Glucose metabolism and programmed cell death: an evolutionary and mechanistic perspective.

Over the last decade, cellular glucose metabolism has emerged as a central player in the mechanisms of programmed cell death (PCD). We examined the metabolic foundations of apoptosis from a Darwinian context and suggest that PCD has evolved from the cellular response to metabolic stress, most notably in relation to glucose metabolism. Whilst apoptosis and other forms of PCD are essential to the development, maintenance and survival of multicellular organisms, it is now evident that controlled and selective cell death confers fitness advantages in unicellular organisms. All species may thus harbour a fundamental relationship between the availability of basic nutrients and life/death decisions. This evolutionary perspective may inform our understanding of PCD in its many guises.

[1]  Guido Kroemer,et al.  Self-eating and self-killing: crosstalk between autophagy and apoptosis , 2007, Nature Reviews Molecular Cell Biology.

[2]  C. Duve,et al.  Functions of lysosomes. , 1966, Annual review of physiology.

[3]  D. Green,et al.  The Release of Cytochrome c from Mitochondria: A Primary Site for Bcl-2 Regulation of Apoptosis , 1997, Science.

[4]  L. Margulis Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Thompson,et al.  Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis , 2003, Cell Death and Differentiation.

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

[7]  Eyal Gottlieb,et al.  Metabolic transformation in cancer. , 2009, Carcinogenesis.

[8]  G. Kroemer,et al.  Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death , 1999, Cell Death and Differentiation.

[9]  W. Craigen,et al.  Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death , 2007, Nature Cell Biology.

[10]  G. Kroemer,et al.  Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells , 2000, Cell Death and Differentiation.

[11]  D. Hockenbery,et al.  Bcl-2 family proteins as regulators of oxidative stress. , 2009, Seminars in cancer biology.

[12]  E. Gottlieb OPA1 and PARL Keep a Lid on Apoptosis , 2006, Cell.

[13]  H. Engelberg-Kulka,et al.  Bacterial Programmed Cell Death and Multicellular Behavior in Bacteria , 2006, PLoS genetics.

[14]  Luca Scorrano,et al.  A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. , 2002, Developmental cell.

[15]  D. Chao,et al.  BCL-2 family: regulators of cell death. , 1998, Annual review of immunology.

[16]  R. Losick,et al.  Crisscross regulation of cell-type-specific gene expression during development in B. subtilis , 1992, Nature.

[17]  J. Hoek,et al.  Mitochondrial Binding of Hexokinase II Inhibits Bax-induced Cytochrome c Release and Apoptosis* , 2002, The Journal of Biological Chemistry.

[18]  George Androutsos,et al.  A Brief History of Apoptosis: From Ancient to Modern Times , 2008, Oncology Research and Treatment.

[19]  J. Hoek,et al.  Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. , 2005, Cancer research.

[20]  M. Dworkin,et al.  Morphogenesis and developmental interactions in myxobacteria. , 1975, Science.

[21]  C. Thompson,et al.  Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. , 2004, Molecular cell.

[22]  N. Hay,et al.  Mitochondrial Hexokinases: Guardians of the Mitochondria , 2005, Cell cycle.

[23]  N. Holbrook,et al.  Cellular response to oxidative stress: Signaling for suicide and survival * , 2002, Journal of cellular physiology.

[24]  M. V. Vander Heiden,et al.  Bcl-xL Prevents the Initial Decrease in Mitochondrial Membrane Potential and Subsequent Reactive Oxygen Species Production during Tumor Necrosis Factor Alpha-Induced Apoptosis , 2000, Molecular and Cellular Biology.

[25]  W Baumeister,et al.  Proteasomes and other self-compartmentalizing proteases in prokaryotes. , 1999, Trends in microbiology.

[26]  Hua Li,et al.  Structural and Biochemical Studies of TIGAR (TP53-induced Glycolysis and Apoptosis Regulator)* , 2009, Journal of Biological Chemistry.

[27]  V. Shoshan-Barmatz,et al.  Voltage-dependent Anion Channel 1-based Peptides Interact with Hexokinase to Prevent Its Anti-apoptotic Activity* , 2009, Journal of Biological Chemistry.

[28]  Guy C. Brown,et al.  Mitochondrial Regulation of Caspase Activation by Cytochrome Oxidase and Tetramethylphenylenediamine via Cytosolic Cytochrome c Redox State* , 2007, Journal of Biological Chemistry.

[29]  M. Lipsitch,et al.  SpxB Is a Suicide Gene of Streptococcus pneumoniae and Confers a Selective Advantage in an In Vivo Competitive Colonization Model , 2007, Journal of bacteriology.

[30]  Michael D. Schneider,et al.  Bcl-2 Antiapoptotic Proteins Inhibit Beclin 1-Dependent Autophagy , 2005, Cell.

[31]  S. Snyder,et al.  Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis , 2008, Nature Cell Biology.

[32]  Xiaodong Wang,et al.  Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c , 1996, Cell.

[33]  N. Chandel,et al.  Mitochondrial complex III regulates hypoxic activation of HIF , 2008, Cell Death and Differentiation.

[34]  S. Pattingre,et al.  JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. , 2008, Molecular cell.

[35]  D. Kaiser,et al.  How and why bacteria talk to each other , 1993, Cell.

[36]  Yigong Shi,et al.  Molecular mechanisms of caspase regulation during apoptosis , 2004, Nature Reviews Molecular Cell Biology.

[37]  C. Thompson,et al.  Akt-dependent transformation: there is more to growth than just surviving , 2005, Oncogene.

