Apoptosis in the pathogenesis and treatment of disease

In multicellular organisms, homeostasis is maintained through a balance between cell proliferation and cell death. Although much is known about the control of cell proliferation, less is known about the control of cell death. Physiologic cell death occurs primarily through an evolutionarily conserved form of cell suicide termed apoptosis. The decision of a cell to undergo apoptosis can be influenced by a wide variety of regulatory stimuli. Recent evidence suggests that alterations in cell survival contribute to the pathogenesis of a number of human diseases, including cancer, viral infections, autoimmune diseases, neurodegenerative disorders, and AIDS (acquired immunodeficiency syndrome). Treatments designed to specifically alter the apoptotic threshold may have the potential to change the natural progression of some of these diseases.

[1]  W. Bursch,et al.  Cell death by apoptosis and its protective role against disease. , 1992, Trends in pharmacological sciences.

[2]  Matthew J. Brauer,et al.  Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. , 1994, Science.

[3]  Xin Lu,et al.  Differential induction of transcriptionally active p53 following UV or lonizing radiation: Defects in chromosome instability syndromes? , 1993, Cell.

[4]  D. Bredesen,et al.  bcl-2 inhibits death of central neural cells induced by multiple agents. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Raff,et al.  Programmed cell death and Bcl‐2 protection in the absence of a nucleus. , 1994, The EMBO journal.

[6]  C. Croce,et al.  The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. , 1985, Science.

[7]  M. Koury,et al.  Survival or death of individual proerythroblasts results from differing erythropoietin sensitivities: a mechanism for controlled rates of erythrocyte production. , 1993, Blood.

[8]  A. Abbas,et al.  The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. , 1994, Immunity.

[9]  M. Colombel,et al.  Hormone-regulated apoptosis results from reentry of differentiated prostate cells onto a defective cell cycle. , 1992, Cancer research.

[10]  M. Fishman,et al.  Prevention of vertebrate neuronal death by the crmA gene. , 1994, Science.

[11]  Y. Yoshida Hypothesis: apoptosis may be the mechanism responsible for the premature intramedullary cell death in the myelodysplastic syndrome. , 1993, Leukemia.

[12]  J. Cohen,et al.  Apoptosis: the physiologic pathway of cell death. , 1993, Hospital practice.

[13]  C. Haslett,et al.  Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. , 1994, Journal of immunology.

[14]  J. Lotem,et al.  Control of programmed cell death in normal and leukemic cells: new implications for therapy. , 1993, Blood.

[15]  V. Fadok,et al.  Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. , 1992, Journal of immunology.

[16]  O. Isacson,et al.  On neuronal health , 1993, Trends in Neurosciences.

[17]  K. M. Lam,et al.  Apoptosis induced by infectious bursal disease virus. , 1994, The Journal of general virology.

[18]  M. Rowe,et al.  Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Kloner,et al.  Reperfusion injury induces apoptosis in rabbit cardiomyocytes. , 1994, The Journal of clinical investigation.

[20]  J. Guthridge,et al.  Activation-dependent apoptosis in CD4+ T cells during murine AIDS. , 1993, Cellular immunology.

[21]  A. Strasser,et al.  Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2 , 1990, Nature.

[22]  N. Copeland,et al.  Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis , 1992, Nature.

[23]  J. Lotem,et al.  Regulation by bcl-2, c-myc, and p53 of susceptibility to induction of apoptosis by heat shock and cancer chemotherapy compounds in differentiation-competent and -defective myeloid leukemic cells. , 1993, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[24]  F. Marumo,et al.  Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. , 1994, Circulation research.

[25]  R. Goldin,et al.  Apoptotic bodies in a murine model of alcoholic liver disease: Reversibility of ethanol‐induced changes , 1993, The Journal of pathology.

[26]  Gerard I. Evan,et al.  Induction of apoptosis in fibroblasts by c-myc protein , 1992, Cell.

[27]  John Calvin Reed Bcl-2 and the regulation of programmed cell death , 1994, The Journal of cell biology.

[28]  J C Reed,et al.  Antisense-mediated inhibition of BCL2 protooncogene expression and leukemic cell growth and survival: comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. , 1990, Cancer research.

[29]  Shai Shaham,et al.  The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme , 1993, Cell.

