Autophagic Vacuolation Induced by Excess ROS Generation in HABP1/p32/gC1qR Overexpressing Fibroblasts and Its Reversal by Polymeric Hyaluronan

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Saha, Paramita ^a   Chowdhury, Anindya Roy ^a   Dutta, Shubhra ^a   Chatterjee, Soumya ^a   Ghosh, Ilora ^a   Datta, Kasturi ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGIC MODULATOR; BAFILOMYCIN A1; BECLIN 1; CELL PROTEIN; DANSYLCADAVERINE; DRAM PROTEIN; HYALURONAN BINDING PROTEIN 1; HYALURONIC ACID; MAP LC3 II PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL CULTURE; CELL VACUOLE; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME INHIBITION; FIBROBLAST; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UPREGULATION;

ANIMALS; ANTIGENS, CD44; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HYALURONIC ACID; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LEUPEPTINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, ELECTRON, TRANSMISSION; RATS; REACTIVE OXYGEN SPECIES; VACUOLES;

EID: 84885698888     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078131     Document Type: Article

References (70)

1. Sato H, Takahashi T, Ide H, Fukushima T, Tabata M, et al. (1988) Antioxidant Activity of Synovial Fluid, Hyaluronic Acid, And Two Subcomponents Of Hyaluronic Acid. Arthritis Rheum 31: 63-71. doi:10.1002/art.1780310110. PubMed: 3345232.
2. Artola A, Alio JL, Bellot JL, Ruiz JM, (1993) Lipid peroxidation in the iris and its protection by means of viscoelastic substances (sodium hyaluronate and hydroxypropylmethylcellulose). Ophthal Res 25: 172-176. doi:10.1159/000267286.
3. Campo GM, Avenoso A, Campo S, D'Ascola A, Traina P, et al. (2008) NF-kB and caspases are involved in the hyaluronan and chondroitin-4-sulphate-exerted antioxidant effect in fibroblast cultures exposed to oxidative stress. J Appl Toxicol 28: 509-517. doi:10.1002/jat.1302. PubMed: 17879260.
4. Hascall VC, Majors AK, De La Motte CA, Evanko SP, Wang A, et al. (2004) Intracellular hyaluronan: a new frontier for inflammation? Biochim Biophys Acta 1673: 3-12. doi:10.1016/j.bbagen.2004.02.013. PubMed: 15238245.
5. Hawkins CL, Davies MJ, (1998) Degradation of hyaluronic acid, poly and mono-saccharides, and model compounds by hypochlorite: Evidence for radical intermediates and fragmentation. Free Radic Biol Med 24: 1396-1410. doi:10.1016/S0891-5849(98)00009-4. PubMed: 9641257.
6. Rees MD, Hawkins CL, Davies MJ, (2003) Hypochlorite-mediated fragmentation of hyaluronan, chondroitin sulfates, and related N-acetyl glycosamines: Evidence for chloramide intermediates, free radical transfer reactions, and site-specific fragmentation. J Am Chem Soc 125: 13719-13733. doi:10.1021/ja0370591. PubMed: 14599211.
7. Ghatak S, Misra S, Toole BP, (2002) Hyaluronan oligosaccharides inhibit anchorage independent growth of tumor cells by suppressing the phosphoinositide3-kinase/akt survival pathway. J Biol Chem 277: 38013-38020. doi:10.1074/jbc.M202404200. PubMed: 12145277.
8. Ghatak S, Misra S, Toole BP, (2005) Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J Biol Chem 11: 8875-8883. PubMed: 15632176.
9. Kaul R, Saha P, Saradhi M, LARC Prasad, Chatterjee Set al. (2012) Overexpression of Hyaluronan Binding Protein 1 (HABP1/p32/gC1qR) in HepG2 Cell Leads to Increased Hyaluronan Synthesis and Cell Proliferation by Upregulation of Cyclin D1 in AKT-Dependent Pathway. J Biol Chem 287: 19750-19764. doi:10.1074/jbc.M111.266270. PubMed: 22451658.
10. Toole BP, (1990) Hyaluronan and its binding proteins, the hyaladherins. Curr Opin Cell Biol 2: 839-844. doi:10.1016/0955-0674(90)90081-O. PubMed: 1707285.
11. Krainer AR, Mayeda A, Kozak D, Binns G, (1991) Functional expression of cloned human splicing factor SF2. Homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66: 383-394. doi:10.1016/0092-8674(91)90627-B. PubMed: 1830244.
12. Deb TB, Datta K, (1996) Molecular cloning of human fibroblast hyaluronic acid-binding protein confirms its identity with P-32, a protein co-purified with splicing factor SF2. J Biol Chem 271: 2206-2212. doi:10.1074/jbc.271.4.2206. PubMed: 8567680.
