In vitro labeling of hydroxyapatite minerals by an engineered protein

Biotechnology and Bioengineering

Volumn 108, Issue 5, 2011, Pages 1021-1030

  Yuca, Esra ^a,b,c   Karatas, Ayten Yazgan ^a   Seker, Urartu Ozgur Safak ^a   Gungormus, Mustafa ^c   Dinler Doganay, Gizem ^a   Sarikaya, Mehmet ^a,c   Tamerler, Candan ^a,c  

^a ISTANBUL TECHNICAL UNIVERSITY   (Turkey)

^b YILDIZ TECHNICAL UNIVERSITY   (Turkey)

^c University of Washington   (United States)

Author keywords

Green fluorescent protein; Hydroxyapatite binding peptides; Inorganic surfaces; Mineralization; Mineralized tissues; Nanobiotechnology

Indexed keywords

ADVANCED MATERIALS; ALKALINE PHOSPHATASE; BINDING ACTIVITIES; BINDING PEPTIDE; BIO-IMAGING; BIOLOGICAL PROCESS; BIOMIMETIC SYNTHESIS; CELL-FREE; FLUORESCENCE LABELING; FUNCTIONAL PROTEINS; FUSION PROTEINS; GREEN FLUORESCENCE PROTEINS; GREEN FLUORESCENT PROTEIN; GREEN PROCESSING; IN-VITRO; INORGANIC SURFACES; INORGANICS; MINERALIZATION; MINERALIZED TISSUE; MOLECULAR PROBES; NUCLEOTIDE SEQUENCES; OPEN READING FRAME; PHOSPHATE RELEASE; TIME POINTS;

APATITE; BIOMIMETIC MATERIALS; BIOMIMETICS; BIOMINERALIZATION; CALCIUM; ESCHERICHIA COLI; FLUORESCENCE; FLUORESCENCE MICROSCOPY; HISTOLOGY; HYDROXYAPATITE; MINERALOGY; MINERALS; PEPTIDES; PHOSPHATASES; PHOSPHATE MINERALS; QUARTZ; SILICATE MINERALS; SYNTHESIS (CHEMICAL); TISSUE; TISSUE ENGINEERING; VISUALIZATION;

CALCIUM PHOSPHATE;

ALKALINE PHOSPHATASE; CALCIUM PHOSPHATE; DNA; DNA FRAGMENT; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN HYDROXYAPATITE BINDING PEPTIDE FUSION PROTEIN 1; GREEN FLUORESCENT PROTEIN HYDROXYAPATITE BINDING PEPTIDE FUSION PROTEIN 2; HYBRID PROTEIN; HYDROXYAPATITE; PEPTIDE DERIVATIVE; POLYHISTIDINE TAG; UNCLASSIFIED DRUG;

ARTICLE; BIOMIMETICS; BIOMINERALIZATION; CIRCULAR DICHROISM; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE AMPLIFICATION; HUMAN; HUMAN TISSUE; INCISOR; MOLECULAR PROBE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; QUARTZ CRYSTAL MICROBALANCE;

BASE SEQUENCE; DNA PRIMERS; DURAPATITE; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; OPEN READING FRAMES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, SECONDARY;

ESCHERICHIA COLI;

EID: 79953136776     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23041     Document Type: Article

References (54)

