The mechanisms of hsp27 antibody-mediated apoptosis in retinal neuronal cells

Journal of Neuroscience

Volumn 20, Issue 10, 2000, Pages 3552-3562

  Tezel, Gülgün ^a   Wax, Martin B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Antibody; Apoptosis; Caspase; Heat shock protein 27; Retina

Indexed keywords

ACTIN; ASPARTIC ACID; CASPASE; CYSTEINE PROTEINASE; DNA FRAGMENT; HEAT SHOCK PROTEIN 27; PROTEIN ANTIBODY;

ADULT; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELLULAR DISTRIBUTION; CYTOSKELETON; DEPOLYMERIZATION; ENDOCYTOSIS; GLAUCOMA; HUMAN; HUMAN CELL; INTERNALIZATION; MOUSE; NERVE CELL NECROSIS; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RETINA;

EID: 0034657707     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-10-03552.2000     Document Type: Article

References (88)

1. Adamus G, Machnicki M, Seigel GM (1997) Apoptotic retinal cell death induced by autoantibodies of cancer-associated retinopathy. Invest Ophthalmol Vis Sci 38:283-291.
2. Alarcon-Segovia D, Lorente L (1983) Antibody penetration into living cells IV. Different effects of anti-native DNA and antiribonucleoprotein IgG on the cell cycle of activated T cells. Clin Exp Immunol 52:365-371.
3. Alarcon-Segovia D, Ruiz-Argüelles A, Fishbein E (1978) Antibody to nuclear ribonucleoprotein penetrates live human mononuclear cells through Fc receptors. Nature 271:67-69.
4. Alarcon-Segovia D, Ruiz-Argüelles A, Lorente L (1996) Broken dogma: penetration of autoantibodies into living cells. Immunol Today 17:163-164.
5. Aquino DA, Capello E, Weisstein J, Sanders V, Lopez C, Tourtellotte WW, Brosnan CF, Raine CS, Norton WT (1997) Multiple sclerosis: altered expression of 70-and 27-kDa heat shock proteins in lesions and myelin. J Neuropathol Exp Neurol 56:664-672.
6. Assimakopoulou M, Sotiropoulou-Bonikou G, Maraziotis T, Varakis I (1997) Prognostic significance of Hsp-27 in astrocytic brain tumors: an immunohistochemical study. Anticancer Res 17:2677-2682.
7. r heat-shock protein with the nucleus of heat-shocked and ecdysone-stimulated culture cells. J Cell Sci 92:29-36.
8. Bitar KN, Kaminski MS, Hailat N, Cease KB, Strahler JR (1991) Hsp27 is a mediator of sustained smooth muscle contraction in response to bombesin. Biochem Biophys Res Commun 181:1192-1200.
9. Bonfoco E, Ceccatelli S, Manzo L, Nicotera P (1995) Colchicine induces apoptosis in cerebellar granule cells. Exp Cell Res 218:189-200.
10. Boudreau N, Sympson CJ, Werb Z, Bissell MJ (1995) Supression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267:891-893.
11. Brancolini C, Lazarevic D, Rodriguez J, Schneider C (1997) Dismantling cell-cell contacts during apoptosis is coupled to a caspase-dependent proteolytic cleavage of β-catenin. J Cell Biol 139:759-771.
12. Bump NJ, Hackett M, Hugunin M, Seshagiri S, Brady K, Chen P, Ferenz C, Franklin S, Ghayur T, Li P, Licari P, Mankovich J, Shi L, Greenberg AH, Miller LK, Wong WW (1995) Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-1888.
13. Conroy SE, Sasieni PD, Amin V, Wang DY, Smith P, Fentiman IS, Latchman DS (1998) Antibodies to heat-shock protein 27 are associated with improved survival in patients with breast cancer. Br J Cancer 77:1875-1879.
14. Deshmukh M, Vasilakos J, Deckwerth TL, Lampe PA, Shivers BD, Johnson Jr EM (1996) Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE family proteases. J Cell Biol 135:1341-1354.
15. Dolzhanskiy A, Basch RS (1995) Flow cytometric determination of apoptosis in heterogeneous cell populations. J Immunol Methods 180:131-140.
16. Gabai VL, Kabakov AE (1993) Tumor cell resistance to energy deprivation and hyperthermia can be determined by the actin skeleton stability. Cancer Lett 70:25-31.
17. Graybill TL, Dolle RE, Helaszek CT, Miller RE, Ator MA (1994) Preparation and evaluation of peptidic aspartyl hemiacetala as reversible inhibitors of interleukin-1 β converting enzyme (ICE). Int J Pept Protein Res 44:173-182.
