Skip to main content
Top
Published in: Metabolic Brain Disease 2/2018

01-04-2018 | Original Article

A profound computational study to prioritize the disease-causing mutations in PRPS1 gene

Authors: Ashish Kumar Agrahari, P. Sneha, C. George Priya Doss, R. Siva, Hatem Zayed

Published in: Metabolic Brain Disease | Issue 2/2018

Login to get access

Abstract

Charcot-Marie-Tooth disease (CMT) is one of the most commonly inherited congenital neurological disorders, affecting approximately 1 in 2500 in the US. About 80 genes were found to be in association with CMT. The phosphoribosyl pyrophosphate synthetase 1 (PRPS1) is an essential enzyme in the primary stage of de novo and salvage nucleotide synthesis. The mutations in the PRPS1 gene leads to X-linked Charcot-Marie-Tooth neuropathy type 5 (CMTX5), PRS super activity, Arts syndrome, X-linked deafness-1, breast cancer, and colorectal cancer. In the present study, we obtained 20 missense mutations from UniProt and dbSNP databases and applied series of comprehensive in silico prediction methods to assess the degree of pathogenicity and stability. In silico tools predicted four missense mutations (D52H, M115 T, L152P, and D203H) to be potential disease causing mutations. We further subjected the four mutations along with native protein to 50 ns molecular dynamics simulation (MDS) using Gromacs package. The resulting trajectory files were analyzed to understand the stability differences caused by the mutations. We used the Root Mean Square Deviation (RMSD), Radius of Gyration (Rg), solvent accessibility surface area (SASA), Covariance matrix, Principal Component Analysis (PCA), Free Energy Landscape (FEL), and secondary structure analysis to assess the structural changes in the protein upon mutation. Our study suggests that the four mutations might affect the PRPS1 protein function and stability of the structure. The proposed study may serve as a platform for drug repositioning and personalized medicine for diseases that are caused by the PRPS1 deficiency.
Appendix
Available only for authorised users
Literature
go back to reference Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249CrossRefPubMedPubMedCentral Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249CrossRefPubMedPubMedCentral
go back to reference Agrahari A, George Priya Doss C (2015) Impact of I30T and I30M substitution in MPZ gene associated with Dejerine–Sottas syndrome type B (DSSB): a molecular modeling and dynamics. J Theor Biol 382:23–33CrossRefPubMed Agrahari A, George Priya Doss C (2015) Impact of I30T and I30M substitution in MPZ gene associated with Dejerine–Sottas syndrome type B (DSSB): a molecular modeling and dynamics. J Theor Biol 382:23–33CrossRefPubMed
go back to reference Ali SK, Sneha P, Priyadharshini Christy J, Zayed H, George Priya Doss C (2016) Molecular dynamics-based analyses of the structural instability and secondary structure of the fibrinogen gamma chain protein with the D356V mutation. J Biomol Struct Dyn 35(12):2714–2724 Ali SK, Sneha P, Priyadharshini Christy J, Zayed H, George Priya Doss C (2016) Molecular dynamics-based analyses of the structural instability and secondary structure of the fibrinogen gamma chain protein with the D356V mutation. J Biomol Struct Dyn 35(12):2714–2724
go back to reference Alm E, Baker D (1999) Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc Natl Acad Sci U S A 96:11305–11310CrossRefPubMedPubMedCentral Alm E, Baker D (1999) Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc Natl Acad Sci U S A 96:11305–11310CrossRefPubMedPubMedCentral
go back to reference Arts WF, Loonen MC, Sengers RC, Slooff JL (1933) X-linked ataxia, weakness, deafness, and loss of vision in early childhood with a fatal course. Ann Neurol 33:535–539CrossRef Arts WF, Loonen MC, Sengers RC, Slooff JL (1933) X-linked ataxia, weakness, deafness, and loss of vision in early childhood with a fatal course. Ann Neurol 33:535–539CrossRef
