Skip to main content
SpringerLink
Log in

Quartz crystal microbalance, a valuable tool for elucidation of interactions between apoB-100 peptides and extracellular matrix components

  • Paper in Forefront
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Atherosclerosis has received wide attention as a primary cause of premature death in developed countries. The retention of low-density lipoprotein (LDL) particles in the intima, the inner layer of the capillaries, has been imputed as the main cause of the development of atherosclerotic plaques. The entrapment of LDL is mainly due to the specific interaction between the lysine-rich site on apolipoprotein B-100 (apoB-100), a major apolipoprotein of LDL, and extracellular matrix (ECM) components such as collagen, proteoglycans, and glycosaminoglycans (GAGs). Although valuable techniques already exist for studies on apoB-100 and ECM interactions, there is continued need for miniaturized tools that can complement the tools already available and even provide totally new data. This work explores the applicability of the quartz crystal microbalance (QCM) for interaction studies between apoB-100 peptide fragments and various components of the ECM. Two positive peptide fragments, PP and PP2, and two components of the ECM, collagen I and a selected GAG, chondroitin 6-sulfate (C6S), were immobilized on polystyrene and carboxyl sensor chips. C6S was injected as analyte for PP- and PP2-coated surfaces, while PP was the analyte for collagen I and C6S surfaces. The estimated dissociation constant (K D) indicates that the interactions occur via the positive residues, lysine and arginine, of apoB-100. The continuous-flow QCM system employed in this study is shown to be an excellent tool for the elucidation of interactions between these types of biomolecules.

Binding of PP to a C6S aldehyde coupled carboxyl crystal. PP concentrations ranged from 50 to 250 µg/mL. Running buffer: PBS pH 7.4. Flow rate: 25 µL/min. Experiments were carried out at room temperature

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

Similar content being viewed by others

References

  1. Biggerstaff KD, Wooten JS (2004) Understanding lipoproteins as transporters of cholesterol and other lipids. ADV Physiol Educ 28:105–106

    Article  Google Scholar 

  2. Castellani WJ (2004) Metabolic and nutritional aspects of the atherogenic atypical lipoproteins: lipoprotein(a), remnant lipoproteins, and oxidized low-density lipoprotein. Nutr Res 24:681–693

    Article  CAS  Google Scholar 

  3. Hevonoja T, Pentikäinen MO, Hyvönen MT, Kovanen PT, Ala-Korpela M (2000) Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim Biophys Acta 1488:189–210

    CAS  Google Scholar 

  4. Yang C-Y, Chen S-H, Gianturco SH, Bradley WA, Sparrow JT, Tanimura M, Li W-H, Sparrow DA, Deloof H, Rosseneu M, Lee F-S, Gu Z-W, Gotto AM Jr, Chan L (1986) Sequence, structure, receptor-binding domains and internal repeats of human apolipoprotein B-100. Nature 323:738–742

    Article  CAS  Google Scholar 

  5. Segrest JP, Jones MK, De Loof H, Dashti N (2001) Structure of apolipoprotein B-100 in low density lipoproteins. J Lipid Res 42:1346–1367

    CAS  Google Scholar 

  6. Wight TN (1989) Cell biology of arterial proteoglycans. Arteriosclerosis 9:1–20

    CAS  Google Scholar 

  7. Skålén K, Gustafsson M, Rydberg EK, Hultén LM, Wiklund O, Innerarity TL, Borén J (2002) Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 417:750–754

    Article  Google Scholar 

  8. Kadler KE, Holmes DF, Trotter JA, Chapman JA (1996) Collagen fibril formation. Biochem J 316:1–11

    CAS  Google Scholar 

  9. Chan VC, Ramshaw JAM, Kirkpatrick A, Beck K, Brodsky B (1997) Positional preferences of ionizable residues in Gly-X-Y triplets of the collagen triple-helix. J Biol Chem 272:31441–31446

    Article  CAS  Google Scholar 

  10. Kovanen PT, Pentikäinen M (1999) Decorin links low-density lipoproteins (LDL) to collagen: a novel mechanism for retention of LDL in the atherosclerotic plaque. Trends Cardiovasc Med 9:86–91

