A testis-specific regulator of complex and hybrid N-glycan synthesis

Journal of Cell Biology

Volumn 190, Issue 5, 2010, Pages 893-910

  Huang, Hung Hsiang ^a   Stanley, Pamela ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN DERIVATIVE; INHIBITOR PROTEIN; N ACETYLGLUCOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE I INHIBITOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOHYDRATE SYNTHESIS; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE EXPRESSION; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPERMATOGENESIS; TESTIS;

ANIMALS; CHIMERA; CHO CELLS; CRICETINAE; CRICETULUS; GLYCOPROTEINS; GOLGI APPARATUS; MALE; MANNOSE; MICE; N-ACETYLGLUCOSAMINYLTRANSFERASES; POLYSACCHARIDES; SERTOLI CELLS; SPERMATOGENESIS; TESTIS;

EID: 77956374916     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201004102     Document Type: Article

References (67)

1. Akama, T.O., H. Nakagawa, K. Sugihara, S. Narisawa, C. Ohyama, S. Nishimura, D.A. O'Brien, K.W. Moremen, J.L. Millan, and M.N. Fukuda. 2002. Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science. 295:124-127. doi:10.1126/science.1065570
2. Akama, T.O., H. Nakagawa, N.K. Wong, M. Sutton-Smith, A. Dell, H.R. Morris, J. Nakayama, S. Nishimura, A. Pai, K.W. Moremen, 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. USA. 103:8983-8988. doi:10.1073/pnas.0603248103
3. Akasaka-Manya, K., H. Manya, A. Nakajima, M. Kawakita, and T. Endo. 2006. Physical and functional association of human protein O-mannosyltransferases 1 and 2. J. Biol. Chem. 281:19339-19345. doi:10.1074/jbc.M601091200
4. Aryal, R.P., T. Ju, and R.D. Cummings. 2010. The endoplasmic reticulum chaperone Cosmc directly promotes in vitro folding of T-synthase. J. Biol. Chem. 285:2456-2462. doi:10.1074/jbc.M109.065169
5. Bhattacharyya, R., M. Bhaumik, T.S. Raju, and P. Stanley. 2002. Truncated, inactive N-acetylglucosaminyltransferase III (GlcNAc-TIII) induces neurological and other traits absent in mice that lack GlcNAc-TIII. J. Biol. Chem. 277:26300-26309. doi:10.1074/jbc.M202276200
6. Bhaumik, M., T. Harris, S. Sundaram, L. Johnson, J. Guttenplan, C. Rogler, and P. Stanley. 1998. Progression of hepatic neoplasms is severely retarded in mice lacking the bisecting N-acetylglucosamine on N-glycans: evidence for a glycoprotein factor that facilitates hepatic tumor progression. Cancer Res. 58:2881-2887.
7. Breton, C., and A. Imberty. 1999. Structure/function studies of glycosyltransferases. Curr. Opin. Struct. Biol. 9:563-571. doi:10.1016/S0959- 440X(99)00006-8
8. Campbell, C., and P. Stanley. 1984. A dominant mutation to ricin resistance in Chinese hamster ovary cells induces UDP-GlcNAc:glycopeptide beta-4-N-acetylglucosaminyltransferase III activity. J. Biol. Chem. 259:13370-13378.
9. Cantarel, B.L., P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37(Database issue):D233-D238. doi:10.1093/nar/gkn663
10. Carter, P. 2001. Improving the efficacy of antibody-based cancer therapies. Nat. Rev. Cancer. 1:118-129. doi:10.1038/35101072
11. Chalmel, F., A.D. Rolland, C. Niederhauser-Wiederkehr, S.S. Chung, P. Demougin, A. Gattiker, J. Moore, J.J. Patard, D.J. Wolgemuth, B. Jégou, and M. Primig. 2007. The conserved transcriptome in human and rodent male gametogenesis. Proc. Natl. Acad. Sci. USA. 104:8346-8351. doi:10.1073/pnas. 0701883104
12. Chaney, W., and P. Stanley. 1986. Lec1A Chinese hamster ovary cell mutants appear to arise from a structural alteration in N- acetylglucosaminyltransferase I. J. Biol. Chem. 261:10551-10557.
13. Chen, W., and P. Stanley. 2003. Five Lec1 CHO cell mutants have distinct Mgat1 gene mutations that encode truncated N-acetylglucosaminyltransferase I. Glycobiology. 13:43-50. doi:10.1093/glycob/cwg003
14. Chiu, R., L. Novikov, S. Mukherjee, and D. Shields. 2002. A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J. Cell Biol. 159:637-648. doi:10.1083/jcb.200208013
