The casein kinases Yck1p and Yck2p act in the secretory pathway, in part, by regulating the Rab exchange factor Sec2p

Molecular Biology of the Cell

Volumn 27, Issue 4, 2016, Pages 686-701

  Stalder, Danièle ^a   Novick, Peter J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BGL2P PROTEIN; CASEIN KINASE; CASEIN KINASE YCK1P; CASEIN KINASE YCK2P; GLUCAN GLUCOSIDASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; RAB PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SEC15P PROTEIN; SEC2P PROTEIN; UNCLASSIFIED DRUG; YPT32P PROTEIN; BGL2 PROTEIN, S CEREVISIAE; CASEIN KINASE I; GLUCAN ENDO 1,3 BETA GLUCOSIDASE; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; POLYPHOSPHOINOSITIDE; PROTEIN BINDING; SEC15 PROTEIN, S CEREVISIAE; SEC2 PROTEIN, S CEREVISIAE; VESICULAR TRANSPORT PROTEIN; YCK1 PROTEIN, S CEREVISIAE; YCK2 PROTEIN, S CEREVISIAE; YPT32 PROTEIN, S CEREVISIAE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOPLASM; ENZYME RELEASE; GOLGI COMPLEX; LOSS OF FUNCTION MUTATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; SECRETORY VESICLE; YEAST CELL; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT;

CASEIN KINASE I; GLUCAN ENDO-1,3-BETA-D-GLUCOSIDASE; GOLGI APPARATUS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MUTATION; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECRETORY PATHWAY; SECRETORY VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 84958618482     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-09-0651     Document Type: Article

References (46)

1. Babu P, Bryan JD, Panek HR, Jordan SL, Forbrich BM, Kelley SC, Colvin RT, Robinson LC (2002). Plasma membrane localization of the Yck2p yeast casein kinase 1 isoform requires the C-terminal extension and secretory pathway function. J Cell Sci 115, 4957-4968.
2. Baird D, Stefan C, Audhya A, Weys S, Emr SD (2008). Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3. J Cell Biol 183, 1061-1074.
3. Bishop A, Lane R, Beniston R, Chapa-y-Lazo B, Smythe C, Sudbery P (2010). Hyphal growth in Candida albicans requires the phosphorylation of Sec2 by the Cdc28-Ccn1/Hgc1 kinase. EMBO J 29, 2930-2942.
4. Cabrera M, Langemeyer L, Mari M, Rethmeier R, Orban I, Perz A, Bröcker C, Griffth J, Klose D, Steinhoff HJ, et al. (2010). Phosphorylation of a membrane curvature-sensing motif switches function of the HOPS subunit Vps41 in membrane tethering. J Cell Biol 191, 845-859.
5. Chen S, Novick P, Ferro-Novick S (2012). ER network formation requires a balance of the dynamin-like GTPase Sey1p and the Lunapark family member Lnp1p. Nat Cell Biol 14, 707-716.
6. Chiba S, Amagai Y, Homma Y, Fukuda M, Mizuno K (2013). NDR2-mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specifcity from phosphatidylserine to Sec15. EMBO J 32, 874-885.
7. Demmel L, Beck M, Klose C, Schlaitz AL, Gloor Y, Hsu P P, Havlis J.
8. Shevchenko A, Krause E, Kalaidzidis Y, et al. (2008). Nucleocytoplasmic shuttling of the Golgi phosphatidylinositol 4-kinase Pik1 is regulated by 14-3-3 proteins and coordinates Golgi function with cell growth. Mol Biol Cell 19, 1046-1061.
9. Donovan KW, Bretscher A (2015). Tracking individual secretory vesicles during exocytosis reveals an ordered and regulated process. J Cell Biol 210, 181-189.
10. Elkind NB, Walch-Solimena C, Novick PJ (2000). The role of the COOH terminus of Sec2p in the transport of post-Golgi vesicles. J Cell Biol 149, 95-110.
11. Estrada E, Agostinis P, Vandenheede JR, Goris J, Merlevede W, François J, Goffeau A, Ghislain M (1996). Phosphorylation of yeast plasma membrane H+-ATPase by casein kinase I. J Biol Chem 271, 32064-32072.
12. Gadura N, Robinson LC, Michels CA (2006). Glc7-Reg1 phosphatase signals to Yck1, 2 casein kinase 1 to regulate transport activity and glucose-induced inactivation of Saccharomyces maltose permease. Genetics 172, 1427-1439.
13. Gault WJ, Olguin P, Weber U, Mlodzik M (2012). Drosophila CK1-γ, gil-gamesh, controls PCP-mediated morphogenesis through regulation of vesicle traffcking. J Cell Biol 196, 605-621.
14. Grosshans BL, Andreeva A, Gangar A, Niessen S, Yates JR, Brennwald P, Novick P (2006). The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J Cell Biol 172, 55-66.
15. Guo W, Roth D, Walch-Solimena C, Novick P (1999). The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18, 1071-1080.
16. Hergovich A, Stegert MR, Schmitz D, Hemmings Ba (2006). NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 7, 253-264.
17. Hutagalung AH, Novick PJ (2011). Role of Rab GTPases in membrane traffc and cell physiology. Physiol Rev 91, 119-149.
18. Jin Y, Sultana A, Gandhi P, Franklin E, Hamamoto S, Khan AR, Munson M, Schekman R, Weisman LS (2011). Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev Cell 21, 1156-1170.
19. Kurischko C, Kuravi VK, Wannissorn N, Nazarov PA, Husain M, Zhang C, Shokat KM, McCaffery JM, Luca FC (2008). The yeast LATS/Ndr kinase Cbk1 regulates growth via Golgi-dependent glycosylation and secretion. Mol Biol Cell 19, 5559-5578.
20. Lawrence G, Brown CC, Flood BA, Karunakaran S, Cabrera M, Nordmann M, Ungermann C, Fratti RA (2014). Dynamic association of the PI3P-interact-ing Mon1-Ccz1 GEF with vacuoles is controlled through its phosphoryla-tion by the type 1 casein kinase Yck3. Mol Biol Cell 25, 1608-1619.
21. Ling Y, Hayano S, Novick P (2014). Osh4p is needed to reduce the level of phosphatidylinositol-4-phosphate on secretory vesicles as they mature. Mol Biol Cell 25, 3389-3400.
22. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modifcation in Saccharomy-ces cerevisiae. Yeast 14, 953-961.
23. Lord C, Bhandari D, Menon S, Ghassemian M, Nycz D, Hay J, Ghosh P, Ferro-Novick S (2011). Sequential interactions with Sec23 control the direction of vesicle traffc. Nature 473, 181-186.
