Role of silver nanoparticles (AgNPs) on the cardiovascular system

Archives of Toxicology

Volumn 90, Issue 3, 2016, Pages 493-511

  Gonzalez, Carmen ^a,b   Rosas Hernandez, Hector ^a   Ramirez Lee, Manuel Alejandro ^a   Salazar García, Samuel ^a   Ali, Syed F ^b  

^a UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Blood vessels; Cardiovascular system; Endothelium; Silver nanoparticles; Toxicity

Indexed keywords

SILVER NANOPARTICLE; METAL NANOPARTICLE; SILVER;

BLOOD VESSEL; CARDIOVASCULAR SYSTEM; ENDOTHELIUM CELL; HEART; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; VASCULAR ENDOTHELIUM; CARDIOVASCULAR DISEASE; CHEMICALLY INDUCED; DRUG EFFECTS; PATHOPHYSIOLOGY; TISSUE DISTRIBUTION;

BLOOD VESSELS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; ENDOTHELIUM, VASCULAR; HUMANS; METAL NANOPARTICLES; SILVER; TISSUE DISTRIBUTION;

EID: 84958240185     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1447-8     Document Type: Review

References (106)

1. Ahamed M, Alsalhi MS, Siddiqui MKJ (2010) Silver nanoparticle applications and human health. Clin Chim Acta 41(23–24):1841–1848. doi:10.1016/j.cca.2010.08.016
2. Al Sabti H (2007) Therapeutic angiogenesis in cardiovascular disease. J Cardiothorac Surg 2:49. doi:10.1186/1749-8090-2-49
3. Asgharian B, Price OT (2007) Deposition of ultrafine (NANO) particles in the human lung. Inhalation Toxicol 19(13):1045–1054. doi:10.1080/08958370701626501
4. Asharani PV, Lian-Wu Y, Gong Z, Valiyaveettil S (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19(25):225102. doi:10.1088/0957-4484/19/25/255102
5. Asharani PV, Lian-Wu Y, Gong Z, Valiyaveettil S (2011) Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5(1):43–54. doi:10.3109/17435390.2010.489207
6. Bandyopadhyay D, Baruah H, Gupta B, Sharma S (2012) Silver nano particles prevent platelet adhesion on immobilized fibrinogen. Assoc Clin Biochem India 27(2):164–170. doi:10.1007/s12291-011-0169-4
7. Barba-de-la-Rosa AP, Barba-Montoya A, Martinez-Cuevas PP, Hernandez-Ledesma B, León-Galvan MF, De-Leon-Rodriguez A, Gonzalez C (2010) Tryptic amaranth glutelin digests induce endothelial nitric oxide production through inhibition of ACE: antihypertensive role of amaranth peptides. Nitric Oxide 23(2):106–111. doi:10.1016/j.niox.2010.04.006
8. Bednarczyk J, Lukasiuk K (2011) Tight junctions in neurological diseases. Acta Neurobiol Exp 71(4):393–408
9. Behra R, Sigg L, Clift MJ, Herzog F, Minghetti M, Johnston B, Petri-Fink A, Rothen-Rutishauser B (2013) Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J R Soc Interface 10(87):20130396. doi:10.1098/rsif.2013.0396
10. Boop SK, Lettieri T (2008) Comparison of four different colorimetric and fluorometric cytotoxicity assays in a zebrafish liver cell line. BioMed Central Pharmacol 8:8–19. doi:10.1186/1471-2210-8-8
11. Brandt O, Mildner M, Egger AE, Groessl M, Rix U, Posch M, Keppler BK, Strupp C, Mueller B, Stingl G (2012) Nanoscalic silver possesses broad-spectrum antimicrobial activities and exhibits fewer toxicological side effects than silver sulfadiazine. Nanomedicine 8(4):478–488. doi:10.1016/j.nano.2011.07.005
12. Brouillet S, Hoffmann P, Benharouga M, Salomon A, Schaal JP, Feige JJ, Alfaidy N (2010) Molecular characterization of EG-VEGF-mediated angiogenesis: differential effects on microvascular and macrovascular endothelial cells. Mol Biol Cell 21(16):2832–2843. doi:10.1091/mbc.E10-01-0059