15. Cummings, R.D., and J.D. Esko. 2009. Principles of glycan recognition. In Essentials of Glycobiology. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etlzler, editors. Cold Spring Harbor Laboratory Press, New York. 387-402.
16. Cummings, R.D., and F.T. Liu. 2009. Galectins. In Essentials of Glycobiology. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etlzler, editors. Cold Spring Harbor Laboratory Press, New York. 475-487.
17. Dennis, J.W., I.R. Nabi, and M. Demetriou. 2009. Metabolism, cell surface organization, and disease. Cell. 139:1229-1241. doi:10.1016/j.cell.2009.12.008
18. Emanuelsson, O., S. Brunak, G. von Heijne, and H. Nielsen. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971. doi:10.1038/nprot.2007.131
19. Fink, J.L., R.N. Aturaliya, M.J. Davis, F. Zhang, K. Hanson, M.S. Teasdale, C. Kai, J. Kawai, P. Carninci, Y. Hayashizaki, and R.D. Teasdale. 2006. LOCATE: a mouse protein subcellular localization database. Nucleic Acids Res. 34(Database issue):D213-D217. doi:10.1093/nar/gkj069
20. Giraudo, C.G., J.L. Daniotti, and H.J. Maccioni. 2001. Physical and functional association of glycolipid N-acetyl-galactosaminyl and galactosyl transferases in the Golgi apparatus. Proc. Natl. Acad. Sci. USA. 98:1625-1630. doi:10.1073/pnas.031458398
21. Hassinen, A., A. Rivinoja, A. Kauppila, and S. Kellokumpu. 2010. Golgi N-glycosyltransferases form both homo- and heterodimeric enzyme complexes in live cells. J. Biol. Chem. 285:17771-17777. doi:10.1074/jbc.M110.103184
22. Hodgson, U., V. Pulkkinen, M. Dixon, M. Peyrard-Janvid, M. Rehn, P. Lahermo, V. Ollikainen, K. Salmenkivi, V. Kinnula, J. Kere, et al. 2006. ELMOD2 is a candidate gene for familial idiopathic pulmonary fibrosis. Am. J. Hum. Genet. 79:149-154. doi:10.1086/504639
23. Hoe, M.H., P. Slusarewicz, T. Misteli, R. Watson, and G. Warren. 1995. Evidence for recycling of the resident medial/trans Golgi enzyme, N-acetylglucosaminyltransferase I, in ldlD cells. J. Biol. Chem. 270:25057-25063. doi:10.1074/jbc.270.42.25057
24. Hofmann, K., and W. Stoffel. 1993. TMbase - A database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler. 374:166.
25. Huang, C.C., and R. Montgomery. 1970. Microheterogeneity and paucidispersity of glycoproteins. I. The carbohydrate of chicken ovalbumin. Carbohydr. Res. 13:127-137. doi:10.1016/S0008-6215(00)84902-2
26. Iguchi, N., J.W. Tobias, and N.B. Hecht. 2006. Expression profiling reveals meiotic male germ cell mRNAs that are translationally up- and downregulated. Proc. Natl. Acad. Sci. USA. 103:7712-7717. doi:10.1073/pnas. 0510999103
27. Ioffe, E., and P. Stanley. 1994. Mice lacking N- acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc. Natl. Acad. Sci. USA. 91:728-732. doi:10.1073/pnas.91.2.728
28. Jones, C.J., C.A. Morrison, and R.W. Stoddart. 1992. Histochemical analysis of rat testicular glycoconjugates. 1. Subsets of N-linked saccharides in seminiferous tubules. Histochem. J. 24:319-326. doi:10.1007/BF01046163
29. Ju, T., and R.D. Cummings. 2002. A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc. Natl. Acad. Sci. USA. 99:16613-16618. doi:10.1073/pnas.262438199
30. Ju, T., R.P. Aryal, C.J. Stowell, and R.D. Cummings. 2008. Regulation of protein O-glycosylation by the endoplasmic reticulum-localized molecular chaperone Cosmc. J. Cell Biol. 182:531-542. doi:10.1083/jcb.200711151
31. Julenius, K., A. Mølgaard, R. Gupta, and S. Brunak. 2005. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology. 15:153-164. doi:10.1093/glycob/ cwh151
32. Kanda, Y., T. Yamada, K. Mori, A. Okazaki, M. Inoue, K. Kitajima-Miyama, R. Kuni-Kamochi, R. Nakano, K. Yano, S. Kakita, et al. 2007. Comparison of biological activity among nonfucosylated therapeutic IgG1 antibodies with three different N-linked Fc oligosaccharides: the high-mannose, hybrid, and complex types. Glycobiology. 17:104-118. doi:10.1093/glycob/cwl057
