Skip to main content
SpringerLink
Log in

Phosphoinositides in Golgi Complex Function

  • Chapter
  • First Online:
Phosphoinositides II: The Diverse Biological Functions

Part of the book series: Subcellular Biochemistry ((SCBI,volume 59))

Abstract

The Golgi complex is a ribbon-like organelle composed of stacks of flat cisternae interconnected by tubular junctions. It occupies a central position in the endomembrane system as proteins and lipids that are synthesized in the endoplasmic reticulum (ER) pass through the Golgi complex to undergo biosynthetic modification (mainly glycosylation) and to be sorted to their final destinations. In addition the Golgi complex possesses a number of activities, apparently not directly connected with its main role in trafficking and sorting, which have been recently reviewed in Wilson et al. 2011. In spite of the constant massive flux of material the Golgi complex maintains its identity and phosphoinositides (PIs), among other factors, play a central role in this process. The active metabolism of PIs at the Golgi is necessary for the proper functioning of the organelle both in terms of membrane trafficking/sorting and its manifold metabolic and signalling activities. Phosphatidylinositol 4-phosphate (PtdIns4P), in particular, is responsible for the recruitment of numerous cytosolic proteins that recognise and bind PtdIns4P via specific lipid-binding domains. In this chapter we will summarize the findings that have contributed to our current understanding of the role of PIs in the biology of the Golgi complex in terms of the regulation of PI metabolism and the functional roles and regulation of PtdIns4P effectors.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 179.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Banerji S, Ngo M, Lane CF, Robinson CA, Minogue S, Ridgway ND (2010) Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the golgi apparatus requires phosphatidylinositol 4-kinase IIalpha. Mol Biol Cell 21:4141–4150

    Google Scholar 

  • Barylko B, Mao YS, Wlodarski P, Jung G, Binns DD, Sun HQ, Yin HL, Albanesi JP (2009) Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase II{alpha}. J Biol Chem 284:9994–10003

    Article  PubMed  CAS  Google Scholar 

  • Bielas SL, Silhavy JL, Brancati F, Kisseleva MV, Al-Gazali L, Sztriha L, Bayoumi RA, Zaki MS, Abdel-Aleem A, Rosti RO, Kayserili H, Swistun D, Scott LC, Bertini E, Boltshauser E, Fazzi E, Travaglini L, Field SJ, Gayral S, Jacoby M, Schurmans S, Dallapiccola B, Majerus PW, Valente EM, Gleeson JG (2009) Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies. Nat Genet 41:1032–1036

    Article  PubMed  CAS  Google Scholar 

  • Blagoveshchenskaya A, Mayinger P (2009) SAC1 lipid phosphatase and growth control of the secretory pathway. Mol Biosyst 5:36–42

    Article  PubMed  CAS  Google Scholar 

  • Blagoveshchenskaya A, Cheong FY, Rohde HM, Glover G, Knodler A, Nicolson T, Boehmelt G, Mayinger P (2008) Integration of Golgi trafficking and growth factor signaling by the lipid phosphatase SAC1. J Cell Biol 180:803–812

    Article  PubMed  CAS  Google Scholar 

  • Cheong FY, Sharma V, Blagoveshchenskaya A, Oorschot VM, Brankatschk B, Klumperman J, Freeze HH, Mayinger P (2010) Spatial regulation of Golgi phosphatidylinositol-4-phosphate is required for enzyme localization and glycosylation fidelity. Traffic 11:1180–1190

    Google Scholar 

  • D’Angelo G, Polishchuk E, Di Tullio G, Santoro M, Di Campli A, Godi A, West G, Bielawski J, Chuang CC, Spoel AC van der, Platt FM, Hannun YA, Polishchuk R, Mattjus P, De Matteis MA (2007) Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449:62–67

    Article  PubMed  Google Scholar 

  • D’Angelo G, Vicinanza M, Di Campli A, De Matteis MA (2008a) The multiple roles of PtdIns(4)P—not just the precursor of PtdIns(4,5)P2. J Cell Sci 121:1955–1963

    Article  Google Scholar 

  • D’Angelo G, Vicinanza M, De Matteis MA (2008b) Lipid-transfer proteins in biosynthetic pathways. Curr Opin Cell Biol 20:360–370