1. Addadi L, Weiner S. 1985. Interactions between acidic proteins and crystals-Stereochemical requirements in biomineralization. Proc Natl Acad Sci USA 82(12): 4110-4114.
2. Alivisatos AP, Gu WW, Larabell C. 2005. Quantum dots as cellular probes. Annu Rev Biomed Eng 7: 55-76.
3. Boonekamp PM, Vanderweepals LJA, Vanwijkvanlennep MML, Thesing CW, Bijvoet OLM. 1986. 2 Modes of action of bisphosphonates on osteoclastic resorption of mineralized matrix. J Bone Miner Res 1(1): 27-39.
4. Braux J, Guillaume C, Jallot E, Nedelec JM, Laurent-Maquin D, Laquerriere P. 2009. Effect of Strontium treatment on human primary osteoblasts. hydroxyapatite: A drug delivery system? Int J Artif Organs 32(7): 458-458.
5. Brown S, Sarikaya M, Johnson E. 2000. A genetic analysis of crystal growth. J Mol Biol 299(3): 725-735.
6. Chudakov DM, Lukyanov S, Lukyanov KA. 2005. Fluorescent proteins as a toolkit for in vivo imaging. Trends Biotechnol 23(12): 605-613.
7. Dai HX, Choe WS, Thai CK, Sarikaya M, Traxler BA, Baneyx F, Schwartz DT. 2005. Nonequilibrium synthesis and assembly of hybrid inorganic-protein nanostructures using an engineered DNA binding protein. J Am Chem Soc 127(44): 15637-15643.
8. Dash AK, Cudworth GC. 1998. Therapeutic applications of implantable drug delivery systems. J Pharmacol Toxicol Methods 40(1): 1-12.
9. 3+-doped hydroxyapatite for biomedical applications as fluorescent probes. J Mater Sci 42(7): 2236-2243.
10. Dickerson MB, Jones SE, Cai Y, Ahmad G, Naik RR, Kroger N, Sandhage KH. 2008. Identification and design of peptides for the rapid, high-yield formation of nanoparticulate TiO2 from aqueous solutions at room temperature. Chem Mater 20(4): 1578-1584.
11. Gaskin DJH, Starck K, Vulfson EN. 2000. Identification of inorganic crystal-specific sequences using phage display combinatorial library of short peptides: A feasibility study. Biotechnol Lett 22(15): 1211-1216.
12. Gungormus M, Fong H, Kim IW, Evans JS, Tamerler C, Sarikaya M. 2008. Regulation of in vitro calcium phosphate mineralization by combinatorially selected hydroxyapatite-binding peptides. Biomacromolecules 9(3): 966-973.
13. Guo Y, Shi DL, Lian J, Dong ZY, Wang W, Cho HS, Liu GK, Wang LM, Ewing RC. 2008. Quantum dot conjugated hydroxylapatite nanoparticles for in vivo imaging. Nanotechnology 19(17). 6.
14. Hardman R. 2006. A toxicologic review of quantum dots: Toxicity depends on physicochemical and environmental factors. Environ Health Perspect 114(2): 165-172.
15. Hnilova M, Oren EE, Seker UOS, Wilson BR, Collino S, Evans JS, Tamerler C, Sarikaya M. 2008. Effect of molecular conformations on the adsorption behavior of gold-binding peptides. Langmuir 24(21): 12440-12445.
16. Hoffman RM. 2002. Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models. Lancet Oncol 3(9): 546-556.
17. Hsieh MF, Li JKJ, Lin CAJ, Huang SH, Sperling RA, Parak WJ, Chang WH. 2009. Tracking of cellular uptake of hydrophilic CdSe/ZnS quantum Dots/Hydroxyapatite composites nanoparticles in MC3T3-E1 osteoblast cells. J Nanosci Nanotechnol 9(4): 2758-2762.
18. Huang Y, Chiang CY, Lee SK, Gao Y, Hu EL, De Yoreo J, Belcher AM. 2005. Programmable assembly of nanoarchitectures using genetically engineered viruses. Nano Lett 5(7): 1429-1434.
19. Ishii M, Kunimura JS, Jeng HT, Vessoni Penna TC, Cholewa O. 2007. Evaluation of the pH- and thermal stability of the recombinant green fluorescent protein (GFP) in the presence of sodium chloride. Appl Biochem Biotechnol 137: 555-571.
20. Kacar T, Ray J, Gungormus M, Oren EE, Tamerler C, Sarikaya M. 2009a. Quartz binding peptides as molecular linkers towards fabricating multifunctional micropatterned substrates. Adv Mater 21(3): 295-299.
21. Kacar T, Zin MT, So C, Wilson B, Ma H, Gul-Karaguler N, Jen AKY, Sarikaya M, Tamerler C. 2009b. Directed self-immobilization of alkaline phosphatase on micro-patterned substrates via genetically fused metal-binding peptide. Biotechnol Bioeng 103(4): 696-705.
22. Kasaj A, Willershausen B, Reichert C, Gortan-Kasaj A, Zafiropoulos GG, Schmidt M. 2008. Human periodontal fibroblast response to a nanostructured hydroxyapatite bone replacement graft in vitro. Arch Oral Biol 53(7): 683-689.
23. Kramer RM, Li C, Carter DC, Stone MO, Naik RR. 2004. Engineered protein cages for nanomaterial synthesis. J Am Chem Soc 126(41): 13282-13286.
24. Krauland EM, Peelle BR, Wittrup KD, Belcher AM. 2007. Peptide tags for enhanced cellular and protein adhesion to single-crystal line sapphire. Biotechnol Bioeng 97(5): 1009-1020.
25. Lee SW, Mao CB, Flynn CE, Belcher AM. 2002. Ordering of quantum dots using genetically engineered viruses. Science 296(5569): 892-895.
26. Lipman H. 1935. Staining the skeleton of cleared embryos with Alizarin red S. stain. Biotech Histochem 10(2): 61-63.
