Plasma membrane bleb formation and rupture: A common feature of hepatocellular injury

Abstract

HepatologyVolume 11, Issue 4 p. 690-698 Special ArticleFree Access Plasma membrane bleb formation and rupture: A common feature of hepatocellular injury Gregory J. Gores, Gregory J. Gores Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Search for more papers by this authorBrian Herman, Brian Herman Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Search for more papers by this authorDr. John J. Lemasters, Corresponding Author Dr. John J. Lemasters Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Laboratories for Cell Biology, Department of Cell Biology & Anatomy, Campus Box 7090, 236 Swing Building, Chapel Hill, NC 27599-7090===Search for more papers by this author Gregory J. Gores, Gregory J. Gores Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Search for more papers by this authorBrian Herman, Brian Herman Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Search for more papers by this authorDr. John J. Lemasters, Corresponding Author Dr. John J. Lemasters Laboratories for Cell Biology, Department of Cell Biology & Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, Campus Box 7090, 236 Swing Building, Chapel Hill, North Carolina 27599-7090Laboratories for Cell Biology, Department of Cell Biology & Anatomy, Campus Box 7090, 236 Swing Building, Chapel Hill, NC 27599-7090===Search for more papers by this author First published: April 1990 https://doi.org/10.1002/hep.1840110425Citations: 155AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL References 1 Siesjo BK. Cell damage in the brain: a speculative synthesis. J Cereb Blood Flow Metab 1981; 1: 155– 185. 2 Chien KR, Sen A, Reynolds R, Chang A, Kim Y, Gunn MD, Buja LM, et al. Release of arachidonate from membrane phospholipids in cultured neonatal rat myocardial cells during adenosine triphosphate depletion: correlation with the progression of cell injury. J Clin Invest 1985; 75: 1770– 1780. 3 Phelps PC, Smith MW, Trump BF. Cytosolic ionized calcium and bleb formation after acute cell injury of cultured rabbit renal tubule cells. Lab Invest 1989; 60: 630– 642. 4 Lewis MR. Reversible gelation in living cells. Bull John Hopkins Hosp 1923; 34: 373– 379. 5 Zollinger HU. Cytologic studies with the phase microscope: formation of “blisters” on cells in suspension (potocytosis), with observations on the nature of the cellular membrane. Am J Pathol 1948; 24: 545– 567. 6 Costero I, Pomerat CM. Cultivation of neurons from the adult human cerebral and cerebellar cortex. Am J Anat 1951; 89: 405– 467. 7 Trump BF, Goldblatt PJ, Stowell RE. An electron microscopic study of early cytoplasmic alterations in hepatic parenchymal cells of mouse liver during necrosis in vitro (autolysis). Lab Invest 1962; 11: 986– 1015. 8 Lemasters JJ, Ji S, Thurman RG. Centrilobular injury following hypoxia in isolated perfused rat liver. Science 1981; 213: 661– 663. 9 Lemasters JJ, Stemkowski CJ, Ji S, Thurman RG. Cell surface changes and enzyme release during hypoxia and reoxygenation in the isolated, perfused rat liver. J Cell Biol 1983; 97: 778– 786. 10 Lemasters JJ, Ji S, Stemkowski CJ, Thurman RG. Hypoxic hepatocellular injury. Pharmacol Biochem Behav 1983; 18 [suppl. 1]: 455– 459. 11 Lemasters JJ, DiGuiseppi J, Nieminen A-L, Herman B. Blebbing, free Ca+2 and mitochondrial membrane potential preceding cell death in hepatocytes. Nature 1987; 325: 78– 81. 12 Herman B, Nieminen A-L, Gores GJ, Lemasters JJ. Irreversible injury in anoxic hepatocytes precipitated by an abrupt increase in plasma membrane permeability. FASEB J 1988; 2: 146– 151. 