Top

Published in:

Open Access 18-12-2023 | Research

On the Mechanisms of the Cardiotoxic Effect of Lead Oxide Nanoparticles

Authors: Ilzira A. Minigaliyeva, Svetlana V. Klinova, Marina P. Sutunkova, Yuliya V. Ryabova, Irene E. Valamina, Ivan G. Shelomentsev, Tatiana N. Shtin, Tatiana V. Bushueva, Yuri L. Protsenko, Alexander A. Balakin, Ruslan V. Lisin, Daniil A. Kuznetsov, Boris A. Katsnelson, Liubov V. Toropova

Published in: Cardiovascular Toxicology | Issue 1/2024

Abstract

Lead compounds are one of the most common pollutants of the workplace air and the environment. In the occupational setting, the sources of their emission, including in nanoscale form, are various technological processes associated with lead smelting and handling of non-ferrous metals and their alloys, the production of copper and batteries. Both lead poisoning and lead exposure without obvious signs of poisoning have a detrimental effect on the cardiovascular system. The purpose of this research was to investigate the mechanisms of the cardiotoxic effect of lead oxide nanoparticles (PbO NPs). The toxicological experiment involved male albino rats subchronically exposed to PbO NPs (49.6 ± 16.0 nm in size) instilled intraperitoneally in a suspension. We then assessed post-exposure hematological and biochemical parameters of blood and urine, histological and ultrastructural changes in cardiomyocytes, and non-invasively recorded electrocardiograms and blood pressure parameters in the rodents. Myocardial contractility was studied on isolated preparations of cardiac muscles. We established that PbO NPs induced oxidative stress and damage to the ultrastructure of cardiomyocytes, and decreased efficiency of the contractile function of the myocardium and blood pressure parameters. We also revealed such specific changes in the organism of the exposed rats as anemia, hypoxia, and hypocalcemia.

Graphical Abstract

Miller, A., Drake, P. L., Hintz, P., & Habjan, M. (2010). Characterizing exposures to airborne metals and nanoparticle emissions in a refinery. The Annals of occupational hygiene, 54(5), 504–513. https://doi.org/10.1093/annhyg/meq032CrossRefPubMed

Katsnelson, B. A., Privalova, L. I., Kuzmin, S. V., Degtyareva, T. D., Sutunkova, M. P., Yeremenko, O. S., Minigalieva, I. A., Kireyeva, E. P., Khodos, M. Y., Kozitsina, A. N., Malakhova, N. A., Glazyrina, J. A., Shur, V. Y., Shishkin, E. I., & Nikolaeva, E. V. (2010). Some peculiarities of pulmonary clearance mechanisms in rats after intratracheal instillation of magnetite (Fe₃O₄) suspensions with different particle sizes in the nanometer and micrometer ranges: Are we defenseless against nanoparticles? International Journal of Occupational and Environmental Health, 16(4), 508–524. https://doi.org/10.1179/107735210799160011CrossRefPubMed

Katsnelson, B. A., Privalova, L. I., Gurvich, V. B., Makeyev, O. H., Shur, V. Y., Beikin, Y. B., Sutunkova, M. P., Kireyeva, E. P., Minigalieva, I. A., Loginova, N. V., Vasilyeva, M. S., Korotkov, A. V., Shuman, E. A., Vlasova, L. A., Shishkina, E. V., Tyurnina, A. E., Kozin, R. V., Valamina, I. E., Pichugova, S. V., & Tulakina, L. G. (2013). Comparative in vivo assessment of some adverse bioeffects of equidimensional gold and silver nanoparticles and the attenuation of nanosilver’s effects with a complex of innocuous bioprotectors. International Journal of Molecular Sciences, 14(2), 2449–2483. https://doi.org/10.3390/ijms14022449CrossRefPubMedPubMedCentral

Privalova, L. I., Katsnelson, B. A., Loginova, N. V., Gurvich, V. B., Shur, V. Y., Beikin, Y. B., Sutunkova, M. P., Minigalieva, I. A., Shishkina, E. V., Pichugova, S. V., Tulakina, L. G., & Beljayeva, S. V. (2014). Some characteristics of free cell population in the airways of rats after intratracheal instillation of copper-containing nano-scale particles. International Journal of Molecular Sciences, 15(11), 21538–21553. https://doi.org/10.3390/ijms151121538CrossRefPubMedPubMedCentral

