COG7 deficiency in Drosophila generates multifaceted developmental, behavioral and protein glycosylation phenotypes

Journal of Cell Science

Volumn 130, Issue 21, 2017, Pages 3637-3649

  Frappaolo, Anna ^a   Sechi, Stefano ^a   Kumagai, Tadahiro ^b   Robinson, Sarah ^b   Fraschini, Roberta ^c   Karimpour Ghahnavieh, Angela ^a   Belloni, Giorgio ^a   Piergentili, Roberto ^a   Tiemeyer, Katherine H ^b   Tiemeyer, Michael ^b   Giansanti, Maria Grazia ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

COG7; Drosophila; Glycosylation; Golgi; GOLPH3

Indexed keywords

COAT PROTEIN COMPLEX I; CONSERVED OLIGOMERIC GOLGI COMPLEX 7; GOLGI PHOSPHOPROTEIN 3; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; RAB1 PROTEIN; RAB11 PROTEIN; UNCLASSIFIED DRUG; COG7 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GOLPH3 PROTEIN, DROSOPHILA; MANNOSE; OMELETTE PROTEIN, DROSOPHILA; ONCOPROTEIN; POLYSACCHARIDE; RAB PROTEIN; VESICULAR TRANSPORT PROTEIN;

ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CLINICAL FEATURE; COG7 GENE; CONGENITAL DISORDER OF GLYCOSYLATION; CONTROLLED STUDY; CYTOKINESIS; DROSOPHILA MELANOGASTER; GENE; GENE INTERACTION; GENOTYPE; GOLGI MEMBRANE; HETEROZYGOSITY; HOMOZYGOSITY; INSECT LARVA; LONGEVITY; LOSS OF FUNCTION MUTATION; MALE; MUTANT; NEUROMUSCULAR JUNCTION; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; SIALYLATION; WILD TYPE; ANIMAL; DEFICIENCY; DISEASE MODEL; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GLYCOSYLATION; GOLGI COMPLEX; GROWTH, DEVELOPMENT AND AGING; HUMAN; LARVA; METABOLISM; NEUROLOGIC GAIT DISORDER; PATHOLOGY; PHENOTYPE; PROTEIN PROCESSING; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CONGENITAL DISORDERS OF GLYCOSYLATION; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GAIT DISORDERS, NEUROLOGIC; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC COMPLEMENTATION TEST; GLYCOSYLATION; GOLGI APPARATUS; HUMANS; LARVA; MANNOSE; NEUROMUSCULAR JUNCTION; ONCOGENE PROTEINS; PHENOTYPE; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAB GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 85032803343     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.209049     Document Type: Article

References (80)

1. Anumula, K. R. and Taylor, P. B. (1992). A comprehensive procedure for preparation of partially methylated alditol acetates from glycoprotein carbohydrates. Anal. Biochem. 203, 101-108.
2. Aoki, K., Perlman, M., Lim, J.-M., Cantu, R., Wells, L. and Tiemeyer, M. (2007). Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J. Biol. Chem. 282, 9127-9142.
3. Baas, S., Sharrow, M., Kotu, V., Middleton, M., Nguyen, K., Flanagan-Steet, H., Aoki, K. and Tiemeyer, M. (2011). Sugar-free frosting, a homolog of SAD kinase, drives neural-specific glycan expression in the Drosophila embryo. Development 138, 553-563.
4. Bailey Blackburn, J., Pokrovskaya, I., Fisher, P., Ungar, D. and Lupashin, V. V. (2016). COG complex complexities: detailed characterization of a complete set of HEK293T cells lacking individual COG subunits. Front. Cell Dev. Biol. 4, 23.
5. Barone, R., Fiumara, A. and Jaeken, J. (2014). Congenital disorders of glycosylation with emphasis on cerebellar involvement. Semin. Neurol. 34, 357-366.
