Probiotic-fermented purple sweet potato yogurt activates compensatory IGF‑IR/PI3K/Akt survival pathways and attenuates cardiac apoptosis in the hearts of spontaneously hypertensive rats

Lin,Pei-Pei; Hsieh,You-Miin; Kuo,Wei-Wen; Lin,Yueh-Min; Yeh,Yu-Lan; Lin,Chien-Chung; Tsai,Fuu-Jen; Tsai,Chang-Hai; Huang,Chih-Yang; Tsai,Cheng-Chih

doi:10.3892/ijmm.2013.1524

Probiotic-fermented purple sweet potato yogurt activates compensatory IGF‑IR/PI3K/Akt survival pathways and attenuates cardiac apoptosis in the hearts of spontaneously hypertensive rats

Authors:
- Pei-Pei Lin
- You-Miin Hsieh
- Wei-Wen Kuo
- Yueh-Min Lin
- Yu-Lan Yeh
- Chien-Chung Lin
- Fuu-Jen Tsai
- Chang-Hai Tsai
- Chih-Yang Huang
- Cheng-Chih Tsai
View Affiliations

Affiliations: Graduate Institute of Clinical Medical Science, China Medical University, Taichung, Taiwan, R.O.C., Department of Food and Nutrition, Providence University, Taichung, Taiwan, R.O.C., Department of Biological Science and Technology, China Medical University, Taichung, Taiwan, R.O.C., Department of Pathology, Changhua Christian Hospital, Changhua, Taiwan, R.O.C., Department of Orthopaedics, Armed Forces General Hospital, Taichung, Taiwan, R.O.C., Graduate Institute of Chinese Medical Science, Medical Research and Medical Genetics, China Medical University, Taichung, Taiwan, R.O.C., Graduate Institute of Basic Medical Science, China Medical University, Taichung, Taiwan, R.O.C., Department of Food Science and Technology, HungKuang University, Taichung, Taiwan, R.O.C.
Published online on: October 11, 2013 https://doi.org/10.3892/ijmm.2013.1524
Pages: 1319-1328

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Apoptosis is recognized as a predictor of adverse outcomes in subjects with cardiac diseases. The aim of this study was to explore the effects of probiotic-fermented purple sweet potato yogurt (PSPY) with high γ-aminobutyric acid (GABA) content on cardiac apoptosis in spontaneously hypertensive rat (SHR) hearts. The rats were orally adminsitered with 2 different concentrations of PSPY (10 and 100%) or captopril, 15.6 mg/kg, body weight (BW)/day. The control group was administered distilled water. DAPI and TUNEL staining were used to detect the numbers of apoptotic cells. A decrease in the number of TUNEL-positive cardiac myocytes was observed in the SHR-PSPY (10 and 100%) groups. In addition, the levels of key components of the Fas receptor- and mitochondrial-dependent apoptotic pathways were determined by western blot analysis. The results revealed that the levels of the key components of the Fas receptor- and mitochondrial-dependent apoptotic pathway were significantly decreased in the SHR-captopril, and 10 and 100% PSPY groups. Additionally, the levels of phosphorylated insulin-like growth factor‑I receptor (p-IGF‑IR) were increased in SHR hearts from the SHR-control group; however, no recovery in the levels of downstream signaling components was observed. In addition, the levels of components of the compensatory IGF-IR-dependent survival pathway (p-PI3K and p-Akt) were all highly enhanced in the left ventricles in the hearts form the SHR-10 and 100% PSPY groups. Therefore, the oral administration of PSPY may attenuate cardiomyocyte apoptosis in SHR hearts by activating IGF‑IR-dependent survival signaling pathways.