Da Silva, A. B., Miniter, M., Thom, W., Hewitt, R. E., Wills, J., Jugdaohsingh, R., & Powell, J. J. (2020). Gastrointestinal absorption and toxicity of nanoparticles and microparticles: Myth, reality and pitfalls explored through titanium dioxide. Current opinion in toxicology, 19, 112–120. https://doi.org/10.1016/j.cotox.2020.02.007CrossRefPubMedPubMedCentral

National Toxicology Program. (2020) Toxicity studies of fullerene C60 (1 μm and 50 nm) administered by nose-only inhalation to Wistar Han [Crl:WI (Han)] rats and B6C3F1/N mice. Toxic. Rep. Ser. 87, NTP-TOX-87. https://doi.org/10.22427/NTP-TOX-87

Manuja, A., Kumar, B., Kumar, R., Chhabra, D., Ghosh, M., Manuja, M., Brar, B., Pal, Y., Tripathi, B. N., & Prasad, M. (2021). Metal/metal oxide nanoparticles: Toxicity concerns associated with their physical state and remediation for biomedical applications. Toxicology Reports, 8, 1970–1978. https://doi.org/10.1016/j.toxrep.2021.11.020CrossRefPubMedPubMedCentral

Privalova, L. I., Katsnelson, B. A., Loginova, N. V., Gurvich, V. B., Shur, V. Y., Valamina, I. E., Makeyev, O. H., Sutunkova, M. P., Minigalieva, I. A., Kireyeva, E. P., Rusakov, V. O., Tyurnina, A. E., Kozin, R. V., Meshtcheryakova, E. Y., Korotkov, A. V., Shuman, E. A., Zvereva, A. E., & Kostykova, S. V. (2014). Subchronic toxicity of copper oxide nanoparticles and its attenuation with the help of a combination of bioprotectors. International Journal of Molecular Sciences, 15(7), 12379–12406. https://doi.org/10.3390/ijms150712379CrossRefPubMedPubMedCentral

Minigalieva, I. A., Katsnelson, B. A., Privalova, L. I., Sutunkova, M. P., Gurvich, V. B., Shur, V. Y., Shishkina, E. V., Valamina, I. E., Makeyev, O. H., Panov, V. G., Varaksin, A. N., Grigoryeva, E. V., & Meshtcheryakova, E. Y. (2015). Attenuation of combined nickel (II) oxide and manganese(II, III) oxide nanoparticles’ adverse effects with a complex of bioprotectors. International journal of molecular sciences, 16(9), 22555–22583. https://doi.org/10.3390/ijms160922555CrossRefPubMedPubMedCentral

10.

Bushueva, T., Minigalieva, I., Panov, V., Kuznetsova, A., Naumova, A., Shur, V., Shishkina, E., Gurvich, V., Privalova, L., & Katsnelson, B. A. (2019). More data on in vitro assessment of comparative and combined toxicity of metal oxide nanoparticles. Food and Chemical Toxicology, 133, 110753. https://doi.org/10.1016/j.fct.2019.110753CrossRefPubMed

11.

Miri, A., Sarani, M., Hashemzadeh, A., Mardani, Z., & Darroudi, M. (2018). Biosynthesis and cytotoxic activity of lead oxide nanoparticles. Green Chemistry Letters and Reviews, 11(4), 567–572. https://doi.org/10.1080/17518253.2018.1547926CrossRef

12.

Ng, D. Q., Chu, Y., Tan, S. W., Wang, S. L., Lin, Y. P., Chu, C. H., Soo, Y. L., Song, Y. F., & Chen, P. J. (2019). In vivo evidence of intestinal lead dissolution from lead dioxide (PbO₂) nanoparticles and resulting bioaccumulation and toxicity in medaka fish. Environmental Sciences, 6(2), 580–591. https://doi.org/10.1039/C8EN00893KCrossRef

13.

