Non-invasive monitoring of cell metabolism and lipid production in 3D engineered human adipose tissues using label-free multiphoton microscopy

Biomaterials

Volumn 34, Issue 34, 2013, Pages 8607-8616

  Chang, Tyler ^a   Zimmerley, Maxwell S ^b   Quinn, Kyle P ^a   Lamarre Jouenne, Isabelle ^b   Kaplan, David L ^a   Beaurepaire, Emmanuel ^b   Georgakoudi, Irene ^a,b  

^a Tufts University   (United States)

^b LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

Author keywords

Adipogenic differentiation; Lipid droplets; Redox ratio; Stem cell metabolism; Third harmonic generation; Two photon excited fluorescence

Indexed keywords

ADIPOGENIC DIFFERENTIATIONS; CELL METABOLISM; LIPID DROPLETS; REDOX RATIO; THIRD-HARMONIC GENERATION; TWO-PHOTON EXCITED FLUORESCENCE;

CYTOLOGY; DROPS; EXCITED STATES; FLUORESCENCE; HARMONIC GENERATION; HISTOLOGY; METABOLISM; PHOTONS; STEM CELLS; TISSUE;

SCAFFOLDS (BIOLOGY);

BIOLOGICAL MARKER; FAT DROPLET; FATTY ACID; FLAVINE ADENINE NUCLEOTIDE; LIPID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SILK; TISSUE SCAFFOLD;

ADIPOGENESIS; ADIPOGENIC DIFFERENTIATION MEDIA; ADIPOSE TISSUE; ANALYTIC METHOD; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CELL VOLUME; CONTRAST; CONTROLLED STUDY; CULTURE MEDIUM; FATTY ACID SYNTHESIS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; LABELING INDEX; LIPID STORAGE; LIPOGENESIS; MESENCHYMAL STEM CELL; MICROSCOPY; MOLECULAR DYNAMICS; MULTIPHOTON MICROSCOPY; NON INVASIVE PROCEDURE; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROPAGATION MEDIUM; QUANTITATIVE ANALYSIS; THIRD HARMONIC GENERATION; TISSUE ENGINEERING;

ADIPOGENIC DIFFERENTIATION; LIPID DROPLETS; REDOX RATIO; STEM CELL METABOLISM; THIRD-HARMONIC GENERATION; TWO-PHOTON EXCITED FLUORESCENCE;

ADIPOSE TISSUE; CELL DIFFERENTIATION; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIPID METABOLISM; MESENCHYMAL STROMAL CELLS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; OXIDATION-REDUCTION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84882810000     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.07.066     Document Type: Article

References (50)

1. Kershaw E., Flier J. Adipose tissue as an endocrine organ. JClin Endocrinol Metab 2004, 80(6):2548-2556.
2. Ren J., Pulakat L., Whaley-Connell A., Sowers J. Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. JMol Med 2010, 88:993-1001.
3. Guilherme A., Virbasius J.V., Puri V., Czech M.P. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 2008, 9:367-377.
4. Greenberg A.S., Coleman R.A., Kraemer F.B., McManaman J.L., Obin M.S., Puri V., et al. The role of lipid droplets in metabolic disease in rodents and humans. JClin Invest 2011, 121(6):2102-2110.
5. Rice W.L., Kaplan D.L., Georgakoudi I. Quantitative biomarkers of stem cell differentiation based on intrinsic two-photon excited fluorescence. JBiomed Opt 2007, 12(6):060504.
6. Rice W.L., Kaplan D.L., Georgakoudi I. Two-photon microscopy for non-invasive, quantitative monitoring of stem cell differentiation. PLoS One 2010, 5(4):e10075. 10.1371/journal.pone.0010075.
7. Georgakoudi I., Rice W.L., Hronik-Tupaj M., Kaplan D.L. Optical spectroscopy and imaging for the noninvasive evaluation of engineered tissues. Tissue Eng Part B Rev 2008, 14(4):321-340.
8. Georgakoudi I., Quinn K.P. Optical imaging using endogenous contrast to assess metabolic state. Annu Rev Biomed Eng 2012, 14:351-367.
9. Stringari C., Sierra R., Donovan P.J., Gratton E. Label-free separation of human embryonic stem cells and their differentiating progenies by phasor fluorescence lifetime microscopy. JBiomed Opt 2012, 17(4):046012.
10. Quinn K.P., Bellas E., Fourligas N., Lee K., Kaplan D.L., Georgakoudi I. Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios. Biomaterials 2012, 33:5341-5348.
11. Vinegoni C., Ralston T., Tan W., Luo W., Marks D.L., Boppart S.A. Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy. Appl Phys Lett 2006, 88(5).
12. König K., Uchugonova A. Two-photon autofluorescence and second-harmonic imaging of adult stem cells. JBiomed Opt 2008, 13(5):054068.
13. Yannas I.V., Tzeranis D.S., Harley B.A., So P.T.C. Biologically active collagen-based scaffolds: advances in processing and characterization. Philos Trans A Math Phys Eng Sci 2010, 368(1917):2123-2139.
14. Kim J.K., Kim U.J., Leisk G.G., Bayan C., Georgakoudi I., Kaplan D.L. Bone regeneration on macroporous aqueous-derived silk 3-D scaffolds. Macromol Biosci 2007, 7:643-655.
15. Wilson B.C., Vitkin I.A., Matthews D.L. The potential of biophotonic techniques in stem cell tracking and monitoring of tissue regeneration applied to cardiac stem cell therapy. JBiophotonics 2009, 11:669-681.
16. Débarre D., Supatto W., Pena A.M., Fabre A., Tordjmann T., Combettes L., et al. Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy. Nat Methods 2006, 3(1):47-53.
17. Chu S.W., Chen S.Y., Tsai T.H., Liu T.M., Lin C.Y., Tsai H.J., et al. Invivo developmental biology study using noninvasive multi-harmonic generation microscopy. Opt Express 2003, 11(23):3093-3098.
18. Brackmann C., Norbeck J., Akson M., Bosch D., Larsson C., Gustafsson L., et al. CARS microscopy of lipid stores in yeast: the impact of nutritional state and genetic background. JRaman Spectrosc 2009, 40:748-756.
19. Brackmann C., Bodin A., Akeson M., Gatenholm P., Enejder A. Visualization of the cellulose biosynthesis and cell integration into cellulose scaffolds. Biomacromolecules 2010, 11:542-548.
20. Le T.T., Cheng J.X. Single-cell profiling reveals the origin of phenotypic variability in adipogenesis. PloS One 2009, 4:e5189.
21. Slipchenko M.N., Le T.T., Chen H., Cheng J.X. High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy. JPhys Chem B 2009, 113:7681-7686.
22. Palero J.A., de Bruijn H.S., van der Ploeg van den Heuvel A., Sterenborg H.J., Gerritsen H.C. Spectrally resolved multiphoton imaging of invivo and excised mouse skin tissues. Biophys J 2007, 93:992-1007.
23. Zipfel W.R., Williams R.M., Webb W.W. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 2003, 21(11):1369-1377.
24. Skala M.C., Riching K.M., Gendron-Fitzpatrick A., Eickhoff J., Eliceiri K., White J.G., et al. Invivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc Natl Acad Sci U S A 2007, 104(49):19494-19499.
25. Xylas J., Quinn K.P., Hunter M., Georgakoudi I. Improved Fourier-based characterization of intracellular fractal features. Opt Express 2012, 20(21):23442-23455.
26. Levitt J., Hunter M., Mujat C., McLaughlin-Drubin M., Münger K., Georgakoudi I. Diagnostic cellular organization features extracted from autofluorescence images. Opt Lett 2007, 32(22):3305-3307.
27. Levitt J.M., McLaughlin-Drubin M.E., Münger K., Georgakoudi I. Automated biochemical, morphological, and organizational assessment of precancerous changes from endogenous two-photon fluorescence images. PloS One 2011, 6(9):e24765.
28. Wright B.K., Andrews L.M., Markham J., Jones M.R., Stringari C., Digman M.A., et al. NADH distribution in live progenitor stem cells by phasor-fluorescence lifetime image microscopy. Biophys J 2012, 103:L7-L9.
29. Gratton E., Breusegem S., Sutin J., Ruan Q., Barry N. Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods. JBiomed Opt 2003, 8(3):381-390.
30. Konig K., Uchugonova A., Gorjup E. Multiphoton fluorescence lifetime imaging of 3D-stem cell spheroids during differentiation. Microsc Res Tech 2011, 74:9-17.
31. Barad Y., Eisenberg H., Horowitz M., Silberberg Y. Nonlinear scanning laser microscopy by third harmonic generation. Appl Phys Lett 1997, 70(8):922-924.
32. Oron D., Yelin D., Tal E., Raz S., Fachima R., Silberberg Y. Depth-resolved structural imaging by third-harmonic generation microscopy. JStruct Biol 2004, 147:3-11.
33. Débarre D., Supatto W., Farge E., Moulia B., Schanne-Klein M.C., Beaurepaire E. Velocimetric third-harmonic generation microscopy: micrometer-scale quantification of morphogenetic movements in unstained embryos. Opt Lett 2004, 29(24):2881-2883.
34. Tai S.P., Lee W.J., Shieh D.B., Wu P.C., Huang H.Y., Yu C.H., et al. Invivo optical biopsy of hamster oral cavity with epi-third-harmonic-generation microscopy. Opt Express 2006, 14(13):6178-6187.
35. Olivier N., Luengo-Oroz M.A., Duloquin L., Faure E., Savy T., Veilleux I., et al. Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science 2010, 329(5994):967-971.
36. Witte Stefan, Negrean Adrian, Lodder Johannes C., De Kock Christiaan P.J., Testa Silva Guilherme, Mansvelder Huibert D., et al. Label-free live brain imaging and targeted patching with third-harmonic generation microscopy. Proc Natl Acad Sci U S A 2011, 108(15):5970-5975.
37. Débarre D., Beaurepaire E. Quantitative characterization of biological liquids for third-harmonic generation microscopy. Biophys J 2007, 92(2):603-612.
38. Farrar M.J., Wise F.W., Fetcho J.R., Schaffer C. Invivo imaging of myelin in the vertebrate central nervous system using third-harmonic generation microscopy. Biophys J 2011, 100(5):1362-1371.
39. Zimmerley M., Mahou P., Débarre D., Schanne-Klein M.C., Beaurepaire E. Probing ordered lipid assemblies with polarized third-harmonic generation microscopy. Phys Rev X 2013, 3:011002.
40. Aptel F., Olivier N., Deniset-Besseau A., Legeais J.M., Plamann K., Schanne-Klein M.C., et al. Multimodal nonlinear imaging of the human cornea. Invest Opthalmol Vis Sci 2010, 51(5):2459-2465.
41. Mahou P., Zimmerley M., Loulier K., Matho K.S., Labroille G., Morin X., et al. Multicolor two-photon tissue imaging by wavelength mixing. Nat Methods 2012, 9:815-818.
42. Bellas E., Panilaitis B.J.B., Glettig D.L., Kirker-Head C.A., Yoo J.J., Marra K.G., et al. Sustained volume retention invivo with adipocyte and lipoaspirate seeded silk scaffolds. Biomaterials 2013, 34:2960-2968.
43. Mauney J.R., Nguyen T., Gillen K., Kirker-Head C., Gimble J.M., Kaplan D.L. Engineering adipose-like tissue invitro and invivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials 2007, 28:5280-5290.
44. Chen H., Slipchenko M.N., Zhu J., Buhman K.K., Cheng J.X. Coupling CARS with multiphoton fluorescence and high harmonic generation imaging modalities using a femtosecond laser source. Proc SPIE 2009, 7183:718315.
45. Wilson-Fritch L., Nicoloro S., Chouinard M., Lazar M.A., Chui P.C., Leszyk J., et al. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. JClin Invest 2004, 114(9):1281-1289.
46. Murphy D.J., Vance J. Mechanisms of lipid-body formation. Trends Biochem Sci 1999, 24(3):109-115.
47. Martin S., Parton R.G. Lipid droplets: a unified view of a dynamic organelle. Nat Rev Mol Cell Biol 2006, 7:373-378.
48. Walther T.C., Farese R.V. The life of lipid droplets. Biochim Biophys Acta 2009, 1791(6):459-466.
49. Romeo S., Kozlitina J., Xing C., Pertsemlidis A., Cox D., Pennacchio L.A., et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 2008, 40:1461-1465.
50. Bozza P.T., Viola J.P.B. Lipid droplets in inflammation and cancer. Prostaglandins Leukot Essent Fatty Acids 2010, 82(4-6):243-250.