[38]  S. Carmeli,et al.  A Linear Pentapeptide Is a Quorum-Sensing Factor Required for mazEF-Mediated Cell Death in Escherichia coli , 2007, Science.

[39]  J. Downward,et al.  The Serine Protease Omi/HtrA2 Regulates Apoptosis by Binding XIAP through a Reaper-like Motif* , 2002, The Journal of Biological Chemistry.

[40]  S. Van Cruchten,et al.  Morphological and biochemical aspects of apoptosis, oncosis and necrosis. , 2002 .

[41]  C. Watson,et al.  Apoptosis: the germs of death , 1999, Nature Cell Biology.

[42]  T. Mak,et al.  Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death , 2001, Nature.

[43]  David M. Sabatini,et al.  Tumours with PI3K activation are resistant to dietary restriction , 2009, Nature.

[44]  Tim W. Overton,et al.  Mutational and biochemical analysis of cytochrome c', a nitric oxide-binding lipoprotein important for adaptation of Neisseria gonorrhoeae to oxygen-limited growth. , 2005, The Biochemical journal.

[45]  Zdena Palková,et al.  Multicellular microorganisms: laboratory versus nature , 2004, EMBO reports.

[46]  Qing Zhao,et al.  Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors , 2005, Nature chemical biology.

[47]  R. Hengge-aronis,et al.  Survival of hunger and stress: The role of rpoS in early stationary phase gene regulation in E. coli , 1993, Cell.

[48]  Bernhard Brüne,et al.  Nitric oxide: NO apoptosis or turning it ON? , 2003, Cell Death and Differentiation.

[49]  K. Bayles,et al.  Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis , 2006, Molecular microbiology.

[50]  S. Moncada,et al.  The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C–Cdh1 , 2009, Nature Cell Biology.

[51]  M. Deshmukh,et al.  Glucose Metabolism Inhibits Apoptosis in Neurons and Cancer Cells by Redox Inactivation of Cytochrome c , 2008, Nature Cell Biology.

[52]  Dean P. Jones,et al.  Prevention of Apoptosis by Bcl-2: Release of Cytochrome c from Mitochondria Blocked , 1997, Science.

[53]  K. Vousden,et al.  PUMA and Bax-induced Autophagy Contributes to Apoptosis , 2009, Cell Death and Differentiation.

[54]  E. Kandel,et al.  Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. , 2001, Genes & development.

[55]  S. R. Datta,et al.  Dual role of proapoptotic BAD in insulin secretion and beta cell survival , 2008, Nature Medicine.

[56]  G. Kroemer,et al.  Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death , 1995, The Journal of experimental medicine.

[57]  C. Thompson,et al.  Akt and Bcl-xL Promote Growth Factor-independent Survival through Distinct Effects on Mitochondrial Physiology* , 2001, The Journal of Biological Chemistry.

[58]  J. Ameisen On the origin, evolution, and nature of programmed cell death: a timeline of four billion years , 2002, Cell Death and Differentiation.

[59]  Eyal Gottlieb,et al.  TIGAR, a p53-Inducible Regulator of Glycolysis and Apoptosis , 2006, Cell.

[60]  M. Yarmolinsky,et al.  Programmed cell death in bacterial populations , 1995, Science.

[61]  Sébastien Bonnet,et al.  A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. , 2007, Cancer cell.

[62]  Peng Huang,et al.  Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. , 2009, Biochimica et biophysica acta.

[63]  G. Kroemer,et al.  Autophagic cell death: the story of a misnomer , 2008, Nature Reviews Molecular Cell Biology.

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

[65]  P. Leder,et al.  Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. , 2006, Cancer cell.

[66]  P. Vandenabeele,et al.  Are metacaspases caspases? , 2007, The Journal of cell biology.

[67]  P. Verde,et al.  Glucose-6-phosphate dehydrogenase plays a crucial role in protection from redox-stress-induced apoptosis , 2004, Cell Death and Differentiation.

[68]  G. Giaccone,et al.  Cell Death Independent of Caspases: A Review , 2005, Clinical Cancer Research.

[69]  E. Koonin,et al.  Origin and evolution of eukaryotic apoptosis: the bacterial connection , 2002, Cell Death and Differentiation.

[70]  J. Erman,et al.  Yeast cytochrome c peroxidase: mechanistic studies via protein engineering. , 2002, Biochimica et biophysica acta.

[71]  J. Collins,et al.  A Common Mechanism of Cellular Death Induced by Bactericidal Antibiotics , 2007, Cell.

[72]  D. Newmeyer,et al.  Cell-free apoptosis in Xenopus egg extracts: Inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria , 1994, Cell.

[73]  R. Kletzien,et al.  Glucose‐6‐phosphate dehydrogenase: a “housekeeping” enzyme subject to tissue‐specific regulation by hormones, nutrients, and oxidant stress , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[74]  G. Lenaers,et al.  OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. , 2007, Experimental cell research.

[75]  K. Rice,et al.  Molecular Control of Bacterial Death and Lysis , 2008, Microbiology and Molecular Biology Reviews.

[76]  Yuri Lazebnik,et al.  Identification of Omi/HtrA2 as a Mitochondrial Apoptotic Serine Protease That Disrupts Inhibitor of Apoptosis Protein-Caspase Interaction* , 2002, The Journal of Biological Chemistry.

[77]  C. Thompson,et al.  Mitochondrial respiratory control is lost during growth factor deprivation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  S. R. Datta,et al.  BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis , 2003, Nature.