Skip to main content
SpringerLink
Log in

Protein disulphide isomerase-assisted functionalization of keratin-based matrices

  • Biotechnologically Relevant Enzymes and Proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

In living systems, protein disulphide isomerase (PDI, EC 5.3.4.1) regulates the formation of new disulphide bonds in proteins (oxidase activity) and catalyzes the rearrangement of non-native disulphide bonds (isomerase activity), leading proteins towards their native configuration. In this study, PDI was used to attach cysteine-containing compounds (CCCs) onto hair, to enhance compound migration within hair fibre and to trigger protein release. A fluorescent (5(6)-TAMRA)-labelled keratin peptide was incorporated into hair by using PDI. Similarly, PDI promoted the grafting of a cysteine-functionalized dye onto wool, as suggested by matrix-assisted laser desorption and ionization time-of-flight results. These reactions were thought to involve oxidation of disulphide bonds between CCCs and wool or hair cysteine residues, catalyzed by the oxidized PDI active site. On the other hand, PDI was demonstrated to enhance the migration of a disulphide bond-functionalized dye within the keratin matrix and trigger the release of RNase A from wool fibres’ surface. These observations may indicate that an isomerisation reaction occurred, catalyzed by the reduced PDI active site, to achieve the thiol-disulphide exchange, i.e. the rearrangement of disulphide bonds between CCCs and keratin. The present communication aims to highlight promising biotechnological applications of PDI, derived from its almost unique properties within the isomerase family.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Scheme 1
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. Gene information available on Pubmed at www.ncbi.nlm.nih.gov/gene/53622

  2. Calculated with “Peptide Property Calculater” available at www.innovagen.se

References

  • Appenzeller-Herzog C, Ellgaard L (2008) The human PDI family: Versatility packed into a single fold. BBA-Mol Cell Res 1783(4):535–548

    CAS  Google Scholar 

  • Bhushan B (2008) Nanoscale characterization of human hair and hairconditioners. Prog Mater Sci 53(4):585–710

    Article  CAS  Google Scholar 

  • Block RJ, Diana B, Brand FC, Arnold S (1939) The Composition of keratins. The amino acid composition of hair, wool, horn, and other eukeratins. J Biol Chem 128(1):181–186

    CAS  Google Scholar 

  • Bolduc C, Shapiro J (2001) Hair care products: waving, straightening, conditioning, and coloring. Clin Dermatol 19(4):431–436

    Article  CAS  PubMed  Google Scholar 

  • Cavaco-Paulo AM, Silva CJSM (2007) Formulation containing neck domains and/or carbohydrate recognition domains for cosmetic applications, namely for the treatment of keratin fibres like hair. Portugal Patent WO/2007/136286, 29.11.2007

  • Chang J-Y (1999) Quantitative analysis of the composition of the native and scrambled ribonuclease A. Anal Biochem 268(1):147–150

    Article  CAS  PubMed  Google Scholar 

  • Chromá-Keull H, Havlis J, Havel J (2000) Reactive dye Ostazine Black V-B: determination in the dye-bath and hydrolysis monitoring by matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 14:40–43

    Article  PubMed  Google Scholar 

  • Coulombe PA, Tong X, Mazzalupo S, Wang Z, Wong P (2004) Great promises yet to be fulfilled: Defining keratin intermediate filament function in vivo. Eur J Cell Biol 83(11–12):735–746

    Article  CAS  PubMed  Google Scholar 

  • Dawber R (1996) Hair: Its structure and response to cosmetic preparations. Clin Dermatol 14(1):105–112

    Article  CAS  PubMed  Google Scholar 

  • Ferrari DM, Söling HD (1999) The protein disulphide-isomerase family: unravelling a string of folds. Biochem J 339:1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert HF, Lester P (1995) Thiol/disulphide exchange equilibria and disulphide bond stability. Method Enzymol 251:8–28

    Article  CAS  Google Scholar 

  • Goldberger RF, Epstein CJ, Anfinsen CB (1963) Acceleration of reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem 238(2):628–635

    CAS  PubMed  Google Scholar 

  • Gorman JJ, Ferguson BL, Speelman D, Mills J (1997) Determination of the disulphide bond arrangement of human respiratory syncytial virus attachment (G) protein by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Protein Sci 6(6):1308–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gosselin MA, Guo W, Lee RJ (2001) Efficient gene transfer using reversibly cross-linked low molecular weight polyethylenimine. Bioconjug Chem 12(6):989–994. doi:https://doi.org/10.1021/bc0100455

    Article  CAS  PubMed  Google Scholar 

  • Gray J (2001) Hair care and hair care products. Clin Dermatol 19(2):227–236

    Article  CAS  PubMed  Google Scholar 

  • Green H, Corey GD, Compton BJ, Dijan P (2001) Attaching agents to tissue with transglutaminase and a transglutaminase substrate. US Patent 6267957, 01/20/1999

  • Hawkins H, Blackburn E, Freedman R (1991) Comparison of the activities of protein disulphide-isomerase and thioredoxin in catalysing disulphide isomerization in a protein substrate. Biochem J 275(349):53

    Google Scholar 

  • Huang X, Kobos RK, XU G (2008) Peptide-based carbon nanotube hair colorants and their use in hair colorant and cosmetic compositions. US Patent WO/2005/117537, 13.04.2005

  • Ishida T, Kirchmeier MJ, Moase EH, Zalipsky S, Allen TM (2001) Targeted delivery and triggered release of liposomal doxorubicin enhances cytotoxicity against human B lymphoma cells. BBA-Biomembranes 1515(2):144–158

    Article  CAS  PubMed  Google Scholar 

  • Juminaga D, Wedemeyer WJ, Scheraga HA (1998) Proline isomerization in bovine pancreatic ribonuclease A. 1. Unfolding conditions. Biochemistry-US 37(33):11614–11620

    Article  CAS  Google Scholar 

  • Kakizawa Y, Harada A, Kataoka K (2001) Glutathione-sensitive stabilization of block copolymer micelles composed of antisense DNA and thiolated poly(ethylene glycol)-block-poly(L-lysine): a potential carrier for systemic delivery of antisense DNA. Biomacromolecules 2(2):491–497. doi:https://doi.org/10.1021/bm000142l

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Tanabe T, Yamauchi K (2004) Novel approach to fabricate keratin sponge scaffolds with controlled pore size and porosity. Biomaterials 25(18):4255–4262

    Article  CAS  PubMed  Google Scholar 

  • Kersteen EA, Barrows SR, Raines RT (2005) Catalysis of protein disulphide bond isomerization in a homogeneous substrate. Biochemistry-US 44(36):12168–12178

    Article  CAS  Google Scholar 

  • King RD, Brockway BE (1989) Treatment of wool materials. United Kingdom Patent EP0276547, 11/04/1987

  • King T, Li Y, Kochoumian L (1978) Preparation of protein conjugates via intermolecular disulphide bond formation. Biochemistry 18(17):1499–1506

    Article  Google Scholar 

  • Koehn H, Clerens S, Deb-Choudhury S, Morton JD, Dyer JM, Plowman JE (2010) The proteome of the wool cuticle. J Proteome Res 9(6):2920–2928. doi:https://doi.org/10.1021/pr901106m

    Article  CAS  PubMed  Google Scholar 

  • Liakopoulou-Kyriakides M, Tsatsaroni E, Laderos P, Georgiadou K (1998) Dyeing of cotton and wool fibres with pigments from Crocus sativus-Effect of enzymatic treatment. Dyes Pigm 36(3):215–221

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  • Lyles MM, Gilbert HF (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulphide isomerase: dependence of the rate on the composition of the redox buffer. Biochemistry-US 30(3):613–619

    Article  CAS  Google Scholar 

  • McKenzie DL, Kwok KY, Rice KG (2000) A potent new class of reductively activated peptide gene delivery agents. J Biol Chem 275(14):9970–9977. doi:https://doi.org/10.1074/jbc.275.14.9970

