Potential role of the apelin-APJ pathway in sex-related differential cardiotoxicity induced by doxorubicin in mice.


Journal

Journal of applied toxicology : JAT
ISSN: 1099-1263
Titre abrégé: J Appl Toxicol
Pays: England
ID NLM: 8109495

Informations de publication

Date de publication:
04 2023
Historique:
revised: 29 08 2022
received: 15 07 2022
accepted: 10 10 2022
pubmed: 14 10 2022
medline: 22 3 2023
entrez: 13 10 2022
Statut: ppublish

Résumé

Preclinical and clinical findings suggest sexual dimorphism in cardiotoxicity induced by a chemotherapeutic drug, doxorubicin (DOX). However, molecular alterations leading to sex-related differential vulnerability of heart to DOX toxicity are not fully explored. In the present study, RNA sequencing in hearts of B6C3F

Identifiants

pubmed: 36227756
doi: 10.1002/jat.4405
doi:

Substances chimiques

Apelin 0
Doxorubicin 80168379AG
Transforming Growth Factor beta2 0
Aplnr protein, mouse 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

557-576

Informations de copyright

Published 2022. This article is a U.S. Government work and is in the public domain in the USA.

Références

Accornero, F., van Berlo, J. H., Correll, R. N., Elrod, J. W., Sargent, M. A., York, A., Rabinowitz, J. E., Leask, A., & Molkentin, J. D. (2015). Genetic analysis of connective tissue growth factor as an effector of transforming growth factor β signaling and cardiac remodeling. Molecular and Cellular Biology, 35(12), 2154-2164. https://doi.org/10.1128/mcb.00199-15
Arai, M., Tomaru, K., Takizawa, T., Sekiguchi, K., Yokoyama, T., Suzuki, T., & Nagai, R. (1998). Sarcoplasmic reticulum genes are selectively down-regulated in cardiomyopathy produced by doxorubicin in rabbits. Journal of Molecular and Cellular Cardiology, 30(2), 243-254. https://doi.org/10.1006/jmcc.1997.0588
Aryal, B., & Rao, V. A. (2018). Specific protein carbonylation in human breast cancer tissue compared to adjacent healthy epithelial tissue. PLoS ONE, 13(3), e0194164. https://doi.org/10.1371/journal.pone.0194164
Atluri, P., Morine, K. J., Liao, G. P., Panlilio, C. M., Berry, M. F., Hsu, V. M., Hiesinger, W., Cohen, J., & Joseph Woo, Y. (2007). Ischemic heart failure enhances endogenous myocardial apelin and APJ receptor expression. Cellular & Molecular Bilogy Letters, 12(1), 127-138. https://doi.org/10.2478/s11658-006-0058-7
Audebrand, A., Désaubry, L., & Nebigil, C. G. (2019). Targeting GPCRs against cardiotoxicity induced by anticancer treatments. Frontiers in Cardiovascular Medicine, 6, 194. https://doi.org/10.3389/fcvm.2019.00194
Bansal, N., Amdani, S. M., Hutchins, K. K., & Lipshultz, S. E. (2018). Cardiovascular disease in survivors of childhood cancer. Current Opinion in Pediatrics, 30(5), 628-638. https://doi.org/10.1097/MOP.0000000000000675
Barry, E., Alvarez, J. A., Scully, R. E., Miller, T. L., & Lipshultz, S. E. (2007). Anthracycline-induced cardiotoxicity: Course, pathophysiology, prevention and management. Expert Opinion on Pharmacotherapy, 8(8), 1039-1058. https://doi.org/10.1517/14656566.8.8.1039
Berry, M. F., Pirolli, T. J., Jayasankar, V., Burdick, J., Morine, K. J., Gardner, T. J., & Woo, Y. J. (2004). Apelin has in vivo inotropic effects on normal and failing hearts. Circulation, 110(11 Suppl 1), 187-193. https://doi.org/10.1161/01.CIR.0000138382.57325.5c
