Cell cycle regulation of Golgi membrane dynamics.

The Golgi apparatus is a membranous organelle in the cell that plays essential roles in protein and lipid trafficking, sorting, processing, and modification. Its basic structure is a stack of closely aligned flattened cisternae. In mammalian cells, dozens of Golgi stacks are often laterally linked into a ribbon-like structure. Biogenesis of the Golgi during cell division occurs through a sophisticated disassembly and reassembly process that can be divided into three distinct but cooperative steps, including the deformation and reformation of the Golgi cisternae, stacks, and ribbon. Here, we review our current understanding of the protein machineries that control these three steps in the cycle of mammalian cell division: GRASP65 and GRASP55 in Golgi stack and ribbon formation; ubiquitin and AAA ATPases in postmitotic Golgi membrane fusion; and golgins and cytoskeleton in Golgi ribbon formation.

[1]  F. Wieland,et al.  COPI budding within the Golgi stack. , 2011, Cold Spring Harbor perspectives in biology.

[2]  S. Dalal,et al.  Distinct roles for the AAA ATPases NSF and p97 in the secretory pathway. , 2003, Molecular biology of the cell.

[3]  P. Sorensen,et al.  The E3 ligase HACE1 is a critical chromosome 6q21 tumor suppressor involved in multiple cancers , 2007, Nature Medicine.

[4]  J. Yates,et al.  The role of GRASP55 in Golgi fragmentation and entry of cells into mitosis. , 2008, Molecular biology of the cell.

[5]  A. Linstedt,et al.  Golgin160 recruits the dynein motor to position the Golgi apparatus. , 2012, Developmental cell.

[6]  M. Velliste,et al.  Dispersal of Golgi matrix proteins during mitotic Golgi disassembly , 2003, Journal of Cell Science.

[7]  Yi Xiang,et al.  Active ADP-ribosylation Factor-1 (ARF1) Is Required for Mitotic Golgi Fragmentation* , 2007, Journal of Biological Chemistry.

[8]  A. Mogilner,et al.  Concerted effort of centrosomal and Golgi-derived microtubules is required for proper Golgi complex assembly but not for maintenance , 2012, Molecular biology of the cell.

[9]  Zhiping Hu,et al.  The Study of Golgi Apparatus in Alzheimer’s Disease , 2007, Neurochemical Research.

[10]  Andrew W. Folkmann,et al.  Golgi-derived CLASP-dependent Microtubules Control Golgi Organization and Polarized Trafficking in Motile Cells , 2009, Nature Cell Biology.

[11]  C. Rabouille,et al.  Unconventional secretion: a stress on GRASP. , 2011, Current opinion in cell biology.

[12]  P. Freemont,et al.  p37 is a p97 adaptor required for Golgi and ER biogenesis in interphase and at the end of mitosis. , 2006, Developmental cell.

[13]  G. Warren,et al.  A direct role for GRASP65 as a mitotically regulated Golgi stacking factor , 2003, The EMBO journal.

[14]  Yi Xiang,et al.  ERK regulates Golgi and centrosome orientation towards the leading edge through GRASP65 , 2008, The Journal of cell biology.

[15]  L. Kjer-Nielsen,et al.  GRIP Domain-mediated Targeting of Two New Coiled-coil Proteins, GCC88 and GCC185, to Subcompartments of the trans-Golgi Network* , 2003, The Journal of Biological Chemistry.

[16]  G. Beznoussenko,et al.  The Golgi ribbon and the function of the Golgins , 2008 .

[17]  F. Lanni,et al.  GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution , 2006, Nature Cell Biology.

[18]  B. Goud,et al.  The Localization of the Golgin GCC185 Is Independent of Rab6A/A' and Arl1 , 2009, Cell.

[19]  G. Warren,et al.  Partitioning of the Matrix Fraction of the Golgi Apparatus During Mitosis in Animal Cells , 2002, Science.

[20]  Hebao Yuan,et al.  The Role of GRASP65 in Golgi Cisternal Stacking and Cell Cycle Progression , 2010, Traffic.

[21]  Bruno Antonny,et al.  Asymmetric Tethering of Flat and Curved Lipid Membranes by a Golgin , 2008, Science.

[22]  D. Corda,et al.  Mitosis controls the Golgi and the Golgi controls mitosis. , 2007, Current opinion in cell biology.

[23]  Michel Bornens,et al.  GMAP-210 Recruits γ-Tubulin Complexes to cis-Golgi Membranes and Is Required for Golgi Ribbon Formation , 2004, Cell.

[24]  Kimimitsu Oda,et al.  Interaction of Golgin‐84 with the COG Complex Mediates the Intra‐Golgi Retrograde Transport , 2010, Traffic.

[25]  Yanzhuang Wang,et al.  Golgi apparatus inheritance , 2008 .

[26]  G. Warren,et al.  GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell‐free system , 1999, The EMBO journal.

[27]  R. Newman,et al.  Sequential SNARE disassembly and GATE-16–GOS-28 complex assembly mediated by distinct NSF activities drives Golgi membrane fusion , 2002, The Journal of cell biology.

[28]  G. Warren,et al.  Molecular Mechanism of Mitotic Golgi Disassembly and Reassembly Revealed by a Defined Reconstitution Assay* , 2008, Journal of Biological Chemistry.

[29]  J. Lippincott-Schwartz,et al.  Golgi inheritance in mammalian cells is mediated through endoplasmic reticulum export activities. , 2005, Molecular biology of the cell.

[30]  G. Egea,et al.  Actin dynamics at the Golgi complex in mammalian cells. , 2006, Current opinion in cell biology.

[31]  G. Warren,et al.  Golgin‐84 is a rab1 Binding Partner Involved in Golgi Structure , 2003, Traffic.

[32]  G. Beznoussenko,et al.  The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. , 2007, Molecular biology of the cell.

[33]  D. Ungar Golgi linked protein glycosylation and associated diseases. , 2009, Seminars in cell & developmental biology.

[34]  M. Bornens,et al.  Microtubule nucleation at the cis‐side of the Golgi apparatus requires AKAP450 and GM130 , 2009, The EMBO journal.

[35]  J. Rink,et al.  The ubiquitin ligase HACE1 regulates Golgi membrane dynamics during the cell cycle. , 2011, Nature communications.

[36]  Yanzhuang Wang,et al.  Golgi Cisternal Unstacking Stimulates COPI Vesicle Budding and Protein Transport , 2008, PloS one.

[37]  Yi Xiang,et al.  GRASP55 and GRASP65 play complementary and essential roles in Golgi cisternal stacking , 2010, The Journal of cell biology.

[38]  Florence Friggi-Grelin,et al.  The golgi comprises a paired stack that is separated at G2 by modulation of the actin cytoskeleton through Abi and Scar/WAVE. , 2007, Developmental cell.

[39]  A. Linstedt,et al.  Mitotic Inhibition of GRASP65 Organelle Tethering Involves Polo-like Kinase 1 (PLK1) Phosphorylation Proximate to an Internal PDZ Ligand* , 2010, The Journal of Biological Chemistry.

[40]  S. Spanò,et al.  A role for BARS at the fission step of COPI vesicle formation from Golgi membrane , 2005, The EMBO journal.

[41]  A. Linstedt,et al.  GRASP55 regulates Golgi ribbon formation. , 2008, Molecular biology of the cell.

[42]  N. Nakamura Emerging new roles of GM130, a cis-Golgi matrix protein, in higher order cell functions. , 2010, Journal of pharmacological sciences.

[43]  J. Vandekerckhove,et al.  GRASP65, a Protein Involved in the Stacking of Golgi Cisternae , 1997, Cell.

[44]  Yu-Chun Lin,et al.  ARL4A acts with GCC185 to modulate Golgi complex organization , 2011, Journal of Cell Science.

[45]  Xinran Liu,et al.  The Golgi-Associated Hook3 Protein Is a Member of a Novel Family of Microtubule-Binding Proteins , 2001, The Journal of cell biology.

[46]  C. Cericola,et al.  The Golgi mitotic checkpoint is controlled by BARS‐dependent fission of the Golgi ribbon into separate stacks in G2 , 2007, The EMBO journal.

[47]  F. Perez,et al.  Sequential phosphorylation of GRASP65 during mitotic Golgi disassembly , 2012, Biology Open.

[48]  H. Toh,et al.  VCIP135 deubiquitinase and its binding protein, WAC, in p97ATPase‐mediated membrane fusion , 2011, The EMBO journal.

[49]  G. Warren,et al.  Golgi architecture and inheritance. , 2002, Annual review of cell and developmental biology.

[50]  S. Munro,et al.  Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins , 2008, The Journal of cell biology.

[51]  Aipo Diao,et al.  Coordination of Golgin Tethering and SNARE Assembly , 2008, Journal of Biological Chemistry.

[52]  G. Warren,et al.  VCIP135 acts as a deubiquitinating enzyme during p97–p47-mediated reassembly of mitotic Golgi fragments , 2004, The Journal of cell biology.

