Mutations in Four Glycosyl Hydrolases Reveal a Highly Coordinated Pathway for Rhodopsin Biosynthesis and N-Glycan Trimming in Drosophila melanogaster

PLoS Genetics

Volumn 10, Issue 5, 2014, Pages

  Rosenbaum, Erica E ^a   Vasiljevic, Eva ^a   Brehm, Kimberley S ^a   Colley, Nansi Jo ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA MANNOSIDASE II; ALPHA MANNOSIDASE IIB; FUSED LOBE 1; GLYCAN; GLYCOSIDASE; HEXOSAMINIDASE 1; ISOENZYME; OLIGOSACCHARIDE; PHOTORECEPTOR RH1; RHODOPSIN; UNCLASSIFIED DRUG; VISUAL PIGMENT; HYDROLASE; POLYSACCHARIDE;

ALLELE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DEGLYCOSYLATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME RELEASE; HUMAN; IN VIVO STUDY; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; GLYCOSYLATION; METABOLISM; MUTATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DROSOPHILA MELANOGASTER; GLYCOSYLATION; HYDROLASES; MUTATION; POLYSACCHARIDES; RHODOPSIN;

EID: 84901610078     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004349     Document Type: Article

References (94)

1. Roth J, Zuber C, Park S, Jang I, Lee Y, et al. (2010) Protein N-glycosylation, protein folding, and protein quality control. Mol Cells 30: 497-506.
2. Katoh T, Tiemeyer M, (2013) The N's and O's of Drosophila glycoprotein glycobiology. Glycoconj J 30: 57-66.
3. Kornfeld R, Kornfeld S, (1985) Assembly of asparagine linked oligosaccharides. Annu Rev Biochem 54: 631-664.
4. Silberstein S, Gilmore R, (1996) Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase. FASEB J 10: 849-858.
5. Stanley P (2011) Golgi glycosylation. Cold Spring Harb Perspect Biol 3: pii: a005199. doi: 10.1101/cshperspect.a005199.
6. Caramelo JJ, Parodi AJ, (2007) How sugars convey information on protein conformation in the endoplasmic reticulum. Semin Cell Dev Biol 18: 732-742.
7. Kerscher S, Albert S, Wucherpfennig D, Heisenberg M, Schneuwly S, (1995) Molecular and genetic analysis of the Drosophila mas-1 (mannosidase-1) gene which encodes a glycoprotein processing alpha 1,2-mannosidase. Dev Biol 168: 613-626.
8. Parker GF, Williams PJ, Butters TD, Roberts DB, (1991) Detection of the lipid-linked precursor oligosaccharide of N-linked protein glycosylation in Drosophila melanogaster. FEBS Lett 290: 58-60.
9. Williams PJ, Wormald MR, Dwek RA, Rademacher TW, Parker GF, et al. (1991) Characterisation of oligosaccharides from Drosophila melanogaster glycoproteins. Biochim Biophys Acta 1075: 146-153.
10. Leonard R, Rendic D, Rabouille C, Wilson IB, Preat T, et al. (2006) The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J Biol Chem 281: 4867-4875.
11. Cao J, Li Y, Xia W, Reddig K, Hu W, et al. (2011) A Drosophila metallophosphoesterase mediates deglycosylation of rhodopsin. EMBO J 30: 3701-3713.
12. Englebienne P, Fiaux H, Kuntz DA, Corbeil CR, Gerber-Lemaire S, et al. (2007) Evaluation of docking programs for predicting binding of Golgi alpha-mannosidase II inhibitors: a comparison with crystallography. Proteins 69: 160-176.
13. Fiaux H, Kuntz DA, Hoffman D, Janzer RC, Gerber-Lemaire S, et al. (2008) Functionalized pyrrolidine inhibitors of human type II alpha-mannosidases as anti-cancer agents: optimizing the fit to the active site. Bioorg Med Chem 16: 7337-7346.
14. Kawatkar SP, Kuntz DA, Woods RJ, Rose DR, Boons GJ, (2006) Structural basis of the inhibition of Golgi alpha-mannosidase II by mannostatin A and the role of the thiomethyl moiety in ligand-protein interactions. J Am Chem Soc 128: 8310-8319.
15. Kuntz DA, Zhong W, Guo J, Rose DR, Boons GJ, (2009) The molecular basis of inhibition of Golgi alpha-mannosidase II by mannostatin A. Chembiochem 10: 268-277.
16. Kuntz DA, Nakayama S, Shea K, Hori H, Uto Y, et al. (2010) Structural investigation of the binding of 5-substituted swainsonine analogues to Golgi alpha-mannosidase II. Chembiochem 11: 673-680.
17. Numao S, Kuntz DA, Withers SG, Rose DR, (2003) Insights into the mechanism of Drosophila melanogaster Golgi alpha-mannosidase II through the structural analysis of covalent reaction intermediates. J Biol Chem 278: 48074-48083.
18. Polakova M, Sestak S, Lattova E, Petrus L, Mucha J, et al. (2011) alpha-D-mannose derivatives as models designed for selective inhibition of Golgi alpha-mannosidase II. Eur J Med Chem 46: 944-952.
19. Shah N, Kuntz DA, Rose DR, (2003) Comparison of kifunensine and 1-deoxymannojirimycin binding to class I and II alpha-mannosidases demonstrates different saccharide distortions in inverting and retaining catalytic mechanisms. Biochemistry 42: 13812-13816.
20. Shah N, Kuntz DA, Rose DR, (2008) Golgi alpha-mannosidase II cleaves two sugars sequentially in the same catalytic site. Proc Natl Acad Sci U S A 105: 9570-9575.
21. van den Elsen JM, Kuntz DA, Rose DR, (2001) Structure of Golgi alpha-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J 20: 3008-3017.
22. Zhong W, Kuntz DA, Ember B, Singh H, Moremen KW, et al. (2008) Probing the substrate specificity of Golgi alpha-mannosidase II by use of synthetic oligosaccharides and a catalytic nucleophile mutant. J Am Chem Soc 130: 8975-8983.
23. Jaeken J, Matthijs G, (2007) Congenital disorders of glycosylation: a rapidly expanding disease family. Annu Rev Genomics Hum Genet 8: 261-278.
24. Grunewald S, Matthijs G, (2000) Congenital disorders of glycosylation (CDG): a rapidly expanding group of neurometabolic disorders. Neuropediatrics 31: 57-59.
25. Kahook MY, Mandava N, Bateman JB, Thomas JA, (2006) Glycosylation type Ic disorder: idiopathic intracranial hypertension and retinal degeneration. Br J Ophthalmol 90: 115-116.
26. Morava E, Wosik HN, Sykut-Cegielska J, Adamowicz M, Guillard M, et al. (2009) Ophthalmological abnormalities in children with congenital disorders of glycosylation type I. Br J Ophthalmol 93: 350-354.
27. Bedilu R, Nummy KA, Cooper A, Wevers R, Smeitink J, et al. (2002) Variable clinical presentation of lysosomal beta-mannosidosis in patients with null mutations. Mol Genet Metab 77: 282-290.
28. Malm D, Nilssen O, (2008) Alpha-mannosidosis. Orphanet J Rare Dis 3: 21.
29. Kleijer WJ, Hu P, Thoomes R, Boer M, Huijmans JG, et al. (1990) Beta-mannosidase deficiency: heterogeneous manifestation in the first female patient and her brother. J Inherit Metab Dis 13: 867-872.
30. Huynh T, Khan JM, Ranganathan S, (2011) A comparative structural bioinformatics analysis of inherited mutations in beta-D-Mannosidase across multiple species reveals a genotype-phenotype correlation. BMC Genomics 12 (Suppl 3):: S22.
31. Samra ZQ, Athar MA, (2008) Cloning, sequence, expression and characterization of human beta-mannosidase. Acta Biochim Pol 55: 479-490.
32. Mahuran DJ, (1999) Biochemical consequences of mutations causing the GM2 gangliosidoses. Biochim Biophys Acta 1455: 105-138.
33. Patnaik SK, Stanley P, (2006) Lectin-resistant CHO glycosylation mutants. Methods Enzymol 416: 159-182.
34. Elbein AD, (1991) Glycosidase inhibitors as antiviral and/or antitumor agents. Semin Cell Biol 2: 309-317.
35. Moremen KW, (2002) Golgi alpha-mannosidase II deficiency in vertebrate systems: implications for asparagine-linked oligosaccharide processing in mammals. Biochim Biophys Acta 1573: 225-235.
36. de Couet HG, Tanimura T, (1987) Monoclonal antibodies provide evidence that rhodopsin in the outer rhabdomeres of Drosophila melanogaster is not glycosylated. Eur J Cell Biol 44: 50-56.
37. Huber A, Smith DP, Zuker CS, Paulsen R, (1990) Opsin of Calliphora peripheral photoreceptors R1-6. Homology with Drosophila Rh1 and posttranslational processing. J Biol Chem 265: 17906-17910.
38. Webel R, Menon I, O'Tousa J, Colley NJ, (2000) Role of asparagine-linked glycosylation sites in Rhodopsin maturation and association with its molecular chaperone, NinaA. J Biol Chem 275: 24752-24759.
39. Colley NJ, Baker EK, Stamnes MA, Zuker CS, (1991) The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67: 255-263.
40. Colley NJ, Cassill JA, Baker EK, Zuker CS, (1995) Defective intracellular transport is the molecular basis of rhodopsin-dependent dominant retinal degeneration. Proc Natl Acad Sci U S A 92: 3070-3074.
41. Koundakjian EJ, Cowan DM, Hardy RW, Becker AH, (2004) The Zuker collection: a resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167: 203-206.
42. Schneuwly S, Shortridge RD, Larrivee DC, Ono T, Ozaki M, et al. (1989) Drosophila ninaA gene encodes an eye-specific cyclophilin (cyclosporin A binding protein). Proc Natl Acad Sci U S A 86: 5390-5394.
43. Shieh BH, Stamnes MA, Seavello S, Harris GL, Zuker CS, (1989) The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporin A-binding protein. Nature 338: 67-70.
44. Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS, (1991) The cyclophilin homolog NinaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell 65: 219-227.
45. Baker EK, Colley NJ, Zuker CS, (1994) The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J 13: 4886-4895.
46. Nemcovicova I, Sestak S, Rendic D, Plskova M, Mucha J, et al. (2013) Characterisation of class I and II alpha-mannosidases from Drosophila melanogaster. Glycoconj J 30: 899-909.
47. Cattaneo F, Pasini ME, Intra J, Matsumoto M, Briani F, et al. (2006) Identification and expression analysis of Drosophila melanogaster genes encoding beta-hexosaminidases of the sperm plasma membrane. Glycobiology 16: 786-800.
48. Herscovics A, (1999) Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim Biophys Acta 1473: 96-107.
49. Herscovics A, (2001) Structure and function of Class I alpha 1,2-mannosidases involved in glycoprotein synthesis and endoplasmic reticulum quality control. Biochimie 83: 757-762.
50. Mast SW, Moremen KW, (2006) Family 47 alpha-mannosidases in N-glycan processing. Methods Enzymol 415: 31-46.
51. Harpaz N, Schachter H, (1980) Control of glycoprotein synthesis. Processing of asparagine-linked oligosaccharides by one or more rat liver Golgi alpha-D-mannosidases dependent on the prior action of UDP-N-acetylglucosamine: alpha-D-mannoside beta 2-N-acetylglucosaminyltransferase I. J Biol Chem 255: 4894-4902.
52. Schachter H, Chen SH, Zhou S, Tan J, Yip B, et al. (1997) Structure and function of the genes encoding N-acetylglucosaminyltransferases which initiate N-glycan antennae. Biochem Soc Trans 25: 875-880.
53. Schachter H, (1991) The 'yellow brick road' to branched complex N-glycans. Glycobiology 1: 453-461.
54. Howard S, Braun C, McCarter J, Moremen KW, Liao YF, et al. (1997) Human lysosomal and jack bean alpha-mannosidases are retaining glycosidases. Biochem Biophys Res Commun 238: 896-898.
55. Maley F, Trimble RB, Tarentino AL, Plummer TH Jr, (1989) Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 180: 195-204.
56. Akama TO, Nakagawa H, Wong NK, Sutton-Smith M, Dell A, et al. (2006) Essential and mutually compensatory roles of alpha-mannosidase II and alpha-mannosidase IIx in N-glycan processing in vivo in mice. Proc Natl Acad Sci U S A 103: 8983-8988.
57. Moremen KW, Robbins PW, (1991) Isolation, characterization, and expression of cDNAs encoding murine alpha-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans. J Cell Biol 115: 1521-1534.
58. Misago M, Liao YF, Kudo S, Eto S, Mattei MG, et al. (1995) Molecular cloning and expression of cDNAs encoding human alpha-mannosidase II and a previously unrecognized alpha-mannosidase IIx isozyme. Proc Natl Acad Sci U S A 92: 11766-11770.
59. Fukuda MN, Masri KA, Dell A, Luzzatto L, Moremen KW, (1990) Incomplete synthesis of N-glycans in congenital dyserythropoietic anemia type II caused by a defect in the gene encoding alpha-mannosidase II. Proc Natl Acad Sci U S A 87: 7443-7447.
60. Stowers RS, Schwarz TL, (1999) A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152: 1631-1639.
61. Hsiao HY, Jukam D, Johnston R, Desplan C, (2013) The neuronal transcription factor erect wing regulates specification and maintenance of Drosophila R8 photoreceptor subtypes. Dev Biol 381: 482-490.
62. Maccioni HJ, (2007) Glycosylation of glycolipids in the Golgi complex. J Neurochem 103 (Suppl 1):: 81-90.
63. Varki A, (1998) Factors controlling the glycosylation potential of the Golgi apparatus. Trends Cell Biol 8: 34-40.
64. Altmann F, Schwihla H, Staudacher E, Glossl J, Marz L, (1995) Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J Biol Chem 270: 17344-17349.
65. Boquet I, Hitier R, Dumas M, Chaminade M, Preat T, (2000) Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. J Neurobiol 42: 33-48.
66. Liao YF, Lal A, Moremen KW, (1996) Cloning, expression, purification, and characterization of the human broad specificity lysosomal acid alpha-mannosidase. J Biol Chem 271: 28348-28358.
67. Merkle RK, Zhang Y, Ruest PJ, Lal A, Liao YF, et al. (1997) Cloning, expression, purification, and characterization of the murine lysosomal acid alpha-mannosidase. Biochim Biophys Acta 1336: 132-146.
68. Wakamatsu N, Gotoda Y, Saito S, Kawai H, (1997) Characterization of the human MANB gene encoding lysosomal alpha-D-mannosidase. Gene 198: 351-357.
69. Daniel PF, Evans JE, De Gasperi R, Winchester B, Warren CD, (1992) A human lysosomal alpha(1→6)-mannosidase active on the branched trimannosyl core of complex glycans. Glycobiology 2: 327-336.
70. De Gasperi R, Daniel PF, Warren CD, (1992) A human lysosomal alpha-mannosidase specific for the core of complex glycans. J Biol Chem 267: 9706-9712.
71. Park C, Meng L, Stanton LH, Collins RE, Mast SW, et al. (2005) Characterization of a human core-specific lysosomal alpha 1,6-mannosidase involved in N-glycan catabolism. J Biol Chem 280: 37204-37216.
72. Alkhayat AH, Kraemer SA, Leipprandt JR, Macek M, Kleijer WJ, et al. (1998) Human beta-mannosidase cDNA characterization and first identification of a mutation associated with human beta-mannosidosis. Hum Mol Genet 7: 75-83.
73. Winchester B, (2005) Lysosomal metabolism of glycoproteins. Glycobiology 15: 1R-15R.
74. Robinson D, Stirling JL, (1968) N-Acetyl-beta-glucosaminidases in human spleen. Biochem J 107: 321-327.
75. Myerowitz R, Proia RL, (1984) cDNA clone for the alpha-chain of human beta-hexosaminidase: deficiency of alpha-chain mRNA in Ashkenazi Tay-Sachs fibroblasts. Proc Natl Acad Sci U S A 81: 5394-5398.
76. O'Dowd BF, Quan F, Willard HF, Lamhonwah AM, Korneluk RG, et al. (1985) Isolation of cDNA clones coding for the beta subunit of human beta-hexosaminidase. Proc Natl Acad Sci U S A 82: 1184-1188.
77. Tulsiani DR, Abou-Haila A, (2001) Mammalian sperm molecules that are potentially important in interaction with female genital tract and egg vestments. Zygote 9: 51-69.
78. Cattaneo F, Ogiso M, Hoshi M, Perotti ME, Pasini ME, (2002) Purification and characterization of the plasma membrane glycosidases of Drosophila melanogaster spermatozoa. Insect Biochem Mol Biol 32: 929-941.
79. Miller DJ, Gong X, Shur BD, (1993) Sperm require beta-N-acetylglucosaminidase to penetrate through the egg zona pellucida. Development 118: 1279-1289.
80. Mencarelli S, Cavalieri C, Magini A, Tancini B, Basso L, et al. (2005) Identification of plasma membrane associated mature beta-hexosaminidase A, active towards GM2 ganglioside, in human fibroblasts. FEBS Lett 579: 5501-5506.
81. Harrison RL, Jarvis DL, (2006) Protein N-glycosylation in the baculovirus-insect cell expression system and engineering of insect cells to produce "mammalianized" recombinant glycoproteins. Adv Virus Res 68: 159-191.
82. Tomiya N, Betenbaugh MJ, Lee YC, (2003) Humanization of lepidopteran insect-cell-produced glycoproteins. Acc Chem Res 36: 613-620.
83. Geisler C, Aumiller JJ, Jarvis DL, (2008) A fused lobes gene encodes the processing beta-N-acetylglucosaminidase in Sf9 cells. J Biol Chem 283: 11330-11339.
84. Kim JH, Lingwood CA, Williams DB, Furuya W, Manolson MF, et al. (1996) Dynamic measurement of the pH of the Golgi complex in living cells using retrograde transport of the verotoxin receptor. J Cell Biol 134: 1387-1399.
85. O'Tousa JE, (1992) Requirement of N-linked glycosylation site in Drosophila rhodopsin. Visual Neuroscience 8: 385-390.
86. Brown G, Chen DM, Christianson JS, Lee R, Stark WS, (1994) Receptor demise from alteration of glycosylation site in Drosophila opsin: electrophysiology, microspectrophotometry, and electron microscopy. Visual Neuroscience 11: 619-628.
87. Katanosaka K, Tokunaga F, Kawamura S, Ozaki K, (1998) N-Linked glycosylation of Drosophila rhodopsin occurs exclusively in the amino-terminal domain and functions in rhodopsin maturation. FEBS 424: 149-154.
88. Li ZY, Jacobson SG, Milam AH, (1994) Autosomal dominant retinitis pigmentosa caused by the threonine-17-methionine rhodopsin mutation: retinal histopathology and immunocytochemistry. Experimental Eye Research 58: 397-408.
89. Daiger SP, Sullivan LS, Rodriguez JA, (1995) Correlation of phenotype with genotype in inherited retinal degeneration. Behavioral and Brain Sciences 18: 452-467.
90. Papermaster DS, Windle J, (1995) Death at an early age. Apoptosis in inherited retinal degenerations. Investigative Ophthalmology & Visual Science 36: 977-983.
91. Rosenbaum EE, Brehm KS, Vasiljevic E, Gajeski A, Colley NJ, (2012) Drosophila GPI-mannosyltransferase 2 is required for GPI anchor attachment and surface expression of chaoptin. Vis Neurosci 29: 143-156.
92. Rosenbaum EE, Brehm KS, Vasiljevic E, Liu CH, Hardie RC, et al. (2011) XPORT-dependent transport of TRP and rhodopsin. Neuron 72: 602-615.
93. Rosenbaum EE, Hardie RC, Colley NJ, (2006) Calnexin is essential for rhodopsin maturation, Ca2+ regulation, and photoreceptor cell survival. Neuron 49: 229-241.
94. Laemmli UK, (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-685.