Navas-Acien, A., Guallar, E., Silbergeld, E. K., & Rothenberg, S. J. (2007). Lead exposure and cardiovascular disease – A systematic review. Environmental Health Perspectives, 115(3), 472–482. https://doi.org/10.1289/ehp.9785CrossRefPubMed

14.

Shvachiy, L., Geraldes, V., Amaro-Leal, Â., & Rocha, I. (2020). Persistent effects on cardiorespiratory and nervous systems induced by long-term lead exposure: Results from a longitudinal study. Neurotoxicity Research, 37(4), 857–870. https://doi.org/10.1007/s12640-020-00162-8CrossRefPubMed

15.

Charkiewicz, A. E., & Backstrand, J. R. (2020). Lead toxicity and pollution in Poland. International Journal of Environmental Research and Public Health, 17(12), 4385. https://doi.org/10.3390/ijerph17124385CrossRefPubMedPubMedCentral

16.

Chen, Z., Huo, X., Chen, G., Luo, X., & Xu, X. (2021). Lead (Pb) exposure and heart failure risk. Environmental Science and Pollution Research International, 28(23), 28833–28847. https://doi.org/10.1007/s11356-021-13725-9CrossRefPubMed

17.

Machoń-Grecka, A., Dobrakowski, M., Kasperczyk, A., Birkner, E., & Kasperczyk, S. (2022). Angiogenesis and lead (Pb): Is there a connection? Drug and Chemical Toxicology, 45(2), 589–593. https://doi.org/10.1080/01480545.2020.1734607CrossRefPubMed

18.

Elgharabawy, R. M., Alhowail, A. H., Emara, A. M., Aldubayan, M. A., & Ahmed, A. S. (2021). The impact of chicory (Cichoriumintybus L) on hemodynamic functions and oxidative stress in cardiac toxicity induced by lead oxide nanoparticles in male rats. Biomedicine & Pharmacotherapy, 137, 111324. https://doi.org/10.1016/j.biopha.2021.111324CrossRef

19.

Vaziri, N. D. (2008). Mechanisms of lead-induced hypertension and cardiovascular disease. American Journal of Physiology. Heart and Circulatory Physiology, 295(2), H454–H465. https://doi.org/10.1152/ajpheart.00158.2008CrossRefPubMedPubMedCentral

20.

Simões, M. R., Ribeiro Júnior, R. F., Vescovi, M. V., de Jesus, H. C., Padilha, A. S., Stefanon, I., Vassallo, D. V., Salaices, M., & Fioresi, M. (2011). Acute lead exposure increases arterial pressure: role of the renin-angiotensin system. PLoS One, 6(4), e18730. https://doi.org/10.1371/journal.pone.0018730CrossRefPubMedPubMedCentral

21.

Silveira, E. A., Siman, F. D., de Oliveira Faria, T., Vescovi, M. V. A., Furieri, L. B., Lizardo, J. H. F., Stefanon, I., Padilha, A. S., & Vassallo, D. V. (2014). Low-dose chronic lead exposure increases systolic arterial pressure and vascular reactivity of rat aortas. Free Radical Biology & Medicine, 67, 366–376. https://doi.org/10.1016/j.freeradbiomed.2013.11.021CrossRef

22.

Toscano, C. M., Simões, M. R., Alonso, M. J., Salaices, M., Vassallo, D. V., & Fioresi, M. (2017). Sub-chronic lead exposure produces β1-adrenoceptor downregulation decreasing arterial pressure reactivity in rats. Life Sciences, 180, 93–101. https://doi.org/10.1016/j.lfs.2017.05.009CrossRefPubMed

23.

Simões, M. R., Preti, S. C., Azevedo, B. F., Fiorim, J., Freire, D. D., Jr., Covre, E. P., Vassallo, D. V., & Dos Santos, L. (2017). Low-level chronic lead exposure impairs neural control of blood pressure and heart rate in rats. Cardiovascular Toxicology, 17(2), 190–199. https://doi.org/10.1007/s12012-016-9374-yCrossRefPubMed

24.

