The physiological functions of the Golgin vesicle tethering proteins

Frontiers in Cell and Developmental Biology

Volumn 7, Issue JUN, 2019, Pages

  Lowe, Martin ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Animal model; Extracellular matrix; Glycosylation; Golgi apparatus; Golgin; Secretion; Tether; Vesicle traffic

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; GIANTIN; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; GM 130 PROTEIN; GMAP 210 PROTEIN; GOLGIN; GOLGIN 160; GOLGIN 84; GUANOSINE TRIPHOSPHATASE; HYALURONIC ACID; PROTEIN; RAB PROTEIN; SCLEROPROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ACHONDROGENESIS TYPE 1A; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; BONE DYSPLASIA; CLEFT PALATE; CONGENITAL DISORDER OF GLYCOSYLATION; CRANIOFACIAL MALFORMATION; DEVELOPMENTAL DELAY; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX; GENE MUTATION; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; HYPERPHOSPHATEMIA; KNOCKOUT MOUSE; MICROCEPHALY; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; ODONTOCHONDRODYSPLASIA; PHENOTYPE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; RAT; REVIEW; SCOLIOSIS; SECRETORY PATHWAY; SEIZURE; TOOTH MALFORMATION; TRANSPORT VESICLE; TUMOR CALCINOSIS; WILD TYPE MOUSE;

EID: 85069162684     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2019.00094     Document Type: Review

References (98)

1. Barr, F. A., Puype, M., Vandekerckhove, J., and Warren, G. (1997). GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 91, 253-262. doi: 10.1016/s0092-8674(00)80407-9
2. Baschieri, F., Confalonieri, S., Bertalot, G., Di Fiore, P. P., Dietmaier, W., Leist, M., et al. (2014). Spatial control of Cdc42 signalling by a GM130-RasGRF complex regulates polarity and tumorigenesis. Nat. Commun. 5:4839. doi: 10.1038/ncomms5839
3. Baschieri, F., and Farhan, H. (2015). Endomembrane control of cell polarity: relevance to cancer. Small GTPases 6, 104-107. doi: 10.1080/21541248.2015.1018402
4. Bascom, R. A., Srinivasan, S., and Nussbaum, R. L. (1999). Identification and characterization of golgin-84, a novel Golgi integral membrane protein with a cytoplasmic coiled-coil domain. J. Biol. Chem. 274, 2953-2962. doi: 10.1074/jbc.274.5.2953
5. Bekier, M. E. II, Wang, L., Li, J., Huang, H., Tang, D., Zhang, X., et al. (2017). Knockout of the Golgi stacking proteins GRASP55 and GRASP65 impairs Golgi structure and function. Mol. Biol. Cell 28, 2833-2842. doi: 10.1091/mbc.E17-02-0112
6. Bel, S., Elkis, Y., Elifantz, H., Koren, O., Ben-Hamo, R., Lerer-Goldshtein, T., et al. (2014). Reprogrammed and transmissible intestinal microbiota confer diminished susceptibility to induced colitis in TMF-/- mice. Proc. Natl. Acad. Sci. U.S.A. 111, 4964-4969. doi: 10.1073/pnas.1319114111
7. Bel, S., Elkis, Y., Lerer-Goldstein, T., Nyska, A., Shpungin, S., and Nir, U. (2012). Loss of TMF/ARA160 protein renders colonic mucus refractory to bacterial colonization and diminishes intestinal susceptibility to acute colitis. J. Biol. Chem. 287, 25631-25639. doi: 10.1074/jbc.M112.364786
8. Bentson, L. F., Agbor, V. A., Agbor, L. N., Lopez, A. C., Nfonsam, L. E., Bornstein, S. S., et al. (2013). New point mutation in Golga3 causes multiple defects in spermatogenesis. Andrology 1, 440-450. doi: 10.1111/j.2047-2927.2013.00070.x