13. Busse R, Fichtner H, Luckhoff A (1988) Hyperpolarization and increased free calcium in acetylcholine-stimulated endothelial cells. Am J Physiol 255(4/2):H965–H969
14. Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Physiol Biochem 112(43):13608–13619. doi:10.1021/jp712087m
15. Cha K, Hong HW, Choi YG, Lee MJ, Park JH, Chae HK, Ryu G, Myung H (2008) Comparison of acute responses of mice livers to short-term exposure to nano-sized or micro-sized silver particles. Biotechnol Lett 30(11):1893–1899. doi:10.1007/s10529-008-9786-2
16. Chaloupka K, Malam Y, Seifalian AM (2010) Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol 28(11):580–588. doi:10.1016/j.tibtech.2010.07.006
17. Chen X, Schluesener HJ (2008) Nanosilver: a nanoproduct in medical application. Toxicol Lett 176(1):1–12. doi:10.1016/j.toxlet.2007.10.004
18. Clapp C, Aranda J, Gonzalez C, Jeziorski MC, Martinez-de-la-Escalera G (2006) Vasoinhibins: endogenous regulators of angiogenesis and vascular function. Trends Endocrinol Metab 17(8):301–307. doi:10.1016/j.tem.2006.08.002
19. Clapp C, Thebault S, Jeziorski MC, Martinez-De-La-Escalera G (2009) Peptide hormone regulation of angiogenesis. Am Physiol Rev 89(4):1177–1215. doi:10.1152/physrev.00024.2009
20. Clapp C, Martinez-de-la-Escalera L, Martinez-de-la-Escalera G (2012) Prolactin and blood vessels: a comparative endocrinology perspective. Gen Comp Endocrinol 176(3):336–340. doi:10.1016/j.ygcen.2011.12.033
21. Corbacho AM, Martinez-de-la-Escalera G, Clapp C (2002) Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 173(2):219–238. doi:10.1677/joe.0.1730219
22. Costa CS, Ronconi JV, Daufenbach JF, Gonçalves CL, Rezin GT, Streck EL, Paula MM (2010) In vitro effects of silver nanoparticles on the mitochondrial respiratory chain. Mol Cell Biochem 342(1–2):51–56. doi:10.1007/s11010-010-0467-9
23. Cui D, Gao H (2003) Advance and prospect of bionanomaterials. Biotechnol Prog 19(3):683–692. doi:10.1021/bp025791i
24. Drescher D, Büchner T, McNaughton D, Kneipp J (2013) SERS reveals the specific interaction of silver and gold nanoparticles with hemoglobin and red blood cell components. Phys Chem Chem Phys 15(15):5364–5374. doi:10.1039/c3cp43883j
25. Español AJ, Goren N, Ribeiro ML, Sales ME (2010) Nitric oxide synthase 1 and cyclooxygenase-2 enzymes are targets of muscarinic activation in normal and inflamed NIH3T3 cells. Inflamm Res 59(3):227–238. doi:10.1007/s00011-009-0097-4
26. Espinosa-Cristobal LF, Martinez-Castañon GA, Loyola-Rodriguez JP, Patiño-Marin N, Reyes-Macías JF, Vargas-Morales JM, Ruiz F (2013) Toxicity, distribution, and accumulation of silver nanoparticles in Wistar rats. J Nanopart Res. doi:10.1007/S11051-013-1702-6
27. Farley A, Hendry C, McLafferty E (2013) Blood components. Nurs Stand 27(13):35–42. doi:10.7748/ns2012.11.27.13.35.c9449
28. Garcia C, Aranda J, Arnold E, Thebault S, Macotela Y, Lopez-Casillas F, Mendoza V, Quiroz-Mercado H, Hernandez-Montiel HL, Lin SH, de-la-Escalera GM, Clapp C (2008) Vasoinhibins prevent retinal vasopermeability associated with diabetic retinopathy in rats via protein phosphatase 2A dependent eNOs inactivation. J Clin Investig 118(6):2291–2300. doi:10.1172/JCI34508
29. Geiser M, Rothen-Rutishauser B, Kapp N, Schürch S, Kreyling W, Schulz H, Semmler M, Im-Hof V, Heyder J, Gehr P (2005) Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 113(11):1555–1560. doi:10.1289/ehp.8006