6. Belloni, G., Sechi, S., Riparbelli, M. G., Fuller, M. T., Callaini, G. and Giansanti, M. G. (2012). Mutations in Cog7 affect Golgi structure, meiotic cytokinesis and sperm development during Drosophila spermatogenesis. J. Cell Sci. 125, 5441-5452.
7. Cassani, C., Raspelli, E., Santo, N., Chiroli, E., Lucchini, G. and Fraschini, R. (2013). Saccharomyces cerevisiae Dma proteins participate in cytokinesis by controlling two different pathways. Cell Cycle 12, 2794-2808.
8. Chang, W.-L., Chang, C.-W., Chang, Y.-Y., Sung, H.-H., Lin, M.-D., Chang, S.-C., Chen, C.-H., Huang, C.-W., Tung, K.-S. and Chou, T.-B. (2013). The Drosophila GOLPH3 homolog regulates the biosynthesis of heparan sulfate proteoglycans by modulating the retrograde trafficking of exostosins. Development 140, 2798-2807.
9. Chu, J., Mir, A., Gao, N., Rosa, S., Monson, C., Sharma, V., Steet, R., Freeze, H. H., Lehrman, M. A. and Sadler, K. C. (2013). A zebrafishmodel of congenital disorders of glycosylation with phosphomannose isomerase deficiency reveals an early opportunity for corrective mannose supplementation. Dis. Model. Mech. 6, 95-105.
10. Climer, L. K., Dobretsov, M. and Lupashin, V. (2015). Defects in theCOGcomplex and COG-related trafficking regulators affect neuronal Golgi function. Front. Neurosci. 9, 405.
11. Comstra, H. S., McArthy, J., Rudin-Rush, S., Hartwig, C., Gokhale, A., Zlatic, S. A., Blackburn, J. B., Werner, E., Petris, M., D'Souza, P. et al. (2017). The interactome of the copper transporter ATP7A belongs to a network of neurodevelopmental and neurodegeneration factors. Elife 6, e24722.
12. Dani, N., Nahm, M., Lee, S. and Broadie, K. (2012). A targeted glycan-related gene screen reveals heparan sulfate proteoglycan sulfation regulates WNT and BMP trans-synaptic signaling. PLoS Genet. 8, e1003031.
13. Dani, N., Zhu, H. and Broadie, K. (2014). Two protein N-acetylgalactosaminyl transferases regulate synaptic plasticity by activity-dependent regulation of integrin signaling. J. Neurosci. 34, 13047-13065.
14. Eckert, E. S. P., Reckmann, I., Hellwig, A., Röhling, S., El-Battari, A., Wieland, F. T. and Popoff, V. (2014). Golgi phosphoprotein 3 triggers signal-mediated incorporation of glycosyltransferases into coatomer-coated (COPI) vesicles. J. Biol. Chem. 289, 31319-31329.
15. Farkas, R. M., Giansanti, M. G., Gatti, M. and Fuller, M. T. (2003). The Drosophila Cog5 homologue is required for cytokinesis, cell elongation, and assembly of specialized Golgi architecture during spermatogenesis. Mol. Biol. Cell 14, 190-200.
16. Foulquier, F., Vasile, E., Schollen, E., Callewaert, N., Raemaekers, T., Quelhas, D., Jaeken, J., Mills, P., Winchester, B., Krieger, M. et al. (2006). Conserved oligomeric Golgi complex subunit 1 deficiency reveals a previously uncharacterized congenital disorder of glycosylation type II. Proc. Natl. Acad. Sci. USA 103, 3764-3769.
17. Frappaolo, A., Sechi, S., Belloni, G., Piergentili, R. and Giansanti, M. G. (2017). Visualization of cleavage furrow proteins in fixed dividing spermatocytes. Methods Cell Biol. 137, 85-103.
18. Freeze, H. H. and Ng, B. G. (2011). Golgi glycosylation and human inherited diseases. Cold Spring Harb. Perspect. Biol. 3, a005371.
19. Freeze, H. H., Chong, J. X., Bamshad, M. J. and Ng, B. G. (2014). Solving glycosylation disorders: fundamental approaches reveal complicated pathways. Am. J. Hum. Genet. 94, 161-175.
20. Freeze, H. H., Eklund, E. A., Ng, B. G. and Patterson, M. C. (2015). Neurological aspects of human glycosylation disorders. Annu. Rev. Neurosci. 38, 105-125.
21. Fung, C.W., Matthijs, G., Sturiale, L., Garozzo, D., Wong, K. Y., Wong, R., Wong, V. and Jaeken, J. (2012). COG5-CDG with a mild neurohepatic presentation. JIMD Rep. 3, 67-70.
22. Giansanti, M. G. and Fuller, M. T. (2012). What Drosophila spermatocytes tell us about the mechanisms underlying cytokinesis. Cytoskeleton 69, 869-881.
23. Giansanti, M. G., Farkas, R. M., Bonaccorsi, S., Lindsley, D. L., Wakimoto, B. T., Fuller, M. T. and Gatti, M. (2004). Genetic dissection of meiotic cytokinesis in Drosophila males. Mol. Biol. Cell. 15, 2509-2522.
24. Giansanti, M. G., Bonaccorsi, S., Kurek, R., Farkas, R. M., Dimitri, P., Fuller, M. T. and Gatti, M. (2006). The class I PITP giotto is required for Drosophila cytokinesis. Curr. Biol. 16, 195-201.
25. Giansanti, M. G., Vanderleest, T. E., Jewett, C. E., Sechi, S., Frappaolo, A., Fabian, L., Robinett, C. C., Brill, J. A., Loerke, D., Fuller, M. T. et al. (2015). Exocyst-dependent membrane addition is required for anaphase cell elongation and cytokinesis in Drosophila. PLoS Genet. 11, e1005632.
26. Goreta, S. S., Dabelic, S. and Dumic, J. (2012). Insights into complexity of congenital disorders of glycosylation. Biochem. Med. 22, 156-170.
27. Hong, W. J. and Lev, S. (2014). Tethering the assembly of SNARE complexes. Trends Cell. Biol. 24, 35-43.
28. Isaji, T., Im, S., Gu, W., Wang, Y., Hang, Q., Lu, J., Fukuda, T., Hashii, N., Takakura, D., Kawasaki, N. et al. (2014). An oncogenic protein Golgi phosphoprotein 3 up-regulates cell migration via sialylation. J. Biol. Chem. 289, 20694-20705.
29. Itoh, K., Akimoto, Y., Fuwa, T. J., Sato, C., Komatsu, A. and Nishihara, S. (2016). Mucin-type core 1 glycans regulate the localization of neuromuscular junctions and establishment of muscle cell architecture in Drosophila. Dev. Biol. 412, 114-127.
30. Jaeken, J. (2013). Congenital disorders of glycosylation. Handb. Clin. Neurol. 113, 1737-1743.
31. Jan, L. Y. and Jan, Y. N. (1982). Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc. Natl. Acad. Sci. USA 79, 2700-2704.
32. Johnson, K. G., Tenney, A. P., Ghose, A., Duckworth, A. M., Higashi, M. E., Parfitt, K., Marcu, O., Heslip, T. R., Marsh, J. L., Schwarz, T. L. et al. (2006). The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49, 517-531.
33. Jumbo-Lucioni, P., Parkinson, W. and Broadie, K. (2014). Overelaborated synaptic architecture and reduced synaptomatrix glycosylation in a Drosophila classic galactosemia disease model. Dis. Model. Mech. 7, 1365-1378.
34. Jumbo-Lucioni, P. P., Parkinson, W. M., Kopke, D. L. and Broadie, K. (2016). Coordinated movement, neuromuscular synaptogenesis and trans-synaptic signaling defects in Drosophila galactosemia models. Hum. Mol. Genet. 25, 3699-3714.
