Knocking down hmgb1 using dendrimer-delivered sirna unveils its key role in nmda-induced autophagy in rat cortical neurons

Pharmaceutical Research

Volumn 30, Issue 10, 2013, Pages 2584-2595

  Pérez Carrión, María D ^a,b   Ceña, Valentín ^a,b,c  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Universidad de Castilla La Mancha   (Spain)

Author keywords

autophagy; dendrimer; excitotoxicity; neurons; siRNA

Indexed keywords

BECLIN 1; DENDRIMER; HIGH MOBILITY GROUP B1 PROTEIN; SMALL INTERFERING RNA; TRANSGEDEN DENDRIMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN NERVE CELL; COMPLEX FORMATION; CONTROLLED STUDY; EXCITOTOXICITY; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; RNA INTERFERENCE;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; CELL FRACTIONATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DENDRIMERS; DRUG CARRIERS; GENE KNOCKDOWN TECHNIQUES; HMGB1 PROTEIN; NEURONS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, SMALL INTERFERING;

EID: 84883859344     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-013-1049-9     Document Type: Article

References (47)

1. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290(5497):1717-21.
2. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008;9(12):1004-10.
3. Marino G, Madeo F, Kroemer G. Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol. 2011;23(2):198-206.
4. Perez-Carrion MD, Perez-Martinez FC, Merino S, Sanchez-Verdu P, Martinez-Hernandez J, Lujan R, et al. Dendrimer-mediated siRNA delivery knocks down Beclin 1 and potentiates NMDA-mediated toxicity in rat cortical neurons. J Neurochem. 2012;120(2):259-68.
5. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci. 2010;13(7):805-11.
6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A. 1995;92(16):7162-6.
7. White RJ, Reynolds IJ. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci. 1996;16(18):5688-97.
8. Bossy-Wetzel E, Green DR. Assays for cytochrome c release from mitochondria during apoptosis. Methods Enzymol. 2000;32(2):235-42.
9. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, et al. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ. 2005;12(2):162-76.
10. Wang Y, Han R, Liang ZQ, Wu JC, Zhang XD, Gu ZL, et al. An autophagic mechanism is involved in apoptotic death of rat striatal neurons induced by the non-N-methyl-D-aspartate receptor agonist kainic acid. Autophagy. 2008;4(2):214-26.
11. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem. 2000;275(51):40096-105.
12. Huttunen HJ, Kuja-Panula J, Rauvala H. Receptor for advanced glycation end products (RAGE) signaling induces CREB-dependent chromogranin expression during neuronal differentiation. J Biol Chem. 2002;277(41):38635-46.
13. Ulloa L, Messmer D. High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev. 2006;17(3):189-201.
14. Muller S, Scaffidi P, Degryse B, Bonaldi T, Ronfani L, Agresti A, et al. New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J. 2001;20(16):4337-40.
15. Hock R, Furusawa T, Ueda T, Bustin M. HMG chromosomal proteins in development and disease. Trends Cell Biol. 2007;17(2):72-9.
16. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med. 2000;192(4):565-70.
17. Tang D, Shi Y, Kang R, Li T, Xiao W, Wang H, et al. Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J Leukoc Biol. 2007;81(3):741-7.
18. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191-5.
19. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 2003;22(20):5551-60.
20. Tang D, Kang R, Zeh III HJ, Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal. 2011;14(7):1315-35.
21. Aigner A. Gene silencing through RNA interference (RNAi) in vivo: strategies based on the direct application of siRNAs. J Biotechnol. 2006;124(1):12-25.