Possomato-Vieira, J. S., Gonçalves-Rizzi, V. H., Do Nascimento, R. A., Wandekin, R. R., Caldeira-Dias, M., Chimini, J. S., da Silva, M. L. S., & Dias-Junior, C. A. (2018). Clinical and experimental evidences of hydrogen sulfide involvement in lead-induced hypertension. BioMed Research International, 2018, 4627391. https://doi.org/10.1155/2018/4627391CrossRefPubMedPubMedCentral

25.

Simões, M. R., Azevedo, B. F., Alonso, M. J., Salaices, M., & Vassallo, D. V. (2021). Chronic low-level lead exposure increases mesenteric vascular reactivity: Role of cyclooxygenase-2-derived prostanoids. Frontiers in Physiology, 11, 590308. https://doi.org/10.3389/fphys.2020.590308CrossRefPubMedPubMedCentral

26.

Tubsakul, A., Sangartit, W., Pakdeechote, P., Kukongviriyapan, V., Apaijit, K., & Kukongviriyapan, U. (2021). Curcumin mitigates hypertension, endothelial dysfunction and oxidative stress in rats with chronic exposure to lead and cadmium. Tohoku Journal of Experimental Medicine, 253(1), 69–76. https://doi.org/10.1620/tjem.253.69CrossRefPubMed

27.

Fioresi, M., Simões, M. R., Furieri, L. B., Broseghini-Filho, G. B., Vescovi, M. V. A., Stefanon, I., & Vassallo, D. V. (2014). Chronic lead exposure increases blood pressure and myocardial contractility in rats. PLoS ONE, 9(5), e96900. https://doi.org/10.1371/journal.pone.0096900CrossRefPubMedPubMedCentral

28.

Silva, M. A., de Oliveira, T. F., Almenara, C. C., Broseghini-Filho, G. B., Vassallo, D. V., Padilha, A. S., & Silveira, E. A. (2015). Exposure to a low lead concentration impairs contractile machinery in rat cardiac muscle. Biological Trace Element Research, 167(2), 280–287. https://doi.org/10.1007/s12011-015-0300-0CrossRefPubMed

29.

Minigalieva, I. A., Katsnelson, B. A., Panov, V. G., Privalova, L. I., Varaksin, A. N., Gurvich, V. B., Sutunkova, M. P., Shur, V. Y., Shishkina, E. V., Valamina, I. E., Zubarev, I. V., Makeyev, O. H., Meshtcheryakova, E. Y., & Klinova, S. V. (2017). In vivo toxicity of copper oxide, lead oxide and zinc oxide nanoparticles acting in different combinations and its attenuation with a complex of innocuous bio-protectors. Toxicology, 380, 72–93. https://doi.org/10.1016/j.tox.2017.02.007CrossRefPubMed

30.

Sengupta, P. (2013). The laboratory rat: Relating its age with human’s. International journal of preventive medicine, 4(6), 624–630.PubMedPubMedCentral

31.

Wu, A. (2006). Tietz Clinical Guide to Laboratory Tests, 4th ed., Elsevier Health Sciences.

32.

Nartsissov, R. P. (1969). Application of p-nitrotetrazolium violet for quantitative cytochemistry of human lymphocyte dehydrogenases. Archive of Anatomy, Histology and Embrionology, 56(5), 85–91. (In Russ.).

33.

Pavlovskaya, N. A., Kiryakov, A. V., & Pogabalo, A. V. (1998). Behavior of Lead in the Human Body and Features of Early Diagnosis of Lead Poisoning. Lad Publ. (In Russ.).

34.

Klinova, S. V., Katsnelson, B. A., Minigalieva, I. A., Gerzen, O. P., Balakin, A. A., Lisin, R. V., Butova, K. A., Nabiev, S. R., Lookin, O. N., Katsnelson, L. B., Privalova, L. I., Kuznetsov, D. A., Shur, V. Y., Shishkina, E. V., Makeev, O. H., Valamina, I. E., Panov, V. G., Sutunkova, M. P., Nikitina, L. V., & Protsenko, Y. L. (2021). Cardioinotropic effects in subchronic intoxication of rats with lead and/or cadmium oxide nanoparticles. International Journal of Molecular Sciences, 22(7), 3466. https://doi.org/10.3390/ijms22073466CrossRefPubMedPubMedCentral

35.