Bers, D. M. (2008). Calcium cycling and signaling in cardiac myocytes. Annual Review of Physiology, 70, 23-49. https://doi.org/10.1146/annurev.physiol.70.113006.100455
Brown, R. D., Ambler, S. K., Mitchell, M. D., & Long, C. S. (2005). The cardiac fibroblast: Therapeutic target in myocardial remodeling and failure. Annual Review of Pharmacology and Toxicology, 45, 657-687. https://doi.org/10.1146/annurev.pharmtox.45.120403.095802
Bujak, M., & Frangogiannis, N. G. (2007). The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovascular Research, 74(2), 184-195. https://doi.org/10.1016/j.cardiores.2006.10.002
Cadeddu Dessalvi, C., Pepe, A., Penna, C., Gimelli, A., Madonna, R., Mele, D., Monte, I., Novo, G., Nugara, C., Zito, C., Moslehi, J. J., de Boer, R. A., Lyon, A. R., Tocchetti, C. G., & Mercuro, G. (2019). Sex differences in anthracycline-induced cardiotoxicity: The benefits of estrogens. Heart Failure Reviews, 24(6), 915-925. https://doi.org/10.1007/s10741-019-09820-2
Chapman, N. A., Dupré, D. J., & Rainey, J. K. (2014). The apelin receptor: Physiology, pathology, cell signalling, and ligand modulation of a peptide-activated class a GPCR. Biochemistry and Cell Biology, 92(6), 431-440. https://doi.org/10.1139/bcb-2014-0072
Charo, D. N., Ho, M., Fajardo, G., Kawana, M., Kundu, R. K., Sheikh, A. Y., Finsterbach, T. P., Leeper, N. J., Ernst, K. V., Chen, M. M., Ho, Y. D., Chun, H. J., Bernstein, D., Ashley, E. A., & Quertermous, T. (2009). Endogenous regulation of cardiovascular function by apelin-APJ. American Journal of Physiology. Heart and Circulatory Physiology, 297(5), H1904-H1913. https://doi.org/10.1152/ajpheart.00686.2009
Chen, Z., Wu, D., Li, L., & Chen, L. (2016). Apelin/APJ system: A novel therapeutic target for myocardial ischemia/reperfusion injury. DNA and Cell Biology, 35(12), 766-775. https://doi.org/10.1089/dna.2016.3391
Chong, K. S., Gardner, R. S., Morton, J. J., Ashley, E. A., & McDonagh, T. A. (2006). Plasma concentrations of the novel peptide apelin are decreased in patients with chronic heart failure. European Journal of Heart Failure, 8(4), 355-360. https://doi.org/10.1016/j.ejheart.2005.10.007
Dang, M. Q., Zhao, X. C., Lai, S., Wang, X., Wang, L., Zhang, Y. L., Liu, Y., Yu, X. H., Liu, Y., Li, H. H., & Xia, Y. L. (2015). Gene expression profile in the early stage of angiotensin II-induced cardiac remodeling: A time series microarray study in a mouse model. Cellular Physiology and Biochemistry, 35(2), 467-476. https://doi.org/10.1159/000369712
de Bellis, A., de Angelis, G., Fabris, E., Cannatà, A., Merlo, M., & Sinagra, G. (2020). Gender-related differences in heart failure: Beyond the “one-size-fits-all” paradigm. Heart Failure Reviews, 25(2), 245-255. https://doi.org/10.1007/s10741-019-09824-y
Desai, V. G., Vijay, V., Han, T., Moland, C. L., Phanavanh, B., Lee, T., Davis, K. J., Muskhelishvili, L., Stine, K. C., & Fuscoe, J. C. (2022). Doxorubicin-induced delayed-onset subclinical cardiotoxicity in mice. Journal of Applied Toxicology, 42(5), 778-792. https://doi.org/10.1002/jat.4256
