Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) induces cancer cell senescence by interacting with telomerase RNA component

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 33, 2012, Pages 13308-13313

  Nicholls, Craig ^a,b   Pinto, Alexander Ruvantha ^b   Li, He ^a   Li, Ng ^b   Wang, Lihui ^c   Simpson, Richard ^d   Liu, Jun Ping ^a,b,c,e  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c HANGZHOU NORMAL UNIVERSITY   (China)

^d LA TROBE UNIVERSITY   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Gene expression; Mutation; NAD +; Post translational modification; Telomerase reverse transcriptase

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NITRIC OXIDE; S NITROSOGLUTATHIONE; TELOMERASE; TELOMERASE RNA COMPONENT; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CATALYSIS; CELL AGING; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE DISRUPTION; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN RNA BINDING; RNA ANALYSIS; RNA ISOLATION; TELOMERE;

BREAST NEOPLASMS; CELL AGING; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCERALDEHYDE 3-PHOSPHATE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); GREEN FLUORESCENT PROTEINS; HUMANS; NAD; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; S-NITROSOGLUTATHIONE; STRUCTURE-ACTIVITY RELATIONSHIP; TELOMERASE; TELOMERE SHORTENING;

EID: 84865176534     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206672109     Document Type: Article

References (46)

1. Browner WS, et al. (2004) The genetics of human longevity. Am J Med 117:851-860. (Pubitemid 39602795)
2. Sung HJ, et al. (2010) Mitochondrial respiration protects against oxygen-associated DNA damage. Nat Commun 1:5.
3. Sen N, et al. (2008) Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat Cell Biol 10:866-873. (Pubitemid 351934066)
4. Hara MR, et al. (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7:665-674. (Pubitemid 40975747)
5. Chuang DM, Hough C, Senatorov VV (2005) Glyceraldehyde-3-phosphate dehydrogenase, apoptosis, and neurodegenerative diseases. Annu Rev Pharmacol Toxicol 45:269-290. (Pubitemid 40261806)
6. Zheng L, Roeder RG, Luo Y (2003) S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114: 255-266. (Pubitemid 36936918)
7. Sawa A, Khan AA, Hester LD, Snyder SH (1997) Glyceraldehyde-3-phosphate dehydrogenase: Nuclear translocation participates in neuronal and nonneuronal cell death. Proc Natl Acad Sci USA 94:11669-11674. (Pubitemid 27451056)
8. Sundararaj KP, et al. (2004) Rapid shortening of telomere length in response to ceramide involves the inhibition of telomere binding activity of nuclear glyceraldehyde- 3-phosphate dehydrogenase. J Biol Chem 279:6152-6162. (Pubitemid 38220648)
9. Demarse NA, et al. (2009) Direct binding of glyceraldehyde 3-phosphate dehydrogenase to telomeric DNA protects telomeres against chemotherapy-induced rapid degradation. J Mol Biol 394:789-803.
10. Blackburn EH (2001) Switching and signaling at the telomere. Cell 106:661-673.
11. Shay JW (1999) Toward identifying a cellular determinant of telomerase repression. J Natl Cancer Inst 91:4-6.
12. Reddel RR, Bryan TM (2003) Alternative lengthening of telomeres: Dangerous road less travelled. Lancet 361:1840-1841. (Pubitemid 36645174)
13. Pinto AR, Li H, Nicholls C, Liu JP (2011) Telomere protein complexes and interactions with telomerase in telomere maintenance. Front Biosci 16:187-207.
14. Liu JP, et al. (2010) Regulation of telomerase activity by apparently opposing elements. Ageing Res Rev 9:245-256.
15. Nakamura TM, et al. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955-959. (Pubitemid 27366681)
16. Meyerson M, et al. (1997) hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785-795. (Pubitemid 27357969)
17. Chen JL, Blasco MA, Greider CW (2000) Secondary structure of vertebrate telomerase RNA. Cell 100:503-514.
18. Chen JL, Greider CW (2004) An emerging consensus for telomerase RNA structure. Proc Natl Acad Sci USA 101:14683-14684.
19. Bodnar AG, et al. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352. (Pubitemid 28063364)
20. Sarin KY, et al. (2005) Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 436:1048-1052. (Pubitemid 41191691)
21. Bruns GA, Gerald PS (1976) Human glyceraldehyde-3-phosphate dehydrogenase in man-rodent somatic cell hybrids. Science 192:54-56.
