A mutant of phosphomannomutase1 retains full enzymatic activity, but is not activated by IMP: Possible implications for the disease PMM2-CDG

PLoS ONE

Volumn 12, Issue 12, 2017, Pages

  Citro, Valentina ^a   Cimmaruta, Chiara ^a   Liguori, Ludovica ^b,c   Viscido, Gaetano ^a   Cubellis, Maria Vittoria ^a,b   Andreotti, Giuseppina ^b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE 1,6 BISPHOSPHATE; HEXOSE; INOSINE PHOSPHATE; PHOSPHOMANNOMUTASE; PHOSPHOMANNOMUTASE1; UNCLASSIFIED DRUG; BISPHOSPHONIC ACID DERIVATIVE; LIGAND; MUTASE;

ARTICLE; CONGENITAL DISORDER OF GLYCOSYLATION TYPE 1A; CONTROLLED STUDY; ENZYMATIC ASSAY; ENZYME ACTIVITY; GENE MUTATION; GENETIC CODE; GLYCOSYLATION; HUMAN; HYDROLYSIS; ISOMERIZATION; LEPORIDAE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PURIFICATION; THERMOSTABILITY; AMINO ACID SEQUENCE; CHEMISTRY; CONGENITAL DISORDER OF GLYCOSYLATION; DEFICIENCY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; MOLECULAR DOCKING; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SEQUENCE ALIGNMENT; TEMPERATURE;

AMINO ACID SEQUENCE; CONGENITAL DISORDERS OF GLYCOSYLATION; DIPHOSPHONATES; ENZYME ACTIVATION; ENZYME ASSAYS; ENZYME STABILITY; HUMANS; INOSINE MONOPHOSPHATE; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DOCKING SIMULATION; MUTATION; PHOSPHOTRANSFERASES (PHOSPHOMUTASES); SEQUENCE ALIGNMENT; TEMPERATURE;

EID: 85038933160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0189629     Document Type: Article

References (38)