    Article  Google Scholar 

  • Demmel L, Gravert M, Ercan E, Habermann B, Muller-Reichert T, Kukhtina V, Haucke V, Baust T, Sohrmann M, Kalaidzidis Y, Klose C, Beck M, Peter M, Walch-Solimena C (2008) The clathrin adaptor Gga2p is a phosphatidylinositol 4-phosphate effector at the Golgi exit. Mol Biol Cell 19:1991–2002

    Article  PubMed  CAS  Google Scholar 

  • Graaf P de, Zwart WT, Dijken RA van, Deneka M, Schulz TK, Geijsen N, Coffer PJ, Gadella BM, Verkleij AJ, Sluijs P van der, Bergen en Henegouwen PM van (2004) Phosphatidylinositol 4-kinasebeta is critical for functional association of rab11 with the Golgi complex. Mol Biol Cell 15:2038–2047

    Article  PubMed  Google Scholar 

  • De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9:273–284

    Article  PubMed  Google Scholar 

  • Dippold HC, Ng MM, Farber-Katz SE, Lee SK, Kerr ML, Peterman MC, Sim R, Wiharto PA, Galbraith KA, Madhavarapu S, Fuchs GJ, Meerloo T, Farquhar MG, Zhou H, Field SJ (2009) GOLPH3 bridges phosphatidylinositol-4-phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 139:337–351

    Article  PubMed  CAS  Google Scholar 

  • Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000) Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 351:19–31

    Article  PubMed  CAS  Google Scholar 

  • Dumaresq-Doiron K, Savard MF, Akam S, Costantino S, Lefrancois S (2010) The phosphatidylinositol 4-kinase PI4KIIIalpha is required for the recruitment of GBF1 to Golgi membranes. J Cell Sci 123:2273–2280

    Google Scholar 

  • Faulhammer F, Konrad G, Brankatschk B, Tahirovic S, Knodler A, Mayinger P (2005) Cell growth-dependent coordination of lipid signaling and glycosylation is mediated by interactions between Sac1p and Dpm1p. J Cell Biol 168:185–191

    Article  PubMed  CAS  Google Scholar 

  • Faulhammer F, Kanjilal-Kolar S, Knodler A, Lo J, Lee Y, Konrad G, Mayinger P (2007) Growth control of Golgi phosphoinositides by reciprocal localization of Sac1 lipid phosphatase and Pik1 4-Kinase. Traffic 8(11):1554–1567

    Google Scholar 

  • Fugmann T, Hausser A, Schoffler P, Schmid S, Pfizenmaier K, Olayioye MA (2007) Regulation of secretory transport by protein kinase D-mediated phosphorylation of the ceramide transfer protein. J Cell Biol 178:15–22

    Article  PubMed  CAS  Google Scholar 

  • Fukuda M, Kanno E, Ishibashi K, Itoh T (2008) Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol Cell Proteomics 7:1031–1042

    Article  PubMed  CAS  Google Scholar 

  • Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA (1999) ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat Cell Biol 1:280–287

    Article  PubMed  CAS  Google Scholar 

  • Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 6:393–404

    Article  PubMed  CAS  Google Scholar 

  • Halter D, Neumann S, Dijk SM van, Wolthoorn J, Maziere AM de, Vieira OV, Mattjus P, Klumperman J, Meer G van, Sprong H (2007) Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J Cell Biol 179:101–115

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, Nishijima M (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426:803–809

    Article  PubMed  CAS  Google Scholar 

  • Hausser A, Storz P, Martens S, Link G, Toker A, Pfizenmaier K (2005) Protein kinase D regulates vesicular transport by phosphorylating and activating phosphatidylinositol-4 kinase IIIbeta at the Golgi complex. Nat Cell Biol 7:880–886

    Article  PubMed  CAS  Google Scholar 

  • Hausser A, Link G, Hoene M, Russo C, Selchow O, Pfizenmaier K (2006) Phospho-specific binding of 14-3-3 proteins to phosphatidylinositol 4-kinase III beta protects from dephosphorylation and stabilizes lipid kinase activity. J Cell Sci 119:3613–3621

