Protein Kinase D Regulates Vesicular Transport by Phosphorylating and Activating Phosphatidylinositol-4 Kinase IIIbeta at the Golgi Complex

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2005 Aug 16

PMID 16100512

Citations 155

Authors

Angelika Hausser

Peter Storz

Susanne Martens

Gisela Link

Alex Toker

Klaus Pfizenmaier

Affiliations

Soon will be listed here.

Abstract

Protein kinase D (PKD) regulates the fission of vesicles originating from the trans-Golgi network. We show that phosphatidylinositol 4-kinase IIIbeta (PI4KIIIbeta) - a key player in the structure and function of the Golgi complex - is a physiological substrate of PKD. Of the three PKD isoforms, only PKD1 and PKD2 phosphorylated PI4KIIIbeta at a motif that is highly conserved from yeast to humans. PKD-mediated phosphorylation stimulated lipid kinase activity of PI4KIIIbeta and enhanced vesicular stomatitis virus G-protein transport to the plasma membrane. The identification of PI4KIIIbeta as one of the PKD substrates should help to reveal the molecular events that enable transport-carrier formation.

Citing Articles

Inhibition of protein kinase D and its substrate phosphatidylinositol-4 kinase III beta blocks common human coronavirus replication.

Han H, Liu H, Steiner R, Zhao Z, Jin Z Microbiol Spectr. 2024; :e0150124.

PMID: 39540754 PMC: 11619529. DOI: 10.1128/spectrum.01501-24.

Regulation of phosphoinositide metabolism in Apicomplexan parasites.

Arabiotorre A, Bankaitis V, Grabon A Front Cell Dev Biol. 2023; 11:1163574.

PMID: 37791074 PMC: 10543664. DOI: 10.3389/fcell.2023.1163574.

Membrane trafficking in breast cancer progression: protein kinase D comes into play.

Gutierrez-Galindo E, Yilmaz Z, Hausser A Front Cell Dev Biol. 2023; 11:1173387.

PMID: 37293129 PMC: 10246754. DOI: 10.3389/fcell.2023.1173387.

The C10orf76-PI4KB axis orchestrates CERT-mediated ceramide trafficking to the distal Golgi.

Mizuike A, Sakai S, Katoh K, Yamaji T, Hanada K J Cell Biol. 2023; 222(7).

PMID: 37195633 PMC: 10192306. DOI: 10.1083/jcb.202111069.

Endothelial Protein kinase D1 is a major regulator of post-traumatic hyperinflammation.

Schonfelder J, Seibold T, Morawe M, Sroka R, Schneider N, Cai J Front Immunol. 2023; 14:1093022.

PMID: 36936923 PMC: 10017463. DOI: 10.3389/fimmu.2023.1093022.

References

Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C . ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat Cell Biol. 1999; 1(5):280-7. DOI: 10.1038/12993. View

Novick P . The yeast phosphatidylinositol-4-OH kinase pik1 regulates secretion at the Golgi. Nat Cell Biol. 1999; 1(8):523-5. DOI: 10.1038/70319. View

Iglesias T, Mitchell M, Naven T, Rozengurt E, Schiavo G . Identification and cloning of Kidins220, a novel neuronal substrate of protein kinase D. J Biol Chem. 2000; 275(51):40048-56. DOI: 10.1074/jbc.M005261200. View

Liljedahl M, Maeda Y, Colanzi A, Ayala I, Van Lint J, Malhotra V . Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell. 2001; 104(3):409-20. DOI: 10.1016/s0092-8674(01)00228-8. View

Suer S, Sickmann A, Meyer H, Herberg F, Heilmeyer Jr L . Human phosphatidylinositol 4-kinase isoform PI4K92. Expression of the recombinant enzyme and determination of multiple phosphorylation sites. Eur J Biochem. 2001; 268(7):2099-106. DOI: 10.1046/j.1432-1327.2001.02089.x. View

Waldron R, Rey O, Iglesias T, Tugal T, Cantrell D, Rozengurt E . Activation loop Ser744 and Ser748 in protein kinase D are transphosphorylated in vivo. J Biol Chem. 2001; 276(35):32606-15. DOI: 10.1074/jbc.M101648200. View

Maeda Y, Beznoussenko G, Van Lint J, Mironov A, Malhotra V . Recruitment of protein kinase D to the trans-Golgi network via the first cysteine-rich domain. EMBO J. 2001; 20(21):5982-90. PMC: 125696. DOI: 10.1093/emboj/20.21.5982. View

Hausser A, Link G, Bamberg L, Burzlaff A, Lutz S, Pfizenmaier K . Structural requirements for localization and activation of protein kinase C mu (PKC mu) at the Golgi compartment. J Cell Biol. 2002; 156(1):65-74. PMC: 2173578. DOI: 10.1083/jcb.200110047. View

Baron C, Malhotra V . Role of diacylglycerol in PKD recruitment to the TGN and protein transport to the plasma membrane. Science. 2001; 295(5553):325-8. DOI: 10.1126/science.1066759. View

10.

Storz P, Toker A . Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO J. 2002; 22(1):109-20. PMC: 140053. DOI: 10.1093/emboj/cdg009. View

11.

Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, Vandenheede J . Protein kinase D: a family affair. FEBS Lett. 2003; 546(1):81-6. DOI: 10.1016/s0014-5793(03)00487-3. View

12.

Wang Y, Wang J, Sun H, Martinez M, Sun Y, Macia E . Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell. 2003; 114(3):299-310. DOI: 10.1016/s0092-8674(03)00603-2. View

13.

Prigozhina N, Waterman-Storer C . Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr Biol. 2004; 14(2):88-98. DOI: 10.1016/j.cub.2004.01.003. View

14.

Yeaman C, Ayala M, Wright J, Bard F, Bossard C, Ang A . Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat Cell Biol. 2004; 6(2):106-12. PMC: 3372901. DOI: 10.1038/ncb1090. View

15.

Storz P, Doppler H, Toker A . Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-kappaB in oxidative stress signaling. Mol Cell Biol. 2004; 24(7):2614-26. PMC: 371115. DOI: 10.1128/MCB.24.7.2614-2626.2004. View

16.

Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi D, Kular G . FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol. 2004; 6(5):393-404. DOI: 10.1038/ncb1119. View

17.

Nakagawa T, Goto K, Kondo H . Cloning, expression, and localization of 230-kDa phosphatidylinositol 4-kinase. J Biol Chem. 1996; 271(20):12088-94. DOI: 10.1074/jbc.271.20.12088. View

18.

Prestle J, Pfizenmaier K, Brenner J, Johannes F . Protein kinase C mu is located at the Golgi compartment. J Cell Biol. 1996; 134(6):1401-10. PMC: 2121004. DOI: 10.1083/jcb.134.6.1401. View

19.

Nishikawa K, Toker A, Johannes F, Songyang Z, Cantley L . Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem. 1997; 272(2):952-60. DOI: 10.1074/jbc.272.2.952. View

20.

Jamora C, Yamanouye N, Van Lint J, Laudenslager J, Vandenheede J, Faulkner D . Gbetagamma-mediated regulation of Golgi organization is through the direct activation of protein kinase D. Cell. 1999; 98(1):59-68. DOI: 10.1016/S0092-8674(00)80606-6. View