HSP60 is transported through the secretory pathway of 3-MCA-induced fibrosarcoma tumour cells and undergoes N-glycosylation

FEBS Journal

Volumn 279, Issue 12, 2012, Pages 2083-2095

  Hayoun, Dana ^a   Kapp, Tsachi ^a   Edri Brami, Meital ^a   Ventura, Tomer ^a   Cohen, Merav ^a   Avidan, Avi ^a   Lichtenstein, Rachel G ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

3 MCA induced fibrosarcoma cells; ER Golgi; heat shock protein 60; N glycans

Indexed keywords

3 METHYLCHOLANTHRENE; BREFELDIN A; GLYCAN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 60 ANTIBODY; MANNOSE; MESSENGER RNA; MONENSIN; PROTEIN ANTIBODY; TGN38 ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CELL FRACTIONATION; CELL LINE; CONFOCAL MICROSCOPY; ENDOPLASMIC RETICULUM; FIBROBLAST; FIBROSARCOMA; FLOW CYTOMETRY; GOLGI COMPLEX; HEAT SHOCK; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SECRETORY PATHWAY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR MICROENVIRONMENT;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CHAPERONIN 60; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLOPENTANES; ENDOPLASMIC RETICULUM; FIBROSARCOMA; FLOW CYTOMETRY; GLYCOSYLATION; HUMANS; IMMUNOBLOTTING; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

TETRA;

EID: 84861897566     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08594.x     Document Type: Article

References (56)