27. Lippincott-Schwartz J, Patterson GH. 2003. Development and use of fluorescent protein markers in living cells. Science 300(5616): 87-91.
28. Liu TY, Chen SY, Liu DM, Liou SC. 2005. On the study of BSA-loaded calcium-deficient hydroxyapatite nano-carriers for controlled drug delivery. J Control Release 107(1): 112-121.
29. Lowenstam HA. 1981. Minerals formed by organisms. Science 211(4487): 1126-1131.
30. Ma MY, Zhu YJ, Li L, Cao SW. 2008. Nanostructured porous hollow ellipsoidal capsules of hydroxyapatite and calcium silicate: Preparation and application in drug delivery. J Mater Chem 18(23): 2722-2727.
31. Meloan S, Puchtler H. 1985. Chemical mechanisms of staining methods: von Kossas technique. What von Kossa really wrote and a modified reaction for selective demonstration of inorganic phosphate. J Histotechnol 8: 11-13.
32. Miyawaki A, Nagai T, Mizuno H. 2005. Engineering fluorescent proteins Adv Biochem Eng Biotechnol 95: 1-15.
33. Naik RR, Stringer SJ, Agarwal G, Jones SE, Stone MO. 2002. Biomimetic synthesis and patterning of silver nanoparticles. Nat Mater 1(3): 169-172.
34. Nam KT, Lee YJ, Krauland EM, Kottmann ST, Belcher AM. 2008. Peptide-mediated reduction of silver ions on engineered biological scaffolds. ACS Nano 2(7): 1480-1486.
35. Oh SH, Finones RR, Daraio C, Chen LH, Jin SH. 2005. Growth of nano-scale hydroxyapatite using chemically treated titanium oxide nanotubes. Biomaterials 26(24): 4938-4943.
36. Oren EE, Tamerler C, Sahin D, Hnilova M, Seker UOS, Sarikaya M, Samudrala R. 2007. A novel knowledge-based approach to design inorganic-binding peptides. Bioinformatics 23(21): 2816-2822.
37. Park TJ, Hyun MS, Lee HJ, Lee SY, Ko S. 2009. A self-assembled fusion protein-based surface plasmon resonance biosensor for rapid diagnosis of severe acute respiratory syndrome. Talanta 79(2): 295-301.
38. Roy MD, Stanley SK, Amis EJ, Becker ML. 2008. Identification of a highly specific hydroxyapatite-binding peptide using phage display. Adv Mater 20(10): 1830-1836.
39. Sano KI, Shiba K. 2003. A hexapeptide motif that electrostatically binds to the surface of titanium. J Am Chem Soc 125(47): 14234-14235.
40. Sano KI, Sasaki H, Shiba K. 2005. Specificity and biomineralization activities of Ti-binding peptide-1 (TBP-1). Langmuir 21(7): 3090-3095.
41. Seker UOS, Wilson B, Dincer S, Kim IW, Oren EE, Evans JS, Tamerler C, Sarikaya M. 2007. Adsorption behavior of linear and cyclic genetically engineered platinum binding peptides. Langmuir 23(15): 7895-7900.
42. Tamerler C, Duman M, Oren EE, Gungormus M, Xiong XR, Kacar T, Parviz BA, Sarikaya M. 2006. Materials specificity and directed assembly of a gold-binding peptide. Small 2(11): 1372-1378.
43. Tamerler C, Kacar T, Sahin D, Fong H, Sarikaya M. 2007. Genetically engineered polypeptides for inorganics: A utility in biological materials science and engineering. Mater Sci Eng C 27(3): 558-564.
44. Tan K, Cheang P, Ho IAW, Lam PYP, Hui KM. 2007. Nanosized bioceramic particles could function as efficient gene delivery vehicles with target specificity for the spleen. Gene Ther 14(10): 828-835.
45. Thai CK, Dai HX, Sastry MSR, Sarikaya M, Schwartz DT, Baneyx F. 2004. Identification and characterization of Cu2O- and ZnO-binding polypeptides by Escherichia coli cell surface display: Toward an understanding of metal oxide binding. Biotechnol Bioeng 87(2): 129-137.
46. Wang HX, Nakata E, Hamachi I. 2009. Recent progress in strategies for the creation of protein-based fluorescent biosensors. Chembiochem 10(16): 2560-2577.
47. Weiger MC, Park JJ, Roy MD, Stafford CM, Karim A, Becker ML. 2010. Quantification of the binding affinity of a specific hydroxyapatite binding peptide. Biomaterials 31(11): 2955-2963.
48. Weinstein RS, Roberson PK, Manolagas SC. 2009. Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360(1): 53-62.
49. Whaley SR, English DS, Hu EL, Barbara PF, Belcher AM. 2000. Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405(6787): 665-668.
50. Wiedenmann J, Oswald F, Nienhaus GU. 2009. Fluorescent proteins for live cell imaging: Opportunities, limitations, and challenges. IUBMB Life 61(11): 1029-1042.
51. Yang P, Quan Z, Li C, Kang X, Lian H, Lin J. 2008. Bioactive, luminescent and mesoporous europium-doped hydroxyapatite as a drug carrier. Biomaterials 29(32): 4341-4347.
52. Zaheer A, Lenkinski RE, Mahmood A, Jones AG, Cantley LC, Frangioni JV. 2001. In vivo near-infrared fluorescence imaging of osteoblastic activity. Nature Biotechnol 19(12): 1148-1154.
53. Zhang Y, Yuan Y, Liu CS. 2008. Fluorescent labeling of nanometer hydroxyapatite. J Mater Sci Technol 24(2): 187-191.
54. Zimmer M. 2002. Green fluorescent protein (GFP): Applications, structure, and related photophysical behavior. Chem Rev 102(3): 759-781.