13. Ghebrehiwet B, Lim BL, Peerschke EI, Willis AC, Reid KB, (1994) Isolation, cDNA cloning, and overexpression of a 33-kDa cell surface glycoprotein that binds to the globular heads" of C1q. J Exp Med 179: 1809-1821. doi:10.1084/jem.179.6.1809. PubMed: 8195709.
14. Majumdar M, Datta K, (1998) Assignment of cDNA encoding hyaluronic acid-binding protein 1 to human chromosome 17p12-p13. Genomics 51: 476-477. doi:10.1006/geno.1998.5364. PubMed: 9721222.
15. Jiang J, Zhang Y, Krainer AR, Xu RM, (1999) Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc Natl Acad Sci U S A 96: 3572-3577. doi:10.1073/pnas.96.7.3572. PubMed: 10097078.
16. Chowdhury AR, Ghosh I, Datta K, (2008) Excessive reactive oxygen species induces apoptosis in fibroblasts: Role of mitochondrially accumulated Hyaluronic acid binding protein 1 (HABP1/p32/gC1qR). Exp Cell Res 314: 651-667. doi:10.1016/j.yexcr.2007.10.033. PubMed: 18166172.
17. Prakash M, Kale S, Ghosh I, Kundu GC, Datta K, (2011) Hyaluronan-binding protein 1 (HABP1/p32/gC1qR) induces melanoma cell migration and tumor growth by NF-kappa B dependent MMP-2 activation through integrin α(v)β(3) interaction. Cell Signal 23: 1563-1577. doi:10.1016/j.cellsig.2011.04.009. PubMed: 21627988.
18. Yagi M, Uchiumi T, Takazaki S, Okuno B, Nomura M, et al. (2012) Retrieved onpublished at whilst December(year 1111) from p32/gC1qR is indispensable for fetal development and mitochondrial translation: importance of its RNA-binding ability. Nucleic Acids Res 40: 9717-9737.
19. Majumdar M, Meenakshi J, Goswami SK, Datta K, (2002) Hyaluronan binding protein 1 (HABP1)/C1QBP/p32 is an endogenous substrate for MAP kinase and is translocated to the nucleus upon mitogenic stimulation. Biochem Biophys Res Commun 291: 829-833. doi:10.1006/bbrc.2002.6491. PubMed: 11866440.
20. Meenakshi J, Anupama, Goswami SK, Datta K, (2003) Constitutive expression of hyaluronan binding protein 1 (HABP1/p32/gC1qR) in normal fibroblast cells perturbs its growth characteristics and induces apoptosis. Biochem Biophys Res Commun 300: 686-693. doi:10.1016/S0006-291X(02)02788-2. PubMed: 12507504.
21. Haas AL, Rose IA, (1982) The mechanism of ubiquitin activating enzyme: A kinetic and equilibrium analysis. J Biol Chem 257: 10329-10337. PubMed: 6286650.
22. de Duve C, Wattiaux R, (1966) Function of lysosome. Annu Rev Physiol 28: 435-492. doi:10.1146/annurev.ph.28.030166.002251. PubMed: 5322983.
23. Levine B, (2007) Cell Biology: Autophagy and Cancer. Nature 446: 745-747. doi:10.1038/446745a. PubMed: 17429391.
24. Rubinsztein DC, (2007) Autophagy induction rescues toxicity induced by proteasome inhibition. Neuron 54: 854-856. doi:10.1016/j.neuron.2007.06.005. PubMed: 17582326.
25. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, et al. (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760. doi:10.1038/sj.emboj.7601623. PubMed: 17347651.
26. Scherz-Shouval R, Elazar Z, (2007) ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 17: 422-427. doi:10.1016/j.tcb.2007.07.009. PubMed: 17804237.
27. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB, (2007) Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 120: 4155-4166. doi:10.1242/jcs.011163. PubMed: 18032788.
28. Azad MB, Chen Y, Gibson SB, (2009) Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 11: 777-790. doi:10.1089/ars.2008.2270. PubMed: 18828708.
29. Petiot A, Ogier-Denis E, Blommaart EFC, Meijer AJ, Codogno P, (2000) Distinct classes of phosphatidylinositol 3-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275: 992-998. doi:10.1074/jbc.275.2.992. PubMed: 10625637.
30. Arico S, Petiot A, Bauvy C, Dubbelhuis PF, Meijer AJ, et al. (2001) The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the Phosphatidylinositol 3-kinase/Protein kinase B pathway. J Biol Chem 276: 35243-35246. doi:10.1074/jbc.C100319200. PubMed: 11477064.
31. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, et al. (1999) Induction of autophagy and inhibition of tumorigenesis by Beclin 1. Nature 402: 672-667. doi:10.1038/45257. PubMed: 10604474.
32. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T, (2001) Beclin- phosphatidylinositol 3-kinase complex functions at the trans- Golgi network. EMBO Rep 2: 330-335. doi:10.1093/embo-reports/kve061. PubMed: 11306555.