35. Katoh, T. and Tiemeyer, M. (2013). The N's and O's of Drosophila glycoprotein glycobiology. Glycoconj. J. 30, 57-66.
36. Kaufmann, N., DeProto, J., Ranjan, R., Wan, H. and Van Vactor, D. (2002). Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 28, 27-38.
37. Kingsley, D. M., Kozarsky, K. F., Segal, M. and Krieger, M. (1986). Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains. J. Cell Biol. 102, 1576-1585.
38. Kitazawa, D., Yamaguchi, M., Mori, H. and Inoue, Y. H. (2012). COPI-mediated membrane trafficking is required for cytokinesis in Drosophila male meiotic divisions. J. Cell Sci. 125, 3649-3660.
39. Kodera, H., Ando, N., Yuasa, I., Wada, Y., Tsurusaki, Y., Nakashima, M., Miyake, N., Saitoh, S., Matsumoto, N. and Saitsu, H. (2015). Mutations in COG2 encoding a subunit of the conserved oligomeric Golgi complex cause a congenital disorder of glycosylation. Clin. Genet. 87, 455-460.
40. Koles, K., Lim, J.-M., Aoki, K., Porterfield, M., Tiemeyer, M., Wells, L. and Panin, V. (2007). Identification of N-glycosylated proteins from the central nervous system of Drosophila melanogaster. Glycobiology 17, 1388-1403.
41. Kranz, C., Ng, B. G., Sun, L., Sharma, V., Eklund, E. A., Miura, Y., Ungar, D., Lupashin, V., Winkel, R. D., Cipollo, J. F. et al. (2007). COG8 deficiency causes new congenital disorder of glycosylation type IIh. Hum. Mol. Genet. 16, 731-741.
42. Lübbehusen, J., Thiel, C., Rind, N., Ungar, D., Prinsen, B. H., de Koning, T. J., van Hasselt, P. M. and Körner, C. (2010). Fatal outcome due to deficiency of subunit 6 of the conserved oligomeric Golgi complex leading to a new type of congenital disorders of glycosylation. Hum. Mol. Genet. 19, 3623-3633.
43. Mehta, N., Porterfield, M., Struwe, W. B., Heiss, C., Azadi, P., Rudd, P. M., Tiemeyer, M. and Aoki, K. (2016). Mass spectrometric quantification of N-linked glycans by reference to exogenous standards. J. Proteome. Res. 15, 2969-2980.
44. Miller, V. J. and Ungar, D. (2012). Re'COG'nition at the Golgi. Traffic 13, 891-897.
45. Miller, V. J., Sharma, P., Kudlyk, T. A., Frost, L., Rofe, A. P., Watson, I. J., Duden, R., Lowe, M., Lupashin, V. V. and Ungar, D. (2013). Molecular insights into vesicle tethering at the Golgi by the conserved oligomeric Golgi (COG) complex and the Golgin TATA element modulatory factor (TMF). J. Biol. Chem. 288, 4229-4240.
46. Morava, E., Zeevaert, R., Korsch, E., Huijben, K., Wopereis, S., Matthijs, G., Keymolen, K., Lefeber, D. J., De Meirleir, L. and Wevers, R. A. (2007). A common mutation in the COG7 gene with a consistent phenotype including microcephaly, adducted thumbs, growth retardation, VSD and episodes of hyperthermia. Eur. J. Hum. Genet. 156, 638-645.
47. Müller, D., Jagla, T., Bodart, L. M., Jährling, N., Dodt, H.-U., Jagla, K. and Frasch, M. (2010). Regulation and functions of the lms homeobox gene during development of embryonic lateral transverse muscles and direct flight muscles in Drosophila. PLoS ONE 5, e14323.