    Article  PubMed  CAS  Google Scholar 

  • Haynes LP, Thomas GM, Burgoyne RD (2005) Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase beta and trans-Golgi network-plasma membrane traffic. J Biol Chem 280:6047–6054

    Article  PubMed  CAS  Google Scholar 

  • Heilmeyer LM Jr, Vereb G Jr, Vereb G, Kakuk A, Szivak I (2003) Mammalian phosphatidylinositol 4-kinases. IUBMB Life 55:59–65

    Article  PubMed  CAS  Google Scholar 

  • Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T, Harrison SC (2004) Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci U S A 101:14108–14113

    Article  PubMed  CAS  Google Scholar 

  • Hendricks KB, Wang BQ, Schnieders EA, Thorner J (1999) Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase. Nat Cell Biol 1:234–241

    Article  PubMed  CAS  Google Scholar 

  • Hirst J, Motley A, Harasaki K, Peak Chew SY, Robinson MS (2003) EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol Biol Cell 14:625–641

    Article  PubMed  CAS  Google Scholar 

  • Lenoir M, Coskun U, Grzybek M, Cao X, Buschhorn SB, James J, Simons K, Overduin M (2010) Structural basis of wedging the Golgi membrane by FAPP pleckstrin homology domains. EMBO Rep 11:279–284

    Google Scholar 

  • Liljedahl M, Maeda Y, Colanzi A, Ayala I, Van Lint J, Malhotra V (2001) Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 104:409–420

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Boukhelifa M, Tribble E, Morin-Kensicki E, Uetrecht A, Bear JE, Bankaitis VA (2008) The Sac1 phosphoinositide phosphatase regulates Golgi membrane morphology and mitotic spindle organization in mammals. Mol Biol Cell 19:3080–3096

    Article  PubMed  CAS  Google Scholar 

  • Low PC, Misaki R, Schroder K, Stanley AC, Sweet MJ, Teasdale RD, Vanhaesebroeck B, Meunier FA, Taguchi T, Stow JL (2010) Phosphoinositide 3-kinase delta regulates membrane fission of Golgi carriers for selective cytokine secretion. J Cell Biol 190:1053–1065

    Google Scholar 

  • Mayinger P, Bankaitis VA, Meyer DI (1995) Sac1p mediates the adenosine triphosphate transport into yeast endoplasmic reticulum that is required for protein translocation. J Cell Biol 131:1377–1386

    Article  PubMed  CAS  Google Scholar 

  • Mills IG, Praefcke GJ, Vallis Y, Peter BJ, Olesen LE, Gallop JL, Butler PJ, Evans PR, McMahon HT (2003) EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J Cell Biol 160:213–222

    Article  PubMed  Google Scholar 

  • Minogue S, Chu KM, Westover EJ, Covey DF, Hsuan JJ, Waugh MG (2006) Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KIIalpha at the trans-Golgi network. J Lipid Res 51:2314–2324

    Google Scholar 

  • Mizuno-Yamasaki E, Medkova M, Coleman J, Novick P (2010) Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev Cell 18:828–840

    Google Scholar 

  • Natarajan P, Liu K, Patil DV, Sciorra VA, Jackson CL, Graham TR (2009) Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 11:1421–1426

    Article  PubMed  CAS  Google Scholar 

  • Ngo M, Ridgway ND (2009) Oxysterol binding protein-related Protein 9 (ORP9) is a cholesterol transfer protein that regulates Golgi structure and function. Mol Biol Cell 20:1388–1399

    Article  PubMed  CAS  Google Scholar 

  • Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, Kethesparan DS, Mitchell CA (2009) The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J 419:29–49

    Article  PubMed  CAS  Google Scholar 

  • Perry RJ, Ridgway ND (2006) Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein. Mol Biol Cell 17:2604–2616

    Article  PubMed  CAS  Google Scholar 

  • Rohde HM, Cheong FY, Konrad G, Paiha K, Mayinger P, Boehmelt G (2003) The human phosphatidylinositol phosphatase SAC1 interacts with the coatomer I complex. J Biol Chem 278:52689–52699