[30]  R. Fleischman Southwestern Internal Medicine Conference: clinical use of hematopoietic growth factors. , 1993, The American journal of the medical sciences.

[31]  M. Newell,et al.  Death of mature T cells by separate ligation of CD4 and the T-cell receptor for antigen , 1990, Nature.

[32]  G. Delespesse,et al.  Interleukin 4 protects chronic lymphocytic leukemic B cells from death by apoptosis and upregulates Bcl-2 expression , 1992, The Journal of experimental medicine.

[33]  B. Barres,et al.  Programmed cell death and the control of cell survival: lessons from the nervous system. , 1993, Science.

[34]  T. M. Dexter,et al.  Suppression of apoptosis allows differentiation and development of a multipotent hemopoietic cell line in the absence of added growth factors , 1993, Cell.

[35]  R. Craig,et al.  MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Choi Excitotoxic cell death. , 1992, Journal of neurobiology.

[37]  J. Cyster,et al.  Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire , 1994, Nature.

[38]  G. Núñez,et al.  Expression of the apoptosis-suppressing protein bcl-2, in neuroblastoma is associated with unfavorable histology and N-myc amplification. , 1993, The American journal of pathology.

[39]  R. J. Clem,et al.  Control of programmed cell death by the baculovirus genes p35 and iap , 1994, Molecular and cellular biology.

[40]  M. Berger,et al.  Characterization of A1, a novel hemopoietic-specific early-response gene with sequence similarity to bcl-2. , 1993, Journal of immunology.

[41]  I. Weissman,et al.  Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. , 1992, Science.

[42]  M. Campbell,et al.  Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. , 1992, Cancer research.

[43]  Z. Oltvai,et al.  BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax , 1994, Nature.

[44]  S. Korsmeyer,et al.  Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair , 1993, Cell.

[45]  S. Cohen,et al.  PURIFICATION OF A NERVE-GROWTH PROMOTING PROTEIN FROM THE MOUSE SALIVARY GLAND AND ITS NEURO-CYTOTOXIC ANTISERUM. , 1960, Proceedings of the National Academy of Sciences of the United States of America.

[46]  T. Buttke,et al.  Oxidative stress as a mediator of apoptosis. , 1994, Immunology today.

[47]  Y. Hao,et al.  Apoptosis: Final common pathway of photoreceptor death in rd, rds, and mutant mice , 1993, Neuron.

[48]  Lianfa Shi,et al.  Premature p34cdc2 activation required for apoptosis. , 1994, Science.

[49]  L. Wang,et al.  Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death , 1994, Cell.

[50]  A. Barzilai,et al.  Dopamine induces apoptosis-like cell death in cultured chick sympathetic neurons — A possible novel pathogenetic mechanism in Parkinson's disease , 1994, Neuroscience Letters.

[51]  John Calvin Reed,et al.  Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line. , 1993, Blood.

[52]  M. Raff,et al.  Social controls on cell survival and cell death , 1992, Nature.

[53]  C. Thompson,et al.  bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. , 1994, Development.

[54]  Horvitz,et al.  Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. , 1991, Genetics.

[55]  E. Kieff,et al.  Induction of bcl-2 expression by epstein-barr virus latent membrane protein 1 protects infected B cells from programmed cell death , 1991, Cell.

[56]  C. Cotman,et al.  Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Fisher Apoptosis in cancer therapy: Crossing the threshold , 1994, Cell.

[58]  David L. Vaux,et al.  An evolutionary perspective on apoptosis , 1994, Cell.

[59]  H. Lehmann,et al.  Osteoarthrosis of the ankle joints in old rats. , 1992, Zeitschrift fur Rheumatologie.

[60]  P. Neiman,et al.  Induction of apoptosis during normal and neoplastic B-cell development in the bursa of Fabricius. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[61]  W. Emlen,et al.  Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. , 1994, Journal of immunology.

[62]  M. Shelanski,et al.  Down-regulation of copper/zinc superoxide dismutase causes apoptotic death in PC12 neuronal cells. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Goverman,et al.  T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. , 1994, Science.

[64]  S. Mori,et al.  A protective action of chondroitin sulfate proteoglycans against neuronal cell death induced by glutamate , 1994, Brain Research.

[65]  C. Purdie,et al.  Thymocyte apoptosis induced by p53-dependent and independent pathways , 1993, Nature.