48. Ng, B. G., Kranz, C., Hagebeuk, E. E., Duran, M., Abeling, N. G., Wuyts, B., Ungar, D., Lupashin, V., Hartdorff, C. M., Poll-The, B. T. et al. (2007). Molecular and clinical characterization of a Moroccan Cog7 deficient patient. Mol. Genet. Metab. 91, 201-204.
49. Ohtsubo, K. and Marth, J. D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867.
50. Paesold-Burda, P., Maag, C., Troxler, H., Foulquier, F., Kleinert, P., Schnabel, S., Baumgartner, M. and Hennet, T. (2009). Deficiency in COG5 causes a moderate form of congenital disorders of glycosylation. Hum. Mol. Genet. 18, 4350-4356.
51. Parkinson, W., Dear, M. L., Rushton, E. and Broadie, K. (2013). N-glycosylation requirements in neuromuscular synaptogenesis. Development 140, 4970-4981.
52. Parkinson, W. M., Dookwah, M., Dear, M. L., Gatto, C. L., Aoki, K., Tiemeyer, M. and Broadie, K. (2016). Synaptic roles for phosphomannomutase type 2 in a new Drosophila congenital disorder of glycosylation disease model. Dis. Model. Mech. 9, 513-527.
53. Polevoy, G., Wei, H.-C., Wong, R., Szentpetery, Z., Kim, Y. J., Goldbach, P., Steinbach, S. K., Balla, T. and Brill, J. A. (2009). Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J. Cell Biol. 187, 847-858.
54. Repnikova, E., Koles, K., Nakamura, M., Pitts, J., Li, H., Ambavane, A., Zoran, M. J. and Panin, V. M. (2010). Sialyltransferase regulates nervous system function in Drosophila. J. Neurosci. 30, 6466-6476.
55. Reynders, E., Foulquier, F., Leão Teles, E., Quelhas, D., Morelle, W., Rabouille, C., Annaert, W. and Matthijs, G. (2009). Golgi function and dysfunction in the first COG4-deficient CDG type II patient. Hum. Mol. Genet. 18, 3244-3256.
56. Schmitz, K. R., Liu, J., Li, S., Setty, T. G., Wood, C. S., Burd, C. G. and Ferguson, K. M. (2008). Golgi localization of glycosyltransferases requires a Vps74p oligomer. Dev. Cell 14, 523-534.
57. Scott, H. and Panin, V. M. (2014). N-glycosylation in regulation of the nervous system. Adv. Neurobiol. 9, 367-394.
58. Sechi, S., Colotti, G., Belloni, G., Mattei, V., Frappaolo, A., Raffa, G. D., Fuller, M. T. and Giansanti, M. G. (2014). GOLPH3 is essential for contractile ring formation and Rab11 localization to the cleavage site during cytokinesis in Drosophila melanogaster. PLoS Genet. 10, e1004305.
59. Sechi, S., Frappaolo, A., Belloni, G. and Giansanti, M. G. (2015a). The roles of the oncoprotein GOLPH3 in contractile ring assembly and membrane trafficking during cytokinesis. Biochem. Soc. Trans. 43, 117-121.
60. Sechi, S., Frappaolo, A., Belloni, G., Colotti, G. and Giansanti, M. G. (2015b). The multiple cellular functions of the oncoprotein Golgi phosphoprotein 3. Oncotarget 6, 3493-3506.
61. Sechi, S., Frappaolo, A., Fraschini, R., Capalbo, L., Gottardo, M., Belloni, G., Glover, D. M., Wainman, A. and Giansanti, M. G. (2017). Rab1 interacts with GOLPH3 and controls Golgi structure and contractile ring constriction during cytokinesis in Drosophila melanogaster. Open Biol. 7, 160257.
62. Sisson, J. C., Field, C., Ventura, R., Royou, A. and Sullivan, W. (2000). Lava lamp, a novel peripheral Golgi protein, is required for Drosophila melanogaster cellularization. J. Cell Biol. 151, 905-918.
