Hypoxia facilitates the survival of nucleus pulposus cells in serum deprivation by down-regulating excessive autophagy through restricting ROS generation

International Journal of Biochemistry and Cell Biology

Volumn 59, Issue , 2015, Pages 1-10

  Chen, Jiang Wei ^a   Ni, Bin Bin ^a   Zheng, Xin Feng ^a   Li, Bo ^a   Jiang, Sheng Dan ^a   Jiang, Lei Sheng ^a  

^a XINHUA HOSPITAL AFFILIATED TO SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Autophagy; Hypoxia; Nucleus pulpopus cells; ROS

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; WORTMANNIN; ADENYLATE KINASE; CULTURE MEDIUM; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL ACTIVITY; CELL DEATH; CELL SURVIVAL; DOWN REGULATION; ENZYME ACTIVITY; HYPOXIA; NONHUMAN; NUCLEUS PULPOSUS; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL HYPOXIA; CULTURE MEDIUM; CYTOLOGY; INTERVERTEBRAL DISK; METABOLISM; PHAGOSOME; ULTRASTRUCTURE;

ADENYLATE KINASE; ANIMALS; APOPTOSIS; AUTOPHAGY; CELL HYPOXIA; CELL SURVIVAL; CULTURE MEDIA, SERUM-FREE; DOWN-REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERVERTEBRAL DISC; PHAGOSOMES; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84917737871     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.11.009     Document Type: Article

References (60)