    Article  CAS  PubMed  Google Scholar 

  • Morgan ES, Havelka OK, Lochhead YR (2007) Cosmetic nanotechnology: polymers and colloids in cosmetics; ACS Symposium Series 961, vol 961. American Chemical Society, Washington DC

    Book  Google Scholar 

  • Munteanu F-D, Dinca N, Cavaco-Paulo A (2008) MALDI–TOF mass spectrometry in textile industry. In: Popescu C, Zamfir AD, Dinca N (eds) Applications of mass spectrometry in life safety. NATO Science for Peace and Security Series A: Chemistry and Biology. Springer, Dordrecht, pp 193–203

  • Naeem M, Wajid M, Lee K, Leal SM, Ahmad W (2006) A mutation in the hair matrix and cuticle keratin KRTHB5 gene causes ectodermal dysplasia of hair and nail type. J Med Genet 43(3):274–279. doi:https://doi.org/10.1136/jmg.2005.033381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Regismond STA, Heng Y-M, Goddard ED, FoM W (1999) Fluorescence microscopy observation of the adsorption onto hair of a fluorescently labeled cationic cellulose ether. Langmuir 15(8):3007–3010. doi:https://doi.org/10.1021/la9811665

    Article  CAS  Google Scholar 

  • Richardson K, Schilling M, Pocalyko J, Bailey L (1996) Covalent bonding of active agents to skin, hair or nails. United States Patent 5490980, 09/28/1994

  • Rogers MA, Winter H, Schweizer J, Langbein L, Praetzel S, Moll I, Krieg T (1997) Sequences and differential expression of three novel human type-II hair keratins. Differentiation 61(3):187–194

    Article  CAS  PubMed  Google Scholar 

  • Saito G, Swanson JA, Lee K-D (2003) Drug delivery strategy utilizing conjugation via reversible disulphide linkages: role and site of cellular reducing activities. Adv Drug Deliver Rev 55(2):199–215

    Article  CAS  Google Scholar 

  • Schueller R, Romanowski P (1998) The science of reactive hair-care products. Cosmet Toiletries 113:39–44

    Google Scholar 

  • Sierpinski P, Garrett J, Ma J, Apel P, Klorig D, Smith T, Koman LA, Atala A, Van Dyke M (2008) The use of keratin biomaterials derived from human hair for the promotion of rapid regeneration of peripheral nerves. Biomaterials 29(1):118–128

    Article  CAS  PubMed  Google Scholar 

  • Soltzberg LJ, Hagar A, Kridaratikorn S, Mattson A, Newman R (2007) MALDI–TOF Mass spectrometric identification of dyes and pigments. J Am Soc Mass Spectrom 18(11):2001–2006

    Article  CAS  PubMed  Google Scholar 

  • Spencer SD, Raffa RB (2004) Isothermal titration calorimetric study of RNase-A kinetics (cCMP → 3′-CMP) involving end-product inhibition. Pharm Res 21(9):1642–1647. doi:https://doi.org/10.1023/B:PHAM.0000041460.78128.0f

    Article  CAS  PubMed  Google Scholar 

  • Tachibana A, Kaneko S, Tanabe T, Yamauchi K (2005) Rapid fabrication of keratin-hydroxyapatite hybrid sponges toward osteoblast cultivation and differentiation. Biomaterials 26(3):297–302

    Article  CAS  PubMed  Google Scholar 

  • Tanabe T, Okitsu N, Yamauchi K (2004) Fabrication and characterization of chemically crosslinked keratin films. Mater Sci Eng C 24(3):441–446

    Article  CAS  Google Scholar 

  • Vasconcelos A, Freddi G, Cavaco-Paulo A (2008) Biodegradable materials based on silk fibroin and keratin. Biomacromolecules 9(4):1299–1305

