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Dolichol phosphate mannose synthase: a Glycosyltransferase with Unity in molecular diversities

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Abstract

N-glycans provide structural and functional stability to asparagine-linked (N-linked) glycoproteins, and add flexibility. Glycan biosynthesis is elaborative, multi-compartmental and involves many glycosyltransferases. Failure to assemble N-glycans leads to phenotypic changes developing infection, cancer, congenital disorders of glycosylation (CDGs) among others. Biosynthesis of N-glycans begins at the endoplasmic reticulum (ER) with the assembly of dolichol-linked tetra-decasaccharide (Glc3Man9GlcNAc2-PP-Dol) where dolichol phosphate mannose synthase (DPMS) plays a central role. DPMS is also essential for GPI anchor biosynthesis as well as for O- and C-mannosylation of proteins in yeast and in mammalian cells. DPMS has been purified from several sources and its gene has been cloned from 39 species (e.g., from protozoan parasite to human). It is an inverting GT-A folded enzyme and classified as GT2 by CAZy (carbohydrate active enZyme; http://www.cazy.org). The sequence alignment detects the presence of a metal binding DAD signature in DPMS from all 39 species but finds cAMP-dependent protein phosphorylation motif (PKA motif) in only 38 species. DPMS also has hydrophobic region(s). Hydropathy analysis of amino acid sequences from bovine, human, S. crevisiae and A. thaliana DPMS show PKA motif is present between the hydrophobic domains. The location of PKA motif as well as the hydrophobic domain(s) in the DPMS sequence vary from species to species. For example, the domain(s) could be located at the center or more towards the C-terminus. Irrespective of their catalytic similarity, the DNA sequence, the amino acid identity, and the lack of a stretch of hydrophobic amino acid residues at the C-terminus, DPMS is still classified as Type I and Type II enzyme. Because of an apparent bio-sensing ability, extracellular signaling and microenvironment regulate DPMS catalytic activity. In this review, we highlight some important features and the molecular diversities of DPMS.

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References

  1. Kornfeld, R., Kornfeld, S.: Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 6631–6636 (1985)

    Article  Google Scholar 

  2. Helenius, A., Aebi, M.: Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019–1049 (2004)

    Article  CAS  PubMed  Google Scholar 

  3. Trombetta, E.S.: The contribution of N-glycans and their processing in the endoplasmic reticulum to glycoprotein biosynthesis. Glycobiology. 13, 77R–91R (2005)

    Article  Google Scholar 

  4. Tanner, W., Jung, P., Behrens, N.H.: Dolicholmonophosphates: Mannosyl acceptors in a particulate in vitro system of S. cerevisiae. FEBS Lett. 16, 245–248 (1971)

    Article  CAS  PubMed  Google Scholar 

  5. Waechter, C.J., Lennarz, W.J.: The role of polyprenol-linked sugars in glycoprotein synthesis. Annu. Rev. Biochem. 45, 95–112 (1976)

    Article  CAS  PubMed  Google Scholar 

  6. Richards, J.B., Evans, P.J., Hemming, F.W.: Dolichol phosphates as acceptors of mannose from guanosine diphosphate mannose in liver systems. Biochem. J. 124, 957–959 (1971)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Banerjee, D.K.: Amphomycin inhibits mannosylphosphoryldolichol synthesis by forming a complex with dolichylmonophosphate. J. Biol. Chem. 264, 2024–2028 (1989)

    CAS  PubMed  Google Scholar 

  8. Banerjee, D.K., Diaz, A.M., Campos, T.M., Grande, C., Kozek, W.J., Baksi, K.: Monoclonal antibody to amphomycin. A tool to study the topography of dolichol monophosphate in the membrane. Carbohyd Res. 236, 301–313 (1971)

    Article  Google Scholar 

  9. Banerjee, D.K., DaSilva, J.J., Bigio, B.: Mannosylphosphodolichol synthase activity is associated with a 32kDa phosphoprotein. Biosci. Rep. 19, 169–177 (1999)