24. Marchal C, Dupré S, Urban-Grimal D (2002). Casein kinase I controls a late step in the endocytic traffcking of yeast uracil permease. J Cell Sci 115, 217-226.
25. Mazanka E, Alexander J, Yeh BJ, Charoenpong P, Lowery DM, Yaffe M, Weiss EL (2008). The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry. PLoS Biol 6, e203.
26. Medkova M, France YE, Coleman J, Novick P (2006). The rab exchange factor Sec2p reversibly associates with the exocyst. Mol Biol Cell 17, 2757-2769.
27. Mizuno-Yamasaki E, Medkova M, Coleman J, Novick P (2010). Phospha-tidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev Cell 18, 828-840.
28. Mizuno-Yamasaki E, Rivera-Molina F, Novick P (2012). GTPase networks in membrane traffc. Annu Rev Biochem 81, 637-659.
29. Mochida K, Ohsumi Y, Nakatogawa H (2014). Hrr25 phosphorylates the auto-phagic receptor Atg34 to promote vacuolar transport of α-mannosidase under nitrogen starvation conditions. FEBS Lett 588, 3862-3869.
30. Moriya H, Johnston M (2004). Glucose sensing and signaling in Saccharo-myces cerevisiae through the Rgt2 glucose sensor and casein kinase I. Proc Natl Acad Sci USA 101, 1572-1577.
31. Ortiz D, Medkova M, Walch-Solimena C, Novick P (2002). Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157, 1005.
32. Panek HR, Stepp JD, Engle HM, Marks KM, Tan PK, Lemmon SK, Robinson LC (1997). Suppressors of YCK-encoded yeast casein kinase 1 defciency defne the four subunits of a novel clathrin AP-like complex. EMBO J 16, 4194-4204.
33. Pfaffenwimmer T, Reiter W, Brach T, Nogellova VN, Papinski D, Schuschnig M, Abert C, Ammerer G, Martens S, Kraft C (2014). Hrr 25 kinase promotes selective autophagy by phosphorylating the cargo receptor Atg19. EMBO Rep 15, 862-870.
34. Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, Fasolo J, Guo H, Jona G, Breitkreutz A, Sopko R, et al. (2005). Global analysis of protein phos-phorylation in yeast. Nature 438, 679-684.
35. Robinson L, Menold M, Garrett S, Culbertson M (1993). Casein kinase I-like protein kinases encoded by YCKJ and YCK2 are required for yeast morphogenesis. Mol Cell Biol 13, 2870-2881.
36. Stalder D, Mizuno-Yamasaki E, Ghassemian M, Novick PJ (2013). Phosphor-ylation of the Rab exchange factor Sec2p directs a switch in regulatory binding partners. Proc Natl Acad Sci USA 110, 19995-20002.
37. Stalder D, Novick PJ (2015). Rab GTPases. Methods Mol Biol 1298, 85-98.
38. Stock SD, Hama H, DeWald DB, Takemoto JY (1999). SEC14-dependent secretion in Saccharomyces cerevisiae. J Biol Chem 274, 12979-12983.
39. Tanaka C, Tan L-J, Mochida K, Kirisako H, Koizumi M, Asai E, Sakoh-Naka-togawa M, Ohsumi Y, Nakatogawa H (2014). Hrr25 triggers selective autophagy-related pathways by phosphorylating receptor proteins. J Cell Biol 207, 91-105.
40. Ultanir SK, Hertz NT, Li G, Ge W P, Burlingame AL, Pleasure SJ, Shokat KM, Jan LY, Jan YN (2012). Chemical genetic identifcation of NDR1/2 kinase substrates AAK1 and Rabin8 Uncovers their roles in dendrite arborization and spine development. Neuron 73, 1127-1142.
41. Vancura A, Sessler A, Leichus B, Kuret J (1994). A prenylation motif is required for plasma membrane localization and biochemical function of casein kinase I in budding yeast. J Biol Chem 269, 19271-19278.
42. Walch-Solimena C, Collins RN, Novick PJ (1997). Sec2p mediates nucleo-tide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J Cell Biol 137, 1495-1509.
43. Wang J, Davis S, Menon S, Zhang J, Ding J, Cervantes S, Miller E, Jiang Y, Ferro-Novick S (2015a). Ypt1/Rab1 regulates Hrr25/CK1 kinase activity in ER-Golgi traffc and macroautophagy. J Cell Biol 210, 273-285.
44. Wang J, Ren J, Wu B, Feng S, Cai G, Tuluc F, Peränen J, Guo W (2015b). Activation of Rab8 guanine nucleotide exchange factor Rabin8 by ERK1/2 in response to EGF signaling. Proc Natl Acad Sci USA 112, 148-153.
45. Zhai L, Graves PR, Robinson LC, Italiano M, Culbertson MR, Rowles J, Cobb MH, DePaoli-Roach AA, Roach PJ (1995). Casein kinase I gamma subfamily. Molecular cloning, expression, and characterization of three mammalian isoforms and complementation of defects in the Saccharo-myces cerevisiae YCK ganes. J Biol Chem 270, 12717-12724.
46. Zick M, Wickner W (2012). Phosphorylation of the effector complex HOPS by the vacuolar kinase Yck3p confers Rab nucleotide specifcity for vacuole docking and fusion. Mol Biol Cell 23, 3429-3437.