Dodd, D. A., Atkinson, J. B., Olson, R. D., Buck, S., Cusack, B. J., Fleischer, S., & Boucek, R. J. Jr. (1993). Doxorubicin cardiomyopathy is associated with a decrease in calcium release channel of the sarcoplasmic reticulum in a chronic rabbit model. Journal of Clinical Investigation, 91(4), 1697-1705. https://doi.org/10.1172/jci116379
Flevaris, P., Khan, S. S., Eren, M., Schuldt, A. J. T., Shah, S. J., Lee, D. C., Gupta, S., Shapiro, A. D., Burridge, P. W., Ghosh, A. K., & Vaughan, D. E. (2017). Plasminogen activator inhibitor type I controls cardiomyocyte transforming growth factor-β and cardiac fibrosis. Circulation, 136(7), 664-679. https://doi.org/10.1161/circulationaha.117.028145
Földes, G., Horkay, F., Szokodi, I., Vuolteenaho, O., Ilves, M., Lindstedt, K. A., Mäyränpää, M., Sármán, B., Seres, L., Skoumal, R., Lakó-Futó, Z., deChâtel, R., Ruskoaho, H., & Tóth, M. (2003). Circulating and cardiac levels of apelin, the novel ligand of the orphan receptor APJ, in patients with heart failure. Biochemical and Biophysical Research Communications, 308(3), 480-485. https://doi.org/10.1016/s0006-291x(03)01424-4
Gellings Lowe, N., Swaney, J. S., Moreno, K. M., & Sabbadini, R. A. (2009). Sphingosine-1-phosphate and sphingosine kinase are critical for transforming growth factor-beta-stimulated collagen production by cardiac fibroblasts. Cardiovascular Research, 82(2), 303-312. https://doi.org/10.1093/cvr/cvp056
Gonzalez, Y., Pokrzywinski, K. L., Rosen, E. T., Mog, S., Aryal, B., Chehab, L. M., Vijay, V., Moland, C. L., Desai, V. G., Dickey, J. S., & Rao, V. A. (2015). Reproductive hormone levels and differential mitochondria-related oxidative gene expression as potential mechanisms for gender differences in cardiosensitivity to doxorubicin in tumor-bearing spontaneously hypertensive rats. Cancer Chemotherapy and Pharmacology, 76(3), 447-459. https://doi.org/10.1007/s00280-015-2786-8
Hamada, J., Baasanjav, A., Ono, N., Murata, K., Kako, K., Ishida, J., & Fukamizu, A. (2015). Possible involvement of downregulation of the apelin-APJ system in doxorubicin-induced cardiotoxicity. American Journal of Physiology. Heart and Circulatory Physiology, 308(8), H931-H941. https://doi.org/10.1152/ajpheart.00703.2013
Hequet, O., Le, Q. H., Moullet, I., Pauli, E., Salles, G., Espinouse, D., Dumontet, C., Thieblemont, C., Arnaud, P., Antal, D., Bouafia, F., & Coiffier, B. (2004). Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. Journal of Clinical Oncology, 22(10), 1864-1871. https://doi.org/10.1200/jco.2004.06.033
Herman, E. H., & Ferrans, V. J. (1991). Overview of morphologic changes induced by the toxic effects of drugs on the cardiovascular system. In S. I. Baskin (Ed.), Principles of cardiac toxicology (1st ed.) (p. 615). CRC Press, Inc.
Hosoya, M., Kawamata, Y., Fukusumi, S., Fujii, R., Habata, Y., Hinuma, S., Kitada, C., Honda, S., Kurokawa, T., Onda, H., Nishimura, O., & Fujino, M. (2000). Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. Journal of Biological Chemistry, 275(28) 21061-21067. https://doi.org/10.1074/jbc.M908417199
Hsieh, D. J., Kuo, W. W., Lai, Y. P., Shibu, M. A., Shen, C. Y., Pai, P., Yeh, Y. L., Lin, J. Y., Viswanadha, V. P., & Huang, C. Y. (2015). 17β-estradiol and/or estrogen receptor β attenuate the Autophagic and apoptotic effects induced by prolonged hypoxia through HIF-1α-mediated BNIP3 and IGFBP-3 signaling blockage. Cellular Physiology and Biochemistry, 36(1), 274-284. https://doi.org/10.1159/000374070
Jang, Y. M., Kendaiah, S., Drew, B., Phillips, T., Selman, C., Julian, D., & Leeuwenburgh, C. (2004). Doxorubicin treatment in vivo activates caspase-12 mediated cardiac apoptosis in both male and female rats. FEBS Letters, 577(3), 483-490. https://doi.org/10.1016/j.febslet.2004.10.053
Jenkins, G. R., Lee, T., Moland, C. L., Vijay, V., Herman, E. H., Lewis, S. M., Davis, K. J., Muskhelishvili, L., Kerr, S., Fuscoe, J. C., & Desai, V. G. (2016). Sex-related differential susceptibility to doxorubicin-induced cardiotoxicity in B6C3F(1) mice. Toxicology and Applied Pharmacology, 310, 159-174. https://doi.org/10.1016/j.taap.2016.09.012
Jia, Y. X., Pan, C. S., Zhang, J., Geng, B., Zhao, J., Gerns, H., Yang, J., Chang, J. K., Tang, C. S., & Qi, Y. F. (2006). Apelin protects myocardial injury induced by isoproterenol in rats. Regulatory Peptides, 133(1-3), 147-154. https://doi.org/10.1016/j.regpep.2005.09.033
Khalifa, A. R., Abdel-Rahman, E. A., Mahmoud, A. M., Ali, M. H., Noureldin, M., Saber, S. H., Mohsen, M., & Ali, S. S. (2017). Sex-specific differences in mitochondria biogenesis, morphology, respiratory function, and ROS homeostasis in young mouse heart and brain. Physiological Reports, 5(6), e13125. https://doi.org/10.14814/phy2.13125
Krischer, J. P., Epstein, S., Cuthbertson, D. D., Goorin, A. M., Epstein, M. L., & Lipshultz, S. E. (1997). Clinical cardiotoxicity following anthracycline treatment for childhood cancer: The pediatric oncology group experience. Journal of Clinical Oncology, 15(4), 1544-1552. https://doi.org/10.1200/jco.1997.15.4.1544
Kumari, H., Huang, W. H., & Chan, M. W. Y. (2020). Review on the role of epigenetic modifications in doxorubicin-induced cardiotoxicity. Front Cardiovasc Med, 7, 56. https://doi.org/10.3389/fcvm.2020.00056
Lipshultz, S. E., Lipsitz, S. R., Mone, S. M., Goorin, A. M., Sallan, S. E., Sanders, S. P., Orav, E. J., Gelber, R. D., & Colan, S. D. (1995). Female sex and higher drug dose as risk factors for late cardiotoxic effects of doxorubicin therapy for childhood cancer. New England Journal of Medicine, 332(26), 1738-1744. https://doi.org/10.1056/nejm199506293322602
Lipson, K. E., Wong, C., Teng, Y., & Spong, S. (2012). CTGF is a central mediator of tissue remodeling and fibrosis and its inhibition can reverse the process of fibrosis. Fibrogenesis & Tissue Repair, 5(Suppl 1), S24. https://doi.org/10.1186/1755-1536-5-s1-s24
Liu, W., Yan, J., Pan, W., & Tang, M. (2020). Apelin/Elabela-APJ: A novel therapeutic target in the cardiovascular system. Annals of Translational Medicine, 8(5), 243. https://doi.org/10.21037/atm.2020.02.07
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C[T]) method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262
Long, C. S., & Brown, R. D. (2002). The cardiac fibroblast, another therapeutic target for mending the broken heart? Journal of Molecular and Cellular Cardiology, 34(10), 1273-1278. https://doi.org/10.1006/jmcc.2002.2090