30. Ghofrani H, Voswinckel R, Reichenberger F, Olschewski H, Haredza P, Karadaş B, Schermuly RT, Weissmann N, Seeger W, Grimminger F (2004) Differences in hemodynamic and oxygenation response to three different phosphodiesterase-5 inhibitors in patients with pulmonary arterial hypertension. J Am Coll Cardiol 44(7):1488–1496. doi:10.1016/j.jacc.2004.06.060
31. Gnanadhas DP, Ben Thomas M, Thomas R, Raichur AM, Chakravortty D (2013) Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo. Antimicrob Agents Chemother 57(10):4945–4955. doi:10.1128/AAC.00152-13
32. Godin BS, Sakamoto JH, Serda RE, Grattoni A, Bouamrani A, Ferrari M (2010) Emerging applications of nanomedicine for therapy and diagnosis of cardiovascular diseases. Trends Pharmacol Sci 31(5):199–205. doi:10.1016/j.tips.2010.01.003
33. Gonzalez C, Corbacho AM, Eiserich JP, Garcia C, Lopez-Barrera F, Morales-Tlalpan V, Barajas-Espinosa A, Diaz-Muñoz M, Rubio R, Lin SH, Martinez-de-la-Escalera G, Clapp C (2004) 16 K-prolactin inhibits activation of endothelial nitric oxide synthase, intracellular calcium mobilization, and endothelium-dependent vasorelaxation. Endocrinology 145(12):5714–5722. doi:10.1210/en.2004-0647
34. Gonzalez C, Parra A, Ramirez-Peredo J, Garcia C, Rivera JC, Macotela Y, Aranda J, Lemini M, Arias J, Ibargüengoitia F, de-la-Escalera GM, Clapp C (2007) Elevated vasoinhibins may contribute to endothelial cell dysfunction and low birth weight in preeclampsia. Lab Invest 87(10):1009–1017. doi:10.1038/labinvest.3700662
35. Gonzalez C, Lemini M, Garcia L, Ramiro-Diaz JM, Castillo-Hernandez JR, Clapp C, Rubio R (2008) Effects of prolactin and vasoinhibins on nitric oxide synthase activity in coronary endothelial cells and vessels in isolated perfused guinea pig hearts. Toxicol Lett 180(1):S34. doi:10.1016/j.toxlet.2008.06.655
36. Gonzalez C, Salazar-Garcia S, Palestino G, Martinez-Cuevas PP, Ramirez-Lee MA, Jurado-Manzano BB, Rosas-Hernandez H, Gaytan-Pacheco N, Martel G, Espinosa-Tanguma R, Biris AS, Ali SF (2011) Effect of 45 nm silver nanoparticles (AgNPs) upon the smooth muscle of rat trachea: role of nitric oxide. Toxicol Lett 207(3):306–313. doi:10.1016/j.toxlet.2011.09.024
37. Grosse S, Evje L, Syversen T (2013) Silver nanoparticle-induced cytotoxicity in rat brain endothelial cell culture. Toxicol In Vitro 27(1):305–313. doi:10.1016/j.tiv.2012.08.024
38. Gurunathan S, Lee KJ, Kalishwaralal K, Sheikpranbabu S, Vaidyanathan R, Eom SH (2009) Antiangiogenic properties of silver nanoparticles. Biomaterials 30(31):6341–6350. doi:10.1016/j.biomaterials.2009.08.008
39. Gutierrez R, Cubiberti G (2008) Effective models of charge transport in DNA nanowires. In: Shoseyov O, Levy I (eds) NanoBioTechnology bioinspired devices and materials of the future. Human Press Inc., Totowa, pp 108–117
40. Haase A, Mantion A, Graf P, Plendl J, Thuenemann AF, Meier W, Taubert A, Luch A (2012) A novel type of silver nanoparticles and their advantages in toxicity testing in cell culture systems. Arch Toxicol 86(7):1089–1098. doi:10.1007/s00204-012-0836-0
41. Hadrup N, Loeschner K, Bergström A, Wilcks A, Gao X, Vogel U, Frandsen HL, Larsen EH, Lam HR, Mortensen A (2012) Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch Toxicol 86(4):543–551. doi:10.1007/s00204-011-0759-1
42. Hotowy A, Sawosz E, Pineda L, Sawosz F, Grodzik M, Chwalibog A (2012) Silver nanoparticles administered to chicken affect VEGFA and FGF2 gene expression in breast muscle and heart. Nanoscale Res Lett 7(1):418