9. Bergen, D. J. M., Stevenson, N. L., Skinner, R. E. H., Stephens, D. J., and Hammond, C. L. (2017). The Golgi matrix protein giantin is required for normal cilia function in zebrafish. Biol. Open 6, 1180-1189. doi: 10.1242/bio.025502
10. Bird, I. M., Kim, S. H., Schweppe, D. K., Caetano-Lopes, J., Robling, A. G., Charles, J. F., et al. (2018). The skeletal phenotype of achondrogenesis type 1A is caused exclusively by cartilage defects. Development 145:dev156588. doi: 10.1242/dev.156588
11. Boycott, K. M., Vanstone, M. R., Bulman, D. E., and MacKenzie, A. E. (2013). Rare-disease genetics in the era of next-generation sequencing: discovery to translation. Nat. Rev. Genet. 14, 681-691. doi: 10.1038/nrg3555
12. Braun, D. A., and Hildebrandt, F. (2017). Ciliopathies. Cold Spring Harb. Perspect. Biol. 9:a028191. doi: 10.1101/cshperspect.a028191
13. Broekhuis, J. R., Rademakers, S., Burghoorn, J., and Jansen, G. (2013). SQL-1, homologue of the Golgi protein GMAP210, modulates intraflagellar transport in C. elegans. J. Cell Sci. 126, 1785-1795. doi: 10.1242/jcs.116640
14. Chan, W. L., Steiner, M., Witkos, T., Egerer, J., Busse, B., Mizumoto, S., et al. (2018). Impaired proteoglycan glycosylation, elevated TGF-beta signaling, and abnormal osteoblast differentiation as the basis for bone fragility in a mouse model for gerodermia osteodysplastica. PLoS Genet. 14:e1007242. doi: 10.1371/journal.pgen.1007242
15. Cheung, P. Y., Limouse, C., Mabuchi, H., and Pfeffer, S. R. (2015). Protein flexibility is required for vesicle tethering at the Golgi. eLife 4:e12790. doi: 10.7554/eLife.12790
16. Cheung, P. Y., and Pfeffer, S. R. (2016). Transport vesicle tethering at the trans Golgi network: coiled coil proteins in action. Front. Cell Dev. Biol. 4:18. doi: 10.3389/fcell.2016.00018
17. Cui, Y., Carosi, J. M., Yang, Z., Ariotti, N., Kerr, M. C., Parton, R. G., et al. (2019). Retromer has a selective function in cargo sorting via endosome transport carriers. J. Cell Biol. 218, 615-631. doi: 10.1083/jcb.201806153
18. Daane, J. M., Dornburg, A., Smits, P., MacGuigan, D. J., Hawkins, M. B., Near, T. J., et al. (2019). Historical contingency shapes adaptive radiation in Antarctic fishes. Bioarchives. doi: 10.1101/478842
19. Diao, A., Frost, L., Morohashi, Y., and Lowe, M. (2008). Coordination of golgin tethering and SNARE assembly: GM130 binds syntaxin 5 in a p115-regulated manner. J. Biol. Chem. 283, 6957-6967. doi: 10.1074/jbc.M708401200
20. Diao, A., Rahman, D., Pappin, D. J., Lucocq, J., and Lowe, M. (2003). The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J. Cell Biol. 160, 201-212. doi: 10.1083/jcb.200207045
21. Drin, G., Morello, V., Casella, J. F., Gounon, P., and Antonny, B. (2008). Asymmetric tethering of flat and curved lipid membranes by a golgin. Science 320, 670-673. doi: 10.1126/science.1155821
22. Dvorak, K., and Bucek, J. (1970). Postnatal differentiation of the Golgi apparatus and the dendrites of Purkinje cells of the rat cerebellum. A histochemical and electron microscopic study. Z Zellforsch Mikrosk Anat 111, 51-63. doi: 10.1007/bf00342100
23. Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P. M., Andreyeva, N., et al. (2007). Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917-930. doi: 10.1016/j.devcel.2007.04.002