63. Smith, R. D. and Lupashin, V. V. (2008). Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr. Res. 343, 2024-2031.
64. Spaapen, L. J. M., Bakker, J. A., van der Meer, S. B., Sijstermans, H. J., Steet, R. A., Wevers, R. A. and Jaeken, J. (2005). Clinical and biochemical presentation of siblings with COG-7 deficiency, a lethal multiple O-and Nglycosylation disorder. J. Inherit. Metab. Dis. 28, 707-714.
65. Steet, R. and Kornfeld, S. (2006). COG-7-deficient human fibroblasts exhibit altered recycling of Golgi proteins. Mol. Biol. Cell 17, 2312-2321.
66. Struwe, W. B. and Reinhold, V. N. (2012). The conserved oligomeric Golgi complex is required for fucosylation of N-glycans in Caenorhabditis elegans. Glycobiology 22, 863-875.
67. Suvorova, E. S., Duden, R. and Lupashin, V. V. (2002). The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J. Cell Biol. 157, 631-643.
68. Thiel, C. and Körner, C. (2011). Mouse models for congenital disorders of glycosylation. J. Inherit. Metab. Dis. 34, 879-889.
69. Tu, L., Tai, W. C. S., Chen, L. and Banfield, D. K. (2008). Signal-mediated dynamic retention of glycosyltransferases in the Golgi. Science 321, 404-407.
70. Varki, A., Cummings, R. D., Aebi, M., Packer, N. H., Seeberger, P. H., Esko, J. D., Stanley, P., Hart, G., Darvill, A., Kinoshita T. et al. (2015). Symbol nomenclature for graphical representations of glycans. Glycobiology 25, 1323-1324.
71. Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., Buchner, S., Dabauvalle, M.-C., Schmidt, M., Qin, G. et al. (2006). Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833-844.
72. Wells, L. and Hart, G. W. (2013). Glycomics: building upon proteomics to advance glycosciences. Mol. Cell. Proteomics 12, 833-835.
73. Willett, R., Ungar, D. and Lupashin, V. (2013a). The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem. Cell Biol. 140, 271-283.
74. Willett, R., Kudlyk, T., Pokrovskaya, I., Schönherr, R., Ungar, D., Duden, R. and Lupashin, V. (2013b). COG complexes form spatial landmarks for distinct SNARE complexes. Nat. Commun. 4, 1553.
75. Wu, X., Steet, R. A., Bohorov, O., Bakker, J., Newell, J., Krieger, M., Spaapen, L., Kornfeld, S. and Freeze, H. H. (2004). Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nat. Med. 10, 518-523.
76. Xiang, Y., Zhang, X., Nix, D. B., Katoh, T., Aoki, K., Tiemeyer, M. and Wang, Y. (2013). Regulation of protein glycosylation and sorting by the Golgi matrix proteins GRASP55/65. Nat. Commun. 4, 1659.
77. York, W. S., Agravat, S., Aoki-Kinoshita, K. F., McBride, R., Campbell, M. P., Costello, C. E., Dell, A., Feizi, T., Haslam, S. M., Karlsson, N. et al. (2014). MIRAGE: the minimum information required for a glycomics experiment. Glycobiology 24, 402-406.
78. Zaffran, S., Astier, M., Gratecos, D. and Sémériva, M. (1997). The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development 124, 2087-2098.
79. Zeevaert, R., Foulquier, F., Cheillan, D., Cloix, I., Guffon, N., Sturiale, L., Garozzo, D., Matthijs, G. and Jaeken, J. (2009). A new mutation in COG7 extends the spectrum of COG subunit deficiencies. Eur. J. Med. Genet. 52, 303-305.
80. Zhang, J., Schulze, K. L., Hiesinger, P. R., Suyama, K., Wang, S., Fish, M., Acar, M., Hoskins, R. A., Bellen, H. J. and Scott, M. P. (2007). Thirty-one flavors of Drosophila rab proteins. Genetics 176, 1307-1322.