Golgi N-glycan branching N-acetylglucosaminyltransferases I, v and VI promote nutrient uptake and metabolism

Glycobiology

Volumn 25, Issue 2, 2015, Pages 225-240

  Abdel Rahman, Anas M ^a,f   Ryczko, Michael ^a,b   Nakano, Miyako ^d,e   Pawling, Judy ^a   Rodrigues, Tania ^a,b   Johswich, Anita ^a   Taniguchi, Naoyuki ^d   Dennis, James W ^a,b,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b Department of Molecular Genetics ^*  (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d RIKEN   (Japan)

^e HIROSHIMA UNIVERSITY   (Japan)

^f KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

Author keywords

Golgi N glycan branching; hexosamine biosynthetic pathway; metabolism; N acetylglucosaminyltransferase enzymes; nutrient uptake

Indexed keywords

GLUCOSE; GLUTAMINE; GLYCAN; HEXOSAMINE; LACTIC ACID; N ACETYLGLUCOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE 1; N ACETYLGLUCOSAMINYLTRANSFERASE 5; N ACETYLGLUCOSAMINYLTRANSFERASE 6; PROTEIN; TETRACYCLINE; UNCLASSIFIED DRUG; AMINO ACID; AVIAN PROTEIN; MGAT1 PROTEIN, HUMAN; MGAT5 PROTEIN, HUMAN;

AEROBIC METABOLISM; AMINO ACID TRANSPORT; ARTICLE; BIOSYNTHESIS; CATABOLISM; CATION EXCHANGE; CELL GROWTH; CELL PROLIFERATION; CELL SURFACE; CELL VIABILITY; CITRIC ACID CYCLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EMBRYO; ENZYME ACTIVITY; FEMALE; GLYCOLYSIS; GOLGI COMPLEX; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; HYPOTHESIS; KIDNEY CELL; MAMMAL CELL; METABOLISM; NUTRIENT UPTAKE; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; UPREGULATION; WESTERN BLOTTING; ANIMAL; CHICKEN; CONFORMATION; GLYCOSYLATION; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACIDS; ANIMALS; AVIAN PROTEINS; BIOLOGICAL TRANSPORT; BIOSYNTHETIC PATHWAYS; CARBOHYDRATE CONFORMATION; CELL PROLIFERATION; CHICKENS; GLYCOLYSIS; GLYCOSYLATION; HEK293 CELLS; HELA CELLS; HEXOSAMINES; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES;

EID: 84941137578     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu105     Document Type: Article

References (49)