  10. Lahav, M., Chiu, T.H., Lennarz, W.J.: Studies on the biosynthesis of Mannan in micrococcus lysodeikticus II. The enzymatic synthesis of mannosyl-1-phosphoryl-undecaprenol. J. Biol. Chem. 244, 5890–5898 (1969)

    CAS  PubMed  Google Scholar 

  11. Rush, J.S., Waechter, C.J.: Transmembrane movement of a water-soluble analogue of mannosylphosphoryl dolichol is mediated by an endoplasmic reticulum protein. J. Cell Biol. 130, 529–536 (1995)

    Article  CAS  PubMed  Google Scholar 

  12. Shidoji, Y., De Luca, L.M.: Rat liver microsomes catalyse mannosyl transfer from GDP-D-mannose to retinyl phosphate with high efficiency in the absence of detergents. Biochem. J. 200, 529–538 (1981)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Vladimir, N., Shibaev, V.N., Danilov, L.L.: Synthesis of intermediates in the dolichol pathway of protein glycosylation. In: Large, D.G., Warren, C.D. (eds.) Glycopeptides and Related Compounds: Synthesis, Analysis, and Applications, pp. 427–504. Marcel Dekker Inc, NY, Basel, Hong Kong (1997)

    Google Scholar 

  14. Xing, J., Forsee, W.T., Lamani, E., Maltsev, S.D., Danilov, L.L., Shibaev, V.N., Schutzbach, J.S., Cheung, H.C., Jedrzejas, M.J.: Investigations of the active site of Saccharomyces cerevisiae dolichylphosphate-mannose synthase using fluorescent labeled dolichylphosphate derivatives. Biochemistry. 39, 7886–7894 (2000)

    Article  CAS  PubMed  Google Scholar 

  15. Sinhoara, H., Maruyama, T.: Evolution of glycoproteins as judged by the frequency of occurrence of the tripeptides Asn-X-Ser and Asn-X-Thr in proteins. J Molec Evolution. 2, 117–122 (1973)

    Article  Google Scholar 

  16. Chapman, A., Trowbridge, I.S., Hyman, R., Kornfeld, S.: Structure of the lipid-linked oligosaccharides that accumulate in class E thy-1-negative mutant lymphomas. Cell. 17, 509–515 (1979)

    Article  CAS  PubMed  Google Scholar 

  17. Banerjee, D.K., Scher, M.G., Waechter, C.J.: Amphomycin: effect of the lipopeptide antibiotic on the glycosylation and extraction of dolichyl monophosphate in calf brain membranes. Biochemistry. 20, 1561–1568 (1981)

    Article  CAS  PubMed  Google Scholar 

  18. Englund, P.T.: The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu. Rev. Biochem. 62, 121–138 (1993)

    Article  CAS  PubMed  Google Scholar 

  19. Tanner, W., Lehle, L.: Proteins glycosylation in yeast. Biochim. Biophys. Acta. 906, 81–99 (1987)

    Article  CAS  PubMed  Google Scholar 

  20. Manya, H., Chiba, A., Yoshida, A., Wang, X., Chiba, Y., Jigami, Y., Margolis, R.U., Endo, T.: Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity. Proc. Natl. Acad. Sci. U. S. A. 101, 500–505 (2004)

    Article  CAS  PubMed  Google Scholar 

  21. Doucey, M.-A., Hess, D., Cacan, R., Hofsteenge, J.: Protein C-Mannosylation is enzyme-catalyzed and uses Dolichyl-phosphate-mannose as a precursors. Molec Biol Cell. 9, 291–300 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Helenius, J., Ng, D.T., Marolda, C.L., Walter, P., Valvano, M.A., Aebi, M.: Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature. 415, 447–450 (2002)

    Article  CAS  PubMed  Google Scholar 

  23. Sanyal, S., Menon, A.K.: Stereoselective transbilayer translocation of mannosyl phosphoryl dolichol by an endoplasmic reticulum flippase. Proc. Natl. Acad. Sci. U. S. A. 107, 11289–11294 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Schutzbach, J.S., Zimmerman, J.W., Forsee, W.T.: The purification and characterization of recombinant yeast dolichyl-phosphate-mannose synthase. J. Biol. Chem. 268, 24190–24196 (1993)

    CAS  PubMed  Google Scholar 

  25. Baksi, K., Zhang, Z., Banerjee, A., Banerjee, D.K.: Cloning and expression of mannosylphospho dolichol synthase from bovine adrenal medullary capillary endothelial cells. Glycoconj. J. 26, 635–645 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Jensen, J.W., Schutzbach, J.S.: Activation of dolichyl-phospho-mannose synthase by phospholipids. Eur. J. Biochem. 153, 41–48 (1985)

    Article  CAS  PubMed  Google Scholar 

  27. Marquardt, T., Denecke, J.: Congenital disorders of glycosylation: review of their molecular basics, clinical presentations and specific therapies. Eur. J. Pediatr. 162, 359–370 (2003)

    CAS  PubMed  Google Scholar 

  28. Banerjee, D.K.: N-glycans in cell survival and death: cross-talk between glycosyltransferases. Biochim. Biophys. Acta. 1820, 1338–1346 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Baksi, K., Zhang, Z., Banerjee, A., Serrano, J.E., Perez, L.E., Linares, L., Seijo, A., Sanchez, N., Katiyar, U., Banerjee, D.K.: Silencing Mannosylphospho Dolichol synthase with shRNA impacts differentiation of capillary endothelial cells. FASEB J. 30, 844.1 (2016)

    Google Scholar 

  30. Banerjee, D.K., Carrasquillo, E.A., Hughy, P., Schutzbach, J.S., Martinez, J.A., Baksi, K.: In vitro phosphorylation by cAMP-dependent protein kinase up-regulates recombinant Saccharomyces cerevisiae mannosylphospho dolichol synthase. J. Biol. Chem. 280, 4174–4181 (2005)

    Article  CAS  PubMed  Google Scholar 

  31. Elbein, A.D.: Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu. Rev. Biochem. 56, 497–534 (1987)

    Article  CAS  PubMed  Google Scholar 

  32. Banerjee, D.K.: A recent approach to the study of dolichyl monophosphate topology in the rough endoplasmic reticulum. Acta Biochim. Pol. 41, 275–280 (1994)

    CAS  PubMed  Google Scholar 

  33. Rokas, A., Carroll, S.B.: Frequent and widespread parallel evolution of protein sequences. Mol. Biol. Evol. 25, 1943–1953 (2008)

    Article  CAS  PubMed  Google Scholar 

  34. Edrees, B.M., Athar, M., Abduljaleel, Z., Al-Allaf, F.A., Taher, M.M., Khan, W., Bouazzaoui, A., Al-Harbi, N., Safar, R., Al-Edressi, H., Alansary, K., Anazi, A., Altayeb, N., Ahmed, M.A.: Functional alterations due to amino acid changes and evolutionary comparative analysis of ARPKD and ADPKD genes. Genomics Data. 10(complete), 127–134 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  35. Jacquemyn, H., Roldán-Ruiz, I., Honnay, O.: Evidence for demographic bottlenecks and limited gene flow leading to low genetic diversity in a rare thistle. Conserv. Genet. 11, 1979–1987 (2010)

    Article  Google Scholar 

  36. Colussi, F.A., Taron, C.H., Mack, J.C., Orlean, P.: Human and Saccharomyces cerevisiae dolichol phosphate mannose synthases represent two classes of the enzyme, but both function in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. U. S. A. 94, 7873–7878 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tempone, A.J., Furtado, D.R., Gimba, E.R., Oliveira, F.M., Rumjanek, F.D.: Dolichol phosphate mannose synthase is differentially expressed in male and female worms of Schistosoma mansoni. Comp Biochem Physiol B Biochem Mol Biol. 131, 465–474 (2002)

    Article  CAS  PubMed  Google Scholar 

  38. Forsee, W.T., McPherson, D., Schutzbach, J.S.: Characterization of recombinant yeast dolichyl mannosyl phosphate synthase and site-directed mutagenesis of its cysteine residues. Eur. J. Biochem. 244, 953–958 (1997)

    Article  CAS  PubMed  Google Scholar 

  39. Carrasquillo E.A, Role of cAMP-dependent phosphorylation domain on the functions (in vitro/in vivo) of mannosylphosphodolichol (Dol-P-Man) synthase in Saccharomyces cerevisiae. In PhD Thesis. (The University of Puerto Rico Medical Sciences Campus, San Juan, PR, USA) (2002).

  40. Albright, C.F., Orlean, P., Robbins, P.W.: A 13-amino acid peptide in three yeast glycosyltransferases may be involved in dolichol recognition. Proc. Natl. Acad. Sci. U. S. A. 86, 7366–7369 (1989)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zimmerman, J.W., Robbins, P.W.: The hydrophobic domain of dolichyl-phosphate-mannose synthase is not essential for enzyme activity or growth in Saccharomyces cerevisiae. J. Biol. Chem. 268, 16746–16753 (1993)

    CAS  PubMed  Google Scholar 

  42. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., Bairoch, A.: Protein identification and analysis tools on the ExPASy server. In: Walker, J.M. (ed.) The Proteomics Protocols Handbook, pp. 571–607. Humana Press, Totowa (2005)

    Chapter  Google Scholar 

  43. Kyte, J., Doolittle, R.F.: A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132 (1982)

    Article  CAS  PubMed  Google Scholar 

  44. Werstuck, G., Capone, J.P.: Mutational analysis of the herpes simplex virus trans-inducing factor Vmw65. Gene. 75, 213–224 (1989)

    Article  CAS  PubMed  Google Scholar 

  45. Coutinho, P.M., Deleury, E., Davies, G.J., Henrissat, B.: An evolving hierarchical family classification for Glycosyltransferases. J. Mol. Biol. 328, 307–317 (2003)

    Article  CAS  PubMed  Google Scholar 

  46. Lairson, L.L., Henrissat, B., Davies, G.J., Withers, S.G.: Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521–555 (2008)

    Article  CAS  PubMed  Google Scholar 

  47. Liu, J., Mushegian, A.: Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci. 12, 1418–1431 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tarbouriech, N., Charnock, S.J., Davies, G.J.: Three-dimensional structures of the Mn and mg dTDP complexes of the family GT-2 glycosyltransferase SpsA: a comparison with related NDP-sugar glycosyltransferases. J. Mol. Biol. 314, 655–661 (2001)

    Article  CAS  PubMed  Google Scholar 

  49. Ardiccioni, C., Clarke, O.B., Tomasek, D., Issa, H.A., von Alpen, D.C., Pond, H.L., Banerjee, S., Rajashankar, K.R., Liu, Q., Guan, Z., Li, C., Kloss, B., Bruni, R., Kloppmann, E., Rost, B., Manzini, M.C., Shapiro, L., Mancia, F.: Structure of the polyisoprenyl-phosphate glycosyltransferase GtrB and insights into the mechanism of catalysis. Nat. Commun. 7, 10175 (2016)

    Article  CAS  PubMed  Google Scholar 

  50. Igura, M., Maita, N., Kamishikiryo, J., Yamada, M., Obita, T., Maenaka, K., Kohda, D.: Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. EMBO J. 27, 234–243 (2008)

    Article  CAS  PubMed  Google Scholar 

  51. Wiggins, C.A., Munro, S.: Activity of the yeast MNN1 alpha-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl. Acad. Sci. U. S. A. 95, 7945–7950 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Bujnicki, J.M., Elofsson, A., Fischer, D., Rychlewski, L.: Structure prediction meta server. Bioinformatics. 17, 750–751 (2001)

    Article  CAS  PubMed  Google Scholar 

  53. Lamani, E., Mewbourne, R.B., Fletcher, D.S., Maltsev, S.D., Danilov, L.L., Veselovsky, V.V., Lozanova, A.V., Grigorieva, N.Y., Pinsker, O.A., Xing, J., Forsee, W.T., Cheung, H.C., Schutzbach, J.S., Shibaev, V.N., Jedrzejas, M.J.: Structural studies and mechanism of Saccharomyces cerevisiae dolichyl-phosphate-mannose synthase: insights into the initial step of synthesis of dolichyl-phosphate-linked oligosaccharide chains in membranes of endoplasmic reticulum. Glycobiology. 16, 666–678 (2006)

    Article  CAS  PubMed  Google Scholar 

  54. Orlean, P., Albright, C., Robbins, P.W.: Cloning and sequencing of the yeast gene for dolichol phosphate mannose synthase, an essential protein. J. Biol. Chem. 263, 17499–17507 (1988)

    CAS  PubMed  Google Scholar 

  55. Taylor, S.S., Buechler, J.A., Yonemoto, W.: cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971–1005 (1990)

    Article  CAS  PubMed  Google Scholar 

  56. Zimmereman, J.W., Specht, C.A., Cazares, B.X., Robbins, P.W.: The isolation of Dol-P-man synthase from Ustilago maydis that functions in Saccharomyces cerevisiae. Yeast. 12, 765–771 (1996)

    Article  Google Scholar 

  57. Sugiyama, E., DeGasperi, R., Urakaze, M., Chang, H.M., Thomas, L.J., Hyman, R., Warren, C.D., Yeh, E.T.H.: Identification of defects in glycosylphosphatidylinositol anchor biosynthesis in the thy-1 expression mutants. J. Biol. Chem. 266, 12119–12122 (1991)

    CAS  PubMed  Google Scholar 

  58. Chapman, A., Fujimoto, K., Kornfeld, S.: The primary glycosylation defect in class E thy-1-negative mutant mouse lymphoma cells is an inability to synthesize dolichol-P-mannose. J. Biol. Chem. 255, 4441–4446 (1980)

    CAS  PubMed  Google Scholar 

  59. Camp, L.A., Chauhan, P., Farrar, J.D., Lehrman, M.A.: Defective mannosylation of glycosylphosphatidylinositol in Lec35 Chinese hamster ovary cells. J. Biol. Chem. 268, 6721–6728 (1993)

    CAS  PubMed  Google Scholar 

  60. Singh, N., Tartakoff, A.M.: Two different mutants blocked in synthesis of dolichol-phosphoryl-mannose do not add glycophospholipid anchors to membrane proteins: quantitative correction of the phenotype of a CHO cell mutant with tunicamycin. Mol. Cell. Biol. 11, 391–400 (1991)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. DeGasperi, R., Thomas, L.J., Sugiyama, E., Chang, H.M., Beck, P.J., Orlean, P., Albright, C., Waneck, G., Sambrook, J.F., Warren, C.D., Yeh, E.T.H.: Correction of a defect in mammalian GPI anchor biosynthesis by a transfected yeast gene. Science. 250, 988–991 (1990)

    Article  CAS  PubMed  Google Scholar 

  62. Beck, P.J., Orlean, P., Albright, C., Robbins, P.W., Gething, M.J., Sambrook, J.F.: The Saccharomyces cerevisiae DPM1 gene encoding dolichol-phosphate-mannose synthase is able to complement a glycosylation-defective mammalian cell line. Mol. Cell. Biol. 10, 4612–4622 (1990)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Maeda, Y., Tanaka, S., Hino, J., Kangawa, K., Kinoshita, T.: Human dolichol-phosphate-mannose synthase consists of three subunits, DPM1, DPM2 and DPM3. EMBO J. 19, 2475–2482 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tomita, S., Inoue, N., Maeda, Y., Ohishi, K., Takeda, J., Kinoshita, T.: A homologue of Saccharomyces cerevisiae Dpm1p is not sufficient for synthesis of dolichol-phosphate-mannose in mammalian cells. J. Biol. Chem. 273, 9249–9254 (1998)

    Article  CAS  PubMed  Google Scholar 

  65. Jadid, N., Mialoundama, A.S., Heintz, D., Ayoub, D., Erhardt, M., Mutterer, J., Meyer, D., Alioua, A., Dorsselaer, A.V., Rahier, A., Camara, B., Bouvier, F.: Dolichol phosphate mannose synthase1 mediates the biogenesis of isoprenyl-linked glycans and influences development, stress response, and ammonium hypersensitivity in Arabidopsis. Plant Cell. 23, 1985–2005 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Mora-Montes, H.M., Ponce-Noyola, P., Villagómez-Castro, J.C., Gow, N.A., Flores-Carreón, A., López-Romero, E.: Protein glycosylation in Candida. Future Microbiol. 4, 1167–1183 (2009)

    Article  CAS  PubMed  Google Scholar 

  67. Maeda, Y., Tomita, S., Watanabe, R., Ohishi, K., Kinoshita, T.: DPM2 regulates biosynthesis of dolichol phosphate-mannose in mammalian cells: correct subcellular localization and stabilization of DPM1, and binding of dolichol phosphate. EMBO J. 17, 4920–4929 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kruszewska, J.S., Saloheimo, M., Migdalski, A., Orlean, P., Penttilä, M., Palamarczyk, G.: Dolichol phosphate mannose synthase from the filamentous fungus Trichoderma Reesei belongs to the human and Schizosaccharomyces pombe class of the enzyme. Glycobiology. 10, 983–991 (2000)

    Article  CAS  PubMed  Google Scholar 

  69. Juchimiuk, M., Kruszewska, J., Palamarczyk, G.: Dolichol phosphate mannose synthase from the pathogenic yeast Candida albicans is a multimeric enzyme. Biochim. Biophys. Acta. 1850, 2265–2275 (2015)

    Article  CAS  PubMed  Google Scholar 

  70. Banerjee, D.K., Kousvelari, E.E., Baum, B.J.: cAMP-mediated protein phosphorylation of microsomal membranes increases mannosylphospho dolichol synthase activity. Proc. Natl. Acad. Sci. U. S. A. 84, 6389–6393 (1987)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Banerjee, D.K.: Microenvironment of endothelial cell growth and regulation of protein N-glycosylation. Indian J. Biochem. Biophys. 25, 8–13 (1988)

    CAS  PubMed  Google Scholar 

  72. Vander Heiden, M.G., Cantly, L.C., Thompson, C.B.: Undersatnding the Warburg effect: the metabolic requirements of cell proliferation. Science. 324, 1029–1033 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Grant, S.R., Kousvelari, E.E., Banerjee, D.K.: Baum BJ, β-adrenergic stimulation alters oligosaccharide pyrophosphoryl dolichol metabolism in rat parotid acinar cells. Biochem. J. 231, 431–438 (1985)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Banerjee, D.K., Aponte, E., DaSilva, J.J.: Low expression of lipid-linked oligosaccharide due to a functionally altered Dol-P-man synthase reduces protein glycosylation in cAMP-dependent protein kinase deficient Chinese hamster ovary cells. Glycoconj. J. 21, 479–486 (2004)

    Article  CAS  PubMed  Google Scholar 

  75. Banerjee, D.K.: Requirement of protein kinase type I for cAMP-mediated up-regulation of lipid-linked oligosaccharide for asparagine-linked protein glycosylation. Cell Mol Biol (Noisy-le-grand). 53, 55–63 (2007)

    CAS  Google Scholar 

  76. Jozwiak, A.P., Skorupinska-Tudek, K., Maluszynska, J., Kania, M., Danikiewicz, W., Swiezewska, E.: Polyisoprenoid alcohols are accumulated in Arabidopsis roots. Chem Phys Lip. 160, S47 (2009)

