the addition of ISO (1 µmol/L) resulted in increased CaMKII auto-phosphorylation (western blotting). This increase was completely abolished after pre-treatment with TXL (100 µmol/L, 1.5 h). The mechanism was further investigated in human embryonic kidney cells. TXL inhibited the ISO-induced β-arrestin translocation. Interestingly, both knockdown of β-arrestin2 expression using small interfering RNA and inhibition of exchange protein directly activated by cAMP (Epac) blocked the ISO-induced CaMKII auto-phosphorylation similar to TXL. The generation of cAMP, however, was unaltered (Epac1-camps). CaMKII-dependent Na channel function was measured using patch-clamp technique in isolated cardiomyoctes. ISO stimulation failed to induce CaMKII-dependent enhancement of late INa and Na channel inactivation (negative voltage shift in steady-state activation and enhanced intermediate inactivation) after pre-incubation with TXL. Consistent with this, TXL also inhibited ISO-induced CaMKII-specific Na channel phosphorylation (at serine 571 of NaV1.5).
CONCLUSION: Pre-incubation with TXL disrupts the ISO-dependent CaMKII activation and consequent Na channel regulation. This may be important for patients receiving TXL treatments, but also relevant for conditions of increased CaMKII expression and enhanced β-adrenergic stimulation like in heart failure. Published on behalf of the European Society of Cardiology. All rights reserved.
© The Author 2014. For permissions please email: journals.permissions@oup.com.

Entities:  

Keywords:  Adrenergic stimulation; Calcium/calmodulin-dependent protein kinase II; Microtubules; Paclitaxel; Sodium channels

Mesh:

Substances:

Year:  2014        PMID: 24812278      PMCID: PMC4133594          DOI: 10.1093/cvr/cvu120

Source DB:  PubMed          Journal:  Cardiovasc Res        ISSN: 0008-6363            Impact factor:   10.787


  38 in total

1.  Activation of protein kinase A modulates trafficking of the human cardiac sodium channel in Xenopus oocytes.

Authors:  J Zhou; J Yi; N Hu; A L George; K T Murray
Journal:  Circ Res       Date:  2000-07-07       Impact factor: 17.367

2.  Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude.

Authors:  Tracy L Yarbrough; Tong Lu; Hon-Chi Lee; Erwin F Shibata
Journal:  Circ Res       Date:  2002-03-08       Impact factor: 17.367

3.  Novel single chain cAMP sensors for receptor-induced signal propagation.

Authors:  Viacheslav O Nikolaev; Moritz Bünemann; Lutz Hein; Annette Hannawacker; Martin J Lohse
Journal:  J Biol Chem       Date:  2004-07-01       Impact factor: 5.157

4.  Can PKA activators rescue Na+ channel function in epicardial border zone cells that survive in the infarcted canine heart?

Authors:  Shigeo Baba; Wen Dun; Penelope A Boyden
Journal:  Cardiovasc Res       Date:  2004-11-01       Impact factor: 10.787

5.  Dynamic instability of microtubule growth.

Authors:  T Mitchison; M Kirschner
Journal:  Nature       Date:  1984 Nov 15-21       Impact factor: 49.962

6.  An unexpected role for brain-type sodium channels in coupling of cell surface depolarization to contraction in the heart.

Authors:  Sebastian K G Maier; Ruth E Westenbroek; Kenneth A Schenkman; Eric O Feigl; Todd Scheuer; William A Catterall
Journal:  Proc Natl Acad Sci U S A       Date:  2002-03-12       Impact factor: 11.205

7.  Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II.

Authors:  Wei-Zhong Zhu; Shi-Qiang Wang; Khalid Chakir; Dongmei Yang; Tong Zhang; Joan Heller Brown; Eric Devic; Brian K Kobilka; Heping Cheng; Rui-Ping Xiao
Journal:  J Clin Invest       Date:  2003-03       Impact factor: 14.808

8.  Phosphorylation and putative ER retention signals are required for protein kinase A-mediated potentiation of cardiac sodium current.