43. Hu G, Place AT, Minshall RD (2008) Regulation of endothelial permeability by Src kinase signaling: vascular leakage versus transcellular transport of drugs and macromolecules. Chem Biol Interact 171(2):177–189. doi:10.1016/j.cbi.2007.08.006
44. Jensen LS, Peterson RP, Falen L (1974) Inducement of enlarged hearts and muscular dystrophy in turkey poults with dietary silver. Poult Sci 53:57–64
45. Ji JH, Jung JH, Kim SS, Yoon JU, Park JD, Choi BS, Chung YH, Kwon IH, Jeong J, Han BS, Shin JH, Sung JH, Song KS, Yu IJ (2007) Twenty-eight-day inhalation toxicity study of silver nanoparticles in Sprague–Dawley rats. Inhalation Toxicol 19(10):857–871. doi:10.1080/08958370701432108
46. Kabanov AV (2006) Polymer genomics: an insight into pharmacology and toxicology of nanomedicines. Adv Drug Deliv Rev 58(15):1597–1621. doi:10.1016/j.addr.2006.09.019
47. Kalishwaralal K, Banumathi E, Ram-Kumar-Pandian S, Deepak V, Muniyandi J, Eom SH, Gurunathan S (2009) Silver nanoparticles inhibit VEGF induced cell proliferation and migration in bovine retinal endothelial cells. Colloids Surf B 73(1):51–57. doi:10.1016/j.colsurfb.2009.04.025
48. Kang K, Lim DH, Choi IH, Kang T, Lee K, Moon EY, Yang Y, Lee MS, Lim JS (2011) Vascular tube formation and angiogenesis induced by polyvinylpyrrolidone-coated silver nanoparticles. Toxicol Lett 205(3):227–234. doi:10.1016/j.toxlet.2011.05.1033
49. Kawabe J, Ushikubi F, Hasebe N (2010) Prostacylcin in vascular diseases, recent insights and future perspectives. Circ J 74(5):836–843. doi:10.1253/circj.CJ-10-0195
50. Kennedy DC, Tay LL, Lyn RK, Rouleau Y, Hulse J, Pezacki JP (2009) Nanoscale aggregation of cellular β2-adrenergic receptors measured by plasmonic interactions of functionalized nanoparticles. J Nanosci Nanotechnol 3(8):2329–2339. doi:10.1021/nn900488u
51. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, Choi BS, Lim R, Chang HK, Chung YH, Kwon IH, Jeong J, Han BS, Yu IJ (2008) Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague–Dawley rats. Inhal Toxicol 20(6):575–583. doi:10.1080/08958370701874663
52. Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH et al (2010) Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 7(20):1–11. doi:10.1186/1743-8977-7-20
53. Klasen HJ (2000) Historical review of the use of silver in the treatment of burns. I. Early uses. Burns 26(2):117–130
54. Korani M, Rezayat SM, Arbabi Bidgoli S (2013) Sub-chronic dermal toxicity of silver nanoparticles in guinea pig: special emphasis to heart, bone and kidney toxicities. Iran J Pharm Res 12(3):511–519
55. Krajewski S, Prucek R, Panacek A, Krajewski S, Prucek R, Panacek A, Avci-Adali M, Nolte A, Straub A, Zboril R, Wendel HP, Kvitek L (2013) Hemocompatibility evaluation of different silver nanoparticle concentrations employing a modified Chandler-loop in vitro assay on human blood. Acta Biomater 9(7):7460–7468. doi:10.1016/j.actbio.2013.03.016
56. Kumar B, Gupta SK, Saxena R, Srivastava S (2012) Current trends in the pharmacotherapy of diabetic retinopathy. J Postgrad Med 58(2):132–139. doi:10.4103/0022-3859.97176
57. Lankveld DPK, Oomen AG, Krystek P, Neigh A, Troost-de-Jong A, Noorlander CW, Van-Eijkeren JC, Geertsma RE, De-Jong WH (2010) The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials 31(32):8350–8361. doi:10.1016/j.biomaterials.2010.07.045
