Critical role of insulin‑like growth factor binding protein‑5 in methamphetamine‑induced apoptosis in cardiomyocytes

Leung,Ka‑Pui; Qu,Yi‑Hong; Qiao,Dong‑Fang; Xie,Wei‑Bing; Li,Dong‑Ri; Xu,Jing‑Tao; Wang,Hui‑Jun; Yue,Xia

doi:10.3892/mmr.2014.2572

Critical role of insulin‑like growth factor binding protein‑5 in methamphetamine‑induced apoptosis in cardiomyocytes

Authors:
- Ka‑Pui Leung
- Yi‑Hong Qu
- Dong‑Fang Qiao
- Wei‑Bing Xie
- Dong‑Ri Li
- Jing‑Tao Xu
- Hui‑Jun Wang
- Xia Yue
View Affiliations

Affiliations: Department of Forensic Medicine, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China
Published online on: September 16, 2014 https://doi.org/10.3892/mmr.2014.2572
Pages: 2306-2312
Copyright: © Leung et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

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

Methamphetamine (MA) is a highly abused amphetamine‑like psychostimulant. At present, the mechanisms underlying MA‑induced cardiotoxicity are poorly understood. The cardiotoxic effects have yet not been clearly elucidated with respect to the apoptotic pathway. Insulin‑like growth factor binding protein‑5 (IGFBP5) is important for cell growth control and the induction of apoptosis. The aim of the present study was to analyze whether IGFBP5 is involved in MA‑induced apoptosis as a novel target. MA‑induced apoptosis was observed in neonatal rat ventricular myocytes (NRVMs) in a concentration‑dependent manner using a terminal deoxyribonucleotide transferase‑mediated dUTP nick end‑labeling assay. Using reverse transcription polymerase chain reaction and western blotting, MA was demonstrated to induce concentration‑dependent increases in the expression of IGFBP5. Silencing IGFBP5 with small interfering RNA significantly reduced apoptosis and suppressed the expression of caspase‑3 in NRVMs following treatment with MA. To the best of our knowledge, the present study provided the first evidence suggesting that IGFBP5 is a potential therapeutic target in MA‑induced apoptosis in vitro, providing a foundation for future in vivo studies.