1. Matthijs G, Schollen E, Pardon E, Veiga-Da-Cunha M, Jaeken J, Cassiman JJ, et al. Mutations in PMM2, a phosphomannomutase gene on chromosome 16p13, in carbohydrate-deficient glycoprotein type I syndrome (Jaeken syndrome). Nat Genet. 1997; 16(1):88–92. https://doi.org/10.1038/ng0597-88PMID: 9140401.
2. Jaeken J, Hennet T, Freeze HH, Matthijs G. On the nomenclature of congenital disorders of glycosylation (CDG). J Inherit Metab Dis. 2008; 31(6):669–72. Epub 2008/10/25. https://doi.org/10.1007/s10545-008-0983-x PMID: 18949576.
3. Aebi M. N-linked protein glycosylation in the ER. Biochim Biophys Acta. 2013; 1833(11):2430–7. Epub 2013/04/16. https://doi.org/10.1016/j.bbamcr.2013.04.001 [pii]. PMID: 23583305.
4. Maeda Y, Kinoshita T. Dolichol-phosphate mannose synthase: structure, function and regulation. Biochim Biophys Acta. 2008; 1780(6):861–8. Epub 2008/04/05. https://doi.org/10.1016/j.bbagen.2008.03. 005 [pii]. PMID: 18387370.
5. Pirard M, Collet JF, Matthijs G, Van Schaftingen E. Comparison of PMM1 with the phosphomannomutases expressed in rat liver and in human cells. FEBS Lett. 1997; 411(2–3):251–4. PMID: 9271215.
6. Pirard M, Achouri Y, Collet JF, Schollen E, Matthijs G, Van Schaftingen E. Kinetic properties and tissular distribution of mammalian phosphomannomutase isozymes. Biochem J. 1999; 339 (Pt 1):201–7. PMID: 10085245.
7. Veiga-da-Cunha M, Vleugels W, Maliekal P, Matthijs G, Van Schaftingen E. Mammalian phosphomannomutase PMM1 is the brain IMP-sensitive glucose-1,6-bisphosphatase. J Biol Chem. 2008; 283 (49):33988–93. https://doi.org/10.1074/jbc.M805224200 PMID: 18927083.
8. Yuste-Checa P, Gamez A, Brasil S, Desviat LR, Ugarte M, Perez-Cerda C, et al. The Effects of PMM2-CDG-Causing Mutations on the Folding, Activity, and Stability of the PMM2 Protein. Hum Mutat. 2015; 36(9):851–60. Epub 2015/05/28. https://doi.org/10.1002/humu.22817 PMID: 26014514.
9. Matthijs G, Schollen E, Van Schaftingen E, Cassiman JJ, Jaeken J. Lack of homozygotes for the most frequent disease allele in carbohydrate-deficient glycoprotein syndrome type 1A. Am J Hum Genet. 1998; 62(3):542–50. https://doi.org/10.1086/301763 PMID: 9497260.
10. Thiel C, Lubke T, Matthijs G, von Figura K, Korner C. Targeted disruption of the mouse phosphomannomutase 2 gene causes early embryonic lethality. Mol Cell Biol. 2006; 26(15):5615–20. Epub 2006/07/ 19. 26/15/5615 [pii] https://doi.org/10.1128/MCB.02391-05 PMID: 16847317; PubMed Central PMCID: PMC1592760.
11. Cromphout K, Vleugels W, Heykants L, Schollen E, Keldermans L, Sciot R, et al. The normal phenotype of Pmm1-deficient mice suggests that Pmm1 is not essential for normal mouse development. Mol Cell Biol. 2006; 26(15):5621–35. https://doi.org/10.1128/MCB.02357-05 PMID: 16847318.
12. Hansen SH, Frank SR, Casanova JE. Cloning and characterization of human phosphomannomutase, a mammalian homologue of yeast SEC53. Glycobiology. 1997; 7(6):829–34. Epub 1997/10/06. PMID: 9376685.
13. Matthijs G, Schollen E, Pirard M, Budarf ML, Van Schaftingen E, Cassiman JJ. PMM (PMM1), the human homologue of SEC53 or yeast phosphomannomutase, is localized on chromosome 22q13. Genomics. 1997; 40(1):41–7. Epub 1997/02/15. S0888-7543(96)94536-X [pii] https://doi.org/10.1006/geno.1996.4536 PMID: 9070917.
14. Schollen E, Pardon E, Heykants L, Renard J, Doggett NA, Callen DF, et al. Comparative analysis of the phosphomannomutase genes PMM1, PMM2 and PMM2psi: the sequence variation in the processed pseudogene is a reflection of the mutations found in the functional gene. Hum Mol Genet. 1998; 7 (2):157–64. Epub 1998/03/21. ddb040 [pii]. PMID: 9425221.
15. Quental R, Moleirinho A, Azevedo L, Amorim A. Evolutionary history and functional diversification of phosphomannomutase genes. J Mol Evol. 2010; 71(2):119–27. Epub 2010/07/28. https://doi.org/10.1007/s00239-010-9368-5 PMID: 20661555.
16. Silvaggi NR, Zhang C, Lu Z, Dai J, Dunaway-Mariano D, Allen KN. The X-ray crystal structures of human alpha-phosphomannomutase 1 reveal the structural basis of congenital disorder of glycosylation type 1a. J Biol Chem. 2006; 281(21):14918–26. https://doi.org/10.1074/jbc.M601505200 PMID: 16540464.
17. Andreotti G, Cabeza de Vaca I, Poziello A, Monti MC, Guallar V, Cubellis MV. Conformational Response to Ligand Binding in Phosphomannomutase2: INSIGHTS INTO INBORN GLYCOSYLATION DISORDER. J Biol Chem. 2014; 289(50):34900–10. Epub 2014/10/18. https://doi.org/10.1074/jbc. M114.586362 [pii]. PMID: 25324542; PubMed Central PMCID: PMC4263888.
18. Van Schaftingen E, Jaeken J. Phosphomannomutase deficiency is a cause of carbohydrate-deficient glycoprotein syndrome type I. FEBS Lett. 1995; 377(3):318–20. Epub 1995/12/27. 0014-5793(95) 01357-1 [pii] https://doi.org/10.1016/0014-5793(95)01357-1 PMID: 8549746.