58. Levi D, Tulloch A, Ho J, Kealey C, Rigberg D (2012) Vascular and cardiovascular devices. In: Culjat M, Singh R, Lee H (eds) Medical devices. Surgical and image-guided technologies, 1st edn. Wiley, New York, pp 199–218
59. Li Z, Carter JD, Dailey LA, Huang YC (2004) Vanadyl sulfate inhibits NO production via threonine phosphorylation of eNOS. Environ Health Perspect 112(2):201–206. doi:10.1289/ehp.6477
60. Li Z, Carter JD, Dailey LA, Huang YC (2005) Pollutant particles produce vasoconstriction and enhance MAPK signaling via angiotensin type I receptor. Environ Health Perspect 113(8):1009–1014. doi:10.1289/ehp.7736
61. Li N, Xia T, Nel AE (2008) The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radical Biol Med 44(9):1689–1699. doi:10.1016/j.freeradbiomed.2008.01.028
62. Lin Z, Monteiro-Riviere NA, Riviere JE (2014) Pharmacokinetics of metallic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol. doi:10.1002/wnan.1304
63. Lowry GV, Gregory KB, Apte SC, Lead JR (2012) Transformations of nanomaterials in the environment. Environ Sci Technol 46(13):6893–6899. doi:10.1021/es300839e
64. Luoma SN (2008) Silver nanotechnologies and the environment: old problems or new challenges? Woodrow Wilson International Center for Scholars, Project on Emerging Nanotechnologies. Pew Charit Trusts 1:66. doi:10.1093/annhyg/mel071
65. Maillard JK, Hartemann P (2013) Silver as an antimicrobial: facts and gaps in knowledge. Crit Rev Microbiol 39(4):373–383. doi:10.3109/1040841X.2012.713323
66. Mather KJ, Lteif A, Steinberg HO, Baron AD (2004) Interactions between endothelin and nitric oxide in the regulation of vascular tone in obesity and diabetes. Diabetes 53(8):2060–2066. doi:10.2337/diabetes.53.8.2060
67. Moghimi SM, Hunter AC, Murray JC (2001) Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol Rev 53(2):283–318
68. Oberdörster G, Sharp Z, Atudorei V, Elder A, Gelein R, Lunts A, Kreyling W, Cox C (2004) Translocation of inhaled ultrafine particles to the brain. Inhalation Toxicol 16(6–7):437–445. doi:10.1080/00984100290071658
69. Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113(7):823–839. doi:10.1289/ehp.7339
70. Olcott CT (1950) Experimental argyrosis; hypertrophy of the left ventricle of the heart in rats ingesting silver salts. AMA Arch Pathol 49(2):138–149
71. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73(6):1712–1720. doi:10.1128/AEM.02218-06
72. Panyam J, Labhasetwar V (2003) Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev 55(3):329–347. doi:10.1016/S0169-409X(02)00228-4
73. Peters K, Unger RE, Kirkpatrick CJ, Gatti AM, Monari E (2004) Effects of nano-scaled particles on endothelial cell function in vitro: studies on viability, proliferation and inflammation. J Mater Sci - Mater Med 15(4):321–325. doi:10.1023/B:JMSM.0000021095.36878.1b
74. Peterson RP, Jensen LS, Harrison PC (1973) Effect of silver-induced enlarged hearts during the first four weeks of life on subsequent performance of turkeys. Avian Dis 17:802–806
75. Polverini PJ (2002) Angiogenesis in health and disease: insights into basic mechanisms and therapeutic opportunities. J Dent Educ 66(8):962–975
76. Quadros ME, Marr LC (2010) Environmental and human health risks of aerosolized silver nanoparticles. J Air Waste Manag Assoc 60(7):770–781. doi:10.3155/1047-3289.60.7.770
77. Rahman MF, Wang J, Patterson TA, Saini UT, Robinson BL, Newport GD, Murdock RC, Schlager JJ, Hussain SM, Ali SF (2009) Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett 187(1):15–21. doi:10.1016/j.toxlet.2009.01.020