    Article  Google Scholar 

  77. Britto, D.T., Kronzucker, H.J.: NH4 + toxicity in higher plants: a critical review. J. Plant Physiol. 159, 567–584 (2002)

    Article  CAS  Google Scholar 

  78. Gillmore, C.S., Lukowitz, W., Brininostool, G., Sedbrook, J.C., Hamann, T., Poindexter, P., Soerville, C.: Glycophosphatidyl-inositol-anchored proteins are required for cell wall synthesis and morphogenesis in Arabidopsis. Plant Cell. 17, 1128–1140 (2005)

    Article  Google Scholar 

  79. Kousvelari, E.E., Banerjee, D.K., Murty, L., Baum, B.J.: N-linked protein glycosylation in the rat parotid gland during aging. Mech Aging and Dev. 42, 173–181 (1988)

    Article  CAS  Google Scholar 

  80. Nozaki, M., Ohishi, K., Yamada, N., Kinoshita, T., Nagy, A., Takeda, J.: Developmental abnormalities of glycophosphatidylinositol-anchor deficient embryos revealed by Crc/loxP system. Lab. Investig. 79, 293–299 (1999)

    CAS  PubMed  Google Scholar 

  81. Kim, S., Westphal, V., Srikrishna, G., Mehta, D.P., Peterson, S., Filano, J., Karnes, P.S., Patterson, M.C., Freeze, H.H.: Dolichol phosphate mannose synthase (DPM1) mutations define congenital disorder of glycosylation 1c (CDG-1c). J. Clin. Invest. 105, 191–198 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Haeuptle, M.A., Hennet, T.: Congenital disorders of glycosylation: an update on defects affecting the biosynthesis of dolichol-linked oligosaccharides. Hum. Mutat. 30, 1628–1641 (2009)

    Article  CAS  PubMed  Google Scholar 

  83. Lefeber, D.J., Schönberger, J., Morava, E., Guillard, M., Huyben, K.M., Verrijp, K., Grafakou, O., Evangeliou, A., Preijers, F.W., Manta, P., Yildiz, J., Grünewald, S., Spilioti, M., van den Elzen, C., Klein, D., Hess, D., Ashida, H., Hofsteenge, J., Maeda, Y., van den Heuvel, L., Lammens, M., Lehle, L., Wevers, R.A.: Deficiency of Dol-P-man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am. J. Hum. Genet. 85, 76–86 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Endo, T.: Glycobiology of α-dystroglycan and muscular dystrophy. J. Biochem. 157, 1–12 (2015)

    Article  CAS  PubMed  Google Scholar 

  85. Banerjee, D.K., Martinez, J.A., Baksi, K.: Significance of protein N-glycosylation in breast tumor angiogenesis. In: Maragoudakis, M.E., Papadimitriou, E. (eds.) Angiogenesis: basic Science and clinical applications, pp. 281–302. Transworld Research Network, Trivandrum (2007)

    Google Scholar 

  86. Martinez, J.A., Tavarez, J.J., Oliveira, C.M., Banerjee, D.K.: Potentiation of angiogenic switch in capillary endothelial cells by cAMP: a cross-talk between up-regulated LLO biosynthesis and the HSP-70 expression. Glycoconj. J. 23, 209–220 (2006)