    Article  CAS  PubMed  Google Scholar 

  • Walker KW, Lyles MM, Gilbert HF (1996) Catalysis of oxidative protein folding by mutants of protein disulphide isomerase with a single active-site cysteine. Biochemistry-US 35(6):1972–1980

    Article  CAS  Google Scholar 

  • Wang C-C, Tsou C-L (1998) Enzymes as chaperones and chaperones as enzymes. FEBS Lett 425(3):382–384

    Article  CAS  PubMed  Google Scholar 

  • Wilkerson VA (1935) The chemistry of human epidermis. J Biol Chem 112:329–359

    CAS  Google Scholar 

  • Wilkinson B, Gilbert HF (2004) Protein disulphide isomerase. Biochim Biophys Acta 1699(1–2):35–44

    Article  CAS  PubMed  Google Scholar 

  • Wilson RH, Lewis HB (1927) The cystine content of hair and other epidermal tissues. J Biol Chem 73(2):543–553

    CAS  Google Scholar 

  • Wolfram LJ (2003) Human hair: A unique physicochemical composite. J Am Acad Dermatol 48:S106–S114

    Article  PubMed  Google Scholar 

  • Wysocki AP, Mann GV, Stare FJ (1954) The cystine and methionine content of the hair of malnourished children. Am J Clin Nutr 2(4):243–245

    Article  CAS  PubMed  Google Scholar 

  • Xiao R, Lundstrom-Ljung J, Holmgren A, Gilbert HF (2005) Catalysis of thiol/disulphide Exchange: glutaredoxin 1 and protein-disulphide isomerase use different mechanisms to enhance oxidase and reductase activities. J Biol Chem 280(22):21099–21106. doi:https://doi.org/10.1074/jbc.M411476200

    Article  CAS  PubMed  Google Scholar 

  • Zviak C, Milléquant J (2005) Hair bleaching. In: Bouilon C, Wilkinson J (eds) The science of hair care, 2nd edn. CRC, Boca Raton, pp 246–268

    Google Scholar 

Download references

Acknowledgment

We thank to FCT “Fundação para a Ciência e Tecnologia” (scholarship SFRH/BD/38363/2007) for providing Margarida Fernandes the grant for PhD studies.

Author information

Authors and Affiliations

  1. Center of Textile Engineering, University of Minho, Campus of Azurém, 4800-058, Guimarães, Portugal

    Margarida M. Fernandes, Andreia Vasconcelos & Artur Cavaco-Paulo

  2. Department of Biology, Centre of Molecular and Environmental Biology (CBMA), Campus of Gualtar, University of Minho, 4710-057, Braga, Portugal

    Andreia C. Gomes

  3. Faculty of Food Engineering, Tourism and Environmental Protection, University Aurel Vlaicu of Arad, No. 2, 310330, Arad, Romania

    Florentina-Daniela Munteanu

  4. Group of Molecular and Industrial Biotechnology, EUETIT, Technical University of Catalonia, Colom 1, 8222, Terrassa, Barcelona, Spain

    Tzanko Tzanov

  5. Department of Chemistry, Campus of Gualtar, University of Minho, 4710-057, Braga, Portugal

    Maria Sameiro T. Gonçalves

  6. Ciba Inc. (part of BASF), WRO-1059.6.14, 4002, Basel, Switzerland

    Nicole End & Kai-Uwe Schoening

  7. Department of Environmental Biotechnology, Graz University of Technology, Graz, Austria

    Georg M. Guebitz

Authors
  1. Margarida M. Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreia C. Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreia Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florentina-Daniela Munteanu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tzanko Tzanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Sameiro T. Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicole End
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kai-Uwe Schoening
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Georg M. Guebitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Artur Cavaco-Paulo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Artur Cavaco-Paulo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernandes, M.M., Gomes, A.C., Vasconcelos, A. et al. Protein disulphide isomerase-assisted functionalization of keratin-based matrices. Appl Microbiol Biotechnol 90, 1311–1321 (2011). https://doi.org/10.1007/s00253-011-3194-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3194-6

Keywords

Search

Navigation