22. Sirover MA (1999) New insights into an old protein: The functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 1432: 159-184. (Pubitemid 29304525)
23. Tristan C, Shahani N, Sedlak TW, Sawa A (2011) The diverse functions of GAPDH: Views from different subcellular compartments. Cell Signal 23:317-323.
24. Nicholls C, Li H, Liu JP (2011) GAPDH: A common enzyme with uncommon functions. Clin Exp Pharmacol Physiol.
25. Huang Q, et al. (2011) Akt2 kinase suppresses glyceraldehyde-3-phosphate dehydrogenase (GAPDH)-mediated apoptosis in ovarian cancer cells via phosphorylating GAPDH at threonine 237 and decreasing its nuclear translocation. J Biol Chem 286: 42211-42220.
26. Bonafé N, et al. (2005) Glyceraldehyde-3-phosphate dehydrogenase binds to the AURich 3′ untranslated region of colony-stimulating factor-1 (CSF-1) messenger RNA in human ovarian cancer cells: Possible role in CSF-1 posttranscriptional regulation and tumor phenotype. Cancer Res 65:3762-3771. (Pubitemid 40616354)
27. Krynetski EY, Krynetskaia NF, Bianchi ME, Evans WE (2003) A nuclear protein complex containing high mobility group proteins B1 and B2, heat shock cognate protein 70, ERp60, and glyceraldehyde-3-phosphate dehydrogenase is involved in the cytotoxic response to DNA modified by incorporation of anticancer nucleoside analogues. Cancer Res 63:100-106. (Pubitemid 36070426)
28. Dastoor Z, Dreyer JL (2001) Potential role of nuclear translocation of glyceraldehyde- 3-phosphate dehydrogenase in apoptosis and oxidative stress. J Cell Sci 114:1643-1653. (Pubitemid 32454663)
29. Hara MR, et al. (2006) Neuroprotection by pharmacologic blockade of the GAPDH death cascade. Proc Natl Acad Sci USA 103:3887-3889. (Pubitemid 43376650)
30. Kipling D, et al. (1999) Telomere-dependent senescence. Nat Biotechnol 17:313-314.
31. Abdallah P, et al. (2009) A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol 11:988-993.
32. Harley CB (2008) Telomerase and cancer therapeutics. Nat Rev Cancer 8:167-179.
33. Deng Y, Chan SS, Chang S (2008) Telomere dysfunction and tumour suppression: The senescence connection. Nat Rev Cancer 8:450-458. (Pubitemid 351744962)
34. Nagy E, Rigby WF (1995) Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J Biol Chem 270: 2755-2763.
35. Liu ZJ, et al. (1997) The first structure of an aldehyde dehydrogenase reveals novel interactions between NAD and the Rossmann fold. Nat Struct Biol 4:317-326.
36. Fermani S, et al. (2001) Crystal structure of the non-regulatory A(4) isoform of spinach chloroplast glyceraldehyde-3-phosphate dehydrogenase complexed with NADP. J Mol Biol 314:527-542. (Pubitemid 33131855)
37. Brown VM, et al. (2004) A novel CRM1-mediated nuclear export signal governs nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase following genotoxic stress. J Biol Chem 279:5984-5992. (Pubitemid 38220631)
38. Kornberg MD, et al. (2010) GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol 12:1094-1100.
39. Chakravarti R, Aulak KS, Fox PL, Stuehr DJ (2010) GAPDH regulates cellular heme insertion into inducible nitric oxide synthase. Proc Natl Acad Sci USA 107:18004-18009.
40. Hao G, Derakhshan B, Shi L, Campagne F, Gross SS (2006) SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc Natl Acad Sci USA 103:1012-1017. (Pubitemid 43212213)
41. Goodwin PM, Lewis PJ, Davies MI, Skidmore CJ, Shall S (1978) The effect of gamma radiation and neocarzinostatin on NAD and ATP levels in mouse leukaemia cells. Biochim Biophys Acta 543:576-582. (Pubitemid 9043430)
42. Shieh WM, et al. (1998) Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J Biol Chem 273:30069-30072. (Pubitemid 28545464)
43. Nakamura J, et al. (2003) Quantitation of intracellular NAD(P)H can monitor an imbalance of DNA single strand break repair in base excision repair deficient cells in real time. Nucleic Acids Res 31:e104.
44. Kim NW, et al. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011-2015.
45. Sumer H, et al. (2010) Chromosomal and telomeric reprogramming following ES-somatic cell fusion. Chromosoma 119:167-176.
46. Cassar L, et al. (2008) Bone morphogenetic protein-7 inhibits telomerase activity, telomere maintenance, and cervical tumor growth. Cancer Res 68:9157-9166.