    Article  CAS  Google Scholar 

  11. Pentikäinen MO, Öörni K, Lassila R, Kovanen PT (1997) The proteoglycan decorin links low density lipoproteins with collagen type I. J Biol Chem 272:7633–7638

    Article  Google Scholar 

  12. Albertini R, Moratti R, De Luca G (2002) Oxidation of low-density lipoprotein in atherosclerosis from basic biochemistry to clinical studies. Curr Mol Med 2:579–592

    Article  CAS  Google Scholar 

  13. Öörni K, Pentikäinen MO, Ala-Korpela M, Kovanen PT (2000) Aggregation, fusion, and vescicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 41:1703–1714

    Google Scholar 

  14. D’Ulivo L, Yohannes G, Öörni K, Kovanen PT, Riekkola M-L (2007) Open tubular capillary electrochromatography: a new technique for in situ enzymatic modification of low density lipoprotein particles and their protein-free derivatives. Analyst 132:989–996

    Article  Google Scholar 

  15. Borén J, Olin K, Lee I, Chait A, Wight TN, Innerarity TL (1998) Identification of the principal proteoglycan-binding site in LDL. J Clin Invest 101:2658–2664

    Article  Google Scholar 

  16. Olsson U, Camejo G, Bondjers G (1993) Binding of a synthetic apolipoprotein B-100 peptide and peptide analogs to chondroitin 6-sulfate: effects of the lipid environment. Biochemistry 32:1858–1865

    Article  CAS  Google Scholar 

  17. Boren J, Lee I, Zhu W, Arnold K, Taylor S, Innerarity TL (1998) Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J Clin Invest 101:1084–1093

    Article  CAS  Google Scholar 

  18. Camejo G, Olofsson S-O, Lopez F, Carlsson P, Bondjers G (1988) Identification of Apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arterioscler Thromb Vasc Biol 8:368–377

    CAS  Google Scholar 

  19. Camejo G, Hurt-Camejo E, Wiklund O, Bondjers G (1998) Association of apo B lipoproteins with arterial proteoglycans: pathological significance and molecular basis. Atherosclerosis 139:205–222

    Article  CAS  Google Scholar 

  20. Iverius P-H (1972) The interaction between human plasma lipoproteins and connective tissue glycosaminoglycans. J Biol Chem 247:2607–2613

    CAS  Google Scholar 

  21. D’Ulivo L, Witos J, Öörni K, Kovanen PT, Riekkola M-L (2009) Capillary electrochromatography: a tool for mimicking collagen surface interactions with apolipoprotein B-100 peptides. Electrophoresis 30:3838–3845

    Article  Google Scholar 

  22. Marx KA (2003) Quartz crystal microbalance: a useful tool for studying thin polymer films and complex biomolecular systems at the solution–surface interface. Biomacromolecules 4:1099–1120

    Article  CAS  Google Scholar 

  23. Pei Z, Larsson R, Aastrup T, Anderson H, Lehn J-M, Ramström O (2006) Quartz crystal microbalance bioaffinity sensor for rapid identification of glycosyldisulfide lectin inhibitors from a dynamic combinatorial library. Biosens Bioelectron 22:42–48

    Article  CAS  Google Scholar 

  24. Pei Y, Yu H, Pei Z, Theurer M, Ammer C, Andr S, Gabius H-J, Yan M, Ramström O (2007) Photoderivatized polymer thin films at quartz crystal microbalance surfaces: sensors for carbohydrate–protein interactions. Anal Chem 79:6897–6902

    Article  CAS  Google Scholar 

  25. Kuldvee R, D’Ulivo L, Yohannes G, Lindenburg PW, Laine M, Öörni K, Kovanen P, Riekkola M-L (2006) Open tubular capillary electrochromatography: technique for oxidation and interaction studies on human low-density lipoproteins. Anal Chem 78:2665–2671

    Article  CAS  Google Scholar 

  26. Ruiz-Jiménez J, Kuldvee R, Chen J, Öörni K, Kovanen P, Riekkola M-L (2007) Open tubular CE for in vitro oxidation studies of human very-low-density lipoprotein particles. Electrophoresis 28:779–788