    Article  CAS  PubMed  Google Scholar 

  87. Pearl, L.H., Prodromon, C.: Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10, 46–51 (2000)

    Article  CAS  PubMed  Google Scholar 

  88. Bukau, B., Horwich, A.L.: The Hsp70 and Hsp60 chaperone machines. Cell. 92, 351–366 (1998)

    Article  CAS  PubMed  Google Scholar 

  89. Zhang, Z., Banerjee, A., Baksi, K., Banerjee, D.K.: Mannosylphospho dolichol synthase overexpression supports angiogenesis. Biocatal Biotransformation. 28, 90–98 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  90. Li, R., Xie, D.D., Dong, J.H., Li, H., Li, K.S., Su, J., Chen, L.Z., Xu, Y.F., Wang, H.M., Gong, Z., Cui, G.Y., Yu, X., Wang, K., Yao, W., Xin, T., Li, M.Y., Xiao, K.H., An, X., Huo, Y., Xu, Z., Sun, J.P., Pang, Q.: Molecular mechanism of ERK dephosphorylation by striatal-enriched protein tyrosine phosphatase. J Neurochem. 128, 315–329 (2014)

    Article  CAS  PubMed  Google Scholar 

  91. Samaddar, S., Dutta, A., Sinharoy, S., Paul, A., Bhattacharya, A., Saha, S., Chien, K.Y., Goshe, M.B., DasGupta, M.: Autophosphorylation of gatekeeper tyrosine by symbiosis receptor kinase. FEBS Lett. 587, 2972–2979 (2013)

    Article  CAS  PubMed  Google Scholar 

  92. Woe, P.C., Blount, P., Kung, C.: Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol. Microbiol. 28, 583–592 (1998)

    Article  Google Scholar 

  93. Yang, Y., Igumenova, T.I.: The C-terminal V5 domain of protein kinase Ca is intrinsically disordered, with propensity to associate with a membrane mimetic. PLoS One. 8, e65699 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. García-Alai, M.M., Alonso, L.G., De Prat-Gay, G.: The N-terminal module of HPV16 E7 is an intrinsically disordered domain that confers conformational and recognition plasticity to the oncoprotein. Biochemistry. 46, 10405–10412 (2007)

    Article  PubMed  Google Scholar 

  95. Higgins, D.G., Thompson, J.D., Gibson, T.J.: Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383–402 (1996)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are indebted to Juan A. Martínez and Elena A. Carrasquillo to share their unpublished results. The work was partly supported by funds from the Department of Defense DAMD17-03-1-0754, NIH U54-CA096297, Susan G. Komen for the Cure BCTR0600582, the NSF EPS-1002410 (DKB) and NIH/NIMHD 2G12MD007583 (KB).

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Authors and Affiliations

  1. Department of Biochemistry, School of Medicine, University of Puerto Rico, Medical Sciences Campus, San Juan, PR, 00936-5067, USA

    Dipak K. Banerjee, Zhenbo Zhang & Jesús E. Serrano-Negrón

  2. Institute of Functional Nanomaterials, University of Puerto Rico, PR00931, San Juan, PR, -1907, USA

    Dipak K. Banerjee

  3. Department of Anatomy and Cell Biology, School of Medicine, Universidad Central del Caribe, Bayamón, PR, 00960-3001, USA

    Krishna Baksi

  4. Department of Natural Sciences & Mathematics, Interamerican University of Puerto Rico, Bayamón Campus, Bayamón, PR, 00957-6257, USA

    Jesús E. Serrano-Negrón

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  1. Dipak K. Banerjee
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  2. Zhenbo Zhang
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  3. Krishna Baksi
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  4. Jesús E. Serrano-Negrón
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Contributions

Dipak K. Banerjee developed the idea, executed the plan outlined and drafted the manuscript. Zhenbo Zhang isolated, characterized DPMS overexpressing and shRNA knockdown capillary endothelial cell lines, and helped developing some figures. Krishna Baksi cloned, expressed and studied the wild type DMPS from capillary endothelial cells. Jesús Serrano helped with evolution and hydrophobic analysis.

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Correspondence to Dipak K. Banerjee.

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Banerjee, D.K., Zhang, Z., Baksi, K. et al. Dolichol phosphate mannose synthase: a Glycosyltransferase with Unity in molecular diversities. Glycoconj J 34, 467–479 (2017). https://doi.org/10.1007/s10719-017-9777-4

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  • DOI: https://doi.org/10.1007/s10719-017-9777-4

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