go back to reference Bakhit YH, Ibrahim MO, Amin M, Mirghani YA, Hassan MA (2016) In silico analysis of SNPs in PARK2 and PINK1 genes that potentially cause autosomal recessive Parkinson disease. Adv Bioinforma 2016:9313746 Bakhit YH, Ibrahim MO, Amin M, Mirghani YA, Hassan MA (2016) In silico analysis of SNPs in PARK2 and PINK1 genes that potentially cause autosomal recessive Parkinson disease. Adv Bioinforma 2016:9313746
go back to reference Becker MA (2008) Hyperuricemia and Gout In The Online Metabolic and Molecular Bases of Inherited Disease (OMMBID), D Valle, ed New York: McGraw-Hill, chapter 205 Becker MA (2008) Hyperuricemia and Gout In The Online Metabolic and Molecular Bases of Inherited Disease (OMMBID), D Valle, ed New York: McGraw-Hill, chapter 205
go back to reference Bhardwaj A, Dhar YV, Asif MH, Bag SK (2016) In Silico identification of SNP diversity in cultivated and wild tomato species: insight from molecular simulations. Sci Rep 6:38715CrossRefPubMedPubMedCentral Bhardwaj A, Dhar YV, Asif MH, Bag SK (2016) In Silico identification of SNP diversity in cultivated and wild tomato species: insight from molecular simulations. Sci Rep 6:38715CrossRefPubMedPubMedCentral
go back to reference Capriotti E, Fariselli P, Rossi I, Casadio R (2008) A three-state prediction of single point mutations on protein stability changes. BMC Bioinformatics 9:S6CrossRefPubMedPubMedCentral Capriotti E, Fariselli P, Rossi I, Casadio R (2008) A three-state prediction of single point mutations on protein stability changes. BMC Bioinformatics 9:S6CrossRefPubMedPubMedCentral
go back to reference Da Silva Figueiredo Celestino Gomes P, Chauvot De Beauchêne I, Panel N, Lopez S, De Sepulveda P, Geraldo Pascutti P, Solary E, Tchertanov L (2016) Insight on mutation-induced resistance from molecular dynamics simulations of the native and mutated CSF-1R and KIT. PLoS One 11(7):e0160165CrossRefPubMedPubMedCentral Da Silva Figueiredo Celestino Gomes P, Chauvot De Beauchêne I, Panel N, Lopez S, De Sepulveda P, Geraldo Pascutti P, Solary E, Tchertanov L (2016) Insight on mutation-induced resistance from molecular dynamics simulations of the native and mutated CSF-1R and KIT. PLoS One 11(7):e0160165CrossRefPubMedPubMedCentral
go back to reference Doss CGP, Chakraborty C, Chen L, Zhu H (2014) Integrating in silico prediction methods, molecular docking, and molecular dynamics simulation to predict the impact of ALK missense mutations in structural perspective. Biomed Res Int 2014:895831. https://doi.org/10.1155/2014/895831 Doss CGP, Chakraborty C, Chen L, Zhu H (2014) Integrating in silico prediction methods, molecular docking, and molecular dynamics simulation to predict the impact of ALK missense mutations in structural perspective. Biomed Res Int 2014:895831. https://​doi.​org/​10.​1155/​2014/​895831
go back to reference Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723CrossRefPubMed Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723CrossRefPubMed
go back to reference Hess B, Kutzner C, van der Spoel D, Lindahl E (2004) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435–447CrossRef Hess B, Kutzner C, van der Spoel D, Lindahl E (2004) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435–447CrossRef
go back to reference Jorgensen WL, Maxwell DS, Tirado-Rives J (1996) Development and testing of the OPLS all-atom force field on conformational energetic and properties of organic liquids. J Am Chem Soc 118:11225–11236CrossRef Jorgensen WL, Maxwell DS, Tirado-Rives J (1996) Development and testing of the OPLS all-atom force field on conformational energetic and properties of organic liquids. J Am Chem Soc 118:11225–11236CrossRef