    Article  Google Scholar 

  27. Vainikka K, Chen J, Metso J, Jauhiainen M, Riekkola M-L (2007) Coating of open tubular capillaries with discoidal and spherical high-density lipoprotein particles in electrochromatography. Electrophoresis 28:2267–2274

    Article  CAS  Google Scholar 

  28. Pei Z, Anderson H, Aastrup T, Ramström O (2005) Study of real-time lectin-carbohydrate interactions on the surface of a quartz crystal microbalance. Biosens Bioelectron 21:60

    Article  CAS  Google Scholar 

  29. Jacquemart I, Pamula E, De Cupere VM, Rouxhet PG, Dupont-Gillain CC (2004) Nanostructured collagen layers obtained by adsorption and drying. J Colloid Interface Sci 278:63–70

    Article  CAS  Google Scholar 

  30. Elliot JT, Halter M, Plant AL, Woodward JT, Langenbach KJ, Tona A (2008) Evaluating the performance of fibrillar collagen films formed at polystyrene surfaces as cell culture substrates. Biointerphases 3:19–28

    Article  Google Scholar 

  31. Myszka DG, Morton TA (1998) Clamp: a biosensor kinetic data analysis program. Trends Biochem. Sci 23:149–150

    Article  CAS  Google Scholar 

  32. Muratsugu M, Ohta F, Miya Y, Hosokawa T, Kurosawa S, Kamo N, Ikeda H (1993) Quartz crystal microbalance for the detection of microgram quantities of human serum albumin: relationship between the frequency change and the mass of protein adsorbed. Anal Chem 65:2933–2937

    Article  CAS  Google Scholar 

  33. Sauerbrey G (1959) The use of quartz crystal oscillators for weighing thin layers and for micro-weighing. Z Phys 155:206–222

    Article  CAS  Google Scholar 

  34. Melles E, Anderson H, Wallinder D, Shafqat J, Bergman T, Aastrup T, Jörnvall H (2005) Electroimmobilization of proinsulin C-peptide to a quartz crystal microbalance sensor chip for protein affinity purification. Anal Biochem 341:89–93

    Article  CAS  Google Scholar 

  35. Godber B, Thompson KSJ, Rehak M, Uludag Y, Kelling S, Sleptsov A, Frogley M, Wiehler K, Whalen C, Cooper MA (2005) Direct quantification of analyte concentration by resonant acoustic profiling. Clin Chem 51:1962–1972

    Article  CAS  Google Scholar 

  36. Anderson H, Jönsson M, Vestling L, Lindberg U, Aastrup T (2007) Quartz crystal microbalance sensor design I. Experimental study of sensor response and performance. Sens Actuators B Chem 123:27–34

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Teodor Aastrup from Attana AB, Stockholm, Sweden and to Professor Petri T. Kovanen and Dr. Katariina Öörni from Wihuri Research Institute, Helsinki, Finland for valuable discussions and comments. Financial support was provided by CHEMSEM Graduate School (L.D.), the Research Council for Natural Sciences and Engineering, the Academy of Finland under grants 116288 (M.-L.R. and L.D.), and a Research Grant from the University of Helsinki (M.-L.R).

Author information

Authors and Affiliations

  1. Laboratory of Analytical Chemistry, Department of Chemistry, University of Helsinki, P. O. Box 55, 00014, Helsinki, Finland

    Lucia D’Ulivo & Marja-Liisa Riekkola

  2. Attana AB, Björnnäsvägen 21, 114 19, Stockholm, Sweden

    Julien Saint-Guirons & Björn Ingemarsson

Authors
  1. Lucia D’Ulivo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julien Saint-Guirons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Björn Ingemarsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marja-Liisa Riekkola
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marja-Liisa Riekkola.

Rights and permissions

Reprints and permissions

About this article

Cite this article

D’Ulivo, L., Saint-Guirons, J., Ingemarsson, B. et al. Quartz crystal microbalance, a valuable tool for elucidation of interactions between apoB-100 peptides and extracellular matrix components. Anal Bioanal Chem 396, 1373–1380 (2010). https://doi.org/10.1007/s00216-009-3371-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-009-3371-y

Keywords

Search

Navigation