Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2016 Jun 28;11(6):e0158024.
doi: 10.1371/journal.pone.0158024. eCollection 2016.

Mutation in the Pro-Peptide Region of a Cysteine Protease Leads to Altered Activity and Specificity-A Structural and Biochemical Approach

Affiliations

Mutation in the Pro-Peptide Region of a Cysteine Protease Leads to Altered Activity and Specificity-A Structural and Biochemical Approach

Sruti Dutta et al. PLoS One. .

Abstract

Papain-like proteases contain an N-terminal pro-peptide in their zymogen form that is important for correct folding and spatio-temporal regulation of the proteolytic activity of these proteases. Catalytic removal of the pro-peptide is required for the protease to become active. In this study, we have generated three different mutants of papain (I86F, I86L and I86A) by replacing the residue I86 in its pro-peptide region, which blocks the specificity determining S2-subsite of the catalytic cleft of the protease in its zymogen form with a view to investigate the effect of mutation on the catalytic activity of the protease. Steady-state enzyme kinetic analyses of the corresponding mutant proteases with specific peptide substrates show significant alteration of substrate specificity-I86F and I86L have 2.7 and 29.1 times higher kcat/Km values compared to the wild-type against substrates having Phe and Leu at P2 position, respectively, while I86A shows lower catalytic activity against majority of the substrates tested. Far-UV CD scan and molecular mass analyses of the mature form of the mutant proteases reveal similar CD spectra and intact masses to that of the wild-type. Crystal structures of zymogens of I86F and I86L mutants suggest that subtle reorganization of active site residues, including water, upon binding of the pro-peptide may allow the enzyme to achieve discriminatory substrate selectivity and catalytic efficiency. However, accurate and reliable predictions on alteration of substrate specificity require atomic resolution structure of the catalytic domain after zymogen activation, which remains a challenging task. In this study we demonstrate that through single amino acid substitution in pro-peptide, it is possible to modify the substrate specificity of papain and hence the pro-peptide of a protease can also be a useful target for altering its catalytic activity/specificity.