go back to reference Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637CrossRefPubMed Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637CrossRefPubMed
go back to reference Kim JW, Kim HJ (2012) Charcot-Marie-tooth neuropathy X type 5. Gene Reviews http://wwwncbinlmnihgov/books/NBK1876/ Kim JW, Kim HJ (2012) Charcot-Marie-tooth neuropathy X type 5. Gene Reviews http://​wwwncbinlmnihgov​/​books/​NBK1876/​
go back to reference Kim HJ, Sohn KM, Shy ME, Krajewski KM, Hwang M, Park JH, Jang SY, Won HH, Choi BO, Hong SH (2007) Mutations in PRPS1, which encodes the phosphoribosyl pyrophosphate synthetase enzyme critical for nucleotide biosynthesis, cause hereditary peripheral neuropathy with hearing loss and optic neuropathy (cmtx5). Am J Hum Genet 81:552–558CrossRefPubMedPubMedCentral Kim HJ, Sohn KM, Shy ME, Krajewski KM, Hwang M, Park JH, Jang SY, Won HH, Choi BO, Hong SH (2007) Mutations in PRPS1, which encodes the phosphoribosyl pyrophosphate synthetase enzyme critical for nucleotide biosynthesis, cause hereditary peripheral neuropathy with hearing loss and optic neuropathy (cmtx5). Am J Hum Genet 81:552–558CrossRefPubMedPubMedCentral
go back to reference Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1081CrossRefPubMed Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1081CrossRefPubMed
go back to reference Li S, Lu Y, Peng B, Ding J (2007) Crystal structure of human phosphoribosylpyrophosphate synthetase 1 reveals a novel allosteric site. Biochem J 401(1):39–47CrossRefPubMed Li S, Lu Y, Peng B, Ding J (2007) Crystal structure of human phosphoribosylpyrophosphate synthetase 1 reveals a novel allosteric site. Biochem J 401(1):39–47CrossRefPubMed
go back to reference Lobanov MI, Bogatyreva NS, Galzitskaia OV (2008) Radius of gyration is indicator of compactness of protein structure. Mol Biol (Mosk) 42:701–706CrossRef Lobanov MI, Bogatyreva NS, Galzitskaia OV (2008) Radius of gyration is indicator of compactness of protein structure. Mol Biol (Mosk) 42:701–706CrossRef
go back to reference McMurry J (2012) Organic chemistry. Brooks/Cole, Cengage Learning McMurry J (2012) Organic chemistry. Brooks/Cole, Cengage Learning
go back to reference Nagasundaram N, Hailong Z, Jiming L, Karthick V, George Priya Doss C, Chiranjib C, Luonan C (2015) Analysing the effect of mutation on protein function and discovering potential inhibitors of CDK4: molecular modelling and dynamics studies. PLoS One 10(8):e0133969CrossRef Nagasundaram N, Hailong Z, Jiming L, Karthick V, George Priya Doss C, Chiranjib C, Luonan C (2015) Analysing the effect of mutation on protein function and discovering potential inhibitors of CDK4: molecular modelling and dynamics studies. PLoS One 10(8):e0133969CrossRef
go back to reference Ndagi U, Mhlongo NN, Soliman ME (2017) The impact of Thr91 mutation on c-Src resistance to UM-164: molecular dynamics study revealed a new opportunity for drug design. Mol BioSyst 13(6):1157–1171CrossRefPubMed Ndagi U, Mhlongo NN, Soliman ME (2017) The impact of Thr91 mutation on c-Src resistance to UM-164: molecular dynamics study revealed a new opportunity for drug design. Mol BioSyst 13(6):1157–1171CrossRefPubMed
go back to reference Rajasekaran R, Sudandiradoss C, Doss CG, Sethumadhavan R (2007) Identification and in silico analysis of functional SNPs of the BRCA1 gene. Genomics 90(4):447–452CrossRefPubMed Rajasekaran R, Sudandiradoss C, Doss CG, Sethumadhavan R (2007) Identification and in silico analysis of functional SNPs of the BRCA1 gene. Genomics 90(4):447–452CrossRefPubMed
go back to reference Roessler BJ, Bell G, Heidler S, Seino S, Becker M, Palella TD (1990) Cloning of two distinct copies of human phosphoribosylpyrophosphate synthetase cDNA. Nucleic Acids Res 18:193CrossRefPubMedPubMedCentral Roessler BJ, Bell G, Heidler S, Seino S, Becker M, Palella TD (1990) Cloning of two distinct copies of human phosphoribosylpyrophosphate synthetase cDNA. Nucleic Acids Res 18:193CrossRefPubMedPubMedCentral
