Skip to main content
Top
Published in: Heart and Vessels 10/2018

01-10-2018 | Original Article

Linagliptin prevents atrial electrical and structural remodeling in a canine model of atrial fibrillation

Authors: Tazuru Igarashi, Shinichi Niwano, Hiroe Niwano, Tomoharu Yoshizawa, Hironori Nakamura, Hidehira Fukaya, Tamami Fujiishi, Naruya Ishizue, Akira Satoh, Jun Kishihara, Masami Murakami, Junya Ako

Published in: Heart and Vessels | Issue 10/2018

Login to get access

Abstract

Dipeptidyl peptidase 4 (DPP-4) inhibitors have recently been reported to exhibit additional cardioprotective effects; however, their effect in atrial remodeling, such as in atrial fibrillation (AF), remains unclear. In this study, the effect of linagliptin on atrial electrical and structural remodeling was evaluated in a canine AF model. Sixteen beagle dogs with 3-week atrial rapid stimulation were divided into the linagliptin group (9 mg/kg/day, n = 8) and pacing control group (n = 8). Three additional dogs without rapid pacing were assigned into non-pacing group, which was used as sham in this study. In the dogs with rapid pacing, the atrial effective refractory period (AERP), conduction velocity (CV), and AF inducibility were evaluated and blood was sampled every week. After the entire protocol, atrial tissue was sampled for histological examinations using HE, Azan, and dihydroethidium (DHE) staining to evaluate any tissue damage or oxidative stress. The pacing control group exhibited a gradual AERP shortening and CV decrease along the time course as previously reported. In the linagliptin group, the AERP shortening was not affected, but the CV decrease was suppressed in comparison to the control group (p < 0.05). The AF inducibility was increased in the control group and suppressed in the linagliptin group (p < 0.05). The control group exhibited tissue fibrosis, the degree of which was suppressed in the linagliptin group. DHE staining exhibited suppression of the reactive oxygen species expression in the linagliptin group in comparison to the pacing control group. Linagliptin, a DPP-4-inhibitor, suppressed the AF inducibility, CV decrease, and overexpression of oxidative stress in the canine AF model. Such suppressive effects of linagliptin on AF in the canine model may possibly be related to the anti-oxidative effect.
Literature
1.
go back to reference Matsubara J, Sugiyama S, Akiyama E, Iwashita S, Kurokawa H, Ohba K, Maeda H, Fujisue K, Yamamoto E, Kaikita K, Hokimoto S, Jinnouchi H, Ogawa H (2013) Dipeptidyl peptidase-4 inhibitor, sitagliptin, improves endothelial dysfunction in association with its anti-inflammatory effects in patients with coronary artery disease and uncontrolled diabetes. Circ J 77(5):1337–1344CrossRefPubMed Matsubara J, Sugiyama S, Akiyama E, Iwashita S, Kurokawa H, Ohba K, Maeda H, Fujisue K, Yamamoto E, Kaikita K, Hokimoto S, Jinnouchi H, Ogawa H (2013) Dipeptidyl peptidase-4 inhibitor, sitagliptin, improves endothelial dysfunction in association with its anti-inflammatory effects in patients with coronary artery disease and uncontrolled diabetes. Circ J 77(5):1337–1344CrossRefPubMed
2.
go back to reference Monami M, Ahrén B, Dicembrini I, Mannucci E (2013) Dipeptidyl peptidase-4 inhibitors and cardiovascular risk: a meta-analysis of randomized clinical trials. Diabetes Obes Metab 15(2):112–120CrossRefPubMed Monami M, Ahrén B, Dicembrini I, Mannucci E (2013) Dipeptidyl peptidase-4 inhibitors and cardiovascular risk: a meta-analysis of randomized clinical trials. Diabetes Obes Metab 15(2):112–120CrossRefPubMed
3.
go back to reference Avogaro A, de Kreutzenberg S, Fadini G (2014) Dipeptidyl-peptidase 4 inhibition: linking metabolic control to cardiovascular protection. Curr Pharm Des 20(14):2387–2394CrossRefPubMedPubMedCentral Avogaro A, de Kreutzenberg S, Fadini G (2014) Dipeptidyl-peptidase 4 inhibition: linking metabolic control to cardiovascular protection. Curr Pharm Des 20(14):2387–2394CrossRefPubMedPubMedCentral
4.
go back to reference Nystrom T, Gutniak MK, Zhang Q, Zhang F, Holst JJ, Ahrén B, Sjöholm A (2004) Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am J Physiol Endocrinol Metab 287:E1209–E1215CrossRefPubMed Nystrom T, Gutniak MK, Zhang Q, Zhang F, Holst JJ, Ahrén B, Sjöholm A (2004) Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am J Physiol Endocrinol Metab 287:E1209–E1215CrossRefPubMed