Mast, F., & Elzinga, G. (1990). Heat released during relaxation equals force–length area in isometric contractions of rabbit papillary muscle. Circulation Research, 67(4), 893–901. https://doi.org/10.1161/01.res.67.4.893CrossRefPubMed

36.

Sutunkova, M. P., Minigalieva, I. A., Shelomencev, I. G., Privalova, L. I., Ryabova, Y. V., Tazhigulova, A. V., Amromin, L. A., Minigalieva, R. F., Sutunkova, Y. M., Gurvich, V. B., Makoveeva, E. V., & Toropova, L. V. (2022). Electron microscopy study on the transport of lead oxide nanoparticles into brain structures following their subchronic intranasal administration in rats. Scientific Reports, 12, 19444. https://doi.org/10.1038/s41598-022-24018-7CrossRefPubMedPubMedCentral

37.

Gidlow, D. A. (2015). Lead toxicity. Occup. Med. (Lond.), 65(5), 348–356. https://doi.org/10.1093/occmed/kqv018CrossRefPubMed

38.

Glenn, B. S., Stewart, W. F., Schwartz, B. S., & Bressler, J. (2001). Relation of alleles of the sodium-potassium adenosine triphosphatase α2 gene with blood pressure and lead exposure. American Journal of Epidemiology, 153(6), 537–545. https://doi.org/10.1093/aje/153.6.537CrossRefPubMed

39.

Glenn, B. S., Stewart, W. F., Links, J. M., Todd, A. C., & Schwartz, B. S. (2003). The longitudinal association of lead with blood pressure. Epidemiology, 14(1), 30–36. https://doi.org/10.1097/00001648-200301000-00011CrossRefPubMed

40.

Glenn, B. S., Bandeen-Roche, K., Lee, B. K., Weaver, V. M., Todd, A. C., & Schwartz, B. S. (2006). Changes in systolic blood pressure associated with lead in blood and bone. Epidemiology, 17(5), 538–544. https://doi.org/10.1097/01.ede.0000231284.19078.4bCrossRefPubMed

41.

Carmignani, M., Boscolo, P., Poma, A., & Volpe, A. R. (1999). Kininergic system and arterial hypertension following chronic exposure to inorganic lead. Immunopharmacology, 44(1–2), 105–110. https://doi.org/10.1016/S0162-3109(99)00115-0CrossRefPubMed

42.

Carmignani, M., Volpe, A. R., Boscolo, P., Qiao, N., Di Gioacchino, M., Grilli, A., & Felaco, M. (2000). Catcholamine and nitric oxide systems as targets of chronic lead exposure in inducing selective functional impairment. Life Sciences, 68(4), 401–415. https://doi.org/10.1016/s0024-3205(00)00954-1CrossRefPubMed

43.

Fiorim, J., Ribeiro Junior, R. F., Silveira, E. A., Padilha, A. S., Vescovi, M. V. A., de Jesus, H. C., Stefanon, I., Salaices, M., & Vassallo, D. V. (2011). Low-level lead exposure increases systolic arterial pressure and endothelium-derived vasodilator factors in rat aortas. PLoS ONE, 6(2), e17117. https://doi.org/10.1371/journal.pone.0017117CrossRefPubMedPubMedCentral

44.

Vaziri, N. D., & Norris, K. (2011). Lipid disorders and their relevance to outcomes in chronic kidney disease. Blood Purification, 31(1–3), 189–196. https://doi.org/10.1159/000321845CrossRefPubMed

45.

Sutunkova, M. P., Solovyeva, S. N., Chernyshov, I. N., Klinova, S. V., Gurvich, V. B., Shur, V. Y., Shishkina, E. V., Zubarev, I. V., Privalova, L. I., & Katsnelson, B. A. (2020). Manifestation of systemic toxicity in rats after a short-time inhalation of lead oxide nanoparticles. International Journal of Molecular Sciences, 21(3), 690. https://doi.org/10.3390/ijms21030690CrossRefPubMedPubMedCentral

46.

