Quantitative metabolic imaging using endogenous fluorescence to detect stem cell differentiation

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Quinn, Kyle P ^a   Sridharan, Gautham V ^a   Hayden, Rebecca S ^a   Kaplan, David L ^a   Lee, Kyongbum ^a   Georgakoudi, Irene ^a  

^a Tufts University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ADIPOGENESIS; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; FLUORESCENCE MICROSCOPY; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; METABOLOMICS; MITOCHONDRION; MOLECULAR IMAGING; OXIDATION REDUCTION REACTION; PROCEDURES; STEM CELL;

ADIPOGENESIS; CELL DIFFERENTIATION; FATTY ACIDS; HUMANS; MESENCHYMAL STROMAL CELLS; METABOLOMICS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MODELS, BIOLOGICAL; MOLECULAR IMAGING; NAD; OXIDATION-REDUCTION; STEM CELLS;

EID: 84890026443     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03432     Document Type: Article

References (52)

1. Berthiaume, F., Maguire, T. J. & Yarmush, M. L. Tissue engineering and regenerative medicine: history, progress, and challenges. Annu Rev Chem Biomol Eng 2, 403 (2011).
2. Guilak, F. et al. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5 (1), 17 (2009).
3. Kim, H. J., Kim, U. J., Vunjak-Novakovic, G., Min, B. H. & Kaplan, D. L. Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells. Biomaterials 26 (21), 4442 (2005).
4. Quinn, K. P. et al. Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios. Biomaterials 33 (21), 5341 (2012).
5. Stastna, M., Chimenti, I., Marban, E. & Van Eyk, J. E. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics 10 (2), 245 (2010).
6. Denk, W., Strickler, J.H. &Webb, W. W.Two-photon laser scanning fluorescence microscopy. Science 248 (4951), 73 (1990).
7. Georgakoudi, I. & Quinn, K. P. Optical Imaging Using Endogenous Contrast to Assess Metabolic State. Annu Rev Biomed Eng 14, 351 (2012).
8. Chance, B. & Thorell, B. Localization and kinetics of reduced pyridine nucleotide in living cells by microfluorometry. J Biol Chem 234, 3044 (1959).
9. Eng, J., Lynch, R. M. & Balaban, R. S. Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes. Biophys J 55 (4), 621 (1989).
10. Mayevsky, A. & Rogatsky, G. G. Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am J Physiol Cell Physiol 292 (2), C615 (2007).
11. Rocheleau, J.V., Head, W. S.&Piston, D.W.Quantitative NAD(P)H/flavoprotein autofluorescence imaging reveals metabolic mechanisms of pancreatic islet pyruvate response. J Biol Chem 279 (30), 31780 (2004).
12. Huang, S., Heikal, A. A. & Webb, W. W. Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. Biophys J 82 (5), 2811 (2002).
13. Chance, B., Schoener, B., Oshino, R., Itshak, F. & Nakase, Y. Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals. J Biol Chem 254 (11), 4764 (1979).
14. 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. J Biomed Opt 17 (4), 046012 (2012).
15. Kunz, W. S. & Kunz, W. Contribution of different enzymes to flavoprotein fluorescence of isolated rat liver mitochondria. Biochim Biophys Acta 841 (3), 237 (1985).
16. Chance, B., Mayevsky, A., Goodwin, C. & Mela, L. Factors in oxygen delivery to tissue. Microvasc Res 8 (3), 276 (1974).
17. Skala, M. C. et al. In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc Natl Acad Sci U S A 104 (49), 19494 (2007).
18. Rice, W. L., Kaplan, D. L. & Georgakoudi, I. Two-photon microscopy for non-invasive, quantitative monitoring of stem cell differentiation. PLoS One 5 (4), e10075 (2010).
19. Buschke, D. G., Squirrell, J. M., Fong, J. J., Eliceiri, K. W. & Ogle, B. M. Cell death, non-invasively assessed by intrinsic fluorescence intensity of NADH, is a predictive indicator of functional differentiation of embryonic stem cells. Biol Cell 104 (6), 352 (2012).
20. Stringari, C. et al. Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue. Proc Natl Acad Sci U S A 108 (33), 13582 (2011).
