Deconstruction of O-glycosylation - GalNAc-T isoforms direct distinct subsets of the O-glycoproteome

EMBO Reports

Volumn 16, Issue 12, 2015, Pages 1713-1722

  Schjoldager, Katrine T ^a   Joshi, Hiren J ^a   Kong, Yun ^a   Goth, Christoffer K ^a   King, Sarah Louise ^a   Wandall, Hans H ^a   Bennett, Eric P ^a   Vakhrushev, Sergey Y ^a   Clausen, Henrik ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

apolipoproteins; dimethylation; GALNT; mass spectrometry

Indexed keywords

GLYCOPROTEIN; ISOENZYME; POLYPEPTIDE GALNAC TRANSFERASE; POLYPEPTIDE GALNAC TRANSFERASE 1; POLYPEPTIDE GALNAC TRANSFERASE 2; TRANSFERASE; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; DEOXYRIBONUCLEASE; N ACETYLGALACTOSAMINYLTRANSFERASE; POLYPEPTIDE N-ACETYLGALACTOSAMINYLTRANSFERASE; ZINC FINGER PROTEIN;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LIPID METABOLISM; LIVER CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; AMINO ACID SEQUENCE; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GLYCOSYLATION; HEP-G2 CELL LINE; METABOLISM;

AMINO ACID SEQUENCE; ENDODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOPROTEINS; GLYCOSYLATION; HEP G2 CELLS; HUMANS; ISOENZYMES; LIPID METABOLISM; N-ACETYLGALACTOSAMINYLTRANSFERASES; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC; ZINC FINGERS;

EID: 84954205144     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540796     Document Type: Article

References (57)

1. Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA, (2012) Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22: 736-756
2. Gill DJ, Clausen H, Bard F, (2011) Location, location, location: new insights into O-GalNAc protein glycosylation. Trends Cell Biol 21: 149-158
3. Tran DT, Ten Hagen KG, (2013) Mucin-type O-glycosylation during development. J Biol Chem 288: 6921-6929
4. Schjoldager KT, Vakhrushev SY, Kong Y, Steentoft C, Nudelman AS, Pedersen NB, Wandall HH, Mandel U, Bennett EP, Levery SB, et al, (2012) Probing isoform-specific functions of polypeptide GalNAc-transferases using zinc finger nuclease glycoengineered SimpleCells. Proc Natl Acad Sci USA 109: 9893-9898
5. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S, (2002) The protein kinase complement of the human genome. Science 298: 1912-1934
6. Tabak LA, (2010) The role of mucin-type O-glycans in eukaryotic development. Sem Cell Dev Biol 21: 616-621
7. Topaz O, Shurman DL, Bergman R, Indelman M, Ratajczak P, Mizrachi M, Khamaysi Z, Behar D, Petronius D, Friedman V, et al, (2004) Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat Genet 36: 579-581
8. Kato K, Jeanneau C, Tarp MA, Benet-Pages A, Lorenz-Depiereux B, Bennett EP, Mandel U, Strom TM, Clausen H, (2006) Polypeptide GalNAc-transferase T3 and familial tumoral calcinosis. Secretion of fibroblast growth factor 23 requires O-glycosylation. J Biol Chem 281: 18370-18377
9. Benet-Pages A, Orlik P, Strom TM, Lorenz-Depiereux B, (2005) An FGF23 missense mutation causes familial tumoral calcinosis with hyperphosphatemia. Hum Mol Genet 14: 385-390
10. Esapa CT, Head RA, Jeyabalan J, Evans H, Hough TA, Cheeseman MT, McNally EG, Carr AJ, Thomas GP, Brown MA, et al, (2012) A mouse with an N-Ethyl-N-nitrosourea (ENU) Induced Trp589Arg Galnt3 mutation represents a model for hyperphosphataemic familial tumoural calcinosis. PLoS ONE 7: e43205
11. Ichikawa S, Sorenson AH, Austin AM, Mackenzie DS, Fritz TA, Moh A, Hui SL, Econs MJ, (2009) Ablation of the Galnt3 gene leads to low-circulating intact fibroblast growth factor 23 (Fgf23) concentrations and hyperphosphatemia despite increased Fgf23 expression. Endocrinology 150: 2543-2550
12. Duncan EL, Danoy P, Kemp JP, Leo PJ, McCloskey E, Nicholson GC, Eastell R, Prince RL, Eisman JA, Jones G, et al, (2011) Genome-wide association study using extreme truncate selection identifies novel genes affecting bone mineral density and fracture risk. PLoS Genet 7: e1001372
13. Leonhard-Melief C, Haltiwanger RS, (2010) O-fucosylation' of thrombospondin type 1 repeats. Methods Enzymol 480: 401-416
14. Loibl M, Strahl S, (2013) Protein O-mannosylation: what we have learned from baker's yeast. Biochim Biophys Acta 1833: 2438-2446
15. Boskovski MT, Yuan S, Pedersen NB, Goth CK, Makova S, Clausen H, Brueckner M, Khokha MK, (2013) The heterotaxy gene GALNT11 glycosylates Notch to orchestrate cilia type and laterality. Nature 504: 456-459
16. van der Post S, Subramani DB, Backstrom M, Johansson ME, Vester-Christensen MB, Mandel U, Bennett EP, Clausen H, Dahlen G, Sroka A, et al, (2013) Site-specific O-glycosylation on the MUC2 mucin protein inhibits cleavage by the Porphyromonas gingivalis secreted cysteine protease (RgpB). J Biol Chem 288: 14636-14646
17. Zhang L, Syed ZA, van Dijk Hard I, Lim JM, Wells L, Ten Hagen KG, (2014) O-glycosylation regulates polarized secretion by modulating Tango1 stability. Proc Natl Acad Sci USA 111: 7296-7301
18. Schjoldager KT, Clausen H, (2012) Site-specific protein O-glycosylation modulates proprotein processing-deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochim Biophys Acta 1820: 2079-2094
19. Steentoft C, Vakhrushev SY, Vester-Christensen MB, Schjoldager KT, Kong Y, Bennett EP, Mandel U, Wandall H, Levery SB, Clausen H, (2011) Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nat Methods 8: 977-982
20. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT, Lavrsen K, Dabelsteen S, Pedersen NB, Marcos-Silva L, et al, (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J 32: 1478-1488
21. Tenno M, Ohtsubo K, Hagen FK, Ditto D, Zarbock A, Schaerli P, von Andrian UH, Ley K, Le D, Tabak LA, et al, (2007) Initiation of protein O glycosylation by the polypeptide GalNAcT-1 in vascular biology and humoral immunity. Mol Cell Biol 27: 8783-8796
22. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, Clarke R, Heath SC, Timpson NJ, Najjar SS, Stringham HM, et al, (2008) Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat Genet 40: 161-169
23. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, Rieder MJ, Cooper GM, Roos C, Voight BF, Havulinna AS, et al, (2008) Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat Genet 40: 189-197
24. Hozumi Y, Kawano M, Jordan VC, (2000) In vitro study of the effect of raloxifene on lipid metabolism compared with tamoxifen. Eur J Endocrinol 143: 427-430
25. Vallianou I, Peroulis N, Pantazis P, Hadzopoulou-Cladaras M, (2011) Camphene, a plant-derived monoterpene, reduces plasma cholesterol and triglycerides in hyperlipidemic rats independently of HMG-CoA reductase activity. PLoS ONE 6: e20516
26. Sutherlin ME, Nishimori I, Caffrey T, Bennett EP, Hassan H, Mandel U, Mack D, Iwamura T, Clausen H, Hollingsworth MA, (1997) Expression of three UDP-N-acetyl-alpha-D-galactosamine:polypeptide GalNAc N-acetylgalactosaminyltransferases in adenocarcinoma cell lines. Cancer Res 57: 4744-4748
27. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ, (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494
28. Vakhrushev SY, Steentoft C, Vester-Christensen MB, Bennett EP, Clausen H, Levery SB, (2013) Enhanced mass spectrometric mapping of the human GalNAc-type O-glycoproteome with SimpleCells. Mol Cell Proteomics 12: 932-944
29. Yang Z, Halim A, Narimatsu Y, Joshi HJ, Steentoft C, Schjoldager KT, Schulz MA, Sealover NR, Kayser KJ, Bennett EP, et al, (2014) The GalNAc-type O-glycoproteome of CHO cells characterized by the SimpleCell strategy. Mol Cell Proteomics 12: 3224-3235
30. Kong Y, Joshi HJ, Schjoldager KT, Madsen TD, Gerken TA, Vester-Christensen MB, Wandall HH, Bennett EP, Levery SB, Vakhrushev SY, et al, (2015) Probing Polypeptide GalNAc-Transferase Isoform Substrate Specificities by In Vitro Analysis. Glycobiology 25: 55-65
31. Gerken TA, Raman J, Fritz TA, Jamison O, (2006) Identification of common and unique peptide substrate preferences for the UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferases T1 and T2 derived from oriented random peptide substrates. J Biol Chem 281: 32403-32416
32. Tian E, Hoffman MP, Ten Hagen KG, (2012) O-glycosylation modulates integrin and FGF signalling by influencing the secretion of basement membrane components. Nat Commun 3: 869
33. Tian E, Stevens SR, Guan Y, Springer DA, Anderson SA, Starost MF, Patel V, Ten Hagen KG, Tabak LA, (2015) Galnt1 is required for normal heart valve development and cardiac function. PLoS ONE 10: e0115861
34. Miwa HE, Gerken TA, Jamison O, Tabak LA, (2010) Isoform-specific O-glycosylation of osteopontin and bone sialoprotein by polypeptide N-acetylgalactosaminyltransferase-1. J Biol Chem 285: 1208-1219
35. Wang ZQ, Bachvarova M, Morin C, Plante M, Gregoire J, Renaud MC, Sebastianelli A, Bachvarov D, (2014) Role of the polypeptide N-acetylgalactosaminyltransferase 3 in ovarian cancer progression: possible implications in abnormal mucin O-glycosylation. Oncotarget 5: 544-560
36. Taniuchi K, Cerny RL, Tanouchi A, Kohno K, Kotani N, Honke K, Saibara T, Hollingsworth MA, (2011) Overexpression of GalNAc-transferase GalNAc-T3 promotes pancreatic cancer cell growth. Oncogene 30: 4843-4854
37. Kato K, Takeuchi H, Kanoh A, Miyahara N, Nemoto-Sasaki Y, Morimoto-Tomita M, Matsubara A, Ohashi Y, Waki M, Usami K, et al, (2010) Loss of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase 3 and reduced O-glycosylation in colon carcinoma cells selected for hepatic metastasis. Glycoconj J 27: 267-276
38. Pedersen NB, Wang S, Narimatsu Y, Yang Z, Halim A, Schjoldager KT, Madsen TD, Seidah NG, Bennett EP, Levery SB, et al, (2014) Low density lipoprotein receptor class a repeats are o-glycosylated in linker regions. J Biol Chem 289: 17312-17324
39. Hansen L, Lind-Thomsen A, Joshi HJ, Pedersen NB, Have CT, Kong Y, Wang S, Sparso T, Grarup N, Vester-Christensen MB, et al, (2015) A glycogene mutation map for discovery of diseases of glycosylation. Glycobiology 25: 211-224
40. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD, (2013) Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat Protoc 8: 1765-1786
41. Itoh Y, (2015) Membrane-type matrix metalloproteinases: their functions and regulations. Matrix Biol 44-46C: 207-223
42. Buache E, Thai R, Wendling C, Alpy F, Page A, Chenard MP, Dive V, Ruff M, Dejaegere A, Tomasetto C, et al, (2014) Functional relationship between matrix metalloproteinase-11 and matrix metalloproteinase-14. Cancer Med 3: 1197-1210
43. Rouyer N, Wolf C, Chenard MP, Rio MC, Chambon P, Bellocq JP, Basset P, (1994) Stromelysin-3 gene expression in human cancer: an overview. Invasion Metastasis 14: 269-275
44. Anderson IC, Sugarbaker DJ, Ganju RK, Tsarwhas DG, Richards WG, Sunday M, Kobzik L, Shipp MA, (1995) Stromelysin-3 is overexpressed by stromal elements in primary non-small cell lung cancers and regulated by retinoic acid in pulmonary fibroblasts. Cancer Res 55: 4120-4126
45. Porte H, Chastre E, Prevot S, Nordlinger B, Empereur S, Basset P, Chambon P, Gespach C, (1995) Neoplastic progression of human colorectal cancer is associated with overexpression of the stromelysin-3 and BM-40/SPARC genes. Int J Cancer 64: 70-75
46. Bennett EP, Hassan H, Mandel U, Hollingsworth MA, Akisawa N, Ikematsu Y, Merkx G, van Kessel AG, Olofsson S, Clausen H, (1999) Cloning and characterization of a close homologue of human UDP-N-acetyl-alpha-D-galactosamine: Polypeptide N-acetylgalactosaminyltransferase-T3, designated GalNAc-T6. Evidence for genetic but not functional redundancy. J Biol Chem 274: 25362-25370
47. Li Z, Yamada S, Inenaga S, Imamura T, Wu Y, Wang KY, Shimajiri S, Nakano R, Izumi H, Kohno K, et al, (2011) Polypeptide N-acetylgalactosaminyltransferase 6 expression in pancreatic cancer is an independent prognostic factor indicating better overall survival. Br J Cancer 104: 1882-1889
48. Freire-de-Lima L, Gelfenbeyn K, Ding Y, Mandel U, Clausen H, Handa K, Hakomori SI, (2011) Involvement of O-glycosylation defining oncofetal fibronectin in epithelial-mesenchymal transition process. Proc Natl Acad Sci USA 108: 17690-17695
49. Erbilgin A, Civelek M, Romanoski CE, Pan C, Hagopian R, Berliner JA, Lusis AJ, (2013) Identification of CAD candidate genes in GWAS loci and their expression in vascular cells. J Lipid Res 54: 1894-1905
50. Beecham GW, Hamilton K, Naj AC, Martin ER, Huentelman M, Myers AJ, Corneveaux JJ, Hardy J, Vonsattel JP, Younkin SG, et al, (2014) Genome-wide association meta-analysis of neuropathologic features of Alzheimer's disease and related dementias. PLoS Genet 10: e1004606
51. Ng MC, Hester JM, Wing MR, Li J, Xu J, Hicks PJ, Roh BH, Lu L, Divers J, Langefeld CD, et al, (2012) Genome-wide association of BMI in African Americans. Obesity 20: 622-627
52. Desai AA, Zhou T, Ahmad H, Zhang W, Mu W, Trevino S, Wade MS, Raghavachari N, Kato GJ, Peters-Lawrence MH, et al, (2012) A novel molecular signature for elevated tricuspid regurgitation velocity in sickle cell disease. Am J Respir Crit Care Med 186: 359-368
53. Yeh CT, Liang KH, Lin CC, Chang ML, Hsu CL, Hung CF, (2014) A single nucleotide polymorphism on the GALNT14 gene as an effective predictor of response to chemotherapy in advanced hepatocellular carcinoma. Int J Cancer 134: 1214-1224
54. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106
55. McCarthy DJ, Chen Y, Smyth GK, (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40: 4288-4297
56. Falcon S, Gentleman R, (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258
57. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, Dianes JA, Sun Z, Farrah T, Bandeira N, et al, (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32: 223-226