24. Elkis, Y., Bel, S., Rahimi, R., Lerer-Goldstein, T., Levin-Zaidman, S., Babushkin, T., et al. (2015). TMF/ARA160 governs the dynamic spatial orientation of the Golgi apparatus during sperm development. PLoS One 10:e0145277. doi: 10.1371/journal.pone.0145277
25. Follit, J. A., Tuft, R. A., Fogarty, K. E., and Pazour, G. J. (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17, 3781-3792. doi: 10.1091/mbc.e06-02-0133
26. Fridmann-Sirkis, Y., Siniossoglou, S., and Pelham, H. R. (2004). TMF is a golgin that binds Rab6 and influences Golgi morphology. BMC Cell Biol. 5:18. doi: 10.1186/1471-2121-5-181471-2121-5-18
27. Gillingham, A. K. (2018). At the ends of their tethers! How coiled-coil proteins capture vesicles at the Golgi. Biochem. Soc. Trans. 46, 43-50. doi: 10.1042/BST20170188
28. Gillingham, A. K., and Munro, S. (2016). Finding the Golgi: golgin coiled-coil proteins show the way. Trends Cell Biol. 26, 399-408. doi: 10.1016/j.tcb.2016.02.005
29. Gillingham, A. K., Pfeifer, A. C., and Munro, S. (2002). CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol. Biol. Cell 13, 3761-3774. doi: 10.1091/mbc.E02-06-0349
30. Gillingham, A. K., Tong, A. H., Boone, C., and Munro, S. (2004). The GTPase Arf1p and the ER to Golgi cargo receptor Erv14p cooperate to recruit the golgin Rud3p to the cis-Golgi. J. Cell Biol. 167, 281-292. doi: 10.1083/jcb.200407088
31. Goldblatt, J., Carman, P., and Sprague, P. (1991). Unique dwarfing, spondylometaphyseal skeletal dysplasia, with joint laxity and dentinogenesis imperfecta. Am. J. Med. Genet. 39, 170-172. doi: 10.1002/ajmg.1320390211
32. Greenberg, C. R., Rimoin, D. L., Gruber, H. E., DeSa, D. J., Reed, M., and Lachman, R. S. (1988). A new autosomal recessive lethal chondrodystrophy with congenital hydrops. Am. J. Med. Genet. 29, 623-632. doi: 10.1002/ajmg.1320290321
33. Han, F., Liu, C., Zhang, L., Chen, M., Zhou, Y., Qin, Y., et al. (2017). Globozoospermia and lack of acrosome formation in GM130-deficient mice. Cell Death Dis. 8:e2532. doi: 10.1038/cddis.2016.414
34. Hennies, H. C., Kornak, U., Zhang, H., Egerer, J., Zhang, X., Seifert, W., et al. (2008). Gerodermia osteodysplastica is caused by mutations in SCYL1BP1, a Rab-6 interacting golgin. Nat. Genet. 40, 1410-1412. doi: 10.1038/ng.252
35. Hicks, S. W., Horn, T. A., McCaffery, J. M., Zuckerman, D. M., and Machamer, C. E. (2006). Golgin-160 promotes cell surface expression of the beta-1 adrenergic receptor. Traffic 7, 1666-1677. doi: 10.1111/j.1600-0854.2006.00504.x
36. Horton, A. C., Racz, B., Monson, E. E., Lin, A. L., Weinberg, R. J., and Ehlers, M. D. (2005). Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771. doi: 10.1016/j.neuron.2005.11.005
37. Joachim, J., Jefferies, H. B., Razi, M., Frith, D., Snijders, A. P., Chakravarty, P., et al. (2015). Activation of ULK kinase and autophagy by GABARAP trafficking from the centrosome is regulated by WAC and GM130. Mol. Cell 60, 899-913. doi: 10.1016/j.molcel.2015.11.018
38. Kapitein, L. C., and Hoogenraad, C. C. (2015). Building the neuronal microtubule cytoskeleton. Neuron 87, 492-506. doi: 10.1016/j.neuron.2015.05.046
39. Katayama, K., Kuriki, M., Kamiya, T., Tochigi, Y., and Suzuki, H. (2018). Giantin is required for coordinated production of aggrecan, link protein and type XI collagen during chondrogenesis. Biochem. Biophys. Res. Commun. 499, 459-465. doi: 10.1016/j.bbrc.2018.03.163