Ndrepepa, G. (2021). Aspartate aminotransferase and cardiovascular disease—a narrative review. Journal of Laboratory and Precision Medicine. https://doi.org/10.21037/jlpm-20-93CrossRef

47.

Bogden, J. D., Gertner, S. B., Christakos, S., Kemp, F. W., Yang, Z., Katz, S. R., & Chu, C. (1992). Dietary calcium modifies concentrations of lead and other metals and renal calbindin in rats. Journal of Nutrition, 122(7), 1351–1360. https://doi.org/10.1093/jn/122.7.1351CrossRefPubMed

48.

Varnai, V. M., Piasek, M., Blanusa, M., Sarić, M. M., Šimić, D., & Kostial, K. (2001). Calcium supplementation efficiently reduces lead absorption in suckling rats. Pharmacology and Toxicology, 89(6), 326–330. https://doi.org/10.1034/j.1600-0773.2001.d01-169.xCrossRefPubMed

49.

Privalova, L. I. (2005). Lead and its compounds. In: Filov, V.A., (Ed.), Environmental Hazards. Elements of Groups I–IV of the Periodic System and Their Inorganic Compounds. (pp. 400–427). NPO Professional Publ. (In Russ.)

50.

Katsnelson, B. A., Kireyeva, E. P., Kuzmin, S. V., Privalova, L. I., & Burns, K. M. (2007). An association between incipient renal damage and urine cadmium and lead levels in young Russian children: A case control study. European Epi Marker, 11(4), 1–8.

51.

Katsnelson, B. A., Privalova, L. I., Kuzmin, S. V., Malykh, O. L., Gurvitch, V. B., Voronin, S. A., Matyukhina, E. V., Degtyareva, T. D., Marshalkin, A. P., Prokopyev, A. A., Gnezdilova, S. V., Kireyeva, E. P., & Soloboyeva, J. I. (2008). Lead and childhood: Risks and their management (the Middle Urals experience). CEJOEM, 14(3), 215–238.

52.

Katsnelson, B. A., Yeremenko, O. S., Privalova, L. I., Makeyev, O. H., Degtyareva, T. D., Beresneva, OYu., Valamina, I. E., Minihaliyeva, I. A., Sutunkova, M. P., Kireyeva, E. P., Bukhantsev, V. A., Dovzenko, E. I., Minin, V. V., Kulikov, E. S., Kostykova, S. V., & Nazukin, A. S. (2009). Toxicity of monazite particulates and its attenuation with a complex of bio-protectors. Medicina del Lavoro, 100(6), 455–470.PubMed

53.

Katsnelson, B. A., Privalova, L. I., Kireyeva, Y. P., Yeremenko, O. S., Sutunkova, M. P., Valamina, I. E., Varaksin, A. N., Panov, V. G., & Kazmer, J. I. (2012). Combined subchronic fluoride–lead intoxication and its attenuation with the help of a complex of bioprotectors. Medicina del Lavoro, 103(2), 146–159.PubMed

54.

Nawrot, T., Geusens, P., Nulens, T. S., & Nemery, B. (2010). Occupational cadmium exposure and calcium excretion, bone density, and osteoporosis in men. Journal of Bone and Mineral Research, 25(6), 1441–1445. https://doi.org/10.1002/jbmr.22CrossRefPubMed

55.

Savchenko, O. V., Sgrebneva, M. N., Kiselev, V. I., & Khotimchenko, Y. S. (2015). Lead removal in rats using calcium alginate. Environmental Science and Pollution Research International, 22(1), 293–304. https://doi.org/10.1007/s11356-014-3324-7CrossRefPubMed

56.

Panov, V., Minigalieva, I., Bushueva, T., Fröhlich, E., Meindl, C., Absenger-Novak, M., Shur, V., Shishkina, E., Gurvich, V., Privalova, L., & Katsnelson, B. A. (2020). Some peculiarities in the dose dependence of separate and combined in vitro cardiotoxicity effects induced by CdS and PbS nanoparticles with special attention to hormesis manifestations. Dose Response. https://doi.org/10.1177/1559325820914180CrossRefPubMedPubMedCentral

57.

