Promising low-toxicity of viologen-phosphorus dendrimers against embryonic mouse hippocampal cells

Molecules

Volumn 18, Issue 10, 2013, Pages 12222-12240

  Lazniewska, Joanna ^a   Janaszewska, Anna ^a   Miłowska, Katarzyna ^a   Caminade, Anne Marie ^b   Mignani, Serge ^c   Katir, Nadia ^b   Kadib, Abdelkrim El ^d   Bryszewska, Maria ^a   Majoral, Jean Pierre ^b   Gabryelak, Teresa ^a   Klajnert Maculewicz, Barbara ^a  

^a UNIVERSITY OF LODZ   (Poland)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d MOHAMMED V UNIVERSITY   (Morocco)

Author keywords

Apoptosis; Cytotoxicity; Hippocampal cell line; ROS; Viologen phosphorus Dendrimers

Indexed keywords

CATALASE; DENDRIMER; GLUTATHIONE; PHOSPHONIC ACID DERIVATIVE; REACTIVE OXYGEN METABOLITE; VIOLOGEN;

ANIMAL; APOPTOSIS; CELL CYCLE CHECKPOINT; CELL LINE; CELL SHAPE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; DRUG SCREENING; HIPPOCAMPUS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NERVE CELL; PHYSIOLOGY; TOXICITY; ARTICLE; DRUG EFFECT;

ANIMALS; APOPTOSIS; CATALASE; CELL CYCLE CHECKPOINTS; CELL LINE; CELL SHAPE; CELL SURVIVAL; DENDRIMERS; DRUG EVALUATION, PRECLINICAL; GLUTATHIONE; HIPPOCAMPUS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NEURONS; ORGANOPHOSPHONATES; REACTIVE OXYGEN SPECIES; VIOLOGENS;

EID: 84886635770     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules181012222     Document Type: Article

References (65)