33. Reef S, Zalckvar E, Shifman O, Bialik S, Sabanay H, et al. (2006) A short mitochondrial form of p19ARF induces autophagy and caspase-independent cell death. Mol Cell 22: 463-475. doi:10.1016/j.molcel.2006.04.014. PubMed: 16713577.
34. Reef S, Shifman O, Oren M, Kimchi A, (2007) The autophagic inducer smARF interacts with and is stabilized by the mitochondrial p32 protein. Oncogene 26: 6677-6683. doi:10.1038/sj.onc.1210485. PubMed: 17486078.
35. Biederbick A, Kern HF, Elsässer HP, (1995) Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66: 3-14. PubMed: 7750517.
36. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, et al. (2009) In search of an Retrieved onpublished at whilst December year 1111 from autophagomometer". Autophagy 5: 585-589.
37. Bhilocha S, Amin R, Pandya M, Yuan H, Tank M, et al. (2011) Agarose and polyacrylamide gel electrophoresis methods for molecular mass analysis of 5- to 500-kDa Hyaluronan. Anal Biochem 417: 41-49. doi:10.1016/j.ab.2011.05.026. PubMed: 21684248.
38. McCord JM, (1974) Free radicals and inflammation: Protection of synovial fluid by superoxide dismutase. Science 185: 529-531. doi:10.1126/science.185.4150.529. PubMed: 4841157.
39. Greenwald RA, Moy WW, (1980) Effect of oxygen-derived free radicals on hyaluronic acid. Arthritis Rheum 23: 455-463. doi:10.1002/art.1780230408. PubMed: 6245661.
40. McNeil JD, Wiebkin OW, Betts WH, Cleland LG, (1985) Depolymerisation products of hyaluronic acid after exposure to oxygen-derieved free radicals. Ann Rheum Dis 44: 780-789. doi:10.1136/ard.44.11.780. PubMed: 4062391.
41. Yamazaki K, Fukuda K, Matsukawa M, Hara F, Yoshida K, et al. (2003) Reactive oxygen species depolymerize hyaluronan: involvement of the hydroxyl radical. Pathophysiology 4: 215-220. PubMed: 14567924.
42. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42. doi:10.1016/j.cell.2007.12.018. PubMed: 18191218.
43. Kim J, Kundu M, Viollet B, Guan KL, (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13: 132-141. doi:10.1038/ncb2152. PubMed: 21258367.
44. Cardaci S, Filomeni G, Ciriolo MR, (2012) Redox implications of AMPK-mediated signal transduction beyond energetic clues. J Cell Sci 125: 2115-2125. doi:10.1242/jcs.095216. PubMed: 22619229.
45. Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, et al. (2011) Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol Cell Biol 31: 3531-3545. doi:10.1128/MCB.05124-11. PubMed: 21670147.
46. Zhang H, Kong X, Kang J, Su J, Zhong J, et al. (2009) Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol Sci 110: 376-388. doi:10.1093/toxsci/kfp101. PubMed: 19451193.
47. Gorski SM, Chittaranjan S, Pleasance ED, Freeman JD, Anderson CL, et al. (2003) A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 13: 358-363. doi:10.1016/S0960-9822(03)00082-4. PubMed: 12593804.
48. Lee CY, Clough EA, Yellon P, Teslovich TM, Stephan DA, et al. (2003) Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr Biol 13: 350-357. doi:10.1016/S0960-9822(03)00085-X. PubMed: 12593803.
49. Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, et al. (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040. doi:10.1128/MCB.25.3.1025-1040.2005. PubMed: 15657430.
50. Li Y, Wan OW, Xie W, Chung KK, (2011) p32 regulates mitochondrial morphology and dynamics through parkin. Neuroscience 199: 346-358. doi:10.1016/j.neuroscience.2011.10.003. PubMed: 22008525.
51. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, et al. (2007) Linking of Autophagy to Ubiquitin-Proteasome System Is Important for the Regulation of Endoplasmic Reticulum Stress and Cell Viability. Am J Pathol 171: 513-524. doi:10.2353/ajpath.2007.070188. PubMed: 17620365.
52. Zhu Y, Hoell P, Ahlemeyer B, Sure U, Bertalanffy H, et al. (2007) Implication of PTEN in production of reactive oxygen species and neuronal death in in vitro models of stroke and Parkinson's disease. Neurochem Int 50: 507-516. doi:10.1016/j.neuint.2006.10.010. PubMed: 17169462.
53. Weng L, Brown J, Eng C, (2001) PTEN induces apoptosis and cell cycle arrest through phosphoinositol-3-kinase/Akt-dependent and-independent pathways. Hum Mol Genet 10: 237-242. doi:10.1093/hmg/10.3.237. PubMed: 11159942.