18. Guénal I, Fraisse CS, Gaumer S, Mignotte B (1997a) Bcl-2 and hsp27 act at different levels to suppress programmed cell death. Oncogene 15:347-460.
19. Guénal I, Risler Y, Mignotte B (1997b) Down-regulation of actin genes precedes microfilament network disruption and actin cleavage during p53-mcdiated apoptosis. J Cell Sci 110:489-495.
20. Guzhova IV, Arnholdt AC, Darieva ZA, Kinev AV, Lasunskaia EB, Nilsson K, Bozhkov VM, Voronin AP, Margulis BA (1998) Effects of exogeneous stress protein 70 on the functional properties of human promonocytes through binding to cell surface and internalization. Cell Stress Chaperones 3:67-77.
21. Hall AK (1995) Thymosin beta-10 accelerates apoptosis. Cell Mol Biol Res 41:167-180.
22. Hanley T, Merlie JP (1991) Transgene detection in unpurified mouse tail DNA by polymerase chain reaction. Biotechniques 10:56.
23. Hightower LE, Guidon PT (1989) Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol 138:257-266.
24. Hitchcock SE (1980) Actin deoxyribonuclease I interaction. J Biol Chem 255:5668-5673.
25. Hitotsumatsu T, Iwaki T, Fukui M, Tateishi J (1996) Distinctive immunochemical profiles of small heat shock proteins (heat shock protein 27 and alpha B-crystallin) in human brain tumors. Cancer 77:352-361.
26. Hollander H, Makarov F, Dreher Z, van Driel D, Chan-Ling TL, Stone J (1991) Structure of the macroglia of the retina: sharing and division of labor between astrocytes and Müller cells. J Comp Neurol 313:587-603.
27. Howard TH, Meyer WM (1984) Chemotactic peptide modulation of actin assembly and locomotion in neutrophils. J Cell Biol 98:1265-1271.
28. Huot J, Houle F, Spitz DR, Landry J (1996) HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res 56:273-279.
29. Jaattela M (1999) Escaping cell death: survival proteins in cancer. Exp Cell Res 248:30-43.
30. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517-1520.
31. Jans DA (1994) Nuclear signaling pathways for polypeptide ligands and their membrane receptors. FASEB J 8:841-847.
32. Kato H, Kogure K, Liu XH, Araki T, Kato K, Itoyama Y (1995) Immunohistochemical localization of the low molecular weight stress protein HSP27 following focal cerebral ischemia in the rat. Brain Res 679:1-7.
33. Kayalar C, Ord T, Testa MP, Zhong LT, Bredesen DB (1996) Cleavage of actin by interleukin 1β-converting enzyme to reverse DNase I inhibition. Proc Natl Acad Sci USA 93:2234-2238.
34. Kim JW, Wierda WG, Kim YB (1991) Immobilized IgG immune complex induces secretion of tumor necrosis factor-alpha by porcine alveolar macrophages. Am J Respir Cell Mol Biol 5:249-255.
35. Kolber MA, Broschat KO, Landa-Gonzales B (1990) Cytochalasin B induces cellular DNA fragmentation. FASEB J 12:3021-3027.
36. Lavoie JN, Hickey E, Weber LA, Landry J (1993) Induction of Chinese hamster hsp27 gene expression in mouse cells confers resistance to heat shock. Hsp27 stabilization of the microfilament organization. J Biol Chem 268:24210-24214.
37. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15:505-516.
38. Lazarides E, Lindherg U (1974) Actin is the naturally occurring inhibitor of Dnase I. Proc Natl Acad Sci USA 71:4742-4746.
39. Levee MG, Dabrowska MI, Lelli JL Jr, Hinshaw DB (1996) Actin polymerization and depolymerization during apoptosis in HL-60 cells. Am J Physiol 271:C1981-1992.
40. Lowry MB, Duchemin A, Robinson JM, Anderson CL (1998) Functional separation of pseudopod extension and particle internalization during Fcγ receptor-mediated phagocytosis. J Exp Med 187:161-176.
41. Mairesse N, Horman S, Mosselmans R, Galand P (1996) Antisense inhibition of the 27 kDa heat shock protein production affects growth rate and cytoskeletal organization in MCF-7 cells. Cell Biol Int 20:205-212.