1. Heinen, S.; Walder, L. Generation-Dependent Intramolecular CT complexation in a dendrimer electron sponge consisting of a viologen skeleton. Angew. Chem. Int. Ed. Engl. 2000, 39, 806-809.
2. Ghaddar, T.H.; Wishart, J.F.; Thompson, D.W.; Whitesell, J.K.; Fox, M.A. A dendrimer-based electron antenna: paired electron-transfer reactions in dendrimers with a 4,4'-bipyridine core and naphthalene peripheral groups. J. Am. Chem. Soc. 2002, 124, 8285-8289.
3. Bhattacharya, P.; Kaifer, A.E. Preparation, characterization, and electrochemical properties of a new series of hybrid dendrimers containing a viologen core and Frechet and Newkome dendrons. J. Org. Chem. 2008, 73, 5693-5698.
4. Asaftei, S.; De Clercq, E. "Viologen" dendrimers as antiviral agents: The effect of charge number and distance. J. Med. Chem. 2010, 53, 3480-3488.
5. Asaftei, S.; Huskens, D.; Schols, D. HIV-1 X4 activities of polycationic "viologen" based dendrimers by interaction with the chemokine receptor CXCR4: Study of structure-activity relationship. J. Med. Chem. 2012, 55, 10405-10413.
6. Ciepluch, K.; Katir, N.; El Kadib, A.; Felczak, A.; Zawadzka, K.; Weber, M.; Klajnert, B.; Lisowska, K.; Caminade, A.-M.; Bousmina, M.; et al. Biological properties of new viologenphosphorus dendrimers. Mol. Pharm. 2012, 9, 448-457.
7. Bromilow, R.H. Paraquat and sustainable agriculture. Pest. Manag. Sci. 2004, 60, 340-349.
8. Tanner, C.M.; Kamel, F.; Ross, G.W.; Hoppin, J.A.; Goldman, S.M.; Korell, M.; Marras, C.; Bhudhikanok, G.S.; Kasten, M.; Chade, A.R.;et al. Rotenone, paraquat, and Parkinson's disease. Environ. Health Perspect. 2011, 119, 866-872.
9. Baltazar, T.; Dinis-Oliveira, R.J.; Duarte, J.A.; de Lourdes Bastos, M.; Carvalho, F. Paraquat research: Do recent advances in limiting its toxicity make its use safer? Brit. J. Pharmacol. 2013, 168, 44-45.
10. Maksimenko, A.V.; Mandrouguine, V.; Gottikh, M.B.; Bertrand, J.-R.; Majoral, J.-P.; Malvy, C. Optimisation of dendrimer-mediated gene transfer by anionic oligomers. J. Gene. Med. 2003, 5, 61-71.
11. Krishna, T.R.; Parent, M.; Werts, M.H.V.; Moreaux, L.; Gmouh, S.; Charpak, S.; Caminade, A.-M.; Majoral, J.-P.; Blanchard-Desce, M. Water-soluble dendrimeric two-photon tracers for in vivo imaging. Angew. Chem. Int. Ed. Engl. 2006, 45, 4645-4648.
12. Blanzat, M.; Turrin, C.-O.; Aubertin, A.-M.; Couturier-Vidal, C.; Caminade, A.-M.; Majoral, J.-P.; Rico-Lattes, I.; Lattes, A. Dendritic catanionic assemblies: In vitro anti-HIV activity of phosphorus-containing dendrimers bearing galbeta1cer analogues. Chembiochem 2005, 6, 2207-2213.
13. Ottaviani, M.F.; Mazzeo, R.; Cangiotti, M.; Fiorani, L.; Majoral, J.-P.; Caminade, A.-M.; Pedziwiatr, E.; Bryszewska, M.; Klajnert, B. Time evolution of the aggregation process of peptides involved in neurodegenerative diseases and preventing aggregation effect of phosphorus dendrimers studied by EPR. Biomacromolecules 2010, 11, 3014-3021.
14. Wasiak, T.; Ionov, M.; Nieznanski, K.; Nieznanska, H.; Klementieva, O.; Granell, M.; Cladera, J.; Majoral, J.-P.; Caminade, A.-M.; Klajnert, B. Phosphorus dendrimers affect Alzheimer's (Aβ1-28) peptide and MAP-Tau protein aggregation. Mol. Pharm. 2012, 9, 458-469.
15. Gomulak, P.; Klajnert, B.; Bryszewska, M.; Majoral, J.P.; Caminade, A.M.; Blasiak, J. Cytotoxicity and genotoxicity of cationic phosphorus-containing dendrimers. Curr. Med. Chem. 2012, 19, 6233-6240.
16. Lazniewska, J.; Milowska, K.; Zablocka, M.; Mignani, S.; Caminade, A.-M.; Majoral, J.-P.; Bryszewska, M.; Gabryelak, T. Mechanism of cationic phosphorus dendrimers toxicity against murine neural cell lines. Mol. Pharm. 2013, doi:10.1021/mp4003255.
17. Lazniewska, J.; Milowska, K.; Katir, N.; El Kadib, A.; Bryszewska, M.; Majoral, J.-P.; Gabryelak, T. Viologen-phosphorus dendrimers exhibit minor toxicity against a murine neuroblastoma cell line. Cell. Mol. Biol. Lett. 2013, 18, 459-478.
18. Solassol, J.; Crozet, C.; Perrier, V.; Leclaire, J.; Béranger, F.; Caminade, A.-M.; Meunier, B.; Dormont, D.; Majoral, J.-P.; Lehmann, S. Cationic phosphorus-containing dendrimers reduce prion replication both in cell culture and in mice infected with scrapie. J. Gen. Virol. 2004, 85, 1791-1799.
19. Klajnert, B.; Cangiotti, M.; Calici, S.; Majoral, J.P.; Caminade, A.M.; Cladera, J.; Bryszewska, M.; Ottaviani, M.F. EPR study of the interactions between dendrimers and peptides involved in Alzheimer's and prion diseases. Macromol. Biosci. 2007, 7, 1065-1074.
20. Ghaemmaghami, S.; Ullman, J.; Ahn, M.; St Martin, S.; Prusiner, S.B. Chemical induction of misfolded prion protein conformers in cell culture. J. Biol. Chem. 2010, 285, 10415-10423.
21. Mignani, S.; Kazzouli, S.E.; Bousmina, M. Dendrimer space concept for innovative nanomedicine: A futuristic vision for medicinal chemistry. Prog. Polym. Sci. 2013, 38, 993-1008.
22. Milowska, K.; Grochowina, J.; Katir, N.; El Kadib, A.; Majoral, J.-P.; Bryszewska, M.; Gabryelak, T. Viologen-phosphorus dendrimers inhibit α-synuclein fibrillation. Mol. Pharm. 2013, 10, 1131-1137.
23. Ciepluch, K.; Weber, M.; Katir, N.; Caminade, A.-M.; El Kadib, A.; Klajnert, B.; Majoral, J.-P.; Bryszewska, M. Effect of viologen-phosphorus dendrimers on acetylcholinesterase and butyrylcholinesterase activities. Int. J. Biol. Macromol. 2013, 54C, 119-124.
24. Perez-Martinez, F.C.; Ocana, A.V.; Perez-Carrion, M.D.; Cena, V. Dendrimers as vectors for genetic material delivery to the nervous system. Curr. Med. Chem. 2012, 19, 5101-5108.
25. Patel, S.K.; Gajbhiye, V.; Jain, N.K. Synthesis, characterization and brain targeting potential of paclitaxel loaded thiamine-PPI nanoconjugates. J. Drug Targeting 2012, 20, 841-849.
26. Albertazzi, L.; Gherardini, L.; Brondi, M.; Sulis Sato, S.; Bifone, A.; Pizzorusso, T.; Ratto, G.M.; Bardi, G. In vivo distribution and toxicity of PAMAM dendrimers in the central nervous system depend on their surface chemistry. Mol. Pharm. 2013, 10, 249-260.
27. Dai, H.; Navath, R.S.; Balakrishnan, B.; Guru, B.R.; Mishra, M.K.; Romero, R.; Kannan, R.M.; Kannan, S. Intrinsic targeting of inflammatory cells in the brain by polyamidoamine dendrimers upon subarachnoid administration. Nanomedicine 2010, 5, 1317-1329.
28. Iezzi, R.; Guru, B.R.; Glybina, I.V.; Mishra, M.K.; Kennedy, A.; Kannan, R.M. Dendrimer-based targeted intravitreal therapy for sustained attenuation of neuroinflammation in retinal degeneration. Biomaterials 2012, 33, 979-988.
29. Kannan, S.; Dai, H.; Navath, R.S.; Balakrishnan, B.; Jyoti, A.; Janisse, J.; Romero, R.; Kannan, R.M. Dendrimer-based postnatal therapy for neuroinflammation and cerebral palsy in a rabbit model. Sci. Transl. Med. 2012, 4, 130ra46.
30. Gingerich, S.; Kim, G.L.; Chalmers, J.A.; Koletar, M.M.; Wang, X.; Wang, Y.; Belsham, D.D. Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 2010, 170, 54-66.