1. Soltys BJ, &, Gupta RS, (1999) Mitochondrial-matrix proteins at unexpected locations: are they exported? Trends Biochem Sci 24, 174-177.
2. Deocaris CC, Kaul SC, &, Wadhwa R, (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperon 11, 116-128.
3. Quintana FJ, &, Cohen IR, (2011) The HSP60 immune system network. Trends Immunol 32, 89-95.
4. Lin L, Kim SC, Wang Y, Gupta S, Davis B, Simon SI, Torre-Amione G, &, Knowlton AA, (2007) HSP60 in heart failure: abnormal distribution and role in cardiac myocyte apoptosis. Am J Physiol Heart Circ Physiol 293, H2238-H2247.
5. Kaufmann SH, (19891990) Immunity to bacteria. Curr Opin Immunol 2, 353-359.
6. Kaufmann SH, (1990) Heat shock proteins and the immune response. Immunol Today 11, 129-136.
7. Bulut Y, Faure E, Thomas L, Karahashi H, Michelsen KS, Equils O, Morrison SG, Morrison RP, &, Arditi M, (2002) Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J Immunol 168, 1435-1440.
8. Basu S, Binder RJ, Suto R, Anderson KM, &, Srivastava PK, (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol 12, 1539-1546.
9. Merendino AM, Bucchieri F, Campanella C, Marcian V, Ribbene A, David S, Zummo G, Burgio G, Corona DF, Conway de Macario E, et al. (2010) Hsp60 is actively secreted by human tumor cells. PLoS One 5, e9247.
10. Gupta S, &, Knowlton AA, (2007) HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol 292, H3052-H3056.
11. Soltys BJ, Falah M, &, Gupta RS, (1996) Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J Cell Sci 109, 1909-1917.
12. Soltys BJ, &, Gupta RS, (1997) Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 21, 315-320.
13. Helenius A, &, Aebi M, (2001) Intracellular functions of N-linked glycans. Science 291, 2364-2369.
14. Martelli A, Salin B, Dycke C, Louwagie M, Andrieu JP, Richaud P, &, Moulis JM, (2007) Folding and turnover of human iron regulatory protein 1 depend on its subcellular localization. FEBS J 274, 1083-1092.
15. Clausmeyer S, Stürzebecher R, &, Peters J, (1999) An alternative transcript of the rat renin gene can result in a truncated prorenin that is transported into adrenal mitochondria. Circ Res 84, 337-344.
16. Wamboldt Y, Mohammed S, Elowsky C, Wittgren C, de Paula WB, &, Mackenzie SA, (2009) Participation of leaky ribosome scanning in protein dual targeting by alternative translation initiation in higher plants. Plant Cell 21, 157-167.
17. Karniely S, &, Pines O, (2005) Single translation-dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO Rep 6, 420-425.
18. Avidan A, Perlmutter M, Tal S, Oraki O, Kapp T, Krelin Y, Elkabets M, Dotan S, Apte RN, &, Lichtenstein RG, (2009) Differences in the sialylation patterns of membrane stress proteins in chemical carcinogen-induced tumors developed in BALB/c and IL-1alpha deficient mice. Glycoconj J 26, 1181-1195.
19. Klausner RD, Donaldson JG, &, Lippincott-Schwartz J, (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116, 1071-1080.
20. Wang X, Gu J, Ihara H, Miyoshi E, Honke K, &, Taniguchi N, (2006) Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J Biol Chem 281, 2572-2577.
21. Leffler H, Carlsson S, Hedlund M, Qian Y, &, Poirier F, (2004) Introduction to galectins. Glycoconj J 19, 433-440.
22. Yogev O, &, Pines O, (2011) Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim Biophys Acta 1808, 1012-1020.
23. Hayes GR, Williams A, Costello CE, Enns CA, &, Lucas JJ, (1994) The critical glycosylation site of human transferrin receptor contains a high-mannose oligosaccharide. Glycobiology 5, 227-232.
24. Callebaut I, Catelli MG, Portetelle D, Burny A, Baulieu EE, &, Mornon JP, (1994) Structural similarities between chaperone molecules of the HSP60 and HSP70 families deduced from hydrophobic cluster analysis. FEBS Lett 342, 242-248.
25. Barazi HO, Zhou LM, Templeton NS, Krutzsch HC, &, Roberts DD, (2002) Identification of heat shock protein 60 as a molecular mediator of alpha 3 beta 1 integrin activation. Cancer Res 62, 1541-1548.
26. Schneider J, Jiménez E, Marenbach K, Romero H, Marx D, &, Meden H, (1999) Immunohistochemical detection of HSP60-expression in human ovarian cancer: correlation with survival in a series of 247 patients. Anticancer Res 19, 2141-2146.
27. Cappello F, Rappa F, David S, Anzalone R, &, Zummo G, (2003) Immunohistochemical evaluation of PCNA, p53, HSP60, HSP10 and MUC-2 presence and expression in prostate carcinogenesis. Anticancer Res 23, 1325-1331.
28. Cappello F, Di Stefano A, David S, Rappa F, Anzalone R, La Rocca G, D'Anna SE, Magno F, Donner CF, Balbi B, et al. (2006) Hsp60 and Hsp10 down-regulation predicts bronchial epithelial carcinogenesis in smokers with chronic obstructive pulmonary disease. Cancer 107, 2417-2424.
29. Luparello C, &, Sirchia R, (2005) Type V collagen regulates the expression of apoptotic and stress response genes by breast cancer cells. J Cell Physiol 202, 411-421.
30. Apte RN, Krelin Y, Song X, Dotan S, Recih E, Elkabets M, Carmi Y, Dvorkin T, White RM, Gayvoronsky L, et al. (2006) Effects of micro-environment- and malignant cell-derived interleukin-1 in carcinogenesis, tumour invasiveness and tumour-host interactions. Eur J Cancer 42, 751-759.