33. Kudo, T., T. Iwai, T. Kubota, H. Iwasaki, Y. Takayma, T. Hiruma, N. Inaba, Y. Zhang, M. Gotoh, A. Togayachi, and H. Narimatsu. 2002. Molecular cloning and characterization of a novel UDP-Gal:GalNAc(alpha) peptide beta 1,3-galactosyltransferase (C1Gal-T2), an enzyme synthesizing a core 1 structure of O-glycan. J. Biol. Chem. 277:47724-47731. doi:10.1074/jbc.M205839200
34. Lee, J., S. Sundaram, N.L. Shaper, T.S. Raju, and P. Stanley. 2001. Chinese hamster ovary (CHO) cells may express six beta 4-galactosyltransferases (beta 4GalTs). Consequences of the loss of functional beta 4GalT-1, beta 4GalT-6, or both in CHO glycosylation mutants. J. Biol. Chem. 276:13924-13934.
35. Lippincott-Schwartz, J., L.C. Yuan, J.S. Bonifacino, and R.D. Klausner. 1989. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 56:801-813. doi:10.1016/0092-8674(89)90685-5
36. Mather, J.P. 1980. Establishment and characterization of two distinct mouse testicular epithelial cell lines. Biol. Reprod. 23:243-252. doi:10.1095/biolreprod23.1.243
37. Metzler, M., A. Gertz, M. Sarkar, H. Schachter, J.W. Schrader, and J.D. Marth. 1994. Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 13:2056-2065.
38. Millward, T.A., M. Heitzmann, K. Bill, U. Längle, P. Schumacher, and K. Forrer. 2008. Effect of constant and variable domain glycosylation on pharmacokinetics of therapeutic antibodies in mice. Biologicals. 36:41-47. doi:10.1016/j.biologicals.2007.05.003
39. Mori, K., S. Iida, N. Yamane-Ohnuki, Y. Kanda, R. Kuni-Kamochi, R. Nakano, H. Imai-Nishiya, A. Okazaki, T. Shinkawa, A. Natsume, et al. 2007. Nonfucosylated therapeutic antibodies: the next generation of therapeutic antibodies. Cytotechnology. 55:109-114. doi:10.1007/s10616-007-9103-2
40. Mukherjee, S., R. Chiu, S.M. Leung, and D. Shields. 2007. Fragmentation of the Golgi apparatus: an early apoptotic event independent of the cytoskeleton. Traffic. 8:369-378. doi:10.1111/j.1600-0854.2007.00542.x
41. Nilsson, T., M.H. Hoe, P. Slusarewicz, C. Rabouille, R. Watson, F. Hunte, G. Watzele, E.G. Berger, and G. Warren. 1994. Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13:562-574.
42. Nilsson, T., C. Rabouille, N. Hui, R. Watson, and G. Warren. 1996. The role of the membrane-spanning domain and stalk region of N- acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells. J. Cell Sci. 109:1975-1989.
43. Niu, T.K., A.C. Pfeifer, J. Lippincott-Schwartz, and C.L. Jackson. 2005. Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol. Biol. Cell. 16:1213-1222. doi:10.1091/mbc.E04-07-0599
44. North, S.J., H.H. Huang, S. Sundaram, J. Jang-Lee, A.T. Etienne, A. Trollope, S. Chalabi, A. Dell, P. Stanley, and S.M. Haslam. 2010. Glycomics profiling of Chinese hamster ovary cell glycosylation mutants reveals N-glycans of a novel size and complexity. J. Biol. Chem. 285:5759-5775. doi:10.1074/jbc.M109.068353
45. Opat, A.S., F. Houghton, and P.A. Gleeson. 2000. Medial Golgi but not late Golgi glycosyltransferases exist as high molecular weight complexes. Role of luminal domain in complex formation and localization. J. Biol. Chem. 275:11836-11845. doi:10.1074/jbc.275.16.11836
46. Opat, A.S., F. Houghton, and P.A. Gleeson. 2001. Steady-state localization of a medial-Golgi glycosyltransferase involves transit through the trans-Golgi network. Biochem. J. 358:33-40. doi:10.1042/0264-6021:3580033
47. Patnaik, S.K., and P. Stanley. 2006. Lectin-resistant CHO glycosylation mutants. Methods Enzymol. 416:159-182. doi:10.1016/S0076-6879(06)16011-5
48. Patnaik, S.K., B. Potvin, S. Carlsson, D. Sturm, H. Leffler, and P. Stanley. 2006. Complex N-glycans are the major ligands for galectin-1, -3, and -8 on Chinese hamster ovary cells. Glycobiology. 16:305-317. doi:10.1093/glycob/cwj063
49. Rodeheffer, C., and B.D. Shur. 2002. Targeted mutations in beta1,4-galactosyltransferase I reveal its multiple cellular functions. Biochim. Biophys. Acta. 1573:258-270.