40. Katayama, K., Sasaki, T., Goto, S., Ogasawara, K., Maru, H., Suzuki, K., et al. (2011). Insertional mutation in the Golgb1 gene is associated with osteochondrodysplasia and systemic edema in the OCD rat. Bone 49, 1027-1036. doi: 10.1016/j.bone.2011.08.001
41. Kierszenbaum, A. L., Rivkin, E., Tres, L. L., Yoder, B. K., Haycraft, C. J., Bornens, M., et al. (2011). GMAP210 and IFT88 are present in the spermatid golgi apparatus and participate in the development of the acrosome-acroplaxome complex, head-tail coupling apparatus and tail. Dev. Dyn. 240, 723-736. doi: 10.1002/dvdy.22563
42. Kikukawa, K., Kamei, T., and Suzuki, K. (1991). A histological and histochemical study on glycosaminoglycans in epiphysial cartilage of osteochondrodysplasia rat (OCD/OCD). Connect Tissue Res. 25, 301-309. doi: 10.3109/03008209109029165
43. Kikukawa, K., Kamei, T., Suzuki, K., and Maita, K. (1990). Electron microscopic observations and electrophoresis of the glycosaminoglycans in the epiphyseal cartilage of the congenital osteochondrodysplasia rat (ocd/ocd). Matrix 10, 378-387. doi: 10.1016/s0934-8832(11)80145-9
44. Kondylis, V., and Rabouille, C. (2003). A novel role for dp115 in the organization of tER sites in Drosophila. J. Cell Biol. 162, 185-198. doi: 10.1083/jcb.200301136
45. Koreishi, M., Gniadek, T. J., Yu, S., Masuda, J., Honjo, Y., and Satoh, A. (2013). The golgin tether giantin regulates the secretory pathway by controlling stack organization within Golgi apparatus. PLoS One 8:e59821. doi: 10.1371/journal.pone.0059821
46. Lan, Y., Zhang, N., Liu, H., Xu, J., and Jiang, R. (2016). Golgb1 regulates protein glycosylation and is crucial for mammalian palate development. Development 143, 2344-2355. doi: 10.1242/dev.134577
47. Lerer-Goldshtein, T., Bel, S., Shpungin, S., Pery, E., Motro, B., Goldstein, R. S., et al. (2010). TMF/ARA160: a key regulator of sperm development. Dev. Biol. 348, 12-21. doi: 10.1016/j.ydbio.2010.07.033
48. Linstedt, A. D., Foguet, M., Renz, M., Seelig, H. P., Glick, B. S., and Hauri, H. P. (1995). A C-terminally-anchored Golgi protein is inserted into the endoplasmic reticulum and then transported to the Golgi apparatus. Proc. Natl. Acad. Sci. U.S.A. 92, 5102-5105. doi: 10.1073/pnas.92.11.5102
49. Liu, C., Mei, M., Li, Q., Roboti, P., Pang, Q., Ying, Z., et al. (2017). Loss of the golgin GM130 causes Golgi disruption, Purkinje neuron loss, and ataxia in mice. Proc. Natl. Acad. Sci. U.S.A. 114, 346-351. doi: 10.1073/pnas.1608576114
50. Malsam, J., Satoh, A., Pelletier, L., and Warren, G. (2005). Golgin tethers define subpopulations of COPI vesicles. Science 307, 1095-1098. doi: 10.1126/science.1108061
51. Marra, P., Salvatore, L., Mironov, A, Jr., Di Campli, A., Di Tullio, G., Trucco, A., et al. (2007). The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol. Biol. Cell 18, 1595-1608. doi: 10.1091/mbc.e06-10-0886
52. Matsukuma, S., Kondo, M., Yoshihara, M., Matsuda, M., Utakoji, T., and Sutou, S. (1999). Mea2/Golga3 gene is disrupted in a line of transgenic mice with a reciprocal translocation between Chromosomes 5 and 19 and is responsible for a defective spermatogenesis in homozygotes. Mamm. Genome 10, 1-5. doi: 10.1007/s003359900932
53. McGee, L. J., Jiang, A. L., and Lan, Y. (2017). Golga5 is dispensable for mouse embryonic development and postnatal survival. Genesis 55:e23039. doi: 10.1002/dvg.23039
54. Molz, G., and Spycher, M. A. (1980). Achondrogenesis type I: light and electron-microscopic studies. Eur. J. Pediatr. 134, 69-74. doi: 10.1007/bf00442406
55. Monis, W. J., Faundez, V., and Pazour, G. J. (2017). BLOC-1 is required for selective membrane protein trafficking from endosomes to primary cilia. J. Cell Biol. 216, 2131-2150. doi: 10.1083/jcb.201611138
56. Moreno, R. D., Ramalho-Santos, J., Sutovsky, P., Chan, E. K., and Schatten, G. (2000). Vesicular traffic and golgi apparatus dynamics during mammalian spermatogenesis: implications for acrosome architecture. Biol. Reprod. 63, 89-98. doi: 10.1095/biolreprod63.1.89
57. Moyer, B. D., Allan, B. B., and Balch, W. E. (2001). Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2, 268-276. doi: 10.1034/j.1600-0854.2001.1o007.x
58. Munro, S. (2011). The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harb. Perspect. Biol. 3:a005256. doi: 10.1101/cshperspect.a005256
59. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., et al. (1995). Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131, 1715-1726. doi: 10.1083/jcb.131.6.1715
60. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T., and Kanemaki, M. (2009). An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922. doi: 10.1038/nmeth.1401
61. Noda, K., Kitami, M., Kitami, K., Kaku, M., and Komatsu, Y. (2016). Canonical and noncanonical intraflagellar transport regulates craniofacial skeletal development. Proc. Natl. Acad. Sci. U.S.A. 113, E2589-E2597. doi: 10.1073/pnas.1519458113
62. Park, S., Kim, S., Kim, M. J., Hong, Y., Lee, A. Y., Lee, H., et al. (2018). GOLGA2 loss causes fibrosis with autophagy in the mouse lung and liver. Biochem. Biophys. Res. Commun. 495, 594-600. doi: 10.1016/j.bbrc.2017.11.049
63. Preisinger, C., Short, B., De Corte, V., Bruyneel, E., Haas, A., Kopajtich, R., et al. (2004). YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta. J. Cell Biol. 164, 1009-1020. doi: 10.1083/jcb.200310061
64. Puthenveedu, M. A., Bachert, C., Puri, S., Lanni, F., and Linstedt, A. D. (2006). GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat. Cell Biol. 8, 238-248. doi: 10.1038/ncb1366
65. Puthenveedu, M. A., and Linstedt, A. D. (2001). Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130. J. Cell Biol. 155, 227-238. doi: 10.1083/jcb.200105005
66. Ramirez, I. B., and Lowe, M. (2009). Golgins and GRASPs: holding the Golgi together. Semin. Cell Dev. Biol. 20, 770-779. doi: 10.1016/j.semcdb.2009.03.011
67. Ramos-Morales, F., Vime, C., Bornens, M., Fedriani, C., and Rios, R. M. (2001). Two splice variants of Golgi-microtubule-associated protein of 210 kDa (GMAP-210) differ in their binding to the cis-Golgi network. Biochem. J. 357, 699-708. doi: 10.1042/bj3570699
68. Ridsdale, A., Denis, M., Gougeon, P. Y., Ngsee, J. K., Presley, J. F., and Zha, X. (2006). Cholesterol is required for efficient endoplasmic reticulum-to-Golgi transport of secretory membrane proteins. Mol. Biol. Cell 17, 1593-1605. doi: 10.1091/mbc.e05-02-0100
69. Rivero, S., Cardenas, J., Bornens, M., and Rios, R. M. (2009). Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 28, 1016-1028. doi: 10.1038/emboj.2009.47
70. Roboti, P., Sato, K., and Lowe, M. (2015). The golgin GMAP-210 is required for efficient membrane trafficking in the early secretory pathway. J. Cell Sci. 128, 1595-1606. doi: 10.1242/jcs.166710
71. Sato, K., Roboti, P., Mironov, A. A., and Lowe, M. (2015). Coupling of vesicle tethering and Rab binding is required for in vivo functionality of the golgin GMAP-210. Mol. Biol. Cell 26, 537-553. doi: 10.1091/mbc.E14-10-1450
72. Satoh, A., Wang, Y., Malsam, J., Beard, M. B., and Warren, G. (2003). Golgin-84 is a rab1 binding partner involved in Golgi structure. Traffic 4, 153-161. doi: 10.1034/j.1600-0854.2003.00103.x
73. Shamseldin, H. E., Bennett, A. H., Alfadhel, M., Gupta, V., and Alkuraya, F. S. (2016). GOLGA2, encoding a master regulator of golgi apparatus, is mutated in a patient with a neuromuscular disorder. Hum. Genet. 135, 245-251. doi: 10.1007/s00439-015-1632-8
74. Shin, J. J. H., Gillingham, A. K., Begum, F., Chadwick, J., and Munro, S. (2017). TBC1D23 is a bridging factor for endosomal vesicle capture by golgins at the trans-Golgi. Nat. Cell Biol. 19, 1424-1432. doi: 10.1038/ncb3627
75. Short, B., Preisinger, C., Korner, R., Kopajtich, R., Byron, O., and Barr, F. A. (2001). A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic. J. Cell Biol. 155, 877-883. doi: 10.1083/jcb.200108079
76. Smits, P., Bolton, A. D., Funari, V., Hong, M., Boyden, E. D., Lu, L., et al. (2010). Lethal skeletal dysplasia in mice and humans lacking the golgin GMAP-210. N. Engl. J. Med. 362, 206-216. doi: 10.1056/NEJMoa0900158
77. Sonnichsen, B., Lowe, M., Levine, T., Jamsa, E., Dirac-Svejstrup, B., and Warren, G. (1998). A role for giantin in docking COPI vesicles to Golgi membranes. J. Cell Biol. 140, 1013-1021. doi: 10.1083/jcb.140.5.1013
78. Stevenson, N. L., Bergen, D. J. M., Skinner, R. E. H., Kague, E., Martin-Silverstone, E., Robson Brown, K. A., et al. (2017). Giantin-knockout models reveal a feedback loop between Golgi function and glycosyltransferase expression. J. Cell Sci. 130, 4132-4143. doi: 10.1242/jcs.212308
79. Stuven, E., Porat, A., Shimron, F., Fass, E., Kaloyanova, D., Brugger, B., et al. (2003). Intra-Golgi protein transport depends on a cholesterol balance in the lipid membrane. J. Biol. Chem. 278, 53112-53122. doi: 10.1074/jbc.M300402200
80. Tanabe, K., Kani, S., Shimizu, T., Bae, Y. K., Abe, T., and Hibi, M. (2010). Atypical protein kinase C regulates primary dendrite specification of cerebellar Purkinje cells by localizing Golgi apparatus. J. Neurosci. 30, 16983-16992. doi: 10.1523/JNEUROSCI.3352-10.2010
81. Tanaka, M. (2009). Dendrite formation of cerebellar purkinje cells. Neurochem. Res. 34, 2078-2088. doi: 10.1007/s11064-009-0073-y
82. Topaz, O., Shurman, D. L., Bergman, R., Indelman, M., Ratajczak, P., Mizrachi, M., et al. (2004). Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat. Genet. 36, 579-581. doi: 10.1038/ng1358
83. Tsai, P. L., Zhao, C., Turner, E., and Schlieker, C. (2016). The lamin B receptor is essential for cholesterol synthesis and perturbed by disease-causing mutations. eLife 5:e16011. doi: 10.7554/eLife.16011
84. Wehrle, A., Witkos, T. M., Schneider, J. C., Hoppmann, A., Behringer, S., Kottgen, A., et al. (2018). A common pathomechanism in GMAP-210- and LBR-related diseases. JCI Insight 3:121150. doi: 10.1172/jci.insight.121150
85. Wehrle, A., Witkos, T. M., Unger, S., Schneider, J., Follit, J. A., Hermann, J., et al. (2019). Hypomorphic mutations of TRIP11 cause odontochondrodysplasia. JCI Insight doi: 10.1172/jci.insight.124701 [Epub ahead of print].