    Article  PubMed  CAS  Google Scholar 

  • Schmitz KR, Liu J, Li S, Setty TG, Wood CS, Burd CG, Ferguson KM (2008) Golgi localization of glycosyltransferases requires a Vps74p oligomer. Dev Cell 14:523–534

    Article  PubMed  CAS  Google Scholar 

  • Scott KL, Kabbarah O, Liang MC, Ivanova E, Anagnostou V, Wu J, Dhakal S, Wu M, Chen S, Feinberg T, Huang J, Saci A, Widlund HR, Fisher DE, Xiao Y, Rimm DL, Protopopov A, Wong KK, Chin L (2009) GOLPH3 modulates mTOR signalling and rapamycin sensitivity in cancer. Nature 459:1085–1090

    Article  PubMed  CAS  Google Scholar 

  • Szentpetery Z, Varnai P, Balla T (2010) Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc Natl Acad Sci U S A 107:8225–8230

    Google Scholar 

  • Tu L, Tai WC, Chen L, Banfield DK (2008) Signal-mediated dynamic retention of glycosyltransferases in the Golgi. Science 321:404–407

    Article  PubMed  CAS  Google Scholar 

  • Vicinanza M, D’Angelo G, Di Campli A, De Matteis MA (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J 27:2457–2470

    Article  PubMed  CAS  Google Scholar 

  • Vieira OV, Verkade P, Manninen A, Simons K (2005) FAPP2 is involved in the transport of apical cargo in polarized MDCK cells. J Cell Biol 170:521–526

    Article  PubMed  CAS  Google Scholar 

  • Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114:299–310

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Sun HQ, Macia E, Kirchhausen T, Watson H, Bonifacino JS, Yin HL (2007) PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol Biol Cell 18:2646–2655

    Article  PubMed  CAS  Google Scholar 

  • Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363:657–666

    Article  PubMed  CAS  Google Scholar 

  • Whitters EA, Cleves AE, McGee TP, Skinner HB, Bankaitis VA (1993) SAC1p is an integral membrane protein that influences the cellular requirement for phospholipid transfer protein function and inositol in yeast. J Cell Biol 122:79–94

    Article  PubMed  CAS  Google Scholar 

  • Wilson C, Venditti R, Rega LR, Colanzi A, D’Angelo G, De Matteis MA (2011) The Golgi apparatus: an organelle with multiple complex functions. Biochem J 433:1–9

    Google Scholar 

  • Williams C, Choudhury R, McKenzie E, Lowe M (2007) Targeting of the type II inositol polyphosphate 5-phosphatase INPP5B to the early secretory pathway. J Cell Sci 120:3941–3951

    Article  PubMed  CAS  Google Scholar 

  • Wood CS, Schmitz KR, Bessman NJ, Setty TG, Ferguson KM, Burd CG (2009) PtdIns4P recognition by Vps74/GOLPH3 links PtdIns 4-kinase signaling to retrograde Golgi trafficking. J Cell Biol 187:967–975

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Telethon Institute of Genetics and Medicine, Via Pietro Castellino, 111, 80131, Napoli, Italy

    Giovanni D’Angelo, Mariella Vicinanza, Cathal Wilson & Maria Antonietta De Matteis

Authors
  1. Giovanni D’Angelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariella Vicinanza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cathal Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Antonietta De Matteis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Antonietta De Matteis .

Editor information

Editors and Affiliations

  1. , NICHD, National Institutes of Health, Convent Drive 49, Bethesda, 20892-4480, Maryland, USA

    Tamas Balla

  2. , Cancer- and Immunobiology, University of Basel, Mattenstrasse 28, Basel, 4058, Switzerland

    Matthias Wymann

  3. , Pharmacology and Cancer Biology, Duke University Medical Center, Durham, 27710, North Carolina, USA

    John D. York

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

D’Angelo, G., Vicinanza, M., Wilson, C., De Matteis, M. (2012). Phosphoinositides in Golgi Complex Function. In: Balla, T., Wymann, M., York, J. (eds) Phosphoinositides II: The Diverse Biological Functions. Subcellular Biochemistry, vol 59. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-3015-1_8

Download citation

Publish with us

Policies and ethics

Search

Navigation