Acidic Nanoparticles Are Trafficked to Lysosomes and Restore an Acidic Lysosomal pH and Degradative Function to Compromised ARPE-19 Cells

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Baltazar, Gabriel C ^a   Guha, Sonia ^a   Lu, Wennan ^a   Lim, Jason ^a   Boesze Battaglia, Kathleen ^a   Laties, Alan M ^a   Tyagi, Puneet ^b   Kompella, Uday B ^b   Mitchell, Claire H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORON DIPYYROMETHENE DIFLUORIDE; CATHEPSIN D; CHLOROQUINE; FLUORESCENT DYE; LIPOFUSCIN; LYSOSOME ENZYME; NANOPARTICLE; OPSIN; PEPSTATIN; POLYGLACTIN; POLYLACTIDE; UNCLASSIFIED DRUG;

ACIDIFICATION; ARTICLE; AUTOFLUORESCENCE; BIOACCUMULATION; CELL FUNCTION; CELL LEVEL; CELL MIGRATION; CELL PH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LYSOSOME; PIGMENT EPITHELIUM; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

ANIMALS; BORON COMPOUNDS; CATALYTIC DOMAIN; CATHEPSIN D; CATTLE; CELL LINE; CELLS, CULTURED; CHLOROQUINE; FLOW CYTOMETRY; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOBLOTTING; LACTIC ACID; LIPOFUSCIN; LYSOSOMES; NANOPARTICLES; NANOTECHNOLOGY; OPSINS; PEPSTATINS; PHAGOCYTOSIS; POLYGLYCOLIC ACID; POLYMERS; RETINA;

EID: 84871336127     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049635     Document Type: Article

References (40)