21. Konig, K., Uchugonova, A. & Gorjup, E. Multiphoton fluorescence lifetime imaging of 3D-stem cell spheroids during differentiation. Microsc Res Tech 74 (1), 9 (2011).
22. Folmes, C. D., Dzeja, P. P., Nelson, T. J. & Terzic, A. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11 (5), 596 (2012).
23. Varum, S. et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 6 (6), e20914 (2011).
24. Chen, C.T., Shih, Y.R., Kuo, T.K., Lee, O.K.& Wei, Y. H. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26 (4), 960 (2008).
25. Wilson-Fritch, L. et al. Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol Cell Biol 23 (3), 1085 (2003).
26. Xylas, J., Quinn, K. P., Hunter, M. & Georgakoudi, I. Improved Fourier-based characterization of intracellular fractal features. Optics Express 20 (21), 23442 (2012).
27. Si, Y., Shi, H. & Lee, K. Impact of perturbed pyruvate metabolism on adipocyte triglyceride accumulation. Metab Eng 11 (6), 382 (2009).
28. Saks, V. A. et al. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184 (1-2), 81 (1998).
29. Vishwasrao, H. D., Heikal, A. A., Kasischke, K. A. & Webb, W. W. Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy. J Biol Chem 280 (26), 25119 (2005).
30. Blinova, K. et al. Distribution of mitochondrial NADH fluorescence lifetimes: steady-state kinetics of matrix NADH interactions. Biochemistry 44 (7), 2585 (2005).
31. Guo, H. W. et al. Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies. J Biomed Opt 13 (5), 050505 (2008).
32. Blinova, K. et al. Mitochondrial NADH fluorescence is enhanced by complex I binding. Biochemistry 47 (36), 9636 (2008).
33. Vacanti, N. M. & Metallo, C. M. Exploring metabolic pathways that contribute to the stem cell phenotype. Biochim Biophys Acta (2012).
34. Vander Heiden, M. G., Cantley, L. C. & Thompson, C. B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324 (5930), 1029 (2009).
35. Trabold, O. et al. Lactate and oxygen constitute a fundamental regulatory mechanism in wound healing. Wound Repair Regen 11 (6), 504 (2003).
36. Ying, W. NAD1/NADH and NADP1/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10 (2), 179 (2008).
37. De Pauw, A., Tejerina, S., Raes, M., Keijer, J. & Arnould, T. Mitochondrial (dys)function in adipocyte (de)differentiation and systemic metabolic alterations. Am J Pathol 175 (3), 927 (2009).
38. Si, Y., Yoon, J. & Lee, K. Flux profile and modularity analysis of time-dependent metabolic changes of de novo adipocyte formation. Am J Physiol Endocrinol Metab 292 (6), E1637 (2007).
39. Manteiga, S., Choi, K., Jayaraman, A. & Lee, K. Systems biology of adipose tissue metabolism: regulation of growth, signaling and inflammation. Wiley Interdiscip Rev Syst Biol Med (2013).
40. Mitra, K., Rikhy, R., Lilly, M. & Lippincott-Schwartz, J. DRP1-dependent mitochondrial fission initiates follicle cell differentiation during Drosophila oogenesis. J Cell Biol 197 (4), 487 (2012).
41. Duguez, S., Feasson, L., Denis, C. & Freyssenet, D. Mitochondrial biogenesis during skeletal muscle regeneration. Am J Physiol Endocrinol Metab 282 (4), E802 (2002).
42. Rehman, J. Empowering self-renewal and differentiation: the role of mitochondria in stem cells. J Mol Med (Berl) 88 (10), 981 (2010).
43. Chen, C. T., Hsu, S. H. & Wei, Y. H. Mitochondrial bioenergetic function and metabolic plasticity in stem cell differentiation and cellular reprogramming. Biochim Biophys Acta 1820 (5), 571 (2012).
44. Ducluzeau, P. H. et al. Dynamic regulation of mitochondrial network and oxidative functions during 3T3-L1 fat cell differentiation. J Physiol Biochem 67 (3), 285 (2011).
45. Levitt, J. M., McLaughlin-Drubin, M. E., Munger, K. & Georgakoudi, I. Automated biochemical, morphological, and organizational assessment of precancerous changes from endogenous two-photon fluorescence images. PLoS One 6 (9), e24765 (2011).
46. Altman, G. H. et al. Cell differentiation by mechanical stress. FASEB J 16 (2), 270 (2002).
47. Zipfel, W. R. et al. Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci U