A novel role for Bcl-2 associated-athanogene-1 (Bag-1) in regulation of the endoplasmic reticulum stress response in mammalian chondrocytes

Journal of Cellular Biochemistry

Volumn 102, Issue 3, 2007, Pages 786-800

  Yang, Ling ^a   McBurney, Denise ^a   Tang, Shou Ching ^b   Carlson, Sara G ^c   Horton Jr , Walter E ^a,d  

^a Northeastern Ohio Medical University   (United States)

^b UNIVERSITY OF MIAMI   (United States)

^c Stark State College of Technology   (United States)

^d NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

Author keywords

BAG 1; Chondrocytes; ER stress

Indexed keywords

ADENOVIRUS VECTOR; BAG 1 PROTEIN; COLLAGEN TYPE 2; LUCIFERASE; SCLEROPROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DEATH; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GROWTH PLATE; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CHONDROCYTES; COLLAGEN TYPE II; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; MODELS, BIOLOGICAL; PHENOTYPE; RATS; RNA INTERFERENCE; SUBCELLULAR FRACTIONS; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

MAMMALIA;

EID: 35048830516     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21328     Document Type: Article

References (47)

1. Agarraberes FA, Dice JF. 2001. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 114:2491-2499.
2. Alberti S, Demand J, Esser C, Emmerich N, Schild H, Hohfeld J. 2002. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J Biol Chem 277:45920-45927.
3. Alberti S, Esser C, Hohfeld J. 2003. BAG-1 - a nucleotide exchange factor of Hsc70 with multiple cellular functions. Cell Stress Chaperones 8:225-231.
4. Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21.
5. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. 2003. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22:8608-8618.
6. Chen J, Xiong J, Liu H, Chernenko G, Tang SC. 2002. Distinct BAG-1 isoforms have different anti-apoptotic functions in BAG-1-transfected C33A human cervical carcinoma cell line. Oncogene 21:7050-7059.
7. Crocoll A, Blum M, Cato AC. 2000. Isoform-specific expression of BAG-1 in mouse development. Mech Dev 91:355-359.
8. Crocoll A, Herzer U, Ghyselinck NB, Chambon P, Cato AC. 2002. Interdigital apoptosis and downregulation of BAG-1 expression in mouse autopods. Mech Dev 111: 149-152.
9. Doong H, Vrailas A, Kohn EC. 2002. What's in the 'BAG'? - A functional domain analysis of the BAG-family proteins. Cancer Lett 188:25-32.
10. Erickson GR, Northrup DL, Guilak F. 2003. Hypo-osmotic stress induces calcium-dependent actin reorganization in articular chondrocytes. Osteoarthritis Cartilage 11:187-197.
11. Feng L, Precht P, Balakir R, Horton WE Jr. 1998. Evidence of a direct role for Bcl-2 in the regulation of articular chondrocyte apoptosis under the conditions of serum withdrawal and retinoic acid treatment. J Cell Biochem 71:302-309.
12. Gotoh T, Terada K, Oyadomari S, Mori M. 2004. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ 11:390-402.
13. Gotz R, Wiese S, Takayama S, Camarero GC, Rossoll W, Schweizer U, Troppmair J, Jablonka S, Holtmann B, Reed JC, Rapp UR, Sendtner M. 2005. Bag1 is essential for differentiation and survival of hematopoietic and neuronal cells. Nat Neurosci 8:1169-1178.
14. Hammond C, Helenius A. 1995. Quality control in the secretory pathway. Curr Opin Cell Biol 7:523-529.
15. Hecht JT, Sage EH. 2006. Retention of the matricellular protein SPARC in the endoplasmic reticulum of chondrocytes from patients with pseudoachondroplasia. J Histochem Cytochem 54:269-274.
16. Hecht JT, Nelson LD, Crowder E, Wang Y, Elder FF, Harrison WR, Francomano CA, Prange CK, Lennon GG, Deere M, et al. 1995. Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia. Nat Genet 10:325-329.
17. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ. 2006. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312:572-576.
18. Hung WJ, Roberson RS, Taft J, Wu DY. 2003. Human BAG-1 proteins bind to the cellular stress response protein GADD34 and interfere with GADD34 functions. Mol Cell Biol 23:3477-3486.
19. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233.
20. Kinkel MD, Yagi R, McBurney D, Nugent A, Horton WE Jr. 2004. Age-related expression patterns of Bag-1 and Bcl-2 in growth plate and articular chondrocytes. Anat Rec 279A:720-728.
21. Kojima E, Takeuchi A, Haneda M, Yagi A, Hasegawa T, Yamaki K, Takeda K, Akira S, Shimokata K, Isobe K. 2003. The function of GADD34 is a recovery from a shutoff of protein synthesis induced by ER stress: Elucidation by GADD34-deficient mice. Faseb J 17:1573-1575.