View Figures

View References

1	Tocci G, Sciarretta S and Volpe M: Development of heart failure in recent hypertension trials. J Hypertens. 26:1477–1486. 2008. View Article : Google Scholar : PubMed/NCBI
2	Morillas P, de Andrade H, Castillo J, Quiles J, Bertomeu-González V, Cordero A, Tarazón E, Roselló E, Portolés M, Rivera M and Bertomeu-Martínez V: Inflammation and apoptosis in hypertension. Relevance of the extent of target organ damage. Rev Esp Cardiol. 65:819–825. 2012.PubMed/NCBI
3	Lee SD, Chu CH, Huang EJ, Lu MC, Liu JY, Liu CJ, Hsu HH, Lin JA, Kuo WW and Huang CY: Roles of insulin-like growth factor II in cardiomyoblast apoptosis and in hypertensive rat heart with abdominal aorta ligation. Am J Physiol Endocrinol Metab. 291:E306–E314. 2006. View Article : Google Scholar : PubMed/NCBI
4	Kuo WW, Hsu TC, Chain MH, Lai CH, Wang WH, Tsai FJ, Tsai CH, Wu CH, Huang CY and Tzang BS: Attenuated cardiac mitochondrial-dependent apoptotic effects by li-fu formula in hamsters fed with a hypercholesterol diet. Evid Based Complement Alternat Med. 2011:5303452011.PubMed/NCBI
5	Haunstetter A and Izumo S: Apoptosis: basic mechanisms and implications for cardiovascular disease. Circ Res. 82:1111–1129. 1998. View Article : Google Scholar : PubMed/NCBI
6	Narula J, Haider N, Arbustini E and Chandrashekhar Y: Mechanisms of disease: apoptosis in heart failure - seeing hope in death. Nat Clin Pract Cardiovasc Med. 3:681–688. 2006. View Article : Google Scholar : PubMed/NCBI
7	Harrison DG, Cai H, Landmesser U and Griendling KK: Interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease. J Renin Angiotensin Aldosterone Syst. 4:51–61. 2003. View Article : Google Scholar : PubMed/NCBI
8	Filippatos G, Tilak M, Pinillos H and Uhal BD: Regulation of apoptosis by angiotensin II in the heart and lungs (Review). Int J Mol Med. 7:273–280. 2001.PubMed/NCBI
9	Fujio Y, Nguyen T, Wencker D, Kitsis RN and Walsh K: Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation. 101:660–667. 2000. View Article : Google Scholar : PubMed/NCBI
10	Athanasiou A, Clarke AB, Turner AE, Kumaran NM, Vakilpour S, Smith PA, Bagiokou D, Bradshaw TD, Westwell AD, Fang L, Lobo DN, Constantinescu CS, Calabrese V, Loesch A, Alexander SP, Clothier RH, Kendall DA and Bates TE: Cannabinoid receptor agonists are mitochondrial inhibitors: a unified hypothesis of how cannabinoids modulate mitochondrial function and induce cell death. Biochem Biophys Res Commun. 364:131–137. 2007. View Article : Google Scholar
11	Bishopric NH, Andreka P, Slepak T and Webster KA: Molecular mechanisms of apoptosis in the cardiac myocyte. Curr Opin Pharmacol. 1:141–150. 2001. View Article : Google Scholar : PubMed/NCBI
12	Lee SD, Tzang BS, Kuo WW, Lin YM, Yang AL, Chen SH, Tsai FJ, Wu FL, Lu MC and Huang CY: Cardiac fas receptor-dependent apoptotic pathway in obese Zucker rats. Obesity (Silver Spring). 15:2407–2415. 2007. View Article : Google Scholar : PubMed/NCBI
13	Brown GC and Borutaite V: Nitric oxide, cytochrome c and mitochondria. Nitric oxide, cytochrome c and mitochondria. Biochem Soc Symp. 66:17–25. 1999.
14	Ren J, Samson WK and Sowers JR: Insulin-like growth factor I as a cardiac hormone: physiological and pathophysiological implications in heart disease. J Mol Cell Cardiol. 31:2049–2061. 1999. View Article : Google Scholar : PubMed/NCBI
15	Vincent AM and Feldman EL: Control of cell survival by IGF signaling pathways. Growth Horm IGF Res. 12:193–197. 2002. View Article : Google Scholar : PubMed/NCBI
16	Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW and Liao JK: Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature. 407:538–541. 2000. View Article : Google Scholar : PubMed/NCBI