View Figures

View References

1	Scott JC, Woods SP, Matt GE, et al: Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychol Rev. 17:275–297. 2007. View Article : Google Scholar : PubMed/NCBI
2	Shrem MT and Halkitis PN: Methamphetamine abuse in the United States: contextual, psychological and sociological considerations. J Health Psychol. 13:669–679. 2008. View Article : Google Scholar : PubMed/NCBI
3	Carvalho M, Carmo H, Costa VM, et al: Toxicity of amphetamines: an update. Arch Toxicol. 86:1167–1231. 2012. View Article : Google Scholar : PubMed/NCBI
4	Deng X, Wang Y, Chou J and Cadet JL: Methamphetamine causes widespread apoptosis in the mouse brain: evidence from using an improved TUNEL histochemical method. Brain Res Mol Brain Res. 93:64–69. 2001. View Article : Google Scholar
5	Jayanthi S, Deng X, Noailles PA, Ladenheim B and Cadet JL: Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB J. 18:238–251. 2004. View Article : Google Scholar
6	Cadet JL, Jayanthi S and Deng X: Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. FASEB J. 17:1775–1788. 2003. View Article : Google Scholar
7	Li Y, Hu Z, Chen B, et al: Taurine attenuates methamphetamine-induced autophagy and apoptosis in PC12 cells through mTOR signaling pathway. Toxicol Lett. 215:1–7. 2012. View Article : Google Scholar : PubMed/NCBI
8	Darke S, Kaye S, McKetin R and Duflou J: Major physical and psychological harms of methamphetamine use. Drug Alcohol Rev. 27:253–262. 2008. View Article : Google Scholar : PubMed/NCBI
9	Kaye S, McKetin R, Duflou J and Darke S: Methamphetamine and cardiovascular pathology: a review of the evidence. Addiction. 102:1204–1211. 2007. View Article : Google Scholar : PubMed/NCBI
10	Costa GM, Pizzi C, Bresciani B, et al: Acute myocardial infarction caused by amphetamines: a case report and review of the literature. Ital Heart J. 2:478–480. 2001.PubMed/NCBI
11	Waksman J, Taylor RN Jr, Bodor GS, et al: Acute myocardial infarction associated with amphetamine use. Mayo Clin Proc. 76:323–326. 2001. View Article : Google Scholar : PubMed/NCBI
12	Sztajnkrycer MD, Hariharan S and Bond GR: Cardiac irritability and myocardial infarction in a 13-year-old girl following recreational amphetamine overdose. Pediatr Emerg Care. 18:E11–E15. 2002.PubMed/NCBI
13	Hung MJ, Kuo LT and Cherng WJ: Amphetamine-related acute myocardial infarction due to coronary artery spasm. Int J Clin Pract. 57:62–64. 2003.PubMed/NCBI
14	Brennan K, Shurmur S and Elhendy A: Coronary artery rupture associated with amphetamine abuse. Cardiol Rev. 12:282–283. 2004. View Article : Google Scholar : PubMed/NCBI
15	Watts DJ and McCollester L: Methamphetamine-induced myocardial infarction with elevated troponin I. Am J Emerg Med. 24:132–134. 2006. View Article : Google Scholar : PubMed/NCBI
16	Hong R, Matsuyama E and Nur K: Cardiomyopathy associated with the smoking of crystal methamphetamine. JAMA. 265:1152–1154. 1991. View Article : Google Scholar : PubMed/NCBI
17	Wijetunga M, Seto T, Lindsay J and Schatz I: Crystal methamphetamine-associated cardiomyopathy: tip of the iceberg? J Toxicol Clin Toxicol. 41:981–986. 2003. View Article : Google Scholar : PubMed/NCBI
18	Crean AM and Pohl JE: ‘Ally McBeal heart?’ - drug induced cardiomyopathy in a young woman. Br J Clin Pharmacol. 58:558–559. 2004.
19	Olivetti G, Abbi R, Quaini F, et al: Apoptosis in the failing human heart. N Engl J Med. 336:1131–1141. 1997. View Article : Google Scholar : PubMed/NCBI
20	Takemura G and Fujiwara H: Role of apoptosis in remodeling after myocardial infarction. Pharmacol Ther. 104:1–16. 2004. View Article : Google Scholar : PubMed/NCBI
21	Narula J, Haider N, Virmani R, et al: Apoptosis in myocytes in end-stage heart failure. N Engl J Med. 335:1182–1189. 1996. View Article : Google Scholar : PubMed/NCBI
22	Narula J, Kolodgie FD and Virmani R: Apoptosis and cardiomyopathy. Curr Opin Cardiol. 15:183–188. 2000. View Article : Google Scholar
23	Nickerson T, Pollak M and Huynh H: Castration-induced apoptosis in the rat ventral prostate is associated with increased expression of genes encoding insulin-like growth factor binding proteins 2,3,4 and 5. Endocrinology. 139:807–810. 1998. View Article : Google Scholar