Longhi, A., Ferrari, S., Bacci, G., & Specchia, S. (2007). Long-term follow-up of patients with doxorubicin-induced cardiac toxicity after chemotherapy for osteosarcoma. Anti-Cancer Drugs, 18(6), 737-744. https://doi.org/10.1097/CAD.0b013e32803d36fe
Meyer, S., van der Meer, P., van Tintelen, J. P., & van den Berg, M. P. (2014). Sex differences in cardiomyopathies. European Journal of Heart Failure, 16(3), 238-247. https://doi.org/10.1002/ejhf.15
Mori, T., Kawara, S., Shinozaki, M., Hayashi, N., Kakinuma, T., Igarashi, A., Takigawa, M., Nakanishi, T., & Takehara, K. (1999). Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: A mouse fibrosis model. Journal of Cellular Physiology, 181(1), 153-159. doi:10.1002/(sici)1097-4652(199910)181:1<153::Aid-jcp16>3.0.Co;2-k
Moulin, M., Piquereau, J., Mateo, P., Fortin, D., Rucker-Martin, C., Gressette, M., Lefebvre, F., Gresikova, M., Solgadi, A., Veksler, V., Garnier, A., & Ventura-Clapier, R. (2015). Sexual dimorphism of doxorubicin-mediated cardiotoxicity: Potential role of energy metabolism remodeling. Circulation: Heart Failure, 8(1), 98-108. https://doi.org/10.1161/circheartfailure.114.001180
Mulrooney, D. A., Yeazel, M. W., Kawashima, T., Mertens, A. C., Mitby, P., Stovall, M., Donaldson, S. S., Green, D. M., Sklar, C. A., Robison, L. L., & Leisenring, W. M. (2009). Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: Retrospective analysis of the Childhood Cancer Survivor Study cohort. The British Medical Journal, 339, b4606. https://doi.org/10.1136/bmj.b4606
Norton, N., Bruno, K. A., di Florio, D. N., Whelan, E. R., Hill, A. R., Morales-Lara, A. C., Mease, A. A., Sousou, J. M., Malavet, J. A., Dorn, L. E., Salomon, G. R., Macomb, L. P., Khatib, S., Anastasiadis, Z. P., Necela, B. M., McGuire, M. M., Giresi, P. G., Kotha, A., Beetler, D. J., … Fairweather, D. L. (2021). Trpc6 promotes doxorubicin-induced cardiomyopathy in male mice with pleiotropic differences between males and females. Frontiers in Cardiovascular Medicine, 8, 757784. https://doi.org/10.3389/fcvm.2021.757784
Numaga-Tomita, T., & Nishida, M. (2020). TRPC channels in cardiac plasticity. Cell, 9(2), 454. https://doi.org/10.3390/cells9020454
Octavia, Y., Tocchetti, C. G., Gabrielson, K. L., Janssens, S., Crijns, H. J., & Moens, A. L. (2012). Doxorubicin-induced cardiomyopathy: From molecular mechanisms to therapeutic strategies. Journal of Molecular and Cellular Cardiology, 52(6), 1213-1225. https://doi.org/10.1016/j.yjmcc.2012.03.006
Ouyang, Q., You, T., Guo, J., Xu, R., Guo, Q., Lin, J., & Zhao, H. (2019). Effects of Apelin on left ventricular-arterial coupling and mechanical efficiency in rats with ischemic heart failure. Disease Markers, 2019, 4823156. https://doi.org/10.1155/2019/4823156
Pchejetski, D., Foussal, C., Alfarano, C., Lairez, O., Calise, D., Guilbeau-Frugier, C., Schaak, S., Seguelas, M. H., Wanecq, E., Valet, P., Parini, A., & Kunduzova, O. (2012). Apelin prevents cardiac fibroblast activation and collagen production through inhibition of sphingosine kinase 1. European Heart Journal, 33(18), 2360-2369. https://doi.org/10.1093/eurheartj/ehr389