19. Sa-Correia I, Darzins A, Wang SK, Berry A, Chakrabarty AM. Alginate biosynthetic enzymes in mucoid and nonmucoid Pseudomonas aeruginosa: overproduction of phosphomannose isomerase, phosphomannomutase, and GDP-mannose pyrophosphorylase by overexpression of the phosphomannose isomerase (pmi) gene. J Bacteriol. 1987; 169(7):3224–31. Epub 1987/07/01. PMID: 3036776; PubMed Central PMCID: PMC212373.
20. Pindar DF, Bucke C. The biosynthesis of alginic acid by Azotobacter vinelandii. Biochem J. 1975; 152 (3):617–22. Epub 1975/12/01. PMID: 179528; PubMed Central PMCID: PMC1172516.
21. Sharma V, Ichikawa M, He P, Scott DA, Bravo Y, Dahl R, et al. Phosphomannose isomerase inhibitors improve N-glycosylation in selected phosphomannomutase-deficient fibroblasts. J Biol Chem. 2011; 286(45):39431–8. https://doi.org/10.1074/jbc.M111.285502 PMID: 21949237.
22. Borrelli KW, Vitalis A, Alcantara R, Guallar V. PELE: Protein energy landscape exploration. A novel Monte Carlo based technique. J Chem Theory Comput. 2005; 1:1304–11. https://doi.org/10.1021/ ct0501811 PMID: 26631674
23. Takahashi R, Gil VA, Guallar V. Monte Carlo Free Ligand Diffusion with Markov State Model Analysis and Absolute Binding Free Energy Calculations. J Chem Theory Comput. 2014; 10:282–8. https://doi.org/10.1021/ct400678g PMID: 26579911
24. Andreotti G, Pedone E, Giordano A, Cubellis MV. Biochemical phenotype of a common disease-causing mutation and a possible therapeutic approach for the phosphomannomutase 2-associated disorder of glycosylation. Mol Genet Genomic Med. 2013; 1(1):32–44. https://doi.org/10.1002/mgg3.3 PMID: 24498599
25. Andreotti G, Monti MC, Citro V, Cubellis MV. Heterodimerization of Two Pathological Mutants Enhances the Activity of Human Phosphomannomutase2. PLoS One. 2015; 10(10):e0139882. Epub 2015/10/22. https://doi.org/10.1371/journal.pone.0139882 [pii]. PMID: 26488408; PubMed Central PMCID: PMC4619449.
26. Andreotti G, Monticelli M, Cubellis MV. Looking for protein stabilizing drugs with thermal shift assay. Drug Test Anal. 2015; 7(9):831–4. Epub 2015/04/08. https://doi.org/10.1002/dta.1798 PMID: 25845367.
27. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007; 372(3):774–97. https://doi.org/10.1016/j.jmb.2007.05.022 PMID: 17681537.
28. Wizard PP. Epik version 2.2, Impact version 5.7, Prime version 3.0 Ed., Schrödinger, LLC, New York, NY. 2011. PubMed PMID: 1445947.
29. Madadkar-Sobhani A, Guallar V. PELE web server: atomistic study of biomolecular systems at your fingertips. Nucleic Acids Res. 2013; 41(Web Server issue):W322–8. Epub 2013/06/05. https://doi.org/10.1093/nar/gkt454 [pii]. PMID: 23729469; PubMed Central PMCID: PMC3692087.
30. Kaminski GA, Friesner RA. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides. Journal of Physical Chemistry B. 2001; 105:6474–87. PubMed PMID: 8224363.
31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248–54. Epub 1976/05/07. S0003269776699996 [pii]. PMID: 942051.
32. Cammisa M, Correra A, Andreotti G, Cubellis MV. Identification and analysis of conserved pockets on protein surfaces. BMC Bioinformatics. 2013; 14 Suppl 7:S9. https://doi.org/10.1186/1471-2105-14-S7-S9 PMID: 23815589.
33. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605–12. Epub 2004/07/21. https://doi.org/10.1002/jcc.20084 PMID: 15264254.
34. Laskowski RA, Swindells MB. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model. 2011; 51(10):2778–86. Epub 2011/09/17. https://doi.org/10.1021/ci200227u PMID: 21919503.
35. Hay Mele B, Citro V, Andreotti G, Cubellis MV. Drug repositioning can accelerate discovery of pharmacological chaperones. Orphanet J Rare Dis. 2015; 10:55. Epub 2015/05/08. https://doi.org/10.1186/ s13023-015-0273-2 [pii]. PMID: 25947946; PubMed Central PMCID: PMC4429356.
36. Cromphout K, Keldermans L, Snellinx A, Collet JF, Grunewald S, De Geest N, et al. Tissue distribution of the murine phosphomannomutases Pmm1 and Pmm2 during brain development. Eur J Neurosci. 2005; 22(4):991–6. Epub 2005/08/24. EJN4266 [pii] https://doi.org/10.1111/j.1460-9568.2005.04266.x PMID: 16115222.
37. Pirard M, Matthijs G, Heykants L, Schollen E, Grunewald S, Jaeken J, et al. Effect of mutations found in carbohydrate-deficient glycoprotein syndrome type IA on the activity of phosphomannomutase 2. FEBS Lett. 1999; 452(3):319–22. Epub 1999/07/01. S0014-5793(99)00673-0 [pii]. PMID: 10386614.
38. Kjaergaard S, Skovby F, Schwartz M. Carbohydrate-deficient glycoprotein syndrome type 1A: expression and characterisation of wild type and mutant PMM2 in E. coli. Eur J Hum Genet. 1999; 7(8):884–8. Epub 1999/12/22. https://doi.org/10.1038/sj.ejhg.5200398 PMID: 10602363.