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Label-free Noninvasive Characterization of Osteoclast Differentiation Using Raman Spectroscopy Coupled with Multivariate Analysis

  • Jung, Gyeong Bok (Department of Physics Education, Chosun University) ;
  • Kang, In Soon (Department of Pharmacology, Inha University School of Medicine) ;
  • Lee, Young Ju (Department of Biomedical Engineering & Healthcare Industry Research Institute, College of Medicine, Kyung Hee University) ;
  • Kim, Dohyun (Department of Industrial and Management Engineering, Myongji University) ;
  • Park, Hun-Kuk (Department of Biomedical Engineering & Healthcare Industry Research Institute, College of Medicine, Kyung Hee University) ;
  • Lee, Gi-Ja (Department of Biomedical Engineering & Healthcare Industry Research Institute, College of Medicine, Kyung Hee University) ;
  • Kim, Chaekyun (Department of Pharmacology, Inha University School of Medicine)
  • 투고 : 2016.12.22
  • 심사 : 2017.06.27
  • 발행 : 2017.08.25

초록

Multinucleated bone resorptive osteoclasts differentiate from bone marrow-derived monocyte/macrophage precursor cells. During osteoclast differentiation, mononuclear pre-osteoclasts change their morphology and biochemical characteristics. In this study, Raman spectroscopy with multivariate techniques such as Principal Component Analysis (PCA) and Linear Discriminant Analysis (LDA) were used to extract biochemical information related to various cellular events during osteoclastogenesis. This technique allowed for label-free and noninvasive monitoring of differentiating cells, and clearly discriminated four different time points during osteoclast differentiation. The Raman band intensity showed significant time-dependent changes that increased up to day 4. The results of Raman spectroscopy agreed with results from atomic force microscopy (AFM) and tartrate-resistant acid phosphatase (TRAP) staining, a conventional biological assay. Under AFM, normal spindle-like mononuclear pre-osteoclasts became round and smaller at day 2 after treatment with a receptor activator of nuclear $factor-{\kappa}B$ ligand and they formed multinucleated giant cells at day 4. Thus, Raman spectroscopy, in combination with PCA-LDA, may be useful for noninvasive label-free quality assessment of cell status during osteoclast differentiation, enabling more efficient optimization of the bioprocesses.

키워드

참고문헌

  1. G. A. Rodan and T. J. Martin, "Therapeutic approaches to bone diseases," Science 289, 1508-1514 (2000). https://doi.org/10.1126/science.289.5484.1508
  2. W. J. Boyle, W. S. Simonet, and D. L. Lacey, "Osteoclast differentiation and activation," Nature 423, 337-342 (2003). https://doi.org/10.1038/nature01658
  3. T. Wada, T. Nakashima, N. Hiroshi, and J. M. Penninger, "RANKL-RANK signaling in osteoclastogenesis and bone disease," Trends. Mol. Med. 12, 17-25 (2006). https://doi.org/10.1016/j.molmed.2005.11.007
  4. G. D. Roodman, K. J. Ibbotson, B. R. MacKonald, T. J. Kuehl, and G. R. Mundy, "1,25-Dihydroxyvitamin D3 causes formation of multinucleated cells with several osteoclast characteristics in cultures of primate marrow," Proc. Natl. Acad. Sci. USA. 82, 8213-8217 (1985). https://doi.org/10.1073/pnas.82.23.8213
  5. F. Arai, T. Miyamoto, O. Ohneda, T. Inada, T. Sudo, K. Brasel, T. Miyata, D. M. Anderson, and T. Suda, "Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors," J. Exp. Med. 190, 1741-1754 (1999). https://doi.org/10.1084/jem.190.12.1741
  6. S. L. Teitelbaum, "Bone resorption by osteoclasts," Science 289, 1504-1508 (2000). https://doi.org/10.1126/science.289.5484.1504
  7. B. R. Wong, R. Josien, and Y. Choi, "TRANCE is a TNF family member that regulates dendritic cell and osteoclast function," J. Leukoc. Biol. 65, 715-724 (1999). https://doi.org/10.1002/jlb.65.6.715
  8. N. J. Panetta, D. M. Gupta, N. Quarto, and M. T. Longaker, "Mesenchymal cells for skeletal tissue engineering," Panminerva Medica. 51, 25-41 (2009).
  9. M. T. Cheng, H. W. Yang, T. H. Chen, and O. K. S. Lee, "Modulation of proliferation and differentiation of human anterior cruciate ligament-derived stem cells by different growth factors," Tissue Engineering Part A. 15, 3979-3989 (2009). https://doi.org/10.1089/ten.tea.2009.0172
  10. Y. R. V. Shih, C. N. Chen, S. W. Tsai, Y. J. Wang, and O. K. Lee, "Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells," 24, 2391-2397 (2006). https://doi.org/10.1634/stemcells.2006-0253
  11. J. Alock and V. Sottile, "Dynamic distribution and stem cell characteristics of Sox1-expressing cells in the cerebellar cortex," Cell Res. 19, 1324-1333 (2009). https://doi.org/10.1038/cr.2009.119
  12. J. Lin, R. Chen, S. Feng, J. Pan, B. Li, G. Chen, S. Lin, C. Li, L. Sun, and Z. Huang, "Surface-enhanced Raman scattering spectroscopy for potential noninvasive nasopharyngeal cancer detection," J. Raman Spectrosc. 43, 497-502 (2012). https://doi.org/10.1002/jrs.3072
  13. M. M. Mariani, P. J. Day, and V. Deckert, "Applications of modern micro-Raman spectroscopy for cell analyses," Integr. Biol. 2, 94-101 (2010). https://doi.org/10.1039/b920572a
  14. S. Dochow, C. Kra, U. Neugebauer, T. Bocklitz, T. Henkel, G. Mayer, J. Albert, and J. Popp, "Tumour cell identification by means of Raman spectroscopy in combination with optical traps and microfluidic environments," Lab Chip. 11, 1484-1490 (2011). https://doi.org/10.1039/c0lc00612b
  15. W. A. El-Said, T. H. Kim, H. C. Kim, and J. W. Choi, "Analysis of intracellular state based on controlled 3D nanostructures mediated surface enhanced Raman scattering," PLOS ONE 6, e15836 (2011). https://doi.org/10.1371/journal.pone.0015836
  16. S. Feng, R. Chen, J. Lin, J. Pan, Y. Wu, Y. Li, J. Chen, and H. Zeng, "Gastric cancer detection based on blood plasma surface-enhanced Raman spectroscopy excited by polarized laser light," Biosens. Bioelectron. 26, 3167-3174 (2011). https://doi.org/10.1016/j.bios.2010.12.020
  17. J. Lin, R. Chen, S. Feng, J. Pan, Y. Li, G. Chen, M. Cheng, Z. Huang, Y. Yu, and H. Zeng, "A novel blood plasma analysis technique combining membrane electrophoresis with silver nanoparticle-based SERS spectroscopy for potential applications in noninvasive cancer detection," Nanomedicine 7, 655-663 (2011). https://doi.org/10.1016/j.nano.2011.01.012
  18. I. Notingher, J. Selvakumaran, and L. L. Hench, "New detection system for toxic agents based on continuous spectroscopic monitoring of living cells," Biosens. Bioelectron. 20, 780-789 (2004). https://doi.org/10.1016/j.bios.2004.04.008
  19. L. L. McManus, G. A. Burke, M. M. McCafferty, P. O'Hare, M. Modreanu, A. R. Boyd, and B. J. Meenan, "Raman spectroscopic monitoring of the osteogenic differentiation of human mesenchymal stem cells," Analyst 136, 2471-2481 (2011). https://doi.org/10.1039/c1an15167c
  20. I. Notingher, I. Bisson, A. E. Bishop, W. L. Randle, J. M. Polak, and L. L. Hench, "In situ spectral monitoring of mRNA translation in embryonic stem cells during differentiation in vitro," Anal. Chem. 76, 3185-3193 (2004). https://doi.org/10.1021/ac0498720
  21. H. G. Schulze, S. O. Konorov, N. J. Caron, J. M. Piret, M. W. Blades, and R. F. B. Turner, "Assessing differentiation status of human embryonic stem cells noninvasively using Raman microspectroscopy," Anal. Chem. 82, 5020-5027 (2010). https://doi.org/10.1021/ac902697q
  22. F. C. Pascut, T. G. Huey, N. Welch, L. D. Buttery, C. Denning, and I. Notingher, "Noninvasive detection and imaging of molecular markers in live cardiomyocytes derived from human embryonic stem cells," Biophys. J. 100, 251-259 (2011). https://doi.org/10.1016/j.bpj.2010.11.043
  23. S. O. Konorov, G. Schulze, J. M. Piret, R. F. B. Turner, and M. W. Blades, "Evidence of marked glycogen variations in the characteristic Raman signatures of human embryonic stem cells," J. Raman Spectrosc. 42, 1135-1141 (2011). https://doi.org/10.1002/jrs.2829
  24. P. S. Hung, Y. C. Kuo, H. G. Chen, H. H. K. Chiang, and O. K. S. Lee, "Detection of osteogenic differentiation by differential mineralized matrix production in mesenchymal stromal cells by Raman spectroscopy," PLOS ONE 8, e65438 (2013). https://doi.org/10.1371/journal.pone.0065438
  25. M. Xu, D. Fujita, K. Onishi, and K. Miyazawa, "Improving accuracy of sample surface topography by atomic force microscopy," J. Nanosci. Nanotechnol. 9, 6003-6007 (2009). https://doi.org/10.1166/jnn.2009.1232
  26. G. J. Lee, S. Choi, J. Chon, S. Yoo, I. Cho, and H. K. Park, "Changes in collagen fibril pattern and adhesion force with collagenase-induced injury in rat Achilles tendon observed via AFM," J. Nanosci. Nanotechnol. 11, 773-777 (2011). https://doi.org/10.1166/jnn.2011.3275
  27. W. A. Lam, M. J. Rosenbluth, and D. A. Fletcher, "Chemotherapy exposure increases leukemia cell stiffness," Blood 109, 3505-3508 (2007). https://doi.org/10.1182/blood-2006-08-043570
  28. G. Binnig, C. F. Quate, and C. Gerber, "Atomic force microscope," Phys. Rev. Lett. 56, 930-933 (1986). https://doi.org/10.1103/PhysRevLett.56.930
  29. S. S. Schaus and E. R. Henderson, "Cell viability and probecell membrane interactions of XR1 glial cells imaged by atomic force microscopy," Biophys. J. 73, 1205-1214 (1997). https://doi.org/10.1016/S0006-3495(97)78153-0
  30. J. K. Pijanka, K. Kumar, T. Dale, I. Yousef, G. Parkes, V. Untereiner, Y. Yang, P. Dumas, D. Collins, M. Manfait, G. D. Sockalingum, N. R. Forsyth, and J. Sule-Suso, "Vibrational spectroscopy differentiates between multipotent and pluripotent stem cells," Analyst 135, 3126-3132 (2010). https://doi.org/10.1039/c0an00525h
  31. E. Gazi, J. Dwyer, N. P. Lockyer, J. Miyan, P. Gardner, C. Hart, M. Brown, and N. W. Clarke, "Fixation protocols for subcellular imaging by synchrotron-based Fourier transform infrared microspectroscopy," Biopolymers 77, 18-30 (2005). https://doi.org/10.1002/bip.20167
  32. A. D. Meade, F. M. Lyng, P. Knief, and H. J. Byme, "Growth substrate induced functional changes elucidated by FTIR and Raman spectroscopy in in-vitro cultured human keratinocytes," Anal. Bional. Chem. 387, 1717-1728 (2007). https://doi.org/10.1007/s00216-006-0876-5
  33. M. Q. Hu, J. Wang, J. Y. Cai, Y. Z. Wu, and X. P. Wang, "Analysis of sodium benzoate biotoxicity using atomic force microscope," Chin. J. Biotechnol. 24, 1428-1432 (2008). https://doi.org/10.1016/S1872-2075(08)60064-3
  34. J. A. Hessler, A. Budor, K. Putchakayala, A. Mecke, D. Rieger, M. M. Banaszak Holl, B. G. Orr, A. Bielinska, J. Beals, and J. J. Baker, "Atomic force microscopy study of early morphological changes during apoptosis," Langmuir 21, 9280-9286 (2005). https://doi.org/10.1021/la051837g
  35. D. J. Taatjes, B. E. Sobel, and R. C. Budd, "Morphological and cytochemical determination of cell death by apoptosis," Histochem. Cell. Biol. 129, 33-43 (2008). https://doi.org/10.1007/s00418-007-0356-9
  36. Q. Matthews, A. Jirasek, J. Lum, X. Duan, and A. G. Brolo, "Variability in Raman spectra of single human tumor cells cultured in vitro: correlation with cell cycle and culture confluency," Appl. Spectrosc. 64, 871-887 (2010). https://doi.org/10.1366/000370210792080966
  37. J. W. Chan, D. S. Taylor, T. Zwerdling, S. M. Lane, K. Ihara, and T. Huser, "Micro-Raman spectroscopy detects individual neoplastic and normal hematopoietic cells," Biophys. J. 90, 648-656 (2006). https://doi.org/10.1529/biophysj.105.066761
  38. G. B. Jung, Y. J. Lee, G. H. Lee, and H. K. Park, "A simple and rapid detection of tissue adhesive-induced biochemical changes in cells and DNA using Raman spectroscopy," Opt. Express 4, 2673-2682 (2013). https://doi.org/10.1364/BOE.4.002673
  39. H. M. Al-Qadin, M. Lin, M. A. Al-Holy, A. G. Cavinato, and B. A. Rasco, "Detection of sublethal thermal injury in Salmonella enterica serotype typhimurium and Listeria monocytogenes using Fourier transform infrared (FT-IR) spectroscopy (4000 to 600 $cm^{-1}$)," J. Food. Sci. 73, M54-61 (2008). https://doi.org/10.1111/j.1750-3841.2007.00640.x
  40. I. Notingher, G. Jell, P. L. Notingher, I. Bisson, O. Tsigkou, J. M. Polak, M. M. Stevens, and L. L. Hench, "Multivariate analysis of Raman spectra for in vitro non-invasive studies of living cells," J. Mol. Struct. 744-747, 179-185 (2005). https://doi.org/10.1016/j.molstruc.2004.12.046
  41. C. M. Bishop, Pattern Recognition and Machine Learning (Springer, 2006).