Pedram, A., Razandi, M., O'Mahony, F., Lubahn, D., & Levin, E. R. (2010). Estrogen receptor-beta prevents cardiac fibrosis. Molecular Endocrinology, 24(11), 2152-2165. https://doi.org/10.1210/me.2010-0154
Pisarenko, O. I., Serebryakova, L. I., Studneva, I. M., Pelogeykina, Y. A., Tskitishvili, O. V., Bespalova, Z. D., Sidorova, M. V., Az′muko, A. A., Khatri, D. N., Pal′keeva, M. E., & Molokoedov, A. S. (2013). Effects of structural analogues of apelin-12 in acute myocardial infarction in rats. The Journal of Pharmacy and Pharmacology, 4(3), 198-203. https://doi.org/10.4103/0976-500x.114600
Pisarenko, O. I., Shulzhenko, V. S., Pelogeykina, Y. A., & Studneva, I. M. (2015). Enhancement of crystalloid cardioplegic protection by structural analogs of apelin-12. Journal of Surgical Research, 194(1), 18-24. https://doi.org/10.1016/j.jss.2014.11.007
Porter, K. E., & Turner, N. A. (2009). Cardiac fibroblasts: At the heart of myocardial remodeling. Pharmacology and Therapeutics, 123(2), 255-278. https://doi.org/10.1016/j.pharmthera.2009.05.002
Rattanasopa, C., Kirk, J. A., Bupha-Intr, T., Papadaki, M., de Tombe, P. P., & Wattanapermpool, J. (2019). Estrogen but not testosterone preserves myofilament function from doxorubicin-induced cardiotoxicity by reducing oxidative modifications. American Journal of Physiology. Heart and Circulatory Physiology, 316(2), H360-h370. https://doi.org/10.1152/ajpheart.00428.2018
Ribeiro, R. F. Jr., Ronconi, K. S., Morra, E. A., do Val Lima, P. R., Porto, M. L., Vassallo, D. V., Figueiredo, S. G., & Stefanon, I. (2016). Sex differences in the regulation of spatially distinct cardiac mitochondrial subpopulations. Molecular and Cellular Biochemistry, 419(1-2), 41-51. https://doi.org/10.1007/s11010-016-2748-4
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010). edge: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. https://doi.org/10.1093/bioinformatics/btp616
Rodvold, K. A., Rushing, D. A., & Tewksbury, D. A. (1988). Doxorubicin clearance in the obese. Journal of Clinical Oncology, 6(8), 1321-1327. https://doi.org/10.1200/jco.1988.6.8.1321
Sato, T., Kadowaki, A., Suzuki, T., Ito, H., Watanabe, H., Imai, Y., & Kuba, K. (2019). Loss of apelin augments angiotensin II-induced cardiac dysfunction and pathological remodeling. International Journal of Molecular Sciences, 20(2), 239. https://doi.org/10.3390/ijms20020239
Schiller, M., Javelaud, D., & Mauviel, A. (2004). TGF-beta-induced SMAD signaling and gene regulation: Consequences for extracellular matrix remodeling and wound healing. Journal of Dermatological Science, 35(2), 83-92. https://doi.org/10.1016/j.jdermsci.2003.12.006
Sellers, R. S., Mortan, D., Michael, B., Roome, N., Johnson, J. K., Yano, B. L., Perry, R., & Schafer, K. (2007). Society of Toxicologic Pathology position paper: Organ weight recommendations for toxicology studies. Toxicologic Pathology, 35(5), 751-755. https://doi.org/10.1080/01926230701595300
Shan, K., Lincoff, A. M., & Young, J. B. (1996). Anthracycline-induced cardiotoxicity. Annals of Internal Medicine, 125(1), 47-58. https://doi.org/10.7326/0003-4819-125-1-199607010-00008