42. Martin DA, Siegel RM, Zheng L, Lenardo MJ (1998) Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHα1) death signal. J Biol Chem 273:4345-4349.
43. Martin SJ, Green DR (1995) Protease activation during apoptosis: death by a thousand cuts? Cell 82:349-352.
44. Mashima T, Naito M, Kataoka S, Kawai H, Tsuruo T (1995a) Aspartate-based inhibitor of interleukin-1 β-converting enzyme prevents antitumor agent-induced apoptosis in human myeloid leukemia U937 cells. Biochem Biophys Res Commun 209:907-915.
45. Mashima T, Naito M, Fujita N, Noguchi K, Tsuruo T (1995b) Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis. Biochem Biophys Res Commun 217:1185-1192.
46. Mehlen P, Arrigo AP (1994) The serum-induced phosphorylation of mammalian hsp27 correlates with changes in its intracellular localization and levels of oligomerization. Eur J Biochem 221:327-334.
47. Mehlen P, Schulze-Osthoff K, Arrigo AP (1996a) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks fas/ apo-1-and staurosporine-induced cell death. J Biol Chem 271:16510-16514.
48. Mehlen P, Kretz-Remy C, Preville X, Arrigo AP (1996b) Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15:2695-2706.
49. Mehlen P, Hickey A, Weber LA, Arrigo A (1997) Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFα in NIH-3Y3-ras cells. Biochem Biophys Res Commun 241:187-192.
50. Mellman IS, Plutner H, Steinman RM, Unkcless JC, Cohn ZA (1983) Internalization and degradation of macrophage Fc receptors during receptor-mediated phagocytosis. J Cell Biol 96:887-895.
51. Moore A, Donahue CJ, Bauer KD, Mather JP (1998) Simultaneous measurement of cell cycle and apoptotic cell death. Methods Cell Biol 57:265-278.
52. Morino M, Tsuzuki T, Ishikawa Y, Shirakami T, Yoshimura M, Kiyosuke Y, Matsunaga K, Yoshikumi C, Saijo N (1997) Specific expression of HSP27 in human tumor cell lines in vitro. In Vivo 11:179-184.
53. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759-803.
54. Multhoff G, Hightower LE (1996) Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperone 1:167-177.
55. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM (1996) FLICE, a novel FADD homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/Apo-1) death-inducing signaling complex. Cell 85:817-827.
56. Piselli P, Vendetti S, Poccia F, Cicconi R, Mattei M, Bolognesi A, Stirpe F, Colizzi V (1995) In vitro and in vivo efficacy of heat shock protein specific immunotoxins on human tumor cells. J Biol Regul Homeost Agents 9:55-62.
57. Poccia F, Piselli P, Di Cesare S, Bach S, Colizzi V, Mattei M, Bolognesi A, Stirpe F (1992) . Recognition and killing of tumor cells expressing heat shock protein 65 kD with immunotoxins containing saporin. Br J Cancer 66:427-432.
58. Provis JM, Penfold PL, Edwards AJ, van Driel D (1995) Human retinal microglia: expression of immune markers and relationship to the glia limitans. Glia 14:243-256.
59. Raffray M, Cohen GM (1991) Bis(tri-n-butyltin)oxide induces programmed cell death (apoptosis) in immature rat thymocytes. Arch Toxicol 65:135-139.
60. Reichlin M (1995) Cell injury mediated by autoantibodies to intracellular antigens. Clin Immunol Immunopathol 76:215-219.
61. Reichlin M (1998) Cellular dysfunction induced by penetration of autoantibodies into living cells: cellular damage and dysfunction mediated by antibodies to dsDNA and ribosomal P proteins. Autoimmunity 11:557-561.
62. Riabowol K, Mizzen L, Welch WJ (1988) Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 242:433-436.
63. Ronda N, Gatti R, Orlandini G, Borghetti A (1997) Binding and internalization of human IgG by living cultured endothelial cells. Clin Exp Immunol 109:211-216.
64. Samali A, Cotter TG (1996) Heat shock proteins increase resistance to apoptosis. Exp Cell Res 223:163-170.
65. Scanlon M, Laster SM, Wood JG, Gooding LR (1989) Cytolysis by tumor necrosis factor is preceded by a rapid and specific dissolution of microfilaments. Proc Natl Acad Sci USA 86:182-186.
66. Schett G, Xu Q, Amberger A, Van der Zee R, Recheis H, Willeit J, Wick G (1995) Autoantibodies against hsp60 mediates endothelial cytotoxicity. J Clin Invest 96:2569-2577.
67. Schmid SL (1992) The mechanism of receptor-mediated endocytosis: more questions than answers. BioEssays 14:589-596.
68. Schnitzer J, Scherer J (1990) Microglial cell responses in the rabbit retina following transection of the optic nerve. J Comp Neurol 302:779-791.
69. Seigel GM (1996) Establishment of an E1A-immortalized retinal cell culture. In Vitro Cell Dev Biol Anim 32:66-68.
70. Sheller RA, Smyers ME, Grossfeld RM, Ballinger ML, Bittner GD (1998) Heat-shock proteins in axoplasm: high constitutive levels and transfer of inducible isoforms from glia. J Comp Neurol 396:1-11.
71. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8 and -10 in caspase-9-dependent manner. J Cell Biol 144:281-292.
72. Song Q, Wei T, Lees-Miller S, Alnemri E, Watters D, Lavin MF (1997) Resistance of actin to cleavage during apoptosis. Proc Natl Acad Sci USA 94:157-162.
73. Srivastava PK (1994) Heat shock proteins in immune response to cancer: the fourth paradigm. Experientia 50:1054-1060.
74. Tezel G, Wax MB (1999) Inhibition of caspase activity in retinal cell apoptosis induced by various stimuli, in vitro. Invest Ophthalmol Vis Sci 40:2660-2667.
75. Tezel G, Seigel GM, Wax MB (1998) Autoantibodies to small heat shock proteins in glaucoma. Invest Ophthalmol Vis Sci 39:2777-2787.
76. Tezel G, Hernandez MR, Wax MB (2000) Immunostaining of heat shock proteins in the retina and optic nerve head of normal and glaucomatous eyes. Arch Ophthalmol 118:511-518.
77. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, Elliston KO, Ayala JM, Casano FJ, Chin J, Ding GJ-F, Egger LA, Gaffney EP, Limjuco G, Palyha OC, Raju SM, Rolando AM, Salley JP, Yamin T-T, Lee TD, Shively JE, MacCross M, Mumford RA, Schmidt JA, Tocci MJ (1992) A novel heterodimeric cystein protease is required for interleukin-1 β processing in monocytes. Nature 356:768-774.
78. Tsukidate K, Yamamoto K, Snyder JW, Farber JL (1993) Microtubule antagonists activate programmed cell death (apoptosis) in cultured rat hcpatocytcs. Am J Pathol 143:918-925.
79. Tytell M, Greenberg SG, Lasek RG (1986) Heat shock-like protein is transferred from glia to axon. Brain Res 363:161-164.
80. van Engeland M, Kuijpers HJH, Ramackers FCS, Reutelingsperger CPM, Schutte B (1997) Plasma membrane alterations and cytoskeletal changes in apoptosis. Exp Cell Res 235:421-430.
81. Villa PG, Henzel WJ, Sensenbrenner M, Henderson CE, Pettmann B (1998) Calpain inhibitors, but not caspase inhibitors, prevent actin proteolysis and DNA fragmentation during apoptosis. J Cell Sci 111:713-722.
82. Wagstaff MJ, Collaco-Moraes Y, Smith J, de Belleroche JS, Coffin RS, Latchman DS (1999) Protection of neuronal cells from apoptosis by hsp27 delivered with a Herpes Simplex virus-based vector. J Biol Chem 274:5061-5069.
83. Wax MB, Tezel G, Edward DP (1998) Clinical and pathological findings of a patient with normal pressure glaucoma. Arch Ophthalmol 116:993-1001.
84. Welch WJ, Suhan JP (1985) Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol 101:1198-211.
85. Wickstrom ML, Khan SA, Haschek WM, Wyman JF, Eriksson JE, Schaeffer DJ, Beasley VR (1995) Alterations in microtubules, intermediate filaments and microfilaments induced by microcystin-LR in cultured cells. Toxicol Pathol 23:326-337.
86. Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76:4498-4502.
87. Yanase K, Smith RM, Puccetti A, Jarett L, Madaio M (1997) Receptor-mediated cellular entry of nuclear localizing anti-DNA antibodies via myosin 1. J Clin Invest 100:25-31.
88. Young DB (1992) Heat-shock proteins: immunity and autoimmunity. Curr Opin Immunol 4:396-400.