17	Liu CF, Tung YT, Wu CL, Lee BH, Hsu WH and Pan TM: Antihypertensive effects of Lactobacillus-fermented milk orally administered to spontaneously hypertensive rats. J Agric Food Chem. 59:4537–4543. 2011. View Article : Google Scholar : PubMed/NCBI
18	Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M and Sansawa H: Blood-pressure-lowering effect of a novel fermented milk containing gamma-aminobutyric acid (GABA) in mild hypertensives. Eur J Clin Nutr. 57:490–495. 2003. View Article : Google Scholar : PubMed/NCBI
19	Komatsuzaki N, Nakamura T, Kimura T and Shima J: Characterization of glutamate decarboxylase from a high gamma-aminobutyric acid (GABA)-producer, Lactobacillus paracasei. Biosci Biotechnol Biochem. 72:278–285. 2008. View Article : Google Scholar : PubMed/NCBI
20	Wu TY, Tsai CC, Hwang YT and Chiu TH: Effect of antioxidant activity and functional properties of chingshey purple sweet potato fermented milk by Lactobacillus acidophilus, L. delbrueckii subsp lactis, and L. gasseri strains. J Food Sci. 77:M2–M8. 2012. View Article : Google Scholar : PubMed/NCBI
21	Fortuno MA, Ravassa S, Fortuno A, Zalba G and Diez J: Cardiomyocyte apoptotic cell death in arterial hypertension: mechanisms and potential management. Hypertension. 38:1406–1412. 2001. View Article : Google Scholar : PubMed/NCBI
22	Richey PA and Brown SP: Pathological versus physiological left ventricular hypertrophy: a review. J Sports Sci. 16:129–141. 1998. View Article : Google Scholar : PubMed/NCBI
23	Lin PP, Hsieh YM, Kuo WW, Lin CC, Tsai FJ, Tsai CH, Huang CY and Tsai CC: Inhibition of cardiac hypertrophy by probiotic-fermented purple sweet potato yogurt in spontaneously hypertensive rat hearts. Int J Mol Med. 30:1365–1375. 2012.PubMed/NCBI
24	Díez J, Fortuño MA and Ravassa S: Apoptosis in hypertensive heart disease. Curr Opin Cardiol. 13:317–325. 1998.
25	Huang CY, Yang AL, Lin YM, Wu FN, Lin JA, Chan YS, Tsai FJ, Tsai CH, Kuo CH and Lee SD: Anti-apoptotic and pro-survival effects of exercise training on hypertensive hearts. J Appl Physiol. 112:883–891. 2012. View Article : Google Scholar : PubMed/NCBI
26	McGowan BS, Ciccimaro EF, Chan TO and Feldman AM: The balance between pro-apoptotic and anti-apoptotic pathways in the failing myocardium. Cardiovasc Toxicol. 3:191–206. 2003. View Article : Google Scholar : PubMed/NCBI
27	Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, Zias E, Walsh K, Rosenzweig A, Sussman MA, Urbanek K, Nadal-Ginard B, Kajstura J, Anversa P and Leri A: Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res. 94:514–524. 2004. View Article : Google Scholar : PubMed/NCBI
28	Palmen M, Daemen MJ, Bronsaer R, Dassen WR, Zandbergen HR, Kockx M, Smits JF, van der Zee R and Doevendans PA: Cardiac remodeling after myocardial infarction is impaired in IGF-1 deficient mice. Circ Res. 50:516–524. 2001.PubMed/NCBI
29	Wong CM, Bansal G, Pavlickova L, Marcocci L and Suzuki YJ: Reactive oxygen species and antioxidants in pulmonary hypertension. Antioxid Redox Signal. 18:1789–1796. 2012. View Article : Google Scholar : PubMed/NCBI
30	Lam V, Su J, Koprowski S, Hsu A, Tweddell JS, Rafiee P, Gross GJ, Salzman NH and Baker JE: Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J. 26:1727–1735. 2012. View Article : Google Scholar : PubMed/NCBI
31	Sobol KV, Belostotskaya GB and Nesterov VP: The effect of probiotics and their metabolic products on cardiovascular system cells in vitro. Dokl Biol Sci. 436:9–12. 2011. View Article : Google Scholar : PubMed/NCBI