Abstract

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-κB 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.

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  39. H. M. Al-Qadin, M. Lin, M. A. Al-Holy, A. G. Cavinato, and B. A. RascoDetection 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.200873M5461
  40. I. Notingher, G. Jell, P. L. Notingher, I. Bisson, O. Tsigkou, J. M. Polak, M. M. Stevens, and L. L. HenchMultivariate analysis of Raman spectra for in vitro non-invasive studies of living cellsJ. Mol. Struct.2005744-747179185
  41. C. M. BishopPattern Recognition and Machine LearningSpringer2006

Other (41)

G. A. Rodan and T. J. MartinTherapeutic approaches to bone diseasesScience200028915081514

W. J. Boyle, W. S. Simonet, and D. L. LaceyOsteoclast differentiation and activationNature2003423337342

T. Wada, T. Nakashima, N. Hiroshi, and J. M. PenningerRANKL-RANK signaling in osteoclastogenesis and bone diseaseTrends. Mol. Med.2006121725

G. D. Roodman, K. J. Ibbotson, B. R. MacKonald, T. J. Kuehl, and G. R. Mundy1,25-Dihydroxyvitamin D3 causes formation of multinucleated cells with several osteoclast characteristics in cultures of primate marrowProc. Natl. Acad. Sci. USA.19858282138217

F. Arai, T. Miyamoto, O. Ohneda, T. Inada, T. Sudo, K. Brasel, T. Miyata, D. M. Anderson, and T. SudaCommitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptorsJ. Exp. Med.199919017411754

S. L. TeitelbaumBone resorption by osteoclastsScience200028915041508

B. R. Wong, R. Josien, and Y. ChoiTRANCE is a TNF family member that regulates dendritic cell and osteoclast functionJ. Leukoc. Biol.199965715724

N. J. Panetta, D. M. Gupta, N. Quarto, and M. T. LongakerMesenchymal cells for skeletal tissue engineeringPanminerva Medica.2009512541

M. T. Cheng, H. W. Yang, T. H. Chen, and O. K. S. LeeModulation of proliferation and differentiation of human anterior cruciate ligament-derived stem cells by different growth factorsTissue Engineering Part A.20091539793989

Y. R. V. Shih, C. N. Chen, S. W. Tsai, Y. J. Wang, and O. K. LeeGrowth of mesenchymal stem cells on electrospun type I collagen nanofibersStem Cells20062423912397

J. Alock and V. SottileDynamic distribution and stem cell characteristics of Sox1-expressing cells in the cerebellar cortexCell Res.20091913241333

J. Lin, R. Chen, S. Feng, J. Pan, B. Li, G. Chen, S. Lin, C. Li, L. Sun, and Z. HuangSurface-enhanced Raman scattering spectroscopy for potential noninvasive nasopharyngeal cancer detectionJ. Raman Spectrosc.201243497502

M. M. Mariani, P. J. Day, and V. DeckertApplications of modern micro-Raman spectroscopy for cell analysesIntegr. Biol.2010294101

S. Dochow, C. Kra, U. Neugebauer, T. Bocklitz, T. Henkel, G. Mayer, J. Albert, and J. PoppTumour cell identificationby means of Raman spectroscopy in combination withoptical traps and microfluidic environmentsLab Chip.20111114841490

W. A. El-Said, T. H. Kim, H. C. Kim, and J. W. ChoiAnalysis of intracellular state based on controlled 3D nanostructures mediated surface enhanced Raman scatteringPLOS ONE20116e15836

S. Feng, R. Chen, J. Lin, J. Pan, Y. Wu, Y. Li, J. Chen, and H. ZengGastric cancer detection based on blood plasma surface-enhanced Raman spectroscopy excited by polarized laser lightBiosens. Bioelectron.20112631673174

J. Lin, R. Chen, S. Feng, J. Pan, Y. Li, G. Chen, M. Cheng, Z. Huang, Y. Yu, and H. ZengA novel blood plasma analysis technique combining membrane electrophoresis with silver nanoparticle-based SERS spectroscopy for potential applications in noninvasive cancer detectionNanomedicine20117655663

I. Notingher, J. Selvakumaran, and L. L. HenchNew detection system for toxic agents based on continuous spectroscopic monitoring of living cellsBiosens. Bioelectron.200420780789

L. L. McManus, G. A. Burke, M. M. McCafferty, P. O’Hare, M. Modreanu, A. R. Boyd, and B. J. MeenanRaman spectroscopic monitoring of the osteogenic differentiation of human mesenchymal stem cellsAnalyst201113624712481

I. Notingher, I. Bisson, A. E. Bishop, W. L. Randle, J. M. Polak, and L. L. HenchIn situ spectral monitoring of mRNA translation in embryonic stem cells during differentiation in vitroAnal. Chem.20047631853193

H. G. Schulze, S. O. Konorov, N. J. Caron, J. M. Piret, M. W. Blades, and R. F. B. TurnerAssessing differentiation status of human embryonic stem cells noninvasively using Raman microspectroscopyAnal. Chem.20108250205027

F. C. Pascut, T. G. Huey, N. Welch, L. D. Buttery, C. Denning, and I. NotingherNoninvasive detection and imaging of molecular markers in live cardiomyocytes derived from human embryonic stem cellsBiophys. J.2011100251259

S. O. Konorov, G. Schulze, J. M. Piret, R. F. B. Turner, and M. W. BladesEvidence of marked glycogen variations in the characteristic Raman signatures of human embryonic stem cellsJ. Raman Spectrosc.20114211351141

P. S. Hung, Y. C. Kuo, H. G. Chen, H. H. K. Chiang, and O. K. S. LeeDetection of osteogenic differentiation by differential mineralized matrix production in mesenchymal stromal cells by Raman spectroscopyPLOS ONE20138e65438

M. Xu, D. Fujita, K. Onishi, and K. MiyazawaImproving accuracy of sample surface topography by atomic force microscopyJ. Nanosci. Nanotechnol.2009960036007

G. J. Lee, S. Choi, J. Chon, S. Yoo, I. Cho, and H. K. ParkChanges in collagen fibril pattern and adhesion force with collagenase-induced injury in rat Achilles tendon observed via AFMJ. Nanosci. Nanotechnol.201111773777

W. A. Lam, M. J. Rosenbluth, and D. A. FletcherChemotherapy exposure increases leukemia cell stiffnessBlood200710935053508

G. Binnig, C. F. Quate, and C. GerberAtomic force microscopePhys. Rev. Lett.198656930933

S. S. Schaus and E. R. HendersonCell viability and probe-cell membrane interactions of XR1 glial cells imaged by atomic force microscopyBiophys. J.19977312051214

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-SusoVibrational spectroscopy differentiates between multipotent and pluripotent stem cellsAnalyst201013531263132

E. Gazi, J. Dwyer, N. P. Lockyer, J. Miyan, P. Gardner, C. Hart, M. Brown, and N. W. ClarkeFixation protocols for subcellular imaging by synchrotron-based Fourier transform infrared microspectroscopyBiopolymers2005771830

A. D. Meade, F. M. Lyng, P. Knief, and H. J. BymeGrowth substrate induced functional changes elucidated by FTIR and Raman spectroscopy in in-vitro cultured human keratinocytesAnal. Bional. Chem.200738717171728

M. Q. Hu, J. Wang, J. Y. Cai, Y. Z. Wu, and X. P. WangAnalysis of sodium benzoate biotoxicity using atomic force microscopeChin. J. Biotechnol.20082414281432

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. BakerAtomic force microscopy study of early morphological changes during apoptosisLangmuir20052192809286

D. J. Taatjes, B. E. Sobel, and R. C. BuddMorphological and cytochemical determination of cell death by apoptosisHistochem. Cell. Biol.20081293343

Q. Matthews, A. Jirasek, J. Lum, X. Duan, and A. G. BroloVariability in Raman spectra of single human tumor cells cultured in vitro: correlation with cell cycle and culture confluencyAppl. Spectrosc.201064871887

J. W. Chan, D. S. Taylor, T. Zwerdling, S. M. Lane, K. Ihara, and T. HuserMicro-Raman spectroscopy detects individual neoplastic and normal hematopoietic cellsBiophys. J.200690648656

G. B. Jung, Y. J. Lee, G. H. Lee, and H. K. ParkA simple and rapid detection of tissue adhesive-induced biochemical changes in cells and DNA using Raman spectroscopyOpt. Express2013426732682

H. M. Al-Qadin, M. Lin, M. A. Al-Holy, A. G. Cavinato, and B. A. RascoDetection 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.200873M5461

I. Notingher, G. Jell, P. L. Notingher, I. Bisson, O. Tsigkou, J. M. Polak, M. M. Stevens, and L. L. HenchMultivariate analysis of Raman spectra for in vitro non-invasive studies of living cellsJ. Mol. Struct.2005744-747179185

C. M. BishopPattern Recognition and Machine LearningSpringer2006

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