[66]  K. Muta,et al.  Apoptosis of human erythroid colony‐forming cells is decreased by stem cell factor and insulin‐like growth factor I as well as erythropoietin , 1993, Journal of cellular physiology.

[67]  L. Montagnier,et al.  Apoptosis in AIDS. , 1993, Science.

[68]  D. Bredesen,et al.  Expression of the Baculovirus p35 Gene Inhibits Mammalian Neural Cell Death , 1993, Journal of neurochemistry.

[69]  C. Thompson,et al.  bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death , 1993, Cell.

[70]  S. Korsmeyer,et al.  Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around Jh on chromosome 14 and near a transcriptional unit on 18 , 1985, Cell.

[71]  D. Littman Immunodeficiency Viruses: Not enough sans Nef , 1994, Current Biology.

[72]  Z. Oltvai,et al.  Bcl-2 functions in an antioxidant pathway to prevent apoptosis , 1993, Cell.

[73]  Y. Ishizaki,et al.  Autocrine signals enable chondrocytes to survive in culture , 1994, The Journal of cell biology.

[74]  D. Vaux,et al.  Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[75]  P. Henkart Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. , 1994, Immunity.

[76]  Scott W. Lowe,et al.  p53 is required for radiation-induced apoptosis in mouse thymocytes , 1993, Nature.

[77]  K. Imahori,et al.  Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[78]  T. Crawford,et al.  The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy , 1995, Cell.

[79]  S. Butcher,et al.  Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia , 1994, Nature.

[80]  E. Arenas,et al.  Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo , 1994, Nature.

[81]  J. M. Lee,et al.  p53 mutations increase resistance to ionizing radiation. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[82]  J. Haines,et al.  Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis , 1993, Nature.

[83]  J. Sklar,et al.  Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[84]  S. Korsmeyer,et al.  BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[85]  J. Rothman,et al.  Baculovirus p35 prevents developmentally programmed cell death and rescues a ced‐9 mutant in the nematode Caenorhabditis elegans. , 1994, The EMBO journal.

[86]  F. Miedema,et al.  Programmed death of T cells in HIV-1 infection. , 1992, Science.

[87]  N. Copeland,et al.  Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme. , 1994, Genes & development.

[88]  N. Heintz Cell death and the cell cycle: a relationship between transformation and neurodegeneration? , 1993, Trends in biochemical sciences.

[89]  S. Korsmeyer,et al.  The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[90]  A. Wyllie,et al.  Cell death: the significance of apoptosis. , 1980, International review of cytology.

[91]  W. Bursch,et al.  Determination of the length of the histological stages of apoptosis in normal liver and in altered hepatic foci of rats. , 1990, Carcinogenesis.

[92]  Hans Hengartner,et al.  Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice , 1994, Nature.

[93]  T. Dexter,et al.  Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis , 1990, Nature.

[94]  A. Levine The tumor suppressor genes. , 1993, Annual review of biochemistry.

[95]  S. Korsmeyer,et al.  Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death , 1993, Cell.

[96]  Z. Werb,et al.  Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix , 1995, Science.

[97]  R. Black,et al.  Viral inhibition of inflammation: Cowpox virus encodes an inhibitor of the interleukin-1β converting enzyme , 1992, Cell.

[98]  S. Orrenius,et al.  Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. , 1989, The Journal of biological chemistry.

[99]  E. Rozengurt Growth factors and cell proliferation. , 1992, Current opinion in cell biology.

[100]  C. Haslett,et al.  Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. , 1992, Journal of immunology.

[101]  E. Podack,et al.  Apoptosis of lung cancer cells caused by some anti-cancer agents (MMC, CPT-11, ADM) is inhibited by bcl-2. , 1993, Biochemical and biophysical research communications.

[102]  L. Rubin,et al.  The cell cycle and cell death , 1993, Current Biology.

[103]  John Calvin Reed,et al.  Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene , 1993, Nature.

[104]  P. Bedossa,et al.  Genetic analysis of immune dysfunction in non‐obese diabetic (NOD) mice: Mapping of a susceptibility locus close to the Bcl‐2 gene correlates with increased resistance of NOD T cells to apoptosis induction , 1994, European journal of immunology.