78. Red-Horse K, Ueno H, Weissman IL, Krasnow MA (2010) Coronary arteries form by developmental reprogramming of venous cells. Nature 464(7288):549–553. doi:10.1038/nature08873
79. Ricciardolo FL, Maria DGU, Mistretta A (1997) Impairment of bronchoprotection by nitric oxide in severe asthma. The Lancet 350(9087):1297–1298. doi:10.1016/S0140-6736(05)62474-9
80. Rosas-Hernandez H, Jimenez-Badillo S, Martinez-Cuevas PP, Gracia-Espino E, Terrones H, Terrones M, Hussain SM, Ali SF, Gonzalez C (2009) Effects of 45-nm silver nanoparticles on coronary endothelial cells and isolated rat aortic rings. Toxicol Lett 191(2–3):305–313. doi:10.1016/j.toxlet.2009.09.014
81. Salata O (2004) Applications of nanoparticles in biology and medicine. J Nanobiotechnol 2(1):3. doi:10.1186/1477-3155-2-3
82. Sarhan OM, Hussein RM (2014) Effects of intraperitoneally injected silver nanoparticles on histological structures and blood parameters in the albino rat. Int J Nanomed 24(9):1505–1517. doi:10.2147/IJN.S56729
83. Schrand AM, Rahman MF, Hussain SM, Schlager JJ, Smith DA, Syed AF (2010) Metal-based nanoparticles and their toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2(5):544–568. doi:10.1002/wnan.103
84. Sharma HS, Ali SF, Hussain SM, Schlager JJ, Sharma A (2009a) Influence of engineered nanoparticles from metals on the blood–brain barrier permeability, cerebral blood flow, brain edema and neurotoxicity. An experimental study in the rat and mice using biochemical and morphological approaches. J Nanosci Nanotechnol 9(8):5055–5072. doi:10.1166/jnn.2009.GR09
85. Sharma HS, Ali SF, Tian ZR, Hussain SM, Schlager JJ, Sjöquist PO, Sharma A, Muresanu DF (2009b) Chronic treatment with nanoparticles exacerbate hyperthermia induced blood–brain barrier breakdown, cognitive dysfunction and brain pathology in the rat. Neuroprotective effects of nanowired-antioxidant compound H-290/51. J Nanosci Nanotechnol 9(8):5073–5090. doi:10.1166/jnn.2009.GR10
86. Sheikpranbabu S, Kalishwaralal K, Venkataraman D, Eom SH, Park J, Gurunathan S (2009) Silver nanoparticles inhibit VEGF-and IL-1beta—induced vascular permeability via Src dependent pathway in porcine retinal endothelial cells. J Nanobiotechnol 7:8. doi:10.1186/1477-3155-7-8
87. Sheikpranbabu S, Kalishwaralal K, Lee K, Vaidyanathan R, Eom SH, Gurunathan S (2010) The inhibition of advanced glycation end-products-induced retinal vascular permeability by silver nanoparticles. Biomaterials 31(8):2260–2271. doi:10.1016/j.biomaterials.2009.11.076
88. Shi J, Sun X, Lin Y, Zou X, Li Z, Liao Y, Du M, Zhang H (2014) Endothelial cell injury and dysfunction induced by silver nanoparticles through oxidative stress via IKK/NF-κB pathways. Biomaterials 35(24):6657–6666. doi:10.1016/j.biomaterials.2014.04.093
89. Soto K, Garza KM, Murr LE (2007) Cytotoxic effects of aggregated nanomaterials. Acta Biomater 3(3):351–358. doi:10.1016/j.actbio.2006.11.004
90. Sriram M, Kanth S, Kalishwaralal K, Gurunathan S (2010) Antitumor activity of silver nanoparticles in Dalton’s lymphoma ascites tumor model. Int J Nanomed 5:753–762. doi:10.2147/IJN.S11727
91. Sung J, Ji JH, Yoon J, Kim DS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Kim J, Kim TS, Chang HK, Lee EJ, Lee JH, Yu IJ (2008) Lung function changes in Sprague–Dawley rats after prolonged inhalation exposure to silver nanoparticles. Inhalation Toxicol 20(6):567–574. doi:10.1080/08958370701874671