5.
go back to reference Zeisberg M, Zeisberg EM (2015) Kidney Evidence for antifibrotic incretin-independent effects of the DPP-4 inhibitor linagliptin. Kidney Int 88(3):429–431CrossRefPubMed Zeisberg M, Zeisberg EM (2015) Kidney Evidence for antifibrotic incretin-independent effects of the DPP-4 inhibitor linagliptin. Kidney Int 88(3):429–431CrossRefPubMed
6.
go back to reference Inthachai T, Lekawanvijit S, Kumfu S, Apaijai N, Pongkan W, Chattipakorn SC, Chattipakorn N (2015) Dipeptidyl peptidase-4 inhibitor improves cardiac function by attenuating adverse cardiac remodelling in rats with chronic myocardial infarction. Exp Physiol 100(6):667–679CrossRefPubMed Inthachai T, Lekawanvijit S, Kumfu S, Apaijai N, Pongkan W, Chattipakorn SC, Chattipakorn N (2015) Dipeptidyl peptidase-4 inhibitor improves cardiac function by attenuating adverse cardiac remodelling in rats with chronic myocardial infarction. Exp Physiol 100(6):667–679CrossRefPubMed
7.
go back to reference Murase H, Kuno A, Miki T, Tanno M, Yano T, Kouzu H, Ishikawa S, Tobisawa T, Ogasawara M, Nishizawa K, Miura T (2015) Inhibition of DPP-4 reduces acute mortality after myocardial infarction with restoration of autophagic response in type 2 diabetic rats. Cardiovasc Diabetol 14:103CrossRefPubMedPubMedCentral Murase H, Kuno A, Miki T, Tanno M, Yano T, Kouzu H, Ishikawa S, Tobisawa T, Ogasawara M, Nishizawa K, Miura T (2015) Inhibition of DPP-4 reduces acute mortality after myocardial infarction with restoration of autophagic response in type 2 diabetic rats. Cardiovasc Diabetol 14:103CrossRefPubMedPubMedCentral
8.
go back to reference Kiryu M, Niwano S, Niwano H, Kishihara J, Aoyama Y, Fukaya H, Masaki Y, Izumi T (2012) Angiotensin II mediated up-regulation of connective tissue growth factor promotes atrial tissue fibrosis in the canine atrial fibrillation model. Europace 14:1206–1214CrossRefPubMedPubMedCentral Kiryu M, Niwano S, Niwano H, Kishihara J, Aoyama Y, Fukaya H, Masaki Y, Izumi T (2012) Angiotensin II mediated up-regulation of connective tissue growth factor promotes atrial tissue fibrosis in the canine atrial fibrillation model. Europace 14:1206–1214CrossRefPubMedPubMedCentral
9.
go back to reference Kishihara J, Niwano S, Niwano H, Aoyama Y, Satoh A, Oikawa J, Kiryu M, Fukaya H, Masaki Y, Tamaki H, Izumi T, Ako J (2014) Effect of carvedilol on atrial remodeling in canine model of atrial fibrillation. Cardiovasc Diagn Ther 4:28–35PubMedPubMedCentral Kishihara J, Niwano S, Niwano H, Aoyama Y, Satoh A, Oikawa J, Kiryu M, Fukaya H, Masaki Y, Tamaki H, Izumi T, Ako J (2014) Effect of carvedilol on atrial remodeling in canine model of atrial fibrillation. Cardiovasc Diagn Ther 4:28–35PubMedPubMedCentral
10.
go back to reference Satoh A, Niwano S, Niwano H, Kishihara J, Aoyama Y, Oikawa J, Fukaya H, Tamaki H, Ako J (2017) Aliskiren suppresses atrial electrical and structural remodeling in a canine model of atrial fibrillation. Heart Vessels 32(1):90–100CrossRefPubMed Satoh A, Niwano S, Niwano H, Kishihara J, Aoyama Y, Oikawa J, Fukaya H, Tamaki H, Ako J (2017) Aliskiren suppresses atrial electrical and structural remodeling in a canine model of atrial fibrillation. Heart Vessels 32(1):90–100CrossRefPubMed
11.
go back to reference Fukaya H, Niwano S, Satoh D, Masaki Y, Niwano H, Kojima J, Moriguchi M, Izumi T (2008) Inhomogenic effect of bepridil on atrial electrical remodeling in a canine rapid atrial stimulation model. Circ J 72:318–326CrossRefPubMed Fukaya H, Niwano S, Satoh D, Masaki Y, Niwano H, Kojima J, Moriguchi M, Izumi T (2008) Inhomogenic effect of bepridil on atrial electrical remodeling in a canine rapid atrial stimulation model. Circ J 72:318–326CrossRefPubMed
12.
go back to reference Zheng MQ, Tang K, Zimmerman MC, Liu L, Xie B, Rozanski GJ (2009) Role of gamma-glutamyl transpeptidase in redox regulation of K+ channel remodeling in postmyocardial infarction rat hearts. Am J Physiol Cell Physiol 297:C253–C262CrossRefPubMedPubMedCentral Zheng MQ, Tang K, Zimmerman MC, Liu L, Xie B, Rozanski GJ (2009) Role of gamma-glutamyl transpeptidase in redox regulation of K+ channel remodeling in postmyocardial infarction rat hearts. Am J Physiol Cell Physiol 297:C253–C262CrossRefPubMedPubMedCentral
13.