86. Weide, T., Bayer, M., Koster, M., Siebrasse, J. P., Peters, R., and Barnekow, A. (2001). The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b. EMBO Rep. 2, 336-341. doi: 10.1093/embo-reports/kve065
87. Willett, R., Ungar, D., and Lupashin, V. (2013). The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem. Cell Biol. 140, 271-283. doi: 10.1007/s00418-013-1117-6
88. Witkos, T. M., Chan, W. L., Joensuu, M., Rhiel, M., Pallister, E., Thomas-Oates, J., et al. (2019). GORAB scaffolds COPI at the trans-Golgi for efficient enzyme recycling and correct protein glycosylation. Nat. Commun. 10:127. doi: 10.1038/s41467-018-08044-6
89. Witkos, T. M., and Lowe, M. (2015). The golgin family of coiled-coil tethering proteins. Front. Cell Dev. Biol. 3:86. doi: 10.3389/fcell.2015.00086
90. Witkos, T. M., and Lowe, M. (2017). Recognition and tethering of transport vesicles at the Golgi apparatus. Curr. Opin. Cell Biol. 47, 16-23. doi: 10.1016/j.ceb.2017.02.003
91. Wong, M., Gillingham, A. K., and Munro, S. (2017). The golgin coiled-coil proteins capture different types of transport carriers via distinct N-terminal motifs. BMC Biol. 15:3. doi: 10.1186/s12915-016-0345-3
92. Wong, M., and Munro, S. (2014). Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science 346:1256898. doi: 10.1126/science.1256898
93. Yadav, S., Puthenveedu, M. A., and Linstedt, A. D. (2012). Golgin160 recruits the dynein motor to position the Golgi apparatus. Dev. Cell 23, 153-165. doi: 10.1016/j.devcel.2012.05.023
94. Yamane, J., Kubo, A., Nakayama, K., Yuba-Kubo, A., Katsuno, T., Tsukita, S., et al. (2007). Functional involvement of TMF/ARA160 in Rab6-dependent retrograde membrane traffic. Exp. Cell Res. 313, 3472-3485. doi: 10.1016/j.yexcr.2007.07.010
95. Zappa, F., Failli, M., and De Matteis, M. A. (2018). The golgi complex in disease and therapy. Curr. Opin. Cell Biol. 50, 102-116. doi: 10.1016/j.ceb.2018.03.005
96. Zeevaert, R., Foulquier, F., Jaeken, J., and Matthijs, G. (2008). Deficiencies in subunits of the conserved oligomeric golgi (COG) complex define a novel group of congenital disorders of glycosylation. Mol. Genet. Metab. 93, 15-21. doi: 10.1016/j.ymgme.2007.08.118
97. Zhang, Z., Li, W., Zhang, Y., Zhang, L., Teves, M. E., Liu, H., et al. (2016). Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice. Mol Biol Cell doi: 10.1091/mbc.E16-05-0318 [Epub ahead of print].
98. Zhou, W., Chang, J., Wang, X., Savelieff, M. G., Zhao, Y., Ke, S., et al. (2014). GM130 is required for compartmental organization of dendritic golgi outposts. Curr. Biol. 24, 1227-1233. doi: 10.1016/j.cub.2014.04.008