1. Baltazar G, Guha S, Laties AM, Tyagi P, Kompella UB, et al. (2011) Acidic nanoparticles enhance degradative lysosomal enzyme activity in compromised RPE cells. Invest Ophthalmol Vis Sci 52: 3216. ARVO E-Abstract.
2. Baltazar G, Guha S, Laties AM, Kompella UB, Mitchell CH (2010) Acidification of RPE Lysosomes by Nanoparticles. Invest Ophthalmol Vis Sci 51: 700. ARVO-E-Abstract.
3. LaVail MM, (1976) Rod outer segment disc shedding in relation to cyclic lighting. Exp Eye Res 23: 277-280.
4. Wang AL, Lukas TJ, Yuan M, Du N, Tso MO, et al. (2009) Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration. PLoS One 4: e4160.
5. Liu J, Lu W, Reigada D, Nguyen J, Laties AM, et al. (2008) Restoration of lysosomal pH in RPE cells from cultured human and ABCA4(-/-) mice: pharmacologic approaches and functional recovery. Invest Ophthalmol Vis Sci 49: 772-780.
6. Chen Y, Schindler M, Simon SM, (1999) A mechanism for tamoxifen-mediated inhibition of acidification. J Biol Chem 274: 18364-18373.
7. Peters S, Reinthal E, Blitgen-Heinecke P, Bartz-Schmidt KU, Schraermeyer U, (2006) Inhibition of lysosomal degradation in retinal pigment epithelium cells induces exocytosis of phagocytic residual material at the basolateral plasma membrane. Ophthal Res 38: 83-88.
8. Holz FG, Schutt F, Kopitz J, Eldred GE, Kruse FE, et al. (1999) Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 40: 737-743.
9. Hayasaka S, Hara S, Mizuno K, (1977) Partial purification and properties of acid lipase in the bovine retinal pigment epithelium. Exp Eye Res 25: 317-324.
10. Ameis D, Merkel M, Eckerskorn C, Greten H, (1994) Purification, characterization and molecular cloning of human hepatic lysosomal acid lipase. Eur J Biochem 219: 905-914.
11. Barrett A (1977) Protinases in mammalian cells and tissues; Dingle JT, editor. New York: Elsiver/North-Hollard Biomedical press. p 220-224 p.
12. Sparrow JR, Boulton M, (2005) RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 80: 595-606.
13. Elner VM, (2002) Retinal pigment epithelial acid lipase activity and lipoprotein receptors: effects of dietary omega-3 fatty acids. Trans Am Ophthalmol Soc 100: 301-338.
14. Siakotos AN, Armstrong D, Koppang N, Connole E, (1978) Studies on the retina and the pigment epithelium in hereditary canine ceroid lipofuscinosis. II. The subcellular distribution of lysosomal hydrolases and other enzymes. Invest Ophthalmol Vis Sci 17: 618-633.
15. Liu J, Lu W, Guha S, Baltazar GC, Coffey EE, et al. (2012) Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Contributes to Reacidification of Alkalinized Lysosomes in RPE Cells Am J Physiol Cell Physiol. 303: C160-C169.
16. Guha S, Baltazar GC, Tu LA, Liu J, Lim JC, et al. (2012) Stimulation of the D5 dopamine receptor acidifies the lysosomal pH of retinal pigmented epithelial cells and decreases accumulation of autofluorescent photoreceptor debris. J Neurochem 122: 823-833.
17. Diebold Y, Calonge M, (2010) Applications of nanoparticles in ophthalmology. Prog Retin Eye Res 29: 596-609.
18. Kompella UB, (2007) Nanotechnology for drug and gene delivery to the eye. Nanomedicine-Nanotechnology Biology and Medicine 3: 342-342.
19. Roizenblatt R, Weiland JD, Carcieri S, Qiu GT, Behrend M, et al. (2006) Nanobiolistic delivery of indicators to the living mouse retina. J Neuroscience Methods 153: 154-161.
20. Bejjani RA, BenEzra D, Cohen H, Rieger J, Andrieu C, et al. (2005) Nanoparticles for gene delivery to retinal pigment epithelial cells. Mol Vis 11: 124-132.
21. Prow TW, Bhutto I, Kim SY, Grebe R, Merges C, et al. (2008) Ocular nanoparticle toxicity and transfection of the retina and retinal pigment epithelium. Nanomedicine 4: 340-349.
22. Singh SR, Grossniklaus HE, Kang SJ, Edelhauser HF, Ambati BK, et al. (2009) Intravenous transferrin, RGD peptide and dual-targeted nanoparticles enhance anti-VEGF intraceptor gene delivery to laser-induced CNV. Gene Ther 16: 645-659.
23. Li W, Zhao L, Wei T, Zhao Y, Chen C, (2011) The inhibition of death receptor mediated apoptosis through lysosome stabilization following internalization of carboxyfullerene nanoparticles. Biomaterials 32: 4030-4041.
24. Panyam J, Zhou WZ, Prabha S, Sahoo SK, Labhasetwar V, (2002) Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery. FASEB J 16: 1217-1226.
25. Hjelmeland LM, Dunn KC, Marmorstein AD, Bonilha VL, Rodriguez-Boulan E, et al. (1998) Use of the ARPE-19 cell line as a model of RPE polarity: Basolateral secretion of FGF5. Invest Ophthalmol Vis Sci 39: 2744-2749.
26. Chen CS, Chen WNU, Zhou MJ, Arttamangkul S, Haugland RP, (2000) Probing the cathepsin D using a BODIPY EL-pepstatin A: applications in fluorescence polarization and microscopy. Journal of Biochemical and Biophysical Methods 42: 137-151.
27. Finnemann SC, Bonilha VL, Marmorstein AD, Rodriguez-Boulan E, (1997) Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc Natl Acad Sci U S A 94: 12932-12937.
28. Hall MO, Abrams T, (1987) Kinetic studies of rod outer segment binding and ingestion by cultured rat RPE cells. Exp Eye Res 45: 907-922.
29. Hall MO, Abrams TA, Mittag TW, (1993) The phagocytosis of rod outer segments is inhibited by drugs linked to cyclic adenosine monophosphate production. Invest Ophthalmol Vis Sci 34: 2392-2401.
30. Lu W, Reigada D, Sevigny J, Mitchell CH, (2007) Stimulation of the P2Y1 receptor up-regulates nucleoside-triphosphate diphosphohydrolase-1 in human retinal pigment epithelial cells. J Pharmacol Exp Ther 323: 157-164.
31. de Duve C, de Barsy T, Poole B, Trouet A, Tulkens P, et al. (1974) Commentary. Lysosomotropic agents. Biochem Pharmacol 23: 2495-2531.
32. Krogstad DJ, Schlesinger PH, (1987) The basis of antimalarial action: non-weak base effects of chloroquine on acid vesicle pH. Am J Trop Med Hyg 36: 213-220.
33. Chen PM, Gombart ZJ, Chen JW, (2011) Chloroquine treatment of ARPE-19 cells leads to lysosome dilation and intracellular lipid accumulation: possible implications of lysosomal dysfunction in macular degeneration. Cell Biosci 1: 10.
34. Hayasaka S, Hara S, Mizuno K, (1975) Degradation of rod outer segment proteins by cathepsin D. J Biochem. 78: 1365-1367.
35. Luo JT, Xiao K, Li YP, Lee JS, Xiao WW, et al. (2011) The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials 32: 3435-3446.
36. Blanchette CD, Woo YH, Thomas C, Shen N, Sulchek TA, et al. (2009) Decoupling internalization, acidification and phagosomal-endosomal/lysosomal fusion during phagocytosis of InlA coated beads in epithelial cells. PLoS One 4: e6056.
37. Hasilik A, Neufeld EF, (1980) Biosynthesis of lysosomal enzymes in fibroblasts. Phosphorylation of mannose residues. J Biol Chem 255: 4946-4950.
38. Deguchi J, Yamamoto A, Yoshimori T, Sugasawa K, Moriyama Y, et al. (1994) Acidification of phagosomes and degradation of rod outer segments in rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 35: 568-579.
39. Behar-Cohen FF, Bourges JL, Gautier SE, Delie F, Bejjani RA, et al. (2003) Ocular drug delivery targeting the retina and retinal pigment epithelium using polylactide nanoparticles. Invest Ophthalmol Vis Sci 44: 3562-3569.
40. Zhao Y, Fu J, Ng DK, Wu C, (2004) Formation and degradation of poly(D,L-lactide) nanoparticles and their potential application as controllable releasing devices. Macromol Biosci 4: 901-906.