[105]  D. Rock,et al.  An African swine fever virus gene with similarity to the proto-oncogene bcl-2 and the Epstein-Barr virus gene BHRF1 , 1993, Journal of virology.

[106]  D. Oprian,et al.  Rhodopsin mutation G90D and a molecular mechanism for congenital night blindness , 1994, Nature.

[107]  D. Housman,et al.  p53 status and the efficacy of cancer therapy in vivo. , 1994, Science.

[108]  H Hengartner,et al.  Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. , 1994, Science.

[109]  R. Schreiber,et al.  Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death , 1990, Nature.

[110]  D. Hicks,et al.  BCL-2 expression in human colorectal adenomas and carcinomas. , 1994, Oncogene.

[111]  Junying Yuan,et al.  Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3 , 1993, Cell.

[112]  Timothy J. Ley,et al.  Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells , 1994, Cell.

[113]  J. M. Boyd,et al.  Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins , 1994, Cell.

[114]  M. Roederer,et al.  N-acetylcysteine: potential for AIDS therapy. , 1993, Pharmacology.

[115]  J. Mountz,et al.  Autoimmune disease. A problem of defective apoptosis. , 1994, Arthritis and rheumatism.

[116]  A. Capron,et al.  Cell dysfunction and depletion in AIDS: the programmed cell death hypothesis. , 1991, Immunology today.

[117]  S. Estus,et al.  Analysis of cell cycle-related gene expression in postmitotic neurons: Selective induction of cyclin D1 during programmed cell death , 1994, Neuron.

[118]  E. Hirsch,et al.  GM-1 ganglioside promotes the recovery of surviving midbrain dopaminergic neurons in MPTP-treated monkeys , 1993, Neuroscience.

[119]  M. Pericak-Vance,et al.  Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. , 1993, Science.

[120]  H. Horvitz,et al.  C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2 , 1994, Cell.

[121]  A. Ryan Russell , 1996 .

[122]  P. G. Tyler,et al.  Interleukin-3 and bryostatin-1 mediate hyperphosphorylation of BCL2 alpha in association with suppression of apoptosis. , 1994, The Journal of biological chemistry.

[123]  Y. Lévy,et al.  Interleukin-10 prevents spontaneous death of germinal center B cells by induction of the bcl-2 protein. , 1994, The Journal of clinical investigation.

[124]  B. Hoffman,et al.  Molecular controls of apoptosis: differentiation/growth arrest primary response genes, proto-oncogenes, and tumor suppressor genes as positive & negative modulators. , 1994, Oncogene.

[125]  I. Stamenkovic,et al.  Fas and tumor necrosis factor receptor-mediated cell death: similarities and distinctions , 1994, The Journal of experimental medicine.

[126]  S. Korsmeyer,et al.  Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. , 1990, Journal of immunology.

[127]  F. Finkelman,et al.  IL-12 protects bone marrow from and sensitizes intestinal tract to ionizing radiation. , 1994, Journal of immunology.

[128]  A. Capron,et al.  Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals , 1992, The Journal of experimental medicine.

[129]  N. Haigwood,et al.  Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis , 1992, The Journal of experimental medicine.

[130]  David L. Vaux,et al.  Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells , 1988, Nature.

[131]  O. Uyama,et al.  Protective Effects of Human Recombinant Superoxide Dismutase on Transient Ischemic Injury of CA1 Neurons in Gerbils , 1992, Stroke.

[132]  Takashi Suda,et al.  Molecular cloning and expression of the fas ligand, a novel member of the tumor necrosis factor family , 1993, Cell.

[133]  F. Ramsdell,et al.  Fas transduces activation signals in normal human T lymphocytes , 1993, The Journal of experimental medicine.

[134]  M. Lavail,et al.  Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[135]  R. J. Clem,et al.  Prevention of apoptosis by a baculovirus gene during infection of insect cells. , 1991, Science.

[136]  M. Mattson,et al.  Altered Calcium Signaling and Neuronal Injury: Stroke and Alzheimer's Disease as Examples a , 1993, Annals of the New York Academy of Sciences.

[137]  A. Takashima Tau protein I is essential for amyloid β-protein iduced neurotoxicity , 1993 .

[138]  D. Rosenbaum,et al.  Superoxide Dismutase Ameliorates Neuronal Death From Hypoxia in Culture , 1994, Stroke.