Sharma, S., Ghufran, S. M., Ghose, S., & Biswas, S. (2021). Cytoplasmic vacuolation with endoplasmic reticulum stress directs sorafenib induced non-apoptotic cell death in hepatic stellate cells. Scientific Reports, 11(1), 3089. https://doi.org/10.1038/s41598-021-82381-3
Shen, Y., Zhang, H., Ni, Y., Wang, X., Chen, Y., Chen, J., Wang, Y., Lin, J., Xu, Y., Zhao, J. Y., & Cheng, L. (2022). Tripartite motif 25 ameliorates doxorubicin-induced cardiotoxicity by degrading p85α. Cell Death & Disease, 13(7), 643. https://doi.org/10.1038/s41419-022-05100-4
Swain, S. M., Whaley, F. S., & Ewer, M. S. (2003). Congestive heart failure in patients treated with doxorubicin: A retrospective analysis of three trials. Cancer, 97(11), 2869-2879. https://doi.org/10.1002/cncr.11407
Szokodi, I., Tavi, P., Földes, G., Voutilainen-Myllylä, S., Ilves, M., Tokola, H., Pikkarainen, S., Piuhola, J., Rysä, J., Tóth, M., & Ruskoaho, H. (2002). Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circulation Research, 91(5), 434-440. https://doi.org/10.1161/01.res.0000033522.37861.69
Takeshita, K., Hayashi, M., Iino, S., Kondo, T., Inden, Y., Iwase, M., Kojima, T., Hirai, M., Ito, M., Loskutoff, D. J., Saito, H., Murohara, T., & Yamamoto, K. (2004). Increased expression of plasminogen activator inhibitor-1 in cardiomyocytes contributes to cardiac fibrosis after myocardial infarction. The American Journal of Pathology, 164(2), 449-456. https://doi.org/10.1016/s0002-9440(10)63135-5
Tatemoto, K., Hosoya, M., Habata, Y., Fujii, R., Kakegawa, T., Zou, M. X., Kawamata, Y., Fukusumi, S., Hinuma, S., Kitada, C., Kurokawa, T., Onda, H., & Fujino, M. (1998). Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochemical and Biophysical Research Communications, 251(2), 471-476. https://doi.org/10.1006/bbrc.1998.9489
Travers, J. G., Kamal, F. A., Robbins, J., Yutzey, K. E., & Blaxall, B. C. (2016). Cardiac fibrosis: The fibroblast awakens. Circulation Research, 118(6), 1021-1040. https://doi.org/10.1161/circresaha.115.306565
Uehara, H., & Rao, V. A. (2015). Metal-mediated protein oxidation: Applications of a modified ELISA-based carbonyl detection assay for complex proteins. Pharmaceutical Research, 32(2), 691-701. https://doi.org/10.1007/s11095-014-1496-y
Vijay, V., Moland, C. L., Han, T., Fuscoe, J. C., Lee, T., Herman, E. H., Jenkins, G. R., Lewis, S. M., Cummings, C. A., Gao, Y., Cao, Z., Yu, L. R., & Desai, V. G. (2016). Early transcriptional changes in cardiac mitochondria during chronic doxorubicin exposure and mitigation by dexrazoxane in mice. Toxicology and Applied Pharmacology, 295, 68-84. https://doi.org/10.1016/j.taap.2016.02.003
von Hoff, D. D., Layard, M. W., Basa, P., Davis, H. L. Jr., von Hoff, A. L., Rozencweig, M., & Muggia, F. M. (1979). Risk factors for doxorubicin-induced congestive heart failure. Annals of Internal Medicine, 91(5), 710-717. https://doi.org/10.7326/0003-4819-91-5-710
Wang, C., Liu, N., Luan, R., Li, Y., Wang, D., Zou, W., Xing, Y., Tao, L., Cao, F., & Wang, H. (2013). Apelin protects sarcoplasmic reticulum function and cardiac performance in ischaemia-reperfusion by attenuating oxidation of sarcoplasmic reticulum Ca2+-ATPase and ryanodine receptor. Cardiovascular Research, 100(1), 114-124. https://doi.org/10.1093/cvr/cvt160