Ostroumova, O. D. (2001). QT interval prolongation. Russian Medical Journal, 9(18), 750. (In Russ.).

58.

Peralta, A. A., Schwartz, J., Gold, D. R., Coull, B., & Koutrakis, P. (2021). Associations between PM25 metal components and QT interval length in the Normative Aging Study. Environmental Research, 195, 110827. https://doi.org/10.1016/j.envres.2021.110827CrossRefPubMedPubMedCentral

59.

Hussain, T., Tan, B., Yin, Y., Blachier, F., Tossou, M. C., & Rahu, N. (2016). Oxidative stress and inflammation: What polyphenols can do for us? Oxidative Medicine and Cellular Longevity, 2016, 7432797. https://doi.org/10.1155/2016/7432797CrossRefPubMedPubMedCentral

60.

Hansson, G. K., Robertson, A. K., & Söderberg-Nauclér, C. (2006). Inflammation and atherosclerosis. Annual Review of Pathology: Mechanisms of Disease, 1, 297–329. https://doi.org/10.1146/annurev.pathol.1.110304.100100CrossRef

61.

Ademuyiwa, O., Ugbaja, R. N., Idumebor, F., & Adebawo, O. (2005). Plasma lipid profiles and risk of cardiovascular disease in occupational lead exposure in Abeokuta. Nigeria Lipids in Health and Disease, 4, 19. https://doi.org/10.1186/1476-511X-4-19CrossRefPubMed

62.

Wang, C., Levis, G. B. S., Lee, E. B., Levis, W. R., Lee, D. W., Kim, B. S., Park, S. Y., & Park, E. (2004). Platycodin D and D3 isolated from the root of Platycodon grandiflorum modulate the production of nitric oxide and secretion of TNF-α in activated RAW 264.7 cells. International Immunopharmacology, 4(8), 1039–1049. https://doi.org/10.1016/j.intimp.2004.04.005CrossRefPubMed

63.

Chang, C. H., Yu, F. Y., Wu, T. S., Wang, L. T., & Liu, B. H. (2011). Mycotoxin citrinin induced cell cycle G2/M arrest and numerical chromosomal aberration associated with disruption of microtubule formation in human cells. Toxicological Sciences, 119(1), 84–92. https://doi.org/10.1093/toxsci/kfq309CrossRefPubMed

Title: On the Mechanisms of the Cardiotoxic Effect of Lead Oxide Nanoparticles
Authors: Ilzira A. Minigaliyeva
Svetlana V. Klinova
Marina P. Sutunkova
Yuliya V. Ryabova
Irene E. Valamina
Ivan G. Shelomentsev
Tatiana N. Shtin
Tatiana V. Bushueva
Yuri L. Protsenko
Alexander A. Balakin
Ruslan V. Lisin
Daniil A. Kuznetsov
Boris A. Katsnelson
Liubov V. Toropova
Publication date: 18-12-2023
Publisher: Springer US
Published in: Cardiovascular Toxicology / Issue 1/2024
Print ISSN: 1530-7905
Electronic ISSN: 1559-0259
DOI: https://doi.org/10.1007/s12012-023-09814-5

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Keynote webinar | Spotlight on medication adherence

Springer Medicine

On the Mechanisms of the Cardiotoxic Effect of Lead Oxide Nanoparticles

Abstract

Graphical Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Graphical Abstract

Please log in to get access to this content

Other articles of this Issue 1/2024

Human Immunodeficiency Virus as a Risk Factor for Cardiovascular Disease

Arsenic-Induced Cardiovascular Diseases and their Correlation with Mitochondrial DNA Copy Number, Deletion, and Telomere Length in Bangladeshi Population

Simvastatin Significantly Reduced Alcohol-Induced Cardiac Damage in Adolescent Mice

Four‑Dimensional Echocardiographic Evaluation of Cardiac Iron Overload in Patients with Beta-Thalassemia Major

Blood Homocysteine Levels Mediate the Association Between Blood Lead Levels and Cardiovascular Mortality

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page