Noninvasive quantification of in vitro osteoblastic differentiation in 3D engineered tissue constructs using spectral ultrasound imaging

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Gudur, Madhu Sudhan Reddy ^a   Rao, Rameshwar R ^a   Peterson, Alexis W ^a   Caldwell, David J ^a   Stegemann, Jan P ^a   Deng, Cheri X ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COLLAGEN;

ACOUSTIC IMPEDANCE; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; B SCAN; CELL COUNT; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; DNA CONTENT; IMAGE ANALYSIS; IMAGE DISPLAY; IMAGING AND DISPLAY; MOUSE; NONHUMAN; OSTEOBLAST; QUANTITATIVE ANALYSIS; SPECTRAL ULTRASOUND IMAGING; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING; 3T3 CELL LINE; ANIMAL; BONE DEVELOPMENT; CELL SURVIVAL; CULTURE TECHNIQUE; CYTOLOGY; DEVICES; ECHOGRAPHY; METABOLISM; PROCEDURES; REPRODUCIBILITY; TIME;

3T3 CELLS; ANIMALS; CALCIUM; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SIZE; CELL SURVIVAL; COLLAGEN; MICE; OSTEOBLASTS; OSTEOGENESIS; REPRODUCIBILITY OF RESULTS; TIME FACTORS; TISSUE ENGINEERING;

EID: 84899835051     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085749     Document Type: Article

References (40)