22. Perez-Martinez FC, Guerra J, Posadas I, Ceña V. Barriers to non-viral vector-mediated gene delivery in the nervous system. Pharm Res. 2011;28(8):1843-58.
23. Posadas I, Guerra FJ, Ceña V. Nonviral vectors for the delivery of small interfering RNAs to the CNS. Nanomedicine (Lond). 2010;5(8):1219-36.
24. Rodrigo AC, Rivilla I, Perez-Martinez FC, Monteagudo S, Ocana V, Guerra J, et al. Efficient, non-toxic hybrid PPV-PAMAM dendrimer as a gene carrier for neuronal cells. Biomacromolecules. 2011;12(4):1205-13.
25. Posadas I, Perez-Martinez FC, Guerra J, Sanchez-Verdu P, Ceña V. Cofilin activation mediates Bax translocation to mitochondria during excitotoxic neuronal death. J Neurochem. 2012;120(4):515-27.
26. Lopez-Hernandez B, Posadas I, Podlesniy P, Abad MA, Trullas R, Ceña V. HIF-1alpha is neuroprotective during the early phases of mild hypoxia in rat cortical neurons. Exp Neurol. 2012;233(1):543-54.
27. Posadas I, Vellecco V, Santos P, Prieto-Lloret J, Ceña V. Acetaminophen potentiates staurosporine-induced death in a human neuroblastoma cell line. Br J Pharmacol. 2007;150(5):577-85.
28. Sagar AJ, Pandit MW. Denaturation studies on bovine pancreatic ribonuclease. Effect of trichloroacetic acid. Biochim Biophys Acta. 1983;743(3):303-9.
29. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, et al. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res. 2005;65(8):3336-46.
30. Fernandez M, Segura MF, Sole C, Colino A, Comella JX, Ceña V. Lifeguard/neuronal membrane protein 35 regulates Fas ligand-mediated apoptosis in neurons via microdomain recruitment. J Neurochem. 2007;103(1):190-203.
31. Posadas I, Lopez-Hernandez B, Clemente MI, Jimenez JL, Ortega P, de la Mata J, et al. Highly efficient transfection of rat cortical neurons using carbosilane dendrimers unveils a neuroprotective role for HIF-1alpha in early chemical hypoxia-mediated neurotoxicity. Pharm Res. 2009;26(5):1181-91.
32. Perez-Martinez FC, Carrion B, Lucio MI, Rubio N, Herrero MA, Vazquez E, et al. Enhanced docetaxel-mediated cytotoxicity in human prostate cancer cells through knockdown of cofilin-1 by carbon nanohorn delivered siRNA. Biomaterials. 2012;33(32):8152-9.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-8.
34. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007;3(6):542-5.
35. Munafo DB, Colombo MI. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J Cell Sci. 2001;114(Pt 20):3619-29.
36. Rothman SM, Olney JW. Excitotoxicity and the NMDA receptor-still lethal after eight years. Trends Neurosci. 1995;18(2):57-8.
37. Lipton SA, Rosenberg PA. Excitatory amino-acids as a final common pathway for neurologic disorders. N Engl J Med. 1994;330(9):613-22.
38. Mattson MP. Calcium and neurodegeneration. Aging Cell. 2007;6(3):337-50.
39. Bustin M, Neihart NK. Antibodies against chromosomal HMG proteins stain the cytoplasm of mammalian cells. Cell. 1979;16(1):181-9.
40. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 2002;3(10):995-1001.
41. Kim JB, Sig CJ, Yu YM, Nam K, Piao CS, Kim SW, et al. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci. 2006;26(24):6413-21.
42. Sadasivan S, Zhang Z, Larner SF, Liu MC, Zheng W, Kobeissy FH, et al. Acute NMDA toxicity in cultured rat cerebellar granule neurons is accompanied by autophagy induction and late onset autophagic cell death phenotype. BMC Neurosci. 2010;1121.
43. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122(6):927-39.
44. Aagaard L, Rossi JJ. RNAi therapeutics: principles, prospects and challenges. Adv Drug Deliv Rev. 2007;59(2-3):75-86.
45. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441(7095):885-9.
46. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest. 2008;118(6):2190-9.
47. Shibata M, Lu T, Furuya T, Degterev A, Mizushima N, Yoshimori T, et al. Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem. 2006;281(20):14474-85.