Wang, W., McKinnie, S. M., Patel, V. B., Haddad, G., Wang, Z., Zhabyeyev, P., Das, S. K., Basu, R., McLean, B., Kandalam, V., Penninger, J. M., Kassiri, Z., Vederas, J. C., Murray, A. G., & Oudit, G. Y. (2013). Loss of Apelin exacerbates myocardial infarction adverse remodeling and ischemia-reperfusion injury: Therapeutic potential of synthetic apelin analogues. Journal of the American Heart Association, 2(4), e000249. https://doi.org/10.1161/jaha.113.000249
Wilson, A. G. (2001). Short term, subchronic and chronic toxicology studies. In W. Hayes (Ed.), Principles and methods of toxicology (4th ed., pp. 917-958). Taylor and Francis.
Xue, T., Qiu, X., Liu, H., Gan, C., Tan, Z., Xie, Y., Wang, Y., & Ye, T. (2021). Epigenetic regulation in fibrosis progress. Pharmacological Research, 173, 105910. https://doi.org/10.1016/j.phrs.2021.105910
Zeng, X. J., Zhang, L. K., Wang, H. X., Lu, L. Q., Ma, L. Q., & Tang, C. S. (2009). Apelin protects heart against ischemia/reperfusion injury in rat. Peptides, 30(6), 1144-1152. https://doi.org/10.1016/j.peptides.2009.02.010
Zhang, J., Knapton, A., Lipshultz, S. E., Cochran, T. R., Hiraragi, H., & Herman, E. H. (2014). Sex-related differences in mast cell activity and doxorubicin toxicity: A study in spontaneously hypertensive rats. Toxicologic Pathology, 42(2), 361-375. https://doi.org/10.1177/0192623313482778
Zhang, P., Yi, L. H., Meng, G. Y., Zhang, H. Y., Sun, H. H., & Cui, L. Q. (2017). Apelin-13 attenuates cisplatin-induced cardiotoxicity through inhibition of ROS-mediated DNA damage and regulation of MAPKs and AKT pathways. Free Radical Research, 51(5), 449-459. https://doi.org/10.1080/10715762.2017.1313414
Zhang, X., Hu, W., Feng, F., Xu, J., & Wu, F. (2016). Apelin-13 protects against myocardial infarction-induced myocardial fibrosis. Molecular Medicine Reports, 13(6), 5262-5268. https://doi.org/10.3892/mmr.2016.5163
Zhong, S., Guo, H., Wang, H., Xing, D., Lu, T., Yang, J., & Wang, C. (2020). Apelin-13 alleviated cardiac fibrosis via inhibiting the PI3K/Akt pathway to attenuate oxidative stress in rats with myocardial infarction-induced heart failure. Bioscience Reports, 40(4). https://doi.org/10.1042/bsr20200040

Auteurs

Varsha G Desai (VG)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Ana Azevedo-Pouly (A)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Vikrant Vijay (V)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Bounleut Phanavanh (B)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Carrie L Moland (CL)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Tao Han (T)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Javier Revollo (J)

Division of Genetic and Molecular Toxicology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

Baikuntha Aryal (B)

Office of Biotechnology Products, Center for Drug Evaluation and Research, U.S. Food and Drug Administration, Silver Spring, Maryland, USA.

V Ashutosh Rao (VA)

Office of Biotechnology Products, Center for Drug Evaluation and Research, U.S. Food and Drug Administration, Silver Spring, Maryland, USA.

James C Fuscoe (JC)

Division of Systems Biology, National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, Arkansas, USA.

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