24	Tonner E, Barber MC, Allan GJ, et al: Insulin-like growth factor binding protein-5 (IGFBP-5) induces premature cell death in the mammary glands of transgenic mice. Development. 129:4547–4557. 2002.PubMed/NCBI
25	Beilharz EJ, Klempt ND, Klempt M, et al: Differential expression of insulin-like growth factor binding proteins (IGFBP) 4 and 5 mRNA in the rat brain after transient hypoxic-ischemic injury. Brain Res Mol Brain Res. 18:209–215. 1993. View Article : Google Scholar
26	McManus MT and Sharp PA: Gene silencing in mammals by small interfering RNAs. Nat Rev Genet. 3:737–747. 2002. View Article : Google Scholar : PubMed/NCBI
27	Iwasa M, Maeno Y, Inoue H, Koyama H and Matoba R: Induction of apoptotic cell death in rat thymus and spleen after a bolus injection of methamphetamine. Int J Legal Med. 109:23–28. 1996. View Article : Google Scholar : PubMed/NCBI
28	Davidson C, Gow AJ, Lee TH and Ellinwood EH: Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res Brain Res Rev. 36:1–22. 2001. View Article : Google Scholar : PubMed/NCBI
29	Smith HJ, Roche AH, Jausch MF and Herdson PB: Cardiomyopathy associated with amphetamine administration. Am Heart J. 91:792–797. 1976. View Article : Google Scholar : PubMed/NCBI
30	Kalant H and Kalant OJ: Death in amphetamine users: causes and rates. Can Med Assoc J. 112:299–304. 1975.PubMed/NCBI
31	Li X, Wang H, Qiu P and Luo H: Proteomic profiling of proteins associated with methamphetamine-induced neurotoxicity in different regions of rat brain. Neurochem Int. 52:256–264. 2008. View Article : Google Scholar
32	Butt AJ, Dickson KA, Jambazov S and Baxter RC: Enhancement of tumor necrosis factor-alpha-induced growth inhibition by insulin-like growth factor-binding protein-5 (IGFBP-5), but not IGFBP-3 in human breast cancer cells. Endocrinology. 146:3113–3122. 2005. View Article : Google Scholar
33	Su Y, Wagner ER, Luo Q, et al: Insulin-like growth factor binding protein 5 suppresses tumor growth and metastasis of human osteosarcoma. Oncogene. 30:3907–3917. 2011. View Article : Google Scholar : PubMed/NCBI
34	Tanno B, Vitali R, De Arcangelis D, et al: Bim-dependent apoptosis follows IGFBP-5 down-regulation in neuroblastoma cells. Biochem Biophys Res Commun. 351:547–552. 2006. View Article : Google Scholar : PubMed/NCBI
35	Cobb LJ, Salih DA, Gonzalez I, et al: Partitioning of IGFBP-5 actions in myogenesis: IGF-independent anti-apoptotic function. J Cell Sci. 117:1737–1746. 2004. View Article : Google Scholar : PubMed/NCBI
36	Sokolović A, Sokolović M, Boers W, Elferink RP and Bosma PJ: Insulin-like growth factor binding protein 5 enhances survival of LX2 human hepatic stellate cells. Fibrogenesis Tissue Repair. 3:32010.PubMed/NCBI
37	Fischer F, Schulte H, Mohan S, et al: Associations of insulin-like growth factors, insulin-like growth factor binding proteins and acid-labile subunit with coronary heart disease. Clin Endocrinol (Oxf). 61:595–602. 2004. View Article : Google Scholar : PubMed/NCBI
38	Kim KS, Seu YB, Baek SH, et al: Induction of cellular senescence by insulin-like growth factor binding protein-5 through a p53-dependent mechanism. Mol Biol Cell. 18:4543–4552. 2007. View Article : Google Scholar : PubMed/NCBI
39	Godard MP, Whitman SA, Song YH and Delafontaine P: Skeletal muscle molecular alterations precede whole-muscle dysfunction in NYHA Class II heart failure patients. Clin Interv Aging. 7:489–497. 2012. View Article : Google Scholar : PubMed/NCBI
40	Lee DH, Kim JE and Kang YJ: Insulin like growth factor binding protein-5 regulates excessive vascular smooth muscle cell proliferation in spontaneously hypertensive rats via ERK 1/2 phosphorylation. Korean J Physiol Pharmacol. 17:157–162. 2013. View Article : Google Scholar
41	Enari M, Sakahira H, Yokoyama H, et al: A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 391:43–50. 1998. View Article : Google Scholar : PubMed/NCBI
42	Thornberry NA and Lazebnik Y: Caspases: enemies within. Science. 281:1312–1316. 1998. View Article : Google Scholar : PubMed/NCBI
43	Wolf BB, Schuler M, Echeverri F and Green DR: Caspase-3 is the primary activator of apoptotic DNA fragmentation via DNA fragmentation factor-45/inhibitor of caspase-activated DNase inactivation. J Biol Chem. 274:30651–30656. 1999. View Article : Google Scholar : PubMed/NCBI