31. Cappello F, Bellafiore M, Palma A, Marciano V, Martorana G, Belfiore P, Martorana A, Farina F, Zummo G, &, Bucchieri F, (2002-2003) Expression of 60-kD heat shock protein increases during carcinogenesis in the uterine exocervix. Pathobiology 70, 83-88.
32. Di Felice V, Ardizzone N, Marcian V, Bartolotta T, Cappello F, Farina F, &, Zummo G, (2005) Senescence-associated HSP60 expression in normal human skin fibroblasts. Anat Rec A Discov Mol Cell Evol Biol 284, 446-453.
33. Chandra D, Choy G, &, Tang DG, (2007) Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J Biol Chem 282, 31289-31301.
34. Potter MD, &, Nicchitta CV, (2000) Regulation of ribosome detachment from the mammalian endoplasmic reticulum membrane. J Biol Chem 275, 33828-33835.
35. Walter P, &, Johnson AE, (1994) Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol 10, 87-119.
36. Touriol C, Bornes S, Bonnal S, Audigier S, Prats H, Prats AC, &, Vagner S, (2003) Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol Cell 95, 169-178.
37. Pyhtila B, Zheng T, Lager PJ, Keene JD, Reedy MC, &, Nicchitta CV, (2008) Signal sequence- and translation-independent mRNA localization to the endoplasmic reticulum. RNA 14, 445-453.
38. Wegehingel S, Zehe C, &, Nickel W, (2008) Rerouting of fibroblast growth factor 2 to the classical secretory pathway results in post-translational modifications that block binding to heparan sulfate proteoglycans. FEBS Lett 582, 2387-2392.
39. Struewing IT, Toborek A, &, Mao CD, (2006) Mitochondrial and nuclear forms of Wnt13 are generated via alternative promoters, alternative RNA splicing, and alternative translation start sites. J Biol Chem 281, 7282-7293.
40. Korbelik M, Sun J, &, Cecic I, (2005) Photodynamic therapy-induced cell surface expression and release of heat shock proteins: relevance for tumor response. Cancer Res 65, 1018-1026.
41. Kim SC, Stice JP, Chen L, Jung JS, Gupta S, Wang Y, Baumgarten G, Trial J, &, Knowlton AA, (2009) Extracellular heat shock protein 60, cardiac myocytes, and apoptosis. Circ Res 2009 (105), 1186-1195.
42. Chen W, Syldath U, Bellmann K, Burkart V, &, Kolb H, (1999) Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162, 3212-3219.
43. Zanin-Zhorov A, Bruck R, Tal G, Oren S, Aeed H, Hershkoviz R, Cohen IR, &, Lider O, (2005) Heat shock protein 60 inhibits Th1-mediated hepatitis model via innate regulation of Th1/Th2 transcription factors and cytokines. J Immunol 174, 3227-3236.
44. Cohen-Sfady M, Nussbaum G, Pevsner-Fischer M, Mor F, Carmi P, Zanin-Zhorov A, Lider O, &, Cohen IR, (2005) Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J Immunol 175, 3594-3602.
45. Suriano R, Ghosh SK, Chaudhuri D, Mittelman A, Banerjee A, &, Tiwari RK, (2009) Sialic acid content of tissue-specific gp96 and its potential role in modulating gp96-macrophage interactions. Glycobiology 19, 1427-1435.
46. Kim HS, Kim EM, Lee J, Yang WH, Park TY, Kim YM, &, Cho JW, (2006) Heat shock protein 60 modified with O-linked N-acetylglucosamine is involved in pancreatic beta-cell death under hyperglycemic conditions. FEBS Lett 580, 2311-2316.
47. Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrançois L, &, Li Z, (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26, 215-226.
48. Cohen M, Elkabets M, Perlmutter M, Porgador A, Voronov E, Apte RN, &, Lichtenstein RG, (2010) Sialylation of 3-methylcholanthrene-induced fibrosarcoma determines antitumor immune responses during immunoediting. J Immunol 185, 5869-5878.
49. Elkabets M, Krelin Y, Dotan S, Cerwenka A, Porgador A, Lichtenstein RG, White MR, Zoller M, Iwakura Y, Dinarello CA, et al. (2009) Host-derived interleukin-1alpha is important in determining the immunogenicity of 3-methylcholantrene tumor cells. J Immunol 182, 4874-4881.
50. Krelin Y, Voronov E, Dotan S, Elkabets M, Reich E, Fogel M, Huszar M, Iwakura Y, Segal S, Dinarello CA, et al. (2007) Interleukin-1beta-driven inflammation promotes the development and invasiveness of chemical carcinogen-induced tumors. Cancer Res 67, 1062-1071.
51. Mahabeleshwar GH, Somanath PR, &, Byzova TV, (2006) Methods for isolation of endothelial and smooth muscle cells and in vitro proliferation assays. Methods Mol Med 129, 197-208.
52. Wang S, Xie W, Rylander MN, Tucker PW, Aggarwal S, &, Diller KR, (2008) HSP70 kinetics study by continuous observation of HSP-GFP fusion protein expression on a perfusion heating stage. Biotechnol Bioeng 99, 146-154.
53. Bozidis P, Williamson CD, &, Colberg-Poley AM, (2007) Isolation of endoplasmic reticulum mitochondria, and mitochondria-associated membrane fractions from transfected cells and from human cytomegalovirus-infected primary fibroblasts. Curr Protoc Cell Biol 3, unit 3.27, 1-23. doi:10.1002/0471143030. cb0327s37.
54. Peng P, Ménoret A, &, Srivastava PK, (1997) Purification of immunogenic heat shock protein 70-peptide complexes by ADP-affinity chromatography. J Immunol Methods 204, 13.
55. Tokuyasu KT, (1973) A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57, 551-565.
56. Küster B, Wheeler SF, Hunter AP, Dwek RA, &, Harvey DJ, (1997) Sequencing of N-linked oligosaccharides directly from protein gels: in-gel deglycosylation followed by matrix-assisted laser desorption/ionization mass spectrometry and normal-phase high-performance liquid chromatography. Anal Biochem 250, 82-101.