go back to reference Sang P, Hu W, Ye YJ, Li LH, Zhang C, Xie YH, Meng ZH (2016) In silico screening, molecular docking, and molecular dynamics studies of SNP-derived human P5CR mutants. J Biomol Struct Dyn 27:1–13 Sang P, Hu W, Ye YJ, Li LH, Zhang C, Xie YH, Meng ZH (2016) In silico screening, molecular docking, and molecular dynamics studies of SNP-derived human P5CR mutants. J Biomol Struct Dyn 27:1–13
go back to reference Schreiber G, Buckle AM, Fersht AR, Bycroft M, Fersht AR, Tratschin JG (1994) Stability and function: two constraints in the evolution of barstar and other proteins. Structure (London, England : 1993) 2(10):945–951CrossRef Schreiber G, Buckle AM, Fersht AR, Bycroft M, Fersht AR, Tratschin JG (1994) Stability and function: two constraints in the evolution of barstar and other proteins. Structure (London, England : 1993) 2(10):945–951CrossRef
go back to reference Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Res29:308–311 Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Res29:308–311
go back to reference Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314:268–274CrossRefPubMed Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314:268–274CrossRefPubMed
go back to reference Sneha P, Doss CG (2017) Elucidating the mutational landscape in hepatocyte nuclear factor 1β (HNF1B) by computational approach. Adv Protein Chem Struct Biol 107:283–306CrossRefPubMed Sneha P, Doss CG (2017) Elucidating the mutational landscape in hepatocyte nuclear factor 1β (HNF1B) by computational approach. Adv Protein Chem Struct Biol 107:283–306CrossRefPubMed
go back to reference Sneha P, Thirumal Kumar D, Tanwar H, Siva R, George Priya Doss C, Zayed H (2017a) Structural analysis of G1691S variant in the human Filamin B gene responsible for Larsen syndrome: a comparative computational approach. J Cell Biochem 18:1900–1910 Sneha P, Thirumal Kumar D, Tanwar H, Siva R, George Priya Doss C, Zayed H (2017a) Structural analysis of G1691S variant in the human Filamin B gene responsible for Larsen syndrome: a comparative computational approach. J Cell Biochem 18:1900–1910
go back to reference Sneha P, Thirumal Kumar D, George Priya C, Doss C, Siva R, Zayed H (2017b) Determining the role of missense mutations in the POU domain of HNF1A that reduce the DNA-binding affinity: a computational approach. PLoS One 12(4):e0174953CrossRef Sneha P, Thirumal Kumar D, George Priya C, Doss C, Siva R, Zayed H (2017b) Determining the role of missense mutations in the POU domain of HNF1A that reduce the DNA-binding affinity: a computational approach. PLoS One 12(4):e0174953CrossRef
go back to reference Sperling O, Boer P, Persky-Brosh S, Kanarek E, DeVries A (1972) Altered kinetic property of erythrocyte phosphoribosylpsyrophosphate synthetase in excessive purine production. Rev Eur Etud Clin Biol 17:703–706PubMed Sperling O, Boer P, Persky-Brosh S, Kanarek E, DeVries A (1972) Altered kinetic property of erythrocyte phosphoribosylpsyrophosphate synthetase in excessive purine production. Rev Eur Etud Clin Biol 17:703–706PubMed
go back to reference Stanger HE, Syud FA, Espinosa JF, Giriat I, Muir T, Gellman HS (2000) Length-dependent stability and strand length limits in antiparallel β-sheet secondary structure. Proc Natl Acad Sci U S A 98(21):12015–12020CrossRef Stanger HE, Syud FA, Espinosa JF, Giriat I, Muir T, Gellman HS (2000) Length-dependent stability and strand length limits in antiparallel β-sheet secondary structure. Proc Natl Acad Sci U S A 98(21):12015–12020CrossRef