1. A. Agrawal, A. Guttapalli, S. Narayan, T.J. Albert, I.M. Shapiro, and M.V. Risbud Normoxic stabilization of HIF-1alpha drives glycolytic metabolism and regulates aggrecan gene expression in nucleus pulposus cells of the rat intervertebral disk Am J Physiol Cell Physiol 293 2007 C621 C631
2. E.H. Baehrecke Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6 2005 505 510
3. E.M. Bartels, J.C. Fairbank, C.P. Winlove, and J.P. Urban Oxygen and lactate concentrations measured in vivo in the intervertebral discs of patients with scoliosis and back pain Spine 23 1998 1 7 [discussion 8]
4. U. Berlemann, N.C. Gries, and R.J. Moore The relationship between height, shape and histological changes in early degeneration of the lower lumbar discs Eur Spine J 7 1998 212 217
5. J. Bohensky, S. Leshinsky, V. Srinivas, and I.M. Shapiro Chondrocyte autophagy is stimulated by HIF-1 dependent AMPK activation and mTOR suppression Pediatr Nephrol 25 2010 633 642
6. A.L. Boskey Signaling in response to hypoxia and normoxia in the intervertebral disc Arthritis Rheum 58 2008 3637 3639
7. P. Carmeliet, Y. Dor, J.M. Herbert, D. Fukumura, K. Brusselmans, and M. Dewerchin Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis Nature 394 1998 485 490
8. R. Castino, N. Bellio, C. Follo, D. Murphy, and C. Isidoro Inhibition of PI3k class III-dependent autophagy prevents apoptosis and necrosis by oxidative stress in dopaminergic neuroblastoma cells Toxicol Sci 117 2010 152 162
9. R. Castino, I. Fiorentino, M. Cagnin, A. Giovia, and C. Isidoro Chelation of lysosomal iron protects dopaminergic SH-SY5Y neuroblastoma cells from hydrogen peroxide toxicity by precluding autophagy and Akt dephosphorylation Toxicol Sci 123 2011 523 541
10. L. Chaudhuri, E.H. Sarsour, and P.C. Goswami 2-(4-Chlorophenyl)benzo-1,4-quinone induced ROS-signaling inhibits proliferation in human non-malignant prostate epithelial cells Environ Int 36 2010 924 930
11. G. Chen, W. Zhang, Y.P. Li, J.G. Ren, N. Xu, and H. Liu Hypoxia-induced autophagy in endothelial cells: a double-edged sword in the progression of infantile haemangioma? Cardiovasc Res 98 2013 437 448
12. Y. Chen, M.B. Azad, and S.B. Gibson Superoxide is the major reactive oxygen species regulating autophagy Cell Death Differ 16 2009 1040 1052
13. H. Eisler, K.U. Frohlich, and E. Heidenreich Starvation for an essential amino acid induces apoptosis and oxidative stress in yeast Exp Cell Res 300 2004 345 353
14. A. Ejeskar, and S. Holm Oxygen tension measurements in the intervertebral disc. A methodological and experimental study Upsala J Med Sci 84 1979 83 93
15. G. Feng, L. Li, H. Liu, Y. Song, F. Huang, and C. Tu Hypoxia differentially regulates human nucleus pulposus and annulus fibrosus cell extracellular matrix production in 3D scaffolds. Osteoarthritis and cartilage/OARS Osteoarth Res Soc 21 2013 582 588
16. N. Fujita, D. Markova, D.G. Anderson, K. Chiba, Y. Toyama, and I.M. Shapiro Expression of prolyl hydroxylases (PHDs) is selectively controlled by HIF-1 and HIF-2 proteins in nucleus pulposus cells of the intervertebral disc: distinct roles of PHD2 and PHD3 proteins in controlling HIF-1alpha activity in hypoxia J Biol Chem 287 2012 16975 16986
17. H.E. Gruber, N. Ashraf, J. Kilburn, C. Williams, H.J. Norton, and B.E. Gordon Vertebral endplate architecture and vascularization: application of micro-computerized tomography, a vascular tracer, and immunocytochemistry in analyses of disc degeneration in the aging sand rat Spine 30 2005 2593 2600
18. O. Hassler The human intervertebral disc. A micro-angiographical study on its vascular supply at various ages Acta Orthop Scand 40 1969 765 772
19. W.S. He, X.F. Dai, M. Jin, C.W. Liu, and J.H. Rent Hypoxia-induced autophagy confers resistance of breast cancer cells to ionizing radiation Oncol Res 20 2012 251 258
20. H.A. Horner, and J.P. Urban 2001 Volvo Award Winner in Basic Science Studies: effect of nutrient supply on the viability of cells from the nucleus pulposus of the intervertebral disc Spine 26 2001 2543 2549
21. Y.L. Hu, A. Jahangiri, M. De Lay, and M.K. Aghi Hypoxia-induced tumor cell autophagy mediates resistance to anti-angiogenic therapy Autophagy 8 2012 979 981
22. L. Jiang, X. Zhang, X. Zheng, A. Ru, X. Ni, and Y. Wu Apoptosis, senescence, and autophagy in rat nucleus pulposus cells: implications for diabetic intervertebral disc degeneration J Orthop Res 31 2013 692 702
23. M. Jiang, K. Liu, J. Luo, and Z. Dong Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury Am J Pathol 176 2010 1181 1192
24. C. Kang, and L. Avery To be or not to be, the level of autophagy is the question: dual roles of autophagy in the survival response to starvation Autophagy 4 2008 82 84
25. C. Kang, Y.J. You, and L. Avery Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation Genes Dev 21 2007 2161 2171
26. T. Kanzawa, L. Zhang, L. Xiao, I.M. Germano, Y. Kondo, and S. Kondo Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3 Oncogene 24 2005 980 991
27. H. Li, C.Z. Liang, and Q.X. Chen Regulatory role of hypoxia inducible factor in the biological behavior of nucleus pulposus cells Yonsei Med J 54 2013 807 812
28. L. Li, Y. Chen, and S.B. Gibson Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation Cell Signal 25 2013 50 65
29. K.G. Ma, Z.W. Shao, S.H. Yang, J. Wang, B.C. Wang, and L.M. Xiong Autophagy is activated in compression-induced cell degeneration and is mediated by reactive oxygen species in nucleus pulposus cells exposed to compression. Osteoarthritis and cartilage/OARS Osteoarthr Res Soc 21 2013 2030 2038