54. Xu Z, Stokoe D, Kane LP, Weiss A, (2002) The inducible expression of the tumor suppressor gene PTEN promotes apoptosis and decreases cell size by inhibiting the PI3K/Akt pathway in Jurkat T cells. Cell Growth Differ 13: 285-296. PubMed: 12133897.
55. Nho RS, Xia H, Diebold D, Kahm J, Kleidon J, et al. (2006) PTEN regulates fibroblast elimination during collagen matrix contraction. J Biol Chem 281: 33291-33301. doi:10.1074/jbc.M606450200. PubMed: 16963781.
56. Liu B, Chen Y, St Clair DK, (2008) ROS and p53: a versatile partnership. Free Radic Biol Med 44: 1529-1535. doi:10.1016/j.freeradbiomed.2008.01.011. PubMed: 18275858.
57. Desaint S, Luriau S, Aude JC, Rousselet G, Toledano MB, (2004) Mammalian antioxidant defenses are not inducible by H2O2. J Biol Chem 279: 31157-31163. doi:10.1074/jbc.M401888200. PubMed: 15155764.
58. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B, (1997) A model for p53-induced apoptosis. Nature 389: 300-305. doi:10.1038/38525. PubMed: 9305847.
59. Feng Z, Zhang H, Levine AJ, Jin S, (2005) The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci U S A 102: 8204-8209. doi:10.1073/pnas.0502857102. PubMed: 15928081.
60. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, (2006) DRAM, a p53-Induced Modulator of Autophagy Is Critical for Apoptosis. Cell 126: 121-134. doi:10.1016/j.cell.2006.05.034. PubMed: 16839881.
61. Stambolic V, MacPherson D, Sas D, Lin Y, Snow B, et al. (2001) Regulation of PTEN transcription by p53. Mol Cell 8: 317-325. doi:10.1016/S1097-2765(01)00323-9. PubMed: 11545734.
62. Lorin S, Borges A, Ribeiro DSL, Souquère S, Pierron G, et al. (2009) c-Jun NH2-terminal kinase activation is essential for DRAM-dependent induction of autophagy and apoptosis in 2-methoxyestradiol-treated Ewing sarcoma cells. Cancer Res 69: 6924-6931. doi:10.1158/0008-5472.CAN-09-1270. PubMed: 19706754.
63. Lorin S, Pierron G, Ryan KM, Codogno P, Djavaheri-Mergny M, (2010) Evidence for the interplay between JNK and p53-DRAM signalling pathways in the regulation of autophagy. Autophagy 6: 153-154. doi:10.4161/auto.6.1.10537. PubMed: 19949306.
64. Balogh TG, Illés J, Székely Z, Forrai E, Gere A, (2003) Effect of different metal ions on the oxidative damage and antioxidant capacity of hyaluronic acid. Arch Biochem Biophys 410: 76-82. doi:10.1016/S0003-9861(02)00661-6. PubMed: 12559978.
65. Šoltés L, Mendichi R, Kogan G, Schiller J, Stankovska M, et al. (2006) Degradative Action of Reactive Oxygen Species on Hyaluronan. Biomacromolecules 7: 659-668. doi:10.1021/bm050867v. PubMed: 16529395.
66. Lu Y, Lin YZ, LaPushin R, Cuevas B, Fang X, et al. (1999) The PTEN/MMAC1/TEP tumor suppressor gene decreases cell growth and induces apoptosis and anoikis in breast cancer cells. Oncogene 18: 7034-7045. doi:10.1038/sj.onc.1203183. PubMed: 10597304.
67. Tolkacheva T, Chan AM, (2000) Inhibition of H-Ras transformation by the PTEN/MMAC1/TEP1 tumor suppressor gene. Oncogene 19: 680-689. doi:10.1038/sj.onc.1203331. PubMed: 10698513.
68. Nguyen KT, Zong CS, Uttamsingh S, Sachdev P, Bhanot M, et al. (2002) The role of phosphatidylinositol 3-kinase, rho family GTPases, and STAT3 in Ros-induced cell transformation. J Biol Chem 277: 11107-11115. doi:10.1074/jbc.M108166200. PubMed: 11799110.
69. Dutta S, Chowdhury AR, Srivastava SK, Ghosh I, Datta K, (2011) Evidence for Serpentine as a novel antioxidant by a redox sensitive HABP1 overexpressing cell line by inhibiting its nuclear translocation of NF-κB. Free Radic Res 45: 1279-1288. doi:10.3109/10715762.2011.610794. PubMed: 21815883.
70. Grishko V, Xu M, Ho R, Mates A, Watson S, et al. (2009) Effects of hyaluronic acid on mitochondrial function and mitochondria-driven apoptosis following oxidative stress in human chondrocytes. J Biol Chem 284: 9132-9139. doi:10.1074/jbc.M804178200. PubMed: 19193642.