50. Russo, R.N., N.L. Shaper, and J.H. Shaper. 1990. Bovine beta 1-4-galactosyltransferase: two sets of mRNA transcripts encode two forms of the protein with different amino-terminal domains. In vitro translation experiments demonstrate that both the short and the long forms of the enzyme are type II membrane-bound glycoproteins. J. Biol. Chem. 265:3324-3331.
51. Seko, A., and K. Yamashita. 2008. Activation of beta1,3-N- acetylglucosaminyltransferase- 2 (beta3Gn-T2) by beta3Gn-T8. Possible involvement of beta3Gn-T8 in increasing poly-N-acetyllactosamine chains in differentiated HL-60 cells. J. Biol. Chem. 283:33094-33100. doi:10.1074/jbc. M806933200
52. Seko, A., M. Koketsu, M. Nishizono, Y. Enoki, H.R. Ibrahim, L.R. Juneja, M. Kim, and T. Yamamoto. 1997. Occurence of a sialylglycopeptide and free sialylglycans in hen's egg yolk. Biochim. Biophys. Acta. 1335:23-32.
53. Shur, B.D., S. Evans, and Q. Lu. 1998. Cell surface galactosyltransferase: current issues. Glycoconj. J. 15:537-548. doi:10.1023/A:1006951407168
54. Song, Y., J.A. Aglipay, J.D. Bernstein, S. Goswami, and P. Stanley. 2010. The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression. Cancer Res. 70:3361-3371. doi:10.1158/0008-5472.CAN- 09-2719
55. Spiess, A.N., C. Feig, W. Schulze, F. Chalmel, H. Cappallo-Obermann, M. Primig, and C. Kirchhoff. 2007. Cross-platform gene expression signature of human spermatogenic failure reveals inflammatory-like response. Hum. Reprod. 22:2936-2946. doi:10.1093/humrep/dem292
56. Sprenger, J., J. Lynn Fink, S. Karunaratne, K. Hanson, N.A. Hamilton, and R.D. Teasdale. 2008. LOCATE: a mammalian protein subcellular localization database. Nucleic Acids Res. 36(Database issue):D230-D233. doi:10.1093/nar/ gkm950
57. Stanley, P. 1983. Selection of lectin-resistant mutants of animal cells. Methods Enzymol. 96:157-184. doi:10.1016/S0076-6879(83)96015-9
58. Stanley, P., S. Sundaram, J. Tang, and S. Shi. 2005. Molecular analysis of three gain-of-function CHO mutants that add the bisecting GlcNAc to N-glycans. Glycobiology. 15:43-53. doi:10.1093/glycob/cwh136
59. Stanley, P., H. Schachter, and N. Taniguchi. 2009. N-glycans. In Essentials of Glycobiology. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etlzler, editors. Cold Spring Harbor Laboratory Press, New York. 101-114.
60. Su, A.I., T. Wiltshire, S. Batalov, H. Lapp, K.A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, G. Kreiman, et al. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA. 101:6062-6067. doi:10.1073/pnas.0400782101
61. Teasdale, R.D., and M.R. Jackson. 1996. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu. Rev. Cell Dev. Biol. 12:27-54. doi:10.1146/annurev.cellbio.12.1.27
62. Thierry-Mieg, D., and J. Thierry-Mieg. 2006. AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol. 7: S12:1-14. doi:10.1186/gb-2006-7-s1-s12
63. Varki, A., and J. Lowe. 2009. Biological roles of glycans. In Essentials of Glycobiology. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etlzler, editors. Cold Spring Harbor Laboratory Press, New York. 75-88.
64. Ward, T.H., R.S. Polishchuk, S. Caplan, K. Hirschberg, and J. Lippincott-Schwartz. 2001. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155:557-570. doi:10.1083/jcb. 200107045
65. Wu, H., S.C. Shekar, R.J. Flinn, M. El-Sibai, B.S. Jaiswal, K.I. Sen, V. Janakiraman, S. Seshagiri, G.J. Gerfen, M.E. Girvin, and J.M. Backer. 2009. Regulation of Class IA PI 3-kinases: C2 domain-iSH2 domain contacts inhibit p85/ p110alpha and are disrupted in oncogenic p85 mutants. Proc. Natl. Acad. Sci. USA. 106:20258-20263. doi:10.1073/pnas.0902369106
66. Zhao, Y., Y. Sato, T. Isaji, T. Fukuda, A. Matsumoto, E. Miyoshi, J. Gu, and N. Taniguchi. 2008. Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J. 275:1939-1948. doi:10.1111/j.1742-4658.2008. 06346.x
67. Zhou, Q., S. Shankara, A. Roy, H. Qiu, S. Estes, A. McVie-Wylie, K. Culm- Merdek, A. Park, C. Pan, and T. Edmunds. 2008. Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function. Biotechnol. Bioeng. 99:652-665. doi:10.1002/bit.21598