go back to reference Taira M, Ishijima S, Kita K, Yamada K, Iizasa T, Tatibana M (1987) Nucleotide and deduced amino acid sequences of two distinct cDNAs for rat phosphoribosylpyrophosphate synthetase. J Biol Chem 262:14867–14870PubMed Taira M, Ishijima S, Kita K, Yamada K, Iizasa T, Tatibana M (1987) Nucleotide and deduced amino acid sequences of two distinct cDNAs for rat phosphoribosylpyrophosphate synthetase. J Biol Chem 262:14867–14870PubMed
go back to reference Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, de Silva D, Zharkikh A, Thomas A (2006) Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43:295–305CrossRefPubMed Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, de Silva D, Zharkikh A, Thomas A (2006) Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43:295–305CrossRefPubMed
go back to reference Teng S, Srivastava AK, Wang L (2010) Sequence feature-based prediction of protein stability changes upon amino acid substitutions. BMC Genomics 11:2–5CrossRef Teng S, Srivastava AK, Wang L (2010) Sequence feature-based prediction of protein stability changes upon amino acid substitutions. BMC Genomics 11:2–5CrossRef
go back to reference Vacic V, Markwick PR, Oldfield CJ, Zhao X, Haynes C, Uversky VN, Iakoucheva LM (2012) Disease-associated mutations disrupt functionally important regions of intrinsic protein disorder. PLoS Comput Biol 8:e1002709CrossRefPubMedPubMedCentral Vacic V, Markwick PR, Oldfield CJ, Zhao X, Haynes C, Uversky VN, Iakoucheva LM (2012) Disease-associated mutations disrupt functionally important regions of intrinsic protein disorder. PLoS Comput Biol 8:e1002709CrossRefPubMedPubMedCentral
go back to reference Zaki OK, Priya Doss CG, Ali SA, Murad GG, Elashi SA, Ebnou MS, Thirumal Kumar D, Khalifa O, Gamal R, El Abd HSA, Nasr BN, Zayed H (2017b) Genotype-phenotype correlation in patients with Isovaleric Acidemia: comparative structural modelling and computational analysis of novel variants. Hum Mol Genet. https://doi.org/10.1093/hmg/ddx195 Zaki OK, Priya Doss CG, Ali SA, Murad GG, Elashi SA, Ebnou MS, Thirumal Kumar D, Khalifa O, Gamal R, El Abd HSA, Nasr BN, Zayed H (2017b) Genotype-phenotype correlation in patients with Isovaleric Acidemia: comparative structural modelling and computational analysis of novel variants. Hum Mol Genet. https://​doi.​org/​10.​1093/​hmg/​ddx195
go back to reference Zimmermann MT, Urrutia R, Oliver GR, Blackburn PR, Cousin MA, Bozeck NJ, Klee EW (2017) Molecular modeling and molecular dynamic simulation of the effects of variants in the TGFBR2 kinase domain as a paradigm for interpretation of variants obtained by next generation sequencing. PLoS One 12(2):e0170822CrossRefPubMedPubMedCentral Zimmermann MT, Urrutia R, Oliver GR, Blackburn PR, Cousin MA, Bozeck NJ, Klee EW (2017) Molecular modeling and molecular dynamic simulation of the effects of variants in the TGFBR2 kinase domain as a paradigm for interpretation of variants obtained by next generation sequencing. PLoS One 12(2):e0170822CrossRefPubMedPubMedCentral
go back to reference Zoref E, De Vries A, Sperling O (1975) Mutant feedback-resistant phosphoribosylpyrophosphate synthetase associated with purine over production and gout Phosphoribosylpyrophosphate and purine metabolism in cultured fibroblasts. J Clin Invest 56:1093–1099CrossRefPubMedPubMedCentral Zoref E, De Vries A, Sperling O (1975) Mutant feedback-resistant phosphoribosylpyrophosphate synthetase associated with purine over production and gout Phosphoribosylpyrophosphate and purine metabolism in cultured fibroblasts. J Clin Invest 56:1093–1099CrossRefPubMedPubMedCentral
Metadata
Title
A profound computational study to prioritize the disease-causing mutations in PRPS1 gene
Authors
Ashish Kumar Agrahari
P. Sneha
C. George Priya Doss
R. Siva
Hatem Zayed
Publication date
01-04-2018
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 2/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-017-0121-2

Other articles of this Issue 2/2018

Metabolic Brain Disease 2/2018 Go to the issue