13 Walker RM, McElligott TF, Massey TE, Racz WJ. Ultrastructural effects of acetaminophen in isolated mouse hepatocytes. Exp Mol Pathol 1983; 39: 163– 175. 14 Reynold ES. Liver parenchymal cell injury. I. Initial alterations of the cell following poisoning with carbon tetrachloride. J Cell Biol 1963; 19: 139– 157. 15 Nordstoga K, Aasen AO. Hepatic changes in late canine endotoxin shock, a light and electron microscopic investigation. Acta Path Microbiol Scand Sect A 1979; 87: 335– 346. 16 Donohoe MJ, Rush BF Jr, Machiedo GW, Barillo DJ, Murphy TF. Biochemical and morphologic changes in hepatocytes from the shock injured liver. Surg Gynecol Obstet 1986; 162: 323– 333. 17 Vital A, Bioulac-Sage P, Bedin C, Balabaud C. Bile canaliculi morphology after bile duct ligation in the rat with portacaval shunt: a time-course study. Liver 1982; 2: 230– 235. 18 Caldwell-Kenkel JC, Thurman RG, Lemasters JJ. Selective loss of nonparenchymal cell viability after cold ischemic storage of rat livers. Transplantation 1987; 45: 834– 837. 19 McKeown CMB, Edwards V, Phillips MJ, Harvey PRC, Petrunka CN, Strasberg SM. Sinusoidal lining cell damage: the critical injury in cold preservation of liver allografts in the rat. Transplantation 1988; 46: 178– 191. 20 Caldwell-Kenkel JC, Currin RT, Tanaka Y, Thurman RG, Lemasters JJ. Reperfusion injury to endothelial cells following cold ischemic storage of rat livers. HEPATOLOGY 1989; 10: 292– 299. 21 Jewell SA, Bellomo G, Thor H, Orrenius S, Smith MT. Bleb formation in hepatocytes during drug metabolism is caused by disturbances in thiol and calcium ion homeostasis. Science 1982; 217: 1257– 1259. 22 Searle J, Harmon BV, Bishop CJ, Kerr JFR. The significance of cell death by apoptosis in hepatobiliary disease. J Gastroenterol Hepatol 1987; 2: 77– 96. 23 Berger ML, Reynolds RC, Hagler HK, Bellotto D, Parsons D, Mulligan KJ, Buja LM. Anoxic injury: role of reversible changes in elemental content and distribution. HEPATOLOGY 1989; 9: 219– 228. 24 Nieminen A-L, Gores GJ, Tanaka Y, Herman B, Lemasters JJ. Calcium dependence of bleb formation and cell death in hepatocytes. Cell Calcium 1988; 9: 237– 246. 25 Berger ML, Reynolds RC, Combes B. Carbon tetrachloride-induced morphologic alterations in isolated rat hepatocytes. Exp Mol Pathol 1987; 46: 245– 257. 26 Prentki M, Chaponnier C, Jeanrenaud B, Gabbiani G. Actin microfilaments, cell shape, and secretory processes in isolated rat hepatocytes. J Cell Biol 1979; 81: 592– 607. 27 Virtanen I, Miettinen A. The role of actin in the surface integrity of cultured rat liver a cells. Cell Biol Int Rep 1980; 4: 29– 36. 28 Koo EW, Hayes A, Wong MK, Gotlieb AI. Aflatoxin B1 and acetaminophen induce different cytoskeletal responses during prelethal hepatocyte injury. Exp Mol Pathol 1987; 47: 37– 47. 29 Steenbergen C, Hill ML, Jennings RB. Cytoskeletal damage during myocardial ischemia: changes in vinculin immunofluorescence staining during total in vitro ischemia in canine heart. Circ Res 1987; 60: 478– 486. 30 Smith MT, Thor H, Jewell SA, Bellomo G, Sandy MS, Orrenius S. Free radical changes in the surface morphology of isolated hepatocytes. In: D Armstrong, RS Sohal, RG Cutler, eds. Free radicals in molecular biology: aging and disease. New York: Raven Press, 1984; 33– 340. 31 Weeds A. Actin-binding proteins: regulators of cell architecture and motility. Nature 1982; 296: 811– 816. 32 Regula CS, Pfeiffer JR, Berlin RD. Microtubule assembly and disassembly at alkaline pH. J Cell Biol 1981; 89: 45– 53. 33 Nachmias VT, Yoshida K, Glennon MC. Lowering pH in blood platelets dissociates myosin phosphorylation from shape change and myosin association with the cytoskeleton. J Cell Biol 1987; 105: 1761– 1769. 