go back to reference Hendarto H, Inoguchi T, Maeda Y, Ikeda N, Zheng J, Takei R, Yokomizo H, Hirata E, Sonoda N, Takayanagi R (2012) GLP-1 analog liraglutide protects against oxidative stress and albuminuria in streptozotocin-induced diabetic rats via protein kinase A-mediated inhibition of renal NAD(p)H oxidase. Metabolism 61:1422–1434CrossRefPubMed Hendarto H, Inoguchi T, Maeda Y, Ikeda N, Zheng J, Takei R, Yokomizo H, Hirata E, Sonoda N, Takayanagi R (2012) GLP-1 analog liraglutide protects against oxidative stress and albuminuria in streptozotocin-induced diabetic rats via protein kinase A-mediated inhibition of renal NAD(p)H oxidase. Metabolism 61:1422–1434CrossRefPubMed
14.
go back to reference Wang X, Ding Z, Yang F, Dai Y, Chen P, Theus S, Singh S, Budhiraja M, Mehta JL (2016) Modulation of myocardial injury and collagen deposition following ischemia-reperfusion by linagliptin and liraglutide, and both together. Clin Sci 130:1353–1362CrossRefPubMed Wang X, Ding Z, Yang F, Dai Y, Chen P, Theus S, Singh S, Budhiraja M, Mehta JL (2016) Modulation of myocardial injury and collagen deposition following ischemia-reperfusion by linagliptin and liraglutide, and both together. Clin Sci 130:1353–1362CrossRefPubMed
15.
go back to reference Alam J, Cook JL (2003) Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9(30):2499–2511CrossRefPubMed Alam J, Cook JL (2003) Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9(30):2499–2511CrossRefPubMed
16.
go back to reference Issan Y, Kornowski R, Aravot D, Shainberg A, Laniado-Schwartzman M, Sodhi K, Abraham NG, Hochhauser E (2014) Heme oxygenase-1 induction improves cardiac function following myocardial ischemia by reducing oxidative stress. PLoS One 9(3):e92246CrossRefPubMedPubMedCentral Issan Y, Kornowski R, Aravot D, Shainberg A, Laniado-Schwartzman M, Sodhi K, Abraham NG, Hochhauser E (2014) Heme oxygenase-1 induction improves cardiac function following myocardial ischemia by reducing oxidative stress. PLoS One 9(3):e92246CrossRefPubMedPubMedCentral
17.
go back to reference Kameoka J, Tanaka T, Nojima Y, Schlossman SF, Morimoto C (1993) Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science 261(5120):466–469CrossRefPubMed Kameoka J, Tanaka T, Nojima Y, Schlossman SF, Morimoto C (1993) Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science 261(5120):466–469CrossRefPubMed
18.
go back to reference Zhong J, Rao X, Rajagopalan S (2013) An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis 226(2):305–314CrossRefPubMed Zhong J, Rao X, Rajagopalan S (2013) An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis 226(2):305–314CrossRefPubMed
19.
go back to reference Narayan P, Mentzer RM Jr, Lasley RD (2001) Adenosine A1 receptor activation reduced reactive oxygen species and attenuates stunning in ventricular myocytes. J Mol Cell Cardiol 33:121–129CrossRefPubMed Narayan P, Mentzer RM Jr, Lasley RD (2001) Adenosine A1 receptor activation reduced reactive oxygen species and attenuates stunning in ventricular myocytes. J Mol Cell Cardiol 33:121–129CrossRefPubMed
20.
go back to reference Xiang F, Huang Y, Zhang D, Chu ZG, Zhang JP, Zhang Q (2010) Adenosine A1 receptor activation reduces opening of mitochondrial permeability transition pores in hypoxic cardiomyocytes. Clin Exp Pharmacol Physiol 37(3):343–349CrossRefPubMed Xiang F, Huang Y, Zhang D, Chu ZG, Zhang JP, Zhang Q (2010) Adenosine A1 receptor activation reduces opening of mitochondrial permeability transition pores in hypoxic cardiomyocytes. Clin Exp Pharmacol Physiol 37(3):343–349CrossRefPubMed
21.
go back to reference Lendeckel U, Arndt M, Wrenger S, Nepple K, Huth C, Ansorge S, Klein HU, Goette A (2001) Expression and activity of ectopeptidases in fibrillating human atria. J Mol Cell Cardiol 33(6):1273–1281CrossRefPubMed Lendeckel U, Arndt M, Wrenger S, Nepple K, Huth C, Ansorge S, Klein HU, Goette A (2001) Expression and activity of ectopeptidases in fibrillating human atria. J Mol Cell Cardiol 33(6):1273–1281CrossRefPubMed
Metadata
Title
Linagliptin prevents atrial electrical and structural remodeling in a canine model of atrial fibrillation
Authors
Tazuru Igarashi
Shinichi Niwano
Hiroe Niwano
Tomoharu Yoshizawa
Hironori Nakamura
Hidehira Fukaya
Tamami Fujiishi
Naruya Ishizue
Akira Satoh
Jun Kishihara
Masami Murakami
Junya Ako
Publication date
01-10-2018
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 10/2018
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-018-1170-0

Other articles of this Issue 10/2018

Heart and Vessels 10/2018 Go to the issue