31. Majd, S.; Chegini, F.; Chataway, T.; Zhou, X.-F.; Gai, W. Reciprocal induction between α-synuclein and β-amyloid in adult rat neurons. Neurotox. Res. 2013, 23, 69-78.
32. Naha, P.C.; Davoren, M.; Lyng, F.M.; Byrne, H.J. Reactive oxygen species (ROS) induced cytokine production and cytotoxicity of PAMAM dendrimers in J774A.1 cells. Toxicol. Appl. Pharmacol. 2010, 246, 91-99.
33. Malik, N.; Wiwattanapatapee, R.; Klopsch, R.; Lorenz, K.; Frey, H.; Weener, J.W.; Meijer, E.W.; Paulus, W.; Duncan, R. Dendrimers: relationship between structure and biocompatibility in vitro, and preliminary studies on the biodistribution of 125I-labelled polyamidoamine dendrimers in vivo. J. Control. Release 2000, 65, 133-148.
34. Stasko, N.A.; Johnson, C.B.; Schoenfisch, M.H.; Johnson, T.A.; Holmuhamedov, E.L. Cytotoxicity of polypropylenimine dendrimer conjugates on cultured endothelial cells. Biomacromolecules 2007, 8, 3853-3859.
35. Albertazzi, L.; Serresi, M.; Albanese, A.; Beltram, F. Dendrimer internalization and intracellular trafficking in living cells. Mol. Pharm. 2010, 7, 680-688.
36. Hong, S.; Leroueil, P.R.; Janus, E.K.; Peters, J.L.; Kober, M.-M.; Islam, M.T.; Orr, B.G.; Baker, J.R.; Banaszak Holl, M.M. Interaction of polycationic polymers with supported lipid bilayers and cells: Nanoscale hole formation and enhanced membrane permeability. Bioconjugate Chem.2006, 17, 728-734.
37. Leroueil, P.R.; Hong, S.; Mecke, A.; Baker, J.R.; Orr, B.G.; Banaszak Holl, M.M. Nanoparticle interaction with biological membranes: does nanotechnology present a Janus face? Acc. Chem. Res. 2007, 40, 335-342.
38. Albertazzi, L.; Fernandez-Villamarin, M.; Riguera, R.; Fernandez-Megia, E. Peripheral functionalization of dendrimers regulates internalization and intracellular trafficking in living cells. Bioconjugate Chem. 2012, 23, 1059-1068.
39. Mathers, J.; Fraser, J.A.; McMahon, M.; Saunders, R.D.C.; Hayes, J.D.; McLellan, L.I. Antioxidant and cytoprotective responses to redox stress. Biochem. Soc. Symp. 2004, 71, 157-176.
40. Circu, M.L.; Aw, T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48, 749-762.
41. Wang, W.; Xiong, W.; Wan, J.; Sun, X.; Xu, H.; Yang, X. The decrease of PAMAM dendrimerinduced cytotoxicity by PEGylation via attenuation of oxidative stress. Nanotechnology 2009, 20, 105103.
42. Kuo, J.-H.S.; Jan, M.-S.; Lin, Y.-L. Interactions between U-937 human macrophages and poly(propyleneimine) dendrimers. J. Control. Release 2007, 120, 51-59.
43. Janaszewska, A.; Ma̧czyńska, K.; Matuszko, G.; Appelhans, D.; Voit, B.; Klajnert, B.; Bryszewska, M. Cytotoxicity of PAMAM, PPI and maltose modified PPI dendrimers in Chinese hamster ovary (CHO) and human ovarian carcinoma (SKOV3) cells. New J. Chem. 2012, 36, 428-437.
44. Mukherjee, S.P.; Lyng, F.M.; Garcia, A.; Davoren, M.; Byrne, H.J. Mechanistic studies of in vitro cytotoxicity of poly(amidoamine) dendrimers in mammalian cells. Toxicol. Appl. Pharmacol. 2010, 248, 259-268.
45. Mukherjee, S.P.; Byrne, H.J. Polyamidoamine dendrimer nanoparticle cytotoxicity, oxidative stress, caspase activation and inflammatory response: experimental observation and numerical simulation. Nanomed. Nanotech. Biol. Med. 2012, 9, 202-211.
46. Simon, H.-U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415-418.
47. Giovannini, C.; Matarrese, P.; Scazzocchio, B.; Sanchez, M.; Masella, R.; Malorni, W. Mitochondria hyperpolarization is an early event in oxidized low-density lipoprotein-induced apoptosis in Caco-2 intestinal cells. FEBS Lett. 2002, 523, 200-206.
