The ATP-binding cassette transporter ABCG2 protects against pressure overload-induced cardiac hypertrophy and heart failure by promoting angiogenesis and antioxidant response

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 3, 2012, Pages 654-661

  Higashikuni, Yasutomi ^a   Sainz, Julie ^a   Nakamura, Kazuto ^a   Takaoka, Minoru ^a   Enomoto, Soichiro ^a   Iwata, Hiroshi ^a   Tanaka, Kimie ^a   Sahara, Makoto ^a   Hirata, Yasunobu ^a   Nagai, Ryozo ^a   Sata, Masataka ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

ABC transporter; angiogenesis; heart failure; hypertrophy; oxidative stress

Indexed keywords

ANTIOXIDANT; ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; BREAST CANCER RESISTANCE PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; FIBRONECTIN; GLUTATHIONE; SUPEROXIDE DISMUTASE; TRANSFORMING GROWTH FACTOR BETA1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HEART FAILURE; HEART MUSCLE; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; ATP-BINDING CASSETTE TRANSPORTERS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENOTYPE; GLUTATHIONE; HEART FAILURE; HINDLIMB; HUMANS; HYPERTROPHY, LEFT VENTRICULAR; ISCHEMIA; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; MYOCYTES, CARDIAC; NEOPLASM PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; PHENOTYPE; RATS; RATS, WISTAR; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; VENTRICULAR FUNCTION; VENTRICULAR REMODELING;

EID: 84857511879     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.240341     Document Type: Article

References (35)

1. Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, Hailpern SM, Ho M, Howard V, Kissela B, Kittner S, Lloyd-Jones D, McDermott M, Meigs J, Moy C, Nichol G, O'Donnell C, Roger V, Sorlie P, Steinberger J, Thom T, Wilson M, Hong Y. Heart disease and stroke statistics: 2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2008;117: e25-e146.
2. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600. (Pubitemid 44325350)
3. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest. 2007;117:568-575. (Pubitemid 46348511)
4. Krishnamurthy P, Schuetz JD. Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmacol Toxicol. 2006;46:381-410. (Pubitemid 43271195)
5. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, Ross DD. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA. 1998;95:15665-15670. (Pubitemid 29018757)
6. Tanaka Y, Slitt AL, Leazer TM, Maher JM, Klaassen CD. Tissue distribution and hormonal regulation of the breast cancer resistance protein (Bcrp/Abcg2) in rats and mice. Biochem Biophys Res Commun. 2005; 326:181-187.
7. Szatmari I, Vamosi G, Brazda P, Balint BL, Benko S, Szeles L, Jeney V, Ozvegy-Laczka C, Szanto A, Barta E, Balla J, Sarkadi B, Nagy L. Peroxisome proliferator-activated receptorα-regulated ABCG2 expression confers cytoprotection to human dendritic cells. J Biol Chem. 2006;281:23812-23823. (Pubitemid 44274157)
8. Mogi M, Yang J, Lambert JF, Colvin GA, Shiojima I, Skurk C, Summer R, Fine A, Quesenberry PJ, Walsh K. Akt signaling regulates side population cell phenotype via Bcrp1 translocation. J Biol Chem. 2003;278: 39068-39075. (Pubitemid 37221810)
9. Martin CM, Ferdous A, Gallardo T, Humphries C, Sadek H, Caprioli A, Garcia JA, Szweda LI, Garry MG, Garry DJ. Hypoxia-inducible factor- 2βtransactivates Abcg2 and promotes cytoprotection in cardiac side population cells. Circ Res. 2008;102:1075-1081. (Pubitemid 351667861)
10. Adachi T, Nakagawa H, Chung I, Hagiya Y, Hoshijima K, Noguchi N, Kuo MT, Ishikawa T. Nrf2-dependent and-independent induction of ABC transporters ABCC1, ABCC2, and ABCG2 in HepG2 cells under oxidative stress. J Exp Ther Oncol. 2007;6:335-348. (Pubitemid 350104822)
11. Shen S, Callaghan D, Juzwik C, Xiong H, Huang P, Zhang W. ABCG2 reduces ROS-mediated toxicity and inflammation: a potential role in Alzheimer's disease. J Neurochem. 2010;114:1590-1604.
12. Higashikuni Y, Sainz J, Nakamura K, Takaoka M, Enomoto S, Iwata H, Sahara M, Tanaka K, Koibuchi N, Ito S, Kusuhara H, Sugiyama Y, Hirata Y, Nagai R, Sata M. The ATP-binding cassette transporter BCRP1/ABCG2 plays a pivotal role in cardiac repair after myocardial infarction via modulation of microvascular endothelial cell survival and function. Arterioscler Thromb Vasc Biol. 2010;30:2128-2135.
13. Jonker JW, Buitelaar M, Wagenaar E, Van Der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, Rosing H, Beijnen JH, Schinkel AH. The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA. 2002;99:15649-15654. (Pubitemid 35403986)
14. Rockman HA, Ross RS, Harris AN, Knowlton KU, Steinhelper ME, Field LJ, Ross J Jr, Chien KR. Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc Natl Acad Sci USA. 1991;88: 8277-8281. (Pubitemid 21915339)
15. Takeda N, Manabe I, Uchino Y, Eguchi K, Matsumoto S, Nishimura S, Shindo T, Sano M, Otsu K, Snider P, Conway SJ, Nagai R. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest. 2010;120:254-265.
16. Tirziu D, Chorianopoulos E, Moodie KL, Palac RT, Zhuang ZW, Tjwa M, Roncal C, Eriksson U, Fu Q, Elfenbein A, Hall AE, Carmeliet P, Moons L, Simons M. Myocardial hypertrophy in the absence of external stimuli is induced by angiogenesis in mice. J Clin Invest. 2007;117: 3188-3197. (Pubitemid 350096977)
17. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005; 115:2108-2118. (Pubitemid 41134152)
18. Sano M, Minamino T, Toko H, Miyauchi H, Orimo M, Qin Y, Akazawa H, Tateno K, Kayama Y, Harada M, Shimizu I, Asahara T, Hamada H, Tomita S, Molkentin JD, Zou Y, Komuro I. p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload. Nature. 2007; 446:444-448. (Pubitemid 46474597)
19. Teodoro JG, Parker AE, Zhu X, Green MR. p53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science. 2006;313:968-971. (Pubitemid 44267388)
20. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;115:500-508. (Pubitemid 40322219)
21. Sawyer DB, Siwik DA, Xiao L, Pimentel DR, Singh K, Colucci WS. Role of oxidative stress in myocardial hypertrophy and failure. J Mol Cell Cardiol. 2002;34:379-388. (Pubitemid 37163454)
22. Sano M, Fukuda K, Kodama H, Pan J, Saito M, Matsuzaki J, Takahashi T, Makino S, Kato T, Ogawa S. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem. 2000;275:29717-29723. (Pubitemid 32043853)
23. Brechbuhl HM, Gould N, Kachadourian R, Riekhof WR, Voelker DR, Day BJ. Glutathione transport is a unique function of the ATP-binding cassette protein ABCG2. J Biol Chem. 2010;285:16582-16587.
24. Kachadourian R, Day BJ. Flavonoid-induced glutathione depletion: potential implications for cancer treatment. Free Radic Biol Med. 2006; 41:65-76. (Pubitemid 43866451)
25. Marcus ML, Koyanagi S, Harrison DG, Doty DB, Hiratzka LF, Eastham CL. Abnormalities in the coronary circulation that occur as a consequence of cardiac hypertrophy. Am J Med. 1983;75:62-66. (Pubitemid 13009936)
26. Tomanek RJ. Response of the coronary vasculature to myocardial hypertrophy. J Am Coll Cardiol. 1990;15:528-533. (Pubitemid 20061475)
27. Liu F, Verin AD, Wang P, Day R, Wersto RP, Chrest FJ, English DK, Garcia JG. Differential regulation of sphingosine-1-phosphate-and VEGF-induced endothelial cell chemotaxis. Involvement of G(iα2)-linked Rho kinase activity. Am J Respir Cell Mol Biol. 2001;24:711-719. (Pubitemid 32550593)
28. Lee MJ, Van Brocklyn JR, Thangada S, Liu CH, Hand AR, Menzeleev R, Spiegel S, Hla T. Sphingosine-1-phosphate as a ligand for the G proteincoupled receptor EDG-1. Science. 1998;279:1552-1555. (Pubitemid 28217081)
29. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, Spiegel S. Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem. 2010;285:10477-10486.
30. Mao Q, Deeley RG, Cole SP. Functional reconstitution of substrate transport by purified multidrug resistance protein MRP1 (ABCC1) in phospholipid vesicles. J Biol Chem. 2000;275:34166-34172.
31. Rius M, Nies AT, Hummel-Eisenbeiss J, Jedlitschky G, Keppler D. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology. 2003;38: 374-384. (Pubitemid 36919858)
32. Kogan I, Ramjeesingh M, Li C, Kidd JF, Wang Y, Leslie EM, Cole SP, Bear CE. CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J. 2003;22:1981-1989. (Pubitemid 36565524)
33. Peterson JD, Herzenberg LA, Vasquez K, Waltenbaugh C. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc Natl Acad Sci USA. 1998;95:3071-3076. (Pubitemid 28135856)
34. Kondo C, Suzuki H, Itoda M, Ozawa S, Sawada J, Kobayashi D, Ieiri I, Mine K, Ohtsubo K, Sugiyama Y. Functional analysis of SNPs variants of BCRP/ABCG2. Pharm Res. 2004;21:1895-1903. (Pubitemid 39390103)
35. Morisaki K, Robey RW, Ozvegy-Laczka C, Honjo Y, Polgar O, Steadman K, Sarkadi B, Bates SE. Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother Pharmacol. 2005;56:161-172. (Pubitemid 40884271)