34 Bellomo G, Orrenius S. Altered thiol and calcium homeostasis in oxidative hepatocellular injury. HEPATOLOGY 1985; 5: 876– 882. 35 Phillips MJ, Satir P. The cytoskeleton of the hepatocyte: organization, relationships and pathology. In: IA Arias, WB Jakoby, H Popper, Schafritz DA Schachter, eds. The liver: biology and pathobiology. New York: Raven Press, 1988: 11– 27. 36 Nicotera P, Thor H, Orrenius S. Cytosolic-free Ca+2 and cell killing in hepatoma 1c1c7 cells exposed to chemical anoxia. FASEB J 1989; 3: 59– 64. 37 Gores GJ, Nieminen A-L, Fleishman KE, Dawson TL, Herman B, Lemasters JJ. Extracellular acidosis delays onset of cell death in ATP-depleted hepatocytes. Am J Physiol 1988; 235: C315– C322. 38 Gores GJ, Nieminen A-L, Wray B, Herman B, Lemasters JJ. Intracellular pH during “chemical hypoxia” in cultured rat hepatocytes: protection by intracellular acidosis against the onset of cell death. J Clin Invest 1989; 83: 386– 396. 39 Gores GJ, Flarsheim CE, Dawson TL, Nieminen A-L, Herman B, Lemasters JJ. Swelling, reductive stress and cell death during chemical hypoxia in hepatocytes. Am J Physiol 1989; 257: C347– C354. 40 Brodie AE, Reed DJ. Reversible oxidation of glyceraldehyde-3-phosphate dehydrogenase thiols in human lung carcinoma cells by hydrogen peroxide. Biochem Biophys Res Commun 1987; 148: 120– 125. 41 Webb JL. Enzyme and metabolic inhibitors. Vol. 3. New York: Academic Press, Inc., 1966: 1028 pp. 42 Kreisberg JI, Mills JW, Jarrel JA, Rabito CA, Leaf A. Protection of cultured renal tubular epithelial cells from anoxic cell swelling and cell death. Proc Natl Acad Sci USA 1980; 77: 5445– 5447. 43 Monte DD, Sandy MS, Ekstrom G, Smith MT. Comparative studies on the mechanism of paraquat and 1-methyl-4-phenylpyridine (MPP1) cytotoxicity. Biochem Biophys Res Comm 1986; 137: 303– 309. 44 Nicotera P, Hartzell P, Baldi C, Svensson SA, Bellomo G, Orrenius S. Cystamine induces toxicity in hepatocytes through the elevation of cytosolic Ca−2 and the stimulation of a nonlysosomal proteolytic system. J Biol Chem 1986; 261: 14628– 14635. 45 Nicotera P, Hartzell P, Davis G, Orrenius S. The formation of plasma membrane blebs in hepatocytes exposed to agents that increase cytosolic Ca2+ is mediated by the activation of a non-lysosomal proteolytic system. FEBS Lett 1986; 209: 139– 144. 46 Lemasters JJ, Nieminen A-L, Gores GJ, Wray BE, Herman B. Cytosolic free calcium and cell injury in hepatocytes. In: G Fiskum, ed. Cell calcium metabolism. New York: Plenum Publishing Corp., 1989: 463– 470. 47 Herman B, Nieminen A-L, Gores GJ, Lemasters JJ. Blebbing, cytosolic free calcium, and mitochondrial membrane potential following toxic or anoxic in In: JJ Lemasters, CR Hackenbrock, RG Thurman, HV Westerhoff, eds. Integration of mitochondrial function. New York: Plenum Press, 1989: 479– 491. 48 Nieminen A-L, Gores GJ, Dawson TL, Herman B, Lemasters JJ. Toxic injury from mercuric chloride in rat hepatocytes. J Biol Chem 1990; 265: 2399– 2408. 49 Mirabelli F, Salis A, Marinoni V, Finardi F, Bellomo G, Thor H, Orrenius S. Menadione-induced bleb formation in hepatocytes is associated with the oxidation of thiol groups in actin. Arch Biochem Biophys 1988; 264: 261– 269. 50 Chien KR, Abrams J, Serroni A, Martin JT, Farber JL. Accelerated phospholipid degradation and associated membrane dysfunction in irreversible ischemic liver cell injury. J Biol Chem 1978; 253: 4809– 4817. 51 Matthys E, Patel Y, Kreisberg J, Stewart JH, Venkatachalam M. Lipid alterations induced by renal ischemia: pathogenic factor in membrane damage. Kidney Int 1984; 26: 153– 161. 52 Sen A, Miller JC, Reynolds R, Willerson JT, Buja M, Chien KR. Inhibition of the release of arachidonic acid prevents the development of sarcolemmal membrane defects in cultured rat myocardial cells during adenosine-triphosphate depletion. J Clin Invest 1988; 82: 1333– 1338. 53 Florine-Casteel K, Lemasters JJ, Herman B. Digitized fluorescence polarization microscopy of DPH and related probes in In: K Jacobson, B Herman, eds. Optical microscopy for biology. New York: Gordon & Breech, 1990; 559– 574. 54 Andersson BS, Aw TY, Jones DP. Mitochondrial transmembrane potential and pH gradient during anoxia. Am J Physiol 1987; 252: C349– C355. 55 Jones DP, Kennedy FG, Andersson BS, Aw TY, Wilson E. When is a mammalian cell hypoxic? Insights from studies of cells vs. mitochondria. Mol Physiol 1985; 8: 473– 482. 56 Gordon PB, Tolleshaug H, Seglen PO. Autophagic sequestration of [14C] sucrose introduced into isolated rat hepatocytes by electrical and nonelectrical methods. Exp Cell Res 1985; 160: 449– 458. 57 Dancygier H, Runne U, Leuschner U, Milbradt R, Classen M. Dacarbazine (DTIC)-induced human liver damage: light and electron-microscope findings. Hepatogastroenterology 1983; 30: 93– 95. 58 Schaffner F. Intralobular changes in hepatocytes and the electron microscopic mesenchymal response in acute viral hepatitis. Medicine 1966; 45: 547– 552. 59 Scheinberg IH, Sternlieb I. Pathology of the liver. In: IH Scheinberg, I Sternlieb, eds. Wilson's disease. Philadelphia: W. B. Saunders, 1984: 38– 63. 60 Gudat F, Spichtin HP, Stocklin E, Krey G, Altorfer J, Schmid M, Bianchi L. Electron microscopic studies of delta infection. Prog Clin Biol Res 1983; 143: 181– 189. 61 Zafrani ES, Bernuau D, Feldman G. Peliosis-like ultrastructural changes of the hepatic sinusoids in human chronic hypervitaminosis A: report of 3 cases. Hum Pathol 1984; 15: 1166– 1170. 62 Zafrani ES, Cazier A, Baudelot A-M, Feldman G. Ultrastructural lesions of the liver in human peliosis: a report of 12 cases. Am J Pathol 1984; 114: 349– 369. 63 Pfeifer U, Aterman K. Shedding of peripheral cytoplasm: a mechanism of liver cell atrophy in human amyloidosis. Virchows Arch [B] 1979; 29: 229– 243. 64 Tobe K. Electron microscopy of liver lesions in primary biliary cirrhosis. I. Intrahepatic bile duct oncocytes. Acta Pathol Jpn 1982; 32: 357– 370. 65 MJ Phillips, S Powell, J Patterson, P Valencia, eds. The liver: an atlas and text of ultrastructural pathology. New York: Raven Press, 1987: 46, 72, 87, 107, 146, 351, 522– 523. 66 French SW, Benson NC, Sun PS. Centrilobular liver necrosis induced by hypoxia in chronic ethanol-fed rats. HEPATOLOGY 1984; 4: 912– 917. 67 Fredricks WM, Myagkaya GL, Bosch KS, Fronik GM, Veen HV, Vogels IMC, James J. The value of enzyme leakage for the prediction of necrosis in liver ischemia. Histochemistry 1983; 78: 459– 472. 68 Yamada G, Sakamoto Y, Mizuno M, Kobayashi T, Nagashima H. Electron microscopic observations of hepatitis B virus budding from hepatocytes into bile canaliculi. Acta Med Okayama 1980; 34: 203– 207. 69 Becker LC, Ambrosio G. Myocardial consequences of reperfusion. Prog Cardiovasc Dis 1987; 30: 23– 44. 70 Searle J, Kerr JF, Bishop CJ. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu 1982; 17: 229– 259. 71 Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251– 306. 72 McConkey DJ, Hartzell P, Duddy SK, Hakansson H, Orrenius S. 2, 3, 7, 8-tetrachlorodibenzo-para-dioxin kills immature thymocytes by Ca+2-mediated endonuclease activation. Science 1988; 242: 256– 259. 73 Searle J, Harmon BV, Bishop CJ, Kerr JFK. The significance of cell death by apoptosis in hepatobiliary disease. J Gastroenterol Hepatol 1987; 2: 77– 96. Citing Literature Volume11, Issue4April 1990Pages 690-698 ReferencesRelatedInformation