[53]  A. Luini,et al.  The multiple activities of CtBP/BARS proteins: the Golgi view. , 2006, Trends in cell biology.

[54]  D. Pappin,et al.  The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation , 2003, The Journal of cell biology.

[55]  R. Pepperkok,et al.  An Ordered Inheritance Strategy for the Golgi Apparatus: Visualization of Mitotic Disassembly Reveals a Role for the Mitotic Spindle , 1998, The Journal of cell biology.

[56]  Stephanie A. Thomas,et al.  Dynamic Nucleation of Golgi Apparatus Assembly from the Endoplasmic Reticulum in Interphase HeLa Cells , 2004, Traffic.

[57]  G. Warren,et al.  Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1–Npl4 , 2002, The EMBO journal.

[58]  Yanzhuang Wang,et al.  Golgi biogenesis. , 2011, Cold Spring Harbor perspectives in biology.

[59]  L. Klein-Hitpass,et al.  Centrosomal CAP350 protein stabilises microtubules associated with the Golgi complex , 2007, Journal of Cell Science.

[60]  F. Perez,et al.  The Golgi complex is a microtubule-organizing organelle. , 2001, Molecular biology of the cell.

[61]  C. Rabouille,et al.  The multiple facets of the Golgi reassembly stacking proteins. , 2011, The Biochemical journal.

[62]  L. Lanzetti,et al.  Actin in membrane trafficking. , 2007, Current opinion in cell biology.

[63]  W. Lehmann,et al.  Plk1 docking to GRASP65 phosphorylated by Cdk1 suggests a mechanism for Golgi checkpoint signalling , 2005, The EMBO journal.

[64]  A. Linstedt,et al.  Mitogen-activated protein kinase kinase 1-dependent Golgi unlinking occurs in G2 phase and promotes the G2/M cell cycle transition. , 2006, Molecular biology of the cell.

[65]  H. Meyer Golgi reassembly after mitosis: the AAA family meets the ubiquitin family. , 2005, Biochimica et biophysica acta.

[66]  F. Barr,et al.  Inheritance and biogenesis of organelles in the secretory pathway , 2007, Nature Reviews Molecular Cell Biology.

[67]  G. Drin,et al.  A general amphipathic α-helical motif for sensing membrane curvature , 2007, Nature Structural &Molecular Biology.

[68]  M. Bornens,et al.  Golgi localisation of GMAP210 requires two distinct cis-membrane binding mechanisms , 2009, BMC Biology.

[69]  Jen-Hsuan Wei,et al.  Unraveling the Golgi Ribbon , 2010, Traffic.

[70]  F. Barr Golgi inheritance , 2004, The Journal of cell biology.

[71]  J. Yates,et al.  Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. , 2007, Developmental cell.

[72]  A. Mironov,et al.  The Golgi apparatus : state of the art 110 years after Camillo Golgi's discovery , 2008 .

[73]  A. Linstedt,et al.  Allosteric Regulation of GRASP Protein-dependent Golgi Membrane Tethering by Mitotic Phosphorylation* , 2012, The Journal of Biological Chemistry.

[74]  G. Warren,et al.  Mapping the Functional Domains of the Golgi Stacking Factor GRASP65* , 2005, Journal of Biological Chemistry.

[75]  V. Malhotra,et al.  The Golgi-associated protein GRASP65 regulates spindle dynamics and is essential for cell division. , 2005, Molecular biology of the cell.

[76]  Yi Xiang,et al.  Reconstitution of the cell cycle-regulated Golgi disassembly and reassembly in a cell-free system , 2010, Nature Protocols.

[77]  L. Johannes,et al.  The Overexpression of GMAP‐210 Blocks Anterograde and Retrograde Transport Between the ER and the Golgi Apparatus , 2002, Traffic.

[78]  V. Allan,et al.  Molecular motors and the Golgi complex: staying put and moving through. , 2009, Seminars in cell & developmental biology.

[79]  G. Drin,et al.  A general amphipathic alpha-helical motif for sensing membrane curvature. , 2007, Nature structural & molecular biology.

[80]  Brian Storrie,et al.  Capacity of the Golgi apparatus for cargo transport prior to complete assembly. , 2006, Molecular biology of the cell.

[81]  A. Linstedt,et al.  Control of organelle size: the Golgi complex. , 2011, Annual review of cell and developmental biology.

[82]  S. Munro The golgin coiled-coil proteins of the Golgi apparatus. , 2011, Cold Spring Harbor perspectives in biology.

[83]  G. Beznoussenko,et al.  Molecular mechanisms responsible for formation of Golgi ribbon. , 2011, Histology and histopathology.