Authors:  Jingsong Zhou; Hyeon-Gyu Shin; Jianxun Yi; Wangzhen Shen; Christine P Williams; Katherine T Murray
Journal:  Circ Res       Date:  2002-09-20       Impact factor: 17.367

9.  Thermodynamics of ligand-induced assembly of tubulin.

Authors:  J F Díaz; M Menéndez; J M Andreu
Journal:  Biochemistry       Date:  1993-09-28       Impact factor: 3.162

10.  Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A).

Authors:  D Woodrow Benson; Dao W Wang; Macaira Dyment; Timothy K Knilans; Frank A Fish; Margaret J Strieper; Thomas H Rhodes; Alfred L George
Journal:  J Clin Invest       Date:  2003-10       Impact factor: 14.808

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  22 in total

Review 1.  Neuronal sodium channels: emerging components of the nano-machinery of cardiac calcium cycling.

Authors:  Rengasayee Veeraraghavan; Sándor Györke; Przemysław B Radwański
Journal:  J Physiol       Date:  2017-03-26       Impact factor: 5.182

Review 2.  Role of sodium and calcium dysregulation in tachyarrhythmias in sudden cardiac death.

Authors:  Stefan Wagner; Lars S Maier; Donald M Bers
Journal:  Circ Res       Date:  2015-06-05       Impact factor: 17.367

3.  Distribution of cardiac sodium channels in clusters potentiates ephaptic interactions in the intercalated disc.

Authors:  Echrak Hichri; Hugues Abriel; Jan P Kucera
Journal:  J Physiol       Date:  2018-01-09       Impact factor: 5.182

4.  Cardiac arrhythmia in a mouse model of sodium channel SCN8A epileptic encephalopathy.

Authors:  Chad R Frasier; Jacy L Wagnon; Yangyang Oliver Bao; Luke G McVeigh; Luis F Lopez-Santiago; Miriam H Meisler; Lori L Isom
Journal:  Proc Natl Acad Sci U S A       Date:  2016-10-26       Impact factor: 11.205

5.  Nonequilibrium reactivation of Na+ current drives early afterdepolarizations in mouse ventricle.

Authors:  Andrew G Edwards; Eleonora Grandi; Johan E Hake; Sonia Patel; Pan Li; Shigeki Miyamoto; Jeffrey H Omens; Joan Heller Brown; Donald M Bers; Andrew D McCulloch
Journal:  Circ Arrhythm Electrophysiol       Date:  2014-09-18

6.  Early effects of Epac depend on the fine-tuning of the sarcoplasmic reticulum Ca2+ handling in cardiomyocytes.

Authors:  N Lezcano; J I E Mariángelo; L Vittone; X H T Wehrens; M Said; C Mundiña-Weilenmann
Journal:  J Mol Cell Cardiol       Date:  2017-10-14       Impact factor: 5.000

7.  Intracellular calcium attenuates late current conducted by mutant human cardiac sodium channels.

Authors:  Franck Potet; Thomas M Beckermann; Jennifer D Kunic; Alfred L George
Journal:  Circ Arrhythm Electrophysiol       Date:  2015-05-28

Review 8.  The role of Epac in the heart.

Authors:  Takayuki Fujita; Masanari Umemura; Utako Yokoyama; Satoshi Okumura; Yoshihiro Ishikawa
Journal:  Cell Mol Life Sci       Date:  2016-08-22       Impact factor: 9.261

9.  C-terminal phosphorylation of NaV1.5 impairs FGF13-dependent regulation of channel inactivation.

Authors:  Sophie Burel; Fabien C Coyan; Maxime Lorenzini; Matthew R Meyer; Cheryl F Lichti; Joan H Brown; Gildas Loussouarn; Flavien Charpentier; Jeanne M Nerbonne; R Reid Townsend; Lars S Maier; Céline Marionneau
Journal:  J Biol Chem       Date:  2017-09-07       Impact factor: 5.157

10.  Exchange protein activated by cyclic-adenosine monophosphate (Epac) regulates atrial fibroblast function and controls cardiac remodelling.

Authors:  Sirirat Surinkaew; Mona Aflaki; Abhijit Takawale; Yu Chen; Xiao-Yan Qi; Marc-Antoine Gillis; Yan-Fen Shi; Jean-Claude Tardif; Nipon Chattipakorn; Stanley Nattel
Journal:  Cardiovasc Res       Date:  2019-01-01       Impact factor: 10.787

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