22. Kronenberg HM. 2003. Developmental regulation of the growth plate. Nature 423:332-336.
23. Lee JH, Takahashi T, Yasuhara N, Inazawa J, Kamada S, Tsujimoto Y. 1999. Bis, a Bcl-2-binding protein that synergizes with Bcl-2 in preventing cell death. Oncogene 18:6183-6190.
24. Lee RB, Wilkins RJ, Razaq S, Urban JP. 2002. The effect of mechanical stress on cartilage energy metabolism. Biorheology 39:133-143.
25. Loeser RF Jr. 2004. Aging cartilage and osteoarthritis - what's the link? Sci Aging Knowledge Environ 2004: pe 31.
26. Luders J, Demand J, Papp O, Hohfeld J. 2000. Distinct isoforms of the cofactor BAG-1 differentially affect Hsc70 chaperone function. J Biol Chem 275:14817-14823.
27. Luo W, Kuwada TS, Chandrasekaran L, Zheng J, Tanzer ML. 1996. Divergent secretory behavior of the opposite ends of aggrecan. J Biol Chem 271:16447-16450.
28. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21: 1249-1259.
29. Mobasheri A, Vannucci SJ, Bondy CA, Carter SD, Innes JF, Arteaga MF, Trujillo E, Ferraz I, Shakibaei M, Martin-Vasallo P. 2002. Glucose transport and metabolism in chondrocytes: a key to understanding chondrogenesis, skeletal development and cartilage degradation in osteoarthritis. Histol Histopathol 17:1239-1267.
30. Oliver BL, Cronin CG, Zhang-Benoit Y, Goldring MB, Tanzer ML. 2005. Divergent stress responses to IL-1beta, nitric oxide, and tunicamycin by chondrocytes. J Cell Physiol 204:45-50.
31. Rao RV, Ellerby HM, Bredesen DE. 2004. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 11:372-380.
32. Schulz JB, Bremen D, Reed JC, Lommatzsch J, Takayama S, Wullner U, Loschmann PA, Klockgether T, Weller M. 1997. Cooperative interception of neuronal apoptosis by BCL-2 and BAG-1 expression: Prevention of caspase activation and reduced production of reactive oxygen species. J Neurochem 69:2075-2086.
33. Song J, Takeda M, Morimoto RI. 2001. Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth. Nat Cell Biol 3:276-282.
34. Takamura A, Adachi M, Wada I, Mitaka T, Takayama S, Imai K. 2003. Accumulation of Hsp70/Hsc70 molecular chaperone regulator BAG-1 on COPI-coated structures in gastric epithelial cells. Int J Oncol 23:1301-1308.
35. Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA, Reed JC. 1995. Cloning and functional analysis of BAG-1: A novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279-284.
36. Takayama S, Bimston DN, Matsuzawa S, Freeman BC, Aime-Sempe C, Xie Z, Morimoto RI, Reed JC. 1997. BAG-1 modulates the chaperone activity of Hsp70/Hsc70. Embo J 16:4887-4896.
37. Tang SC. 2002. BAG-1, an anti-apoptotic tumour marker. IUBMB Life 53:99-105.
38. Townsend PA, Cutress RI, Sharp A, Brimmell M, Packham G. 2003a. BAG-1 prevents stress-induced long-term growth inhibition in breast cancer cells via a chaperone-dependent pathway. Cancer Res 63:4150-4157.
39. Townsend PA, Cutress RI, Sharp A, Brimmell M, Packham G. 2003b. BAG-1: A multifunctional regulator of cell growth and survival. Biochim Biophys Acta 1603:83-98.
40. Townsend PA, Stephanou A, Packham G, Latchman DS. 2005. BAG-1: A multi-functional pro-survival molecule. Int J Biochem Cell Biol 37:251-259.
41. Xiong J, Chen J, Chernenko G, Beck J, Liu H, Pater A, Tang SC. 2003. Antisense BAG-1 sensitizes HeLa cells to apoptosis by multiple pathways. Biochem Biophys Res Commun 312:585-591.
42. Yagi R, McBurney D, Horton WE Jr. 2005. Bcl-2 positively regulates Sox9-dependent chondrocyte gene expression by suppressing the MEK-ERK1/2 signaling pathway. J Biol Chem 280:30517-30525.
43. Yang X, Chernenko G, Hao Y, Ding Z, Pater MM, Pater A, Tang SC. 1998. Human BAG-1/RAP46 protein is generated as four isoforms by alternative translation initiation and overexpressed in cancer cells. Oncogene 17:981-989.
44. Yang X, Pater A, Tang SC. 1999. Cloning and characterization of the human BAG-1 gene promoter: upregulation by tumor-derived p53 mutants. Oncogene 18:4546-4553.
45. Yang L, Carlson SG, McBurney D, Horton WE Jr. 2005. Multiple signals induce endoplasmic reticulum stress in both primary and immortalized chondrocytes resulting in loss of differentiation, impaired cell growth, and apoptosis. J Biol Chem 280:31156-31165.
46. Zeiner M, Niyaz Y, Gehring U. 1999. The hsp70-associating protein Hap46 binds to DNA and stimulates transcription. Proc Natl Acad Sci USA 96:10194-10199.
47. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB. 2003. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162:59-69.