48. Lee, J.-H.; Cha, K.E.; Kim, M.S.; Hong, H.W.; Chung, D.J.; Ryu, G.; Myung, H. Nanosized polyamidoamine (PAMAM) dendrimer-induced apoptosis mediated by mitochondrial dysfunction. Toxicol. Lett. 2009, 190, 202-207.
49. Thomas, T.P.; Majoros, I; Kotlyar, A.; Mullen, D; Banaszak Holl, M.M.; Baker, J.R. Cationic poly(amidoamine) dendrimer induces lysosomal apoptotic pathway at therapeutically relevant concentrations. Biomacromolecules 2009, 10, 3207-3214.
50. Kitchens, K.M.; Kolhatkar, R.B.; Swaan, P.W.; Ghandehari, H. Endocytosis inhibitors prevent poly(amidoamine) dendrimer internalization and permeability across Caco-2 cells. Mol. Pharm. 2008, 5, 364-369.
51. Parimi, S.; Barnes, T.J.; Callen, D.F.; Prestidge, C.A. Mechanistic insight into cell growth, internalization, and cytotoxicity of PAMAM dendrimers. Biomacromolecules 2010, 11, 382-389.
52. Klajnert, B.; Sadowska, M.; Bryszewska, M. The effect of polyamidoamine dendrimers on human erythrocyte membrane acetylcholinesterase activity. Bioelectrochemistry 2004, 65, 23-26.
53. Ciolkowski, M.; Rozanek, M.; Szewczyk, M.; Klajnert, B.; Bryszewska, M. The influence of PAMAM-OH dendrimers on the activity of human erythrocytes ATPases. Biochim. Biophys. Acta 2011, 1808, 2714-2723.
54. Ciolkowski, M.; Rozanek, M.; Bryszewska, M.; Klajnert, B. The influence of PAMAM dendrimers surface groups on their interaction with porcine pepsin. Biochim. Biophys. Acta 2013, 1834, 1982-1987.
55. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol. 2007, 35, 495-516.
56. Bernas, T.; Dobrucki, J. Mitochondrial and nonmitochondrial reduction of MTT: interaction of MTT with TMRE, JC-1, and NAO mitochondrial fluorescent probes. Cytometry 2002, 47, 236-242.
57. Janaszewska, A.; Ciolkowski, M.; Wróbel, D.; Petersen, J.F.; Ficker, M.; Christensen, J.B.; Bryszewska, M.; Klajnert, B. Modified PAMAM dendrimer with 4-carbomethoxypyrrolidone surface groups reveals negligible toxicity against three rodent cell-lines. Nanomed. Nanotech. Biol. Med. 2013, 9, 461-464.
58. Bartosz, G. Use of spectroscopic probes for detection of reactive oxygen species. Clin. Chim. Acta 2006, 368, 53-76.
59. Agnello, M.; Morici, G.; Rinaldi, A.M. A method for measuring mitochondrial mass and activity. Cytotechnology 2008, 56, 145-149.
60. Salvioli, S.; Ardizzoni, A.; Franceschi, C.; Cossarizza, A. JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 1997, 411, 77-82.
61. Michałowicz, J.; Sicińska, P. Chlorophenols and chlorocatechols induce apoptosis in human lymphocytes (in vitro). Toxicol. Lett. 2009, 191, 246-252.
62. Ribble, D.; Goldstein, N.B.; Norris, D.A.; Shellman, Y.G. A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol. 2005, 5, 12.
63. Chang, K.-L.; Kung, M.-L.; Chow, N.-H.; Su, S.-J. Genistein arrests hepatoma cells at G2/M phase: involvement of ATM activation and upregulation of p21waf1/cip1 and Wee1. Biochem. Pharmacol. 2004, 67, 717-726.
64. Milowska, K.; Grochowina, J.; Katir, N.; El Kadib, A.; Majoral, J.-P.; Bryszewska, M.; Gabryelak, T. Interaction between viologen-phosphorus dendrimers and α-synuclein. J. Luminesc. 2013, 134, 132-137.
65. Milowska, K.; Gabryelak, T.; Bryszewska, M.; Caminade, A.-M.; Majoral, J.-P. Phosphorus-containing dendrimers against α-synuclein fibril formation. Int. J. Biol. Macromol. 2012, 50, 1138-1143.