30. N.M. Mazure, and J. Pouyssegur Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol 22 2010 177 180
31. A.E. Morales, A. Perez-Jimenez, M.C. Hidalgo, E. Abellan, and G. Cardenete Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver Comp Biochem Physiol Toxicol Pharmacol 139 2004 153 161
32. I. Papandreou, A.L. Lim, K. Laderoute, and N.C. Denko Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L Cell Death Differ 15 2008 1572 1581
33. S. Pattingre, A. Tassa, X. Qu, R. Garuti, X.H. Liang, and N. Mizushima Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy Cell 122 2005 927 939
34. M. Pei, M. Shoukry, J. Li, S.D. Daffner, J.C. France, and S.E. Emery Modulation of in vitro microenvironment facilitates synovium-derived stem cell-based nucleus pulposus tissue regeneration Spine 37 2012 1538 1547
35. B. Peng, S. Hou, Q. Shi, and L. Jia The relationship between cartilage end-plate calcification and disc degeneration: an experimental study Chin Med J 114 2001 308 312
36. M.V. Risbud, J. Fertala, E.J. Vresilovic, T.J. Albert, and I.M. Shapiro Nucleus pulposus cells upregulate PI3K/Akt and MEK/ERK signaling pathways under hypoxic conditions and resist apoptosis induced by serum withdrawal Spine 30 2005 882 889
37. M.V. Risbud, A. Guttapalli, T.J. Albert, and I.M. Shapiro Hypoxia activates MAPK activity in rat nucleus pulposus cells: regulation of integrin expression and cell survival Spine 30 2005 2503 2509
38. M.V. Risbud, A. Guttapalli, D.G. Stokes, D. Hawkins, K.G. Danielson, and T.P. Schaer Nucleus pulposus cells express HIF-1 alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment J Cell Biochem 98 2006 152 159
39. M.V. Risbud, E. Schipani, and I.M. Shapiro Hypoxic regulation of nucleus pulposus cell survival: from niche to notch Am J Pathol 176 2010 1577 1583
40. S. Roberts, J.P. Urban, H. Evans, and S.M. Eisenstein Transport properties of the human cartilage endplate in relation to its composition and calcification Spine 21 1996 415 420
41. J.M. Rodriguez-Vargas, M.J. Ruiz-Magana, C. Ruiz-Ruiz, J. Majuelos-Melguizo, A. Peralta-Leal, and M.I. Rodriguez ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy Cell Res 22 2012 1181 1198
42. M. Rudert, and B. Tillmann Lymph and blood supply of the human intervertebral disc. Cadaver study of correlations to discitis Acta Orthop Scand 64 1993 37 40
43. R. Scherz-Shouval, and Z. Elazar ROS, mitochondria and the regulation of autophagy Trends Cell Biol 17 2007 422 427
44. R. Scherz-Shouval, and Z. Elazar Regulation of autophagy by ROS: physiology and pathology Trends Biochem Sci 36 2011 30 38
45. R. Scherz-Shouval, E. Shvets, E. Fass, H. Shorer, L. Gil, and Z. Elazar Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4 EMBO J 26 2007 1749 1760
46. G.L. Semenza Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology Trends Mol Med 7 2001 345 350
47. C. Shen, J. Yan, L.S. Jiang, and L.Y. Dai Autophagy in rat annulus fibrosus cells: evidence and possible implications Arthritis Res Ther 13 2011 R132
48. J. Song, X. Guo, X. Xie, X. Zhao, D. Li, and W. Deng Autophagy in hypoxia protects cancer cells against apoptosis induced by nutrient deprivation through a Beclin1-dependent way in hepatocellular carcinoma J Cell Biochem 112 2011 3406 3420
49. V. Srinivas, J. Bohensky, A.M. Zahm, and I.M. Shapiro Autophagy in mineralizing tissues: microenvironmental perspectives Cell Cycle 8 2009 391 393
50. J.W. Stairmand, S. Holm, and J.P. Urban Factors influencing oxygen concentration gradients in the intervertebral disc. A theoretical analysis Spine 16 1991 444 449
51. J.P. Urban, S. Smith, and J.C. Fairbank Nutrition of the intervertebral disc Spine 29 2004 2700 2709
52. L. Vucicevic, M. Misirkic, K. Janjetovic, U. Vilimanovich, E. Sudar, and E. Isenovic Compound C induces protective autophagy in cancer cells through AMPK inhibition-independent blockade of Akt/mTOR pathway Autophagy 7 2011 40 50
53. Y.H. Yang, K. Chen, B. Li, J.W. Chen, X.F. Zheng, and Y.R. Wang Estradiol inhibits osteoblast apoptosis via promotion of autophagy through the ER-ERK-mTOR pathway Apoptosis 18 2013 1363 1375
54. Z. Yang, and D.J. Klionsky An overview of the molecular mechanism of autophagy Curr Top Microbiol Immunol 335 2009 1 32
55. W. Ye, K. Xu, D. Huang, A. Liang, Y. Peng, and W. Zhu Age-related increases of macroautophagy and chaperone-mediated autophagy in rat nucleus pulposus Connect Tissue Res 52 2011 472 478
56. W. Ye, W. Zhu, K. Xu, A. Liang, Y. Peng, and D. Huang Increased macroautophagy in the pathological process of intervertebral disc degeneration in rats Connect Tissue Res 54 2013 22 28
57. B.H. Yoo, X. Wu, M. Derouet, M. Haniff, E.L. Eskelinen, and K. Rosen Hypoxia-induced downregulation of autophagy mediator Beclin 1 reduces the susceptibility of malignant intestinal epithelial cells to hypoxia-dependent apoptosis Autophagy 5 2009 1166 1179
58. F.L. Yuan, H.R. Wang, L. Cao, P.G. Duan, and J. Dong New evidence of the role of the hypoxia-regulated pathway in nucleus pulposus cell survival: comment on the article by Hiyama et al Arthritis Rheum 64 2012 940 941 [author reply 1-2]
59. Y. Zeng, K.G. Danielson, T.J. Albert, I.M. Shapiro, and M.V. Risbud HIF-1 alpha is a regulator of galectin-3 expression in the intervertebral disc J Bone Miner Res 22 2007 1851 1861
60. C.Q. Zhao, L.S. Jiang, and L.Y. Dai Programmed cell death in intervertebral disc degeneration Apoptosis 11 2006 2079 2088