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The structure of papain and its precursor form.
a) A schematic representation of papain precursor and activation mechanism. b) Three dimentional structure of zymogen of papain (PDB ID: 3TNX); catalytic domain is represented as electrostatic potential surface with catalytic dyad residues represented as light-blue CPK model. The pro-peptide is represnted in ribbon. The color scheme used for (a) and (b) are: nevyblue, signal peptide; green, N-terminal pro-domain; yellow, PBL binding β-strand; magenta, the polypeptide blocking the substrate binding subsites; orange, autocatalytic cleavage site; blue-red gradient; catalytic domain. ‘m’ and ‘p’ tags in the sequence number represent mature and pro-peptide region respectively.
Fig 2
Fig 2. SDS-PAGE analyses of the proteases.
a) Purified pro-proteases. b) Gelatin gel zymography for WT (TS) and three mutants. 2μg pro-proteases were loaded in each lane. The lanes of each gel are marked at the bottom. M lane is for molecular weight marker whose values in kDa are given at the left panel.
Fig 3
Fig 3. Analyses of mature proteases.
a) Reducing SDS-PAGE analysis of the generated mature proteases. b) Far-UV CD spectra of mature proteases in the range 190 to 250 nm. c) MALDI-TOF MS spectra of mature proteases as shown in the SDS-PAGE (panel a). d) Peptide mass finger printing analyses after trypsin in-gel digestion of I86L and WT (TS) mature protease. e) Theoretical mass and sequence of the N-terminus of expected cleavages upto 7 residue downstream of the N-terminus of mature papain from plant latex. Sequences marked in red and green correspond to the peaks marked by same colored arrows in panel d. Red and green arrows represent high and low intensity peaks respectively in panel d. f) Sequence of the recombinant WT (TS); yellow, blue and black colour represent vector tag, pro-peptide and mature domain sequence respectively. Red and green arrows indicate cleavages corresponding to the peptide masses indicated in the same color in MS experiment (panels d and e). The sequences which matched with mature domain obtained from MS/MS analyses are underlined.
Fig 4
Fig 4. Effect of substitution at residue 86 of pro-peptide of papain on its proteolytic acivity.
a) relative [normalised to WT (TS)] specific activity values against azo-casein and relative Kcat/Km values for the substrate Pyroglutamyl-Phe-Leu-p-nitroanilide. b) The actual values of the same are given in the table. c) Michaelis-Menten plot of proteolytic activity against different substrates for three mutants and WT (TS) papain. The error bar of each points represents standard error of the mean of replicates.
Fig 5
Fig 5. X-ray structures of the mutants and WT (TS).
(a) Omit map (Fo-Fc) of I86L and I86F. The omit maps, contoured at 3.5σ level, were calculated by omitting the pro-peptide blocking the catalytic cleft. Catalytic domains of the two mutants are represented n electrostatic surfaces with the catalytic dyad in orange sphere superimposed therein. (b) Superposition of pro-peptide of I86L, I86F mutants and WT (TS). The propeptides are represented in ribbon. I86L, coloured in green; I86F, coloured in light blue; WT (TS) in light orange. The mature domain of the WT (TS) is in surface presentation with catalytic dyad in ball and stick. (c) Superposition of the mature catalytic domain with same color code used in (b). (d) and (e) The 2mFo-DFc electron density map at 1.5σ level of residues Tyr168, Tyr174 and Val220 in three proteins. The co-ordinates and structure factors of the WT (TS) have been taken from pdb_id 3TNX. ‘m’ and ‘p’ tags in the sequence number represent mature and pro-peptide region respectively.
Fig 6
Fig 6. Structural comparison of catalytic cleft structures of I86F and I86L with that of the WT (TS).
The catalytic domains are in surface presentation; I86L, coloured in green; I86F, coloured in light blue; WT (TS) in light orange. The pro-peptide parts blocking the catalytic clefts are presented as stick model with Carbon atoms coloured as their respective catalytic domain surface colour. a) and b) Superposition of I86L and I86F mutants with the WT (TS) respectively. c) Individual I86L, I86F and WT (TS) in a similar orientation of a) and b). The arrow indicates a cavity formed by two residues Tyr168 and Tyr174. d) Superposition of I86L, I86F and WT (TS) showing some residues of the catalytic cleft responsible for micro-changes in the cleft conformation of the mutants. The catalytic dyad residues are C132A and H266. The Cɑ trace is drawn on WT (TS)structure with mature domain in light orange and pro-peptide in magenta. The position of pro-peptide also represents the flow of substrate during Michaelis comlex formation.The co-ordinates and structure factors of the WT (TS) have been taken from pdb_id 3TNX. ‘m’ and ‘p’ tags in the sequence number represent mature and pro-peptide region respectively.

Similar articles

Cited by

References

    1. Turk V, Stok V Vasiljeva O, Renko M, Sun T, Turk B, et al.(2012) Cysteine cathepsins: From structure, function and regulation to new frontiers. Biochim Biophys Acta 1824, 68–88. 10.1016/j.bbapap.2011.10.002 - DOI - PMC - PubMed
    1. Wiederanders B, Kaulmann G, Schilling K (2003) Functions of propeptide parts in cysteine proteases. Curr Protein Pept Sci 4, 309–326. - PubMed
    1. Khan AR, James MNG (1998) Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Protein Science 7, 815–836. - PMC - PubMed
    1. Cygler M, Mort JS (1997) Proregion structure of members of the papain superfamily. Mode of inhibition of enzymatic activity. Biochimie 79, 645–652. - PubMed
    1. Coulombe R, Grochulski P, Sivaraman J, Ménard R, Mort JS, Cygler M (1996) Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J 15, 5492–5503. - PMC - PubMed

Grants and funding

The authors thank the beam-line staffs of BM14, at the ESRF for help during data collection and DBT, Govt. of India, for financial support and for providing access to the beam-line. MALDI-TOF experiments were carried out at IPLS-DBT facility of Calcutta University, Kolkata. This project was supported by institutional grant (MSACR project) and funding from DBT, Govt. of India (BT/PR13895/BRB/10/789/2010 dt. 15-06-2011).

LinkOut - more resources