92. Sung J, Ji J, Park JD, Yoon JU, Kim DS, Jeon KS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Chang HK, Lee JH, Cho MH, Kelman BJ, Yu IJ (2009) Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 108(2):452–461. doi:10.1093/toxsci/kfn246
93. Takenaka S, Karg E, Roth C, Schulz H, Ziesenis A, Heinzmann U, Schramel P, Heyder J (2001) Pulmonary and systemic distribution of inhaled ultrafine silver particles in rats. Environ Health Perspect 109(4):547–551. doi:10.1007/s00204-010-0545-5
94. Tang J, Xiong L, Wang S, Wang J, Liu L, Li J, Yuan F, Xi T (2009) Distribution, translocation and accumulation of silver nanoparticles in rats. J Nanosci Nanotechnol 9(8):4924–4932. doi:10.1166/jnn.2009.1269
95. Tang J, Xiong L, Zhou G, Wang S, Wang J, Liu L, Li J, Yuan F, Lu S, Wan Z, Chou L, Xi T (2010) silver nanoparticles crossing through and distribution in the blood–brain barrier in vitro. J Nanosci Nanotechnol 10(10):6313–6317. doi:10.1166/jnn.2010.2625
96. Thum T, Bauersachs J (2006) Growth hormone regulates vascular function what we know from bench and bedside. Eur J Clin Pharmacol 62(1):29–32. doi:10.1007/s00228-005-0018-6
97. Tirapelli CR, Bonaventura D, Tirapelli LF, de-Oliveira AM (2009) Mechanisms underlying the vascular actions of endothelin 1, angiotensin II and bradykinin in the rat carotid. Pharmacology 84(2):111–126. doi:10.1159/000231974
98. Trickler WJ, Lantz SM, Murdock RC, Schrand AM, Robinson BL, Newport GD, Schlager JJ, Oldenburg SJ, Paule MG, Slikker W Jr, Hussain SM, Ali SF (2010) Silver nanoparticle induced blood–brain barrier inflammation and increased permeability in primary rat brain microvessel endothelial cells. Toxicol Sci 118(1):160–170. doi:10.1093/toxsci/kfq244
99. Tsai B, Wang M, Turrentine M, Mahomed Y, Brown JW, Meldrum DR (2004) Hypoxic pulmonary vasoconstriction in cardiothoracic surgery: basic mechanisms to potential therapies. Ann Thorac Surg 78(1):360–368. doi:10.1016/j.athoracsur.2003.11.035
100. Venema VJ, Marrero MB, Venema RC (1996) Bradykinin-stimulated protein tyrosine phosphorylation promotes endothelial nitric oxide synthase translocation to the cytoskeleton. Biochem Biophys Res Commun 226(3):703–710. doi:10.1006/bbrc.1996.1417
101. Westfall TC, Westfall DP (2011) Adrenergic agonists and antagonists. In: Brunton L (ed) Goodman and Gilman’s: the pharmacological basis of therapeutics, 12th edn. McGraw-Hill, New York, pp 277–333
102. Xu Y, Tang H, Liu JH, Wang H, Liu Y (2013) Evaluation of the adjuvant effect of silver nanoparticles both in vitro and in vivo. Toxicol Lett 219(1):42–48. doi:10.1016/j.toxlet.2013.02.010
103. Zamudio A, Elias A, Rodriguez-Manzo JA, Lopez-Urias F, Rodriguez-Gattorno G, Lupo F, Rühle M, Smith DJ, Terrones H, Diaz D, Terrones M (2006) Efficient anchoring of silver nanoparticles on N-doped carbon nanotubes. Small 2(3):346–350. doi:10.1002/smll.200500348
104. Zhang W, Zhang Q, Wang F, Yuan L, Jiang F, Liu Y (2014) Comparison of interactions between human serum albumin and silver nanoparticles of different sizes using spectroscopic methods. Luminescence. doi:10.1002/bio.2748
105. Zheng Y, He M, Congdon N (2012) The worldwide epidemic of diabetic retinopathy. Indian J Ophthalmol 60(5):428–431. doi:10.4103/0301-4738.100542
106. Zlokovic BV (2008) The blood–brain barrier in health and chronic neurodegenerative disorders. Neuron 57(2):178–201. doi:10.1016/j.neuron.2008.01.003