1. Langer R, Vacanti JP (1993) Tissue Engineering. Science 260: 920-926.
2. Yang SY, Hsiung SK, Hung YC, Chang CM, Liao TL, et al. (2006) A cell counting/sorting system incorporated with a microfabricated flow cytometer chip. Measurement Science & Technology 17: 2001-2009.
3. Oliver MH, Harrison NK, Bishop JE, Cole PJ, Laurent GJ (1989) A Rapid and Convenient Assay for Counting Cells Cultured in Microwell Plates - Application for Assessment of Growth-Factors. Journal of Cell Science 92: 513-518. (Pubitemid 19083806)
4. Butler WB (1984) Preparing Nuclei from Cells in Monolayer-Cultures Suitable for Counting and for Following Synchronized Cells through the Cell-Cycle. Analytical Biochemistry 141: 70-73.
5. Han JW, Breckon TP, Randell DA, Landini G (2012) The application of support vector machine classification to detect cell nuclei for automated microscopy. Machine Vision and Applications 23: 15-24.
6. Ho KY, Hu HCH, Keyak JH, Colletti PM, Powers CM (2013) Measuring bone mineral density with fat-water MRI: comparison with computed tomography. Journal of Magnetic Resonance Imaging 37: 237-242.
7. Nazarian A, Snyder BD, Zurakowski D, Muller R (2008) Quantitative microcomputed tomography: A non-invasive method to assess equivalent bone mineral density. Bone 43: 302-311.
8. Jones AC, Milthorpe B, Averdunk H, Limaye A, Senden TJ, et al. (2004) Analysis of 3D bone ingrowth into polymer scaffolds via micro-computed tomography imaging. Biomaterials 25: 4947-4954. (Pubitemid 38520825)
9. Oe K, Miwa M, Nagamune K, Sakai Y, Lee SY, et al. (2010) Nondestructive evaluation of cell numbers in bone marrow stromal cell/beta-tricalcium phosphate composites using ultrasound. Tissue Engineering Part C-Methods 16: 347-353.
10. Fite BZ, Decaris M, Sun YH, Sun Y, Lam A, et al. (2011) Noninvasive multimodal evaluation of bioengineered cartilage constructs combining time-resolved fluorescence and ultrasound imaging. Tissue Engineering Part C-Methods 17: 495-504.
11. Kreitz S, Dohmen G, Hasken S, Schmitz-Rode T, Mela P, et al. (2011) Nondestructive method to evaluate the collagen content of fibrin-based tissue engineered structures via ultrasound. Tissue Engineering Part C-Methods 17: 1021-1026.
12. Walker JM, Myers AM, Schluchter MD, Goldberg VM, Caplan AI, et al. (2011) Nondestructive evaluation of hydrogel mechanical properties using ultrasound. Annals of Biomedical Engineering 39: 2521-2530.
13. Tunis AS, Czarnota GJ, Giles A, Sherar MD, Hunt JW, et al. (2005) Monitoring structural changes in cells with high-frequency ultrasound signal statistics. Ultrasound in Medicine and Biology 31: 1041-1049. (Pubitemid 41115846)
14. Lizzi FL, Ostromogilsky M, Feleppa EJ, Rorke MC, Yaremko MM (1987) Relationship of ultrasonic spectral parameters to features of tissue microstructure. Ieee Transactions on Ultrasonics Ferroelectrics and Frequency Control 34: 319-329. (Pubitemid 17582514)
15. Lizzi FL, Astor M, Liu T, Deng C, Coleman DJ, et al. (1997) Ultrasonic spectrum analysis for tissue assays and therapy evaluation. International Journal of Imaging Systems and Technology 8: 3-10. (Pubitemid 127549455)
16. Nair A, Kuban BD, Tuzcu EM, Schoenhagen P, Nissen SE, et al. (2002) Coronary plaque classification with intravascular ultrasound radiofrequency data analysis. Circulation 106: 2200-2206. (Pubitemid 35222213)
17. Qian J, Maehara A, Mintz GS, Margolis MP, Lerman A, et al. (2009) Impact of Gender and Age on In Vivo Virtual Histology-Intravascular Ultrasound Imaging Plaque Characterization (from the global Virtual Histology Intravascular Ultrasound [VH-IVUS] Registry). American Journal of Cardiology 103: 1210-1214.
18. Gudur MSR, Kumon RE, Zhou Y, Deng CX (2012) High-Frequency Rapid B-Mode Ultrasound Imaging for Real-Time Monitoring of Lesion Formation and Gas Body Activity During High-Intensity Focused Ultrasound Ablation. Ieee Transactions on Ultrasonics Ferroelectrics and Frequency Control 59: 1687-1699.
19. Kumon RE, Gudur MSR, Zhou Y, Deng CX (2012) High-Frequency Ultrasound M-Mode Imaging for Identifying Lesion and Bubble Activity during High-Intensity Focused Ultrasound Ablation. Ultrasound in Medicine and Biology 38: 626-641.
20. Siebers S, Schwabe M, Scheipers U, Welp C, Werner J, et al. (2004) Evaluation of ultrasonic texture and spectral parameters for coagulated tissue characterization. 2004 IEEE Ultrasonics Symposium, Vols 1-3: 1804-1807.
21. Feleppa EJ (2008) Ultrasonic tissue-type imaging of the prostate: Implications for biopsy and treatment guidance. Cancer Biomarkers 4: 201-212.
22. Oelze ML, O'Brien WD, Blue JP, Zachary JF (2004) Differentiation and characterization of rat mammary fibroadenomas and 4T1 mouse carcinomas using quantitative ultrasound imaging. Ieee Transactions on Medical Imaging 23: 764-771.
23. Vlad RM, Alajez NM, Giles A, Kolios MC, Czarnota GJ (2008) Quantitative Ultrasound Characterization of Cancer Radiotherapy Effects in Vitro. International Journal of Radiation Oncology Biology Physics 72: 1236-1243.
24. Lizzi FL (1997) Ultrasonic scatterer property images of the eye and prostate. 1997 Ieee Ultrasonics Symposium Proceedings, Vols 1 & 2: 1109-1117.
25. Lizzi FL, Feleppa EJ, Alam SK, Deng CX (2003) Ultrasonic spectrum analysis for tissue evaluation. Pattern Recognition Letters 24: 637-658. (Pubitemid 35326791)
26. Kumon RE, Repaka A, Atkinson M, Faulx AL, Wong RCK, et al. (2012) Characterization of the pancreas in vivo using EUS spectrum analysis with electronic array echoendoscopes. Gastrointestinal Endoscopy 75: 1175-1183.
27. Kumon RE, Deng CX, Wang XD (2011) Frequency-Domain Analysis of Photoacoustic Imaging Data from Prostate Adenocarcinoma Tumors in a Murine Model. Ultrasound in Medicine and Biology 37: 834-839.
28. Insana MF, Wagner RF, Brown DG, Hall TJ (1990) Describing Small-Scale Structure in Random-Media Using Pulse-Echo Ultrasound. Journal of the Acoustical Society of America 87: 179-192. (Pubitemid 20090722)
29. Kolios MC, Czarnota GJ, Lee M, Hunt JW, Sherar MD (2002) Ultrasonic spectral parameter characterization of apoptosis. Ultrasound in Medicine and Biology 28: 589-597. (Pubitemid 34665417)
30. Czarnota GJ, Kolios MC, Abraham J, Portnoy M, Ottensmeyer FP, et al. (1999) Ultrasound imaging of apoptosis: high-resolution non-invasive monitoring of programmed cell death in vitro, in situ and in vivo. British Journal of Cancer 81: 520-527. (Pubitemid 29458808)
31. Gudur M, Rao RR, Hsiao YS, Peterson AW, Deng CX, et al. (2012) Noninvasive, Quantitative, Spatiotemporal Characterization of Mineralization in Three-Dimensional Collagen Hydrogels Using High-Resolution Spectral Ultrasound Imaging. Tissue Engineering Part C-Methods 18: 935-946.
32. Czekanska EM, Stoddart MJ, Richards RG, Hayes JS (2012) In Search of an Osteoblast Cell Model for in Vitro Research. European Cells & Materials 24: 1-17.
33. Al-Munajjed AA, Plunkett NA, Gleeson JP, Weber T, Jungreuthmayer C, et al. (2009) Development of a Biomimetic Collagen-Hydroxyapatite Scaffold for Bone Tissue Engineering Using a SBF Immersion Technique. Journal of Biomedical Materials Research Part B-Applied Biomaterials 90B: 584-591.
34. Rao RR, Peterson AW, Ceccarelli J, Putnam AJ, Stegemann JP (2012) Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15: 253-264.
35. Rao RR, Peterson AW, Stegemann JP (2013) Winner for outstanding research in the Ph.D. category for the 2013 Society for Biomaterials meeting and exposition, April 10-13, 2013, Boston, Massachusetts: Osteogenic differentiation of adipose-derived and marrow-derived mesenchymal stem cells in modular protein/ceramic microbeads. J Biomed Mater Res A 101: 1531-1538.
36. Declerq HA, Verbeeck RMH, De Ridder LIFJM, Schacht EH, Cornelissen MJ (2005) Calcification as an indicator of osteoinductive capacity of biomaterials in osteoblastic cell cultures. Biomaterials 26: 4964-4974. (Pubitemid 40357686)
37. Wakatsuki T, Elson EL (2003) Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs. Biophysical Chemistry 100: 593-605. (Pubitemid 36338068)
38. Dembo M, Wang YL (1999) Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophysical Journal 76: 2307-2316. (Pubitemid 29266384)
39. Galbraith CG, Sheetz MP (1997) A micromachined device provides a new bend on fibroblast traction forces. Proceedings of the National Academy of Sciences of the United States of America 94: 9114-9118. (Pubitemid 27357791)
40. Zscharnack M, Hepp P, Richter R, Aigner T, Schulz R, et al. (2010) Repair of Chronic Osteochondral Defects Using Predifferentiated Mesenchymal Stem Cells in an Ovine Model. American Journal of Sports Medicine 38: 1857-1869.