1. Abdel Rahman AM, Ryczko M, Pawling J, Dennis JW. 2013. Probing the hexosamine biosynthetic pathway in human tumor cells by multitargeted tandem mass spectrometry. ACS Chem Biol. 8:2053-2062.
2. Abdel Rahman AM, Pawling J, Ryczko M, Dennis JW. 2014. Targeted metabolomics in cultured cells and tissues by mass spectrometry: Method development and validation. Anal Chim Acta. 845:53-61.
3. Beheshti Zavareh R, Sukhai MA, Hurren R, Gronda M, Wang X, Simpson CD, Maclean N, Zih F, Ketela T, Swallow CJ, et al. 2012. Suppression of cancer progression by MGAT1 shRNA knockdown. PLoS ONE. 7:e43721.
4. Buckhaults P, Chen L, Fregien N, Pierce M. 1997. Transcriptional regulation of N-acetylglucosaminyltransferase V by the src Oncogene. J Biol Chem. 272:19575-19581.
5. Cheung P, Dennis JW. 2007. Mgat5 and Pten interact to regulate cell growth and polarity. Glycobiology. 17:767-773.
6. Cheung P, Pawling J, Partridge EA, Sukhu B, GrynpasM, Dennis JW. 2007. Metabolic homeostasis and tissue renewal are dependent on beta1, 6GlcNAcbranched N-glycans. Glycobiology. 17:828-837.
7. D'Arrigo A, Belluco C, Ambrosi A, Digito M, Esposito G, Bertola A, Fabris M, Nofrate V, Mammano E, Leon A, et al. 2005. Metastatic transcriptional pattern revealed by gene expression profiling in primary colorectal carcinoma. Int J Cancer. 115:256-262.
8. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. 2008. The biology of cancer: Metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7:11-20.
9. Demetriou M, Nabi IR, Coppolino M, Dedhar S, Dennis JW. 1995. Reduced contact-inhibition and substratum adhesion in epithelial cells expressing GlcNAc-transferase V. J Cell Biol. 130:383-392.
10. Dennis JW, Brewer CF. 2013. Density-dependent lectin-glycan interactions as a paradigm for conditional regulation by posttranslational modifications. Mol Cell Proteomics. 12:913-920.
11. Dennis JW, Kosh K, Bryce D-M, Breitman ML. 1989. Oncogenes conferring metastatic potential induce increased branching of Asn-linked oligosaccharides in rat2 fibroblasts. Oncogene. 4:853-860.
12. Fernandes B, Sagman U, Auger M, Demetriou M, Dennis JW. 1991. Beta1-6 branched oligosaccharides as a marker of tumor progression in human breast and colon neoplasia. Cancer Res. 51:718-723.
13. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR, Elstrom RL, June CH, Thompson CB. 2002. The CD28 signaling pathway regulates glucose metabolism. Immunity. 16:769-777.
14. Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW. 2000. Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nature Med. 6:306-312.
15. Haga Y, Ishii K, Suzuki T. 2011. N-Glycosylation is critical for the stability and intracellular trafficking of glucose transporter GLUT4. J Biol Chem. 286:31320-31327.
16. Hassanein M, Hoeksema MD, Shiota M, Qian J, Harris BK, Chen H, Clark JE, Alborn WE, Eisenberg R, Massion PP. 2013. SLC1A5 mediates glutamine transport required for lung cancer cell growth and survival. Clin Cancer Res. 19:560-570.
17. Johswich A, Longuet C, Pawling J, Rahman AA, Ryczko M, Drucker DJ, Dennis JW. 2014. N-Glycan remodeling on glucagon receptor is an effector of nutrient sensing by the hexosamine biosynthesis pathway. J Biol Chem. 289:15927-15941.
18. Kang R, Saito H, Ihara Y, Miyoshi E, Koyama N, Sheng Y, Taniguchi N. 1996. Transcriptional regulation of the N-acetylglucosaminyltranserase V gene in human bile duct carcinoma cells (HuCC-T1) is mediated by Ets-1. J Biol Chem. 271:26706-26712.
19. Kaplon J, Zheng L, Meissl K, Chaneton B, Selivanov VA, Mackay G, van der Burg SH, Verdegaal EM, Cascante M, Shlomi T, et al. 2013. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature. 498:109-112.
20. Kitagawa T, Tsuruhara Y, Hayashi M, Endo T, Stanbridge EJ. 1995. A tumorassociated glycosylation change in the glucose transporter GLUT1 controlled by tumor suppressor function in human cell hybrids. J Cell Sci. 108:3735-3743.
21. Korczak B, Le T, Elowe S, Donavan R, Datti A, Dennis JW. 2000. Minimal Catalytic Domain of N-Acetylglucosaminyltransferase V. Glycobiology. 10:595-599.
22. Lau K, Partridge EA, Silvescu CI, Grigorian A, Pawling J, Reinhold VN, Demetriou M, Dennis JW. 2007. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell. 129:123-134.
23. Lau KS, Dennis JW. 2008. N-Glycans in cancer progression. Glycobiology. 18:750-760.
24. Lau KS, Khan S, Dennis JW. 2008. Genome-scale identification of UDP-GlcNAc-dependent pathways. Proteomics. 8:3294-3302.
25. Levine AJ, Puzio-Kuter AM. 2010. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 330:1340-1344.
26. NakanoM, Saldanha R, Gobel A, KavallarisM, PackerNH. 2011. Identification of glycan structure alterations on cellmembrane proteins in desoxyepothilone B resistant leukemia cells. Mol Cell Proteomics. 10:M111 009001.
27. Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang H, Nyfeler B, Yang H, Hild M, Kung C, Wilson C, et al. 2009. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell. 136:521-534.
28. Ohtsubo K, Takamatsu S, Minowa MT, Yoshida A, Takeuchi M, Marth JD. 2005. Dietary and genetic control of glucose transporter 2 glycosylation promotes insulin secretion in suppressing diabetes. Cell. 123:1307-1321.
29. Partridge EA, Le Roy C, Di Guglielmo GM, Pawling J, Cheung P, Granovsky M, Nabi IR, Wrana JL, Dennis JW. 2004. Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science. 306:120-124.
30. Sasai K, Ikeda Y, Fujii T, Tsuda T, TaniguchiN. 2002. UDP-GlcNAc concentration is an important factor in the biosynthesis of beta1, 6-branched oligosaccharides: Regulation based on the kinetic properties of N-acetylglucosaminyltransferase V. Glycobiology. 12:119-127.
31. Schachter H. 1986. Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem Cell Biol. 64:163-181.
32. Seelentag WK, Li WP, Schmitz SF, Metzger U, Aeberhard P, Heitz PU, Roth J. 1998. Prognostic value of beta1, 6-branched oligosaccharides in human colorectal carcinoma. Cancer Res. 58:5559-5564.
33. Shirato K, Nakajima K, Korekane H, Takamatsu S, Gao C, Angata T, Ohtsubo K, Taniguchi N. 2011. Hypoxic regulation of glycosylation via the N-acetylglucosamine cycle. J Clin Biochem Nutr. 48:20-25.
34. Soliman MA, Abdel Rahman AM, Lamming DA, Birsoy K, Pawling J, FrigoletME, Lu H, Fantus IG, Pasculescu A, Zheng Y, et al. 2014. The adaptor protein p66Shc inhibits mTOR-dependent anabolic metabolism. Sci Signal. 7:ra17.
35. Song Y, Aglipay JA, Bernstein JD, Goswami S, Stanley P. 2010. The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression. Cancer Res. 70:3361-3371.
36. Suzuki S, Tanaka T, Poyurovsky MV, Nagano H, Mayama T, Ohkubo S, Lokshin M, Hosokawa H, Nakayama T, Suzuki Y, et al. 2010. Phosphateactivated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Proc Natl Acad Sci USA. 107:7461-7466.
37. Taguchi T, Ogawa T, Inoue S, Inoue Y, Sakamoto Y, Korekane H, Taniguchi N. 2000. Purification and characterization of UDP-GlcNAc: GlcNAcbeta 1-6 (GlcNAcbeta 1-2)Manalpha 1-R[GlcNAc toMan]-beta 1, 4-N-acetylglucosaminyltransferase VI from hen oviduct. J Biol Chem. 275:32598-32602.
38. Takamatsu S, Antonopoulos A, Ohtsubo K, Ditto D, Chiba Y, Le DT, Morris HR, Haslam SM, Dell A, Marth JD, et al. 2010. Physiological and glycomic characterization of N-acetylglucosaminyltransferase-IVa and-IVb double deficient mice. Glycobiology. 20:485-497.
39. Takamatsu S, Oguri S, Minowa MT, Yoshida A, Nakamura K, Takeuchi M, Kobata A. 1999. Unusually high expression of N-acetylglucosaminyltransferase-IV a in human choriocarcinoma cell lines: A possible enzymatic basis of the formaiton of abnormal biantennary sugar chain. Cancer Res. 59:3949-3953.
40. Varki A, Cummings RD, Esko J, Freeze H, Stanley P, Bertozzi C, Hart GW, Etzler ME. 2009. Essentials of Glycobiology. New York: Cold Spring Harbor Laboratory.
41. Ward RJ, Alvarez-Curto E, Milligan G. 2011. Using the Flp-In T-Rex system to regulate GPCR expression. Methods Mol Biol. 746:21-37.
42. Watanabe T, Ihara H, Miyoshi E, Honke K, Taniguchi N, Taguchi T. 2006. A specific detection of GlcNAcbeta1-6Manalpha1 branches in N-linked glycoproteins based on the specificity of N-acetylglucosaminyltransferase VI. Glycobiology. 16:431-439.
43. Wellen KE, Lu C, Mancuso A, Lemons JM, Ryczko M, Dennis JW, Rabinowitz JD, Coller HA, Thompson CB. 2010. The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism. Genes Dev. 24:2784-2799.
44. Wellen KE, Thompson CB. 2012. A two-way street: Reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol. 13:270-276.
45. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK, Nissim I, Daikhin E, Yudkoff M, McMahon SB, et al. 2008. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA. 105 18782-18787.
46. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. 2012. MetaboAnalyst 2. 0-a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 40:W127-W133.
47. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher-Sananikone E, Locasale JW, Son J, Zhang H, Coloff JL, et al. 2012. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell. 149:656-670.
48. Yoshimura M, Nishikawa A, Ihara Y, Taniguchi S, Taniguchi N. 1995. Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA. 92:8753-8758.
49. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, Rajagopalan H, Schmidt K, Willson JK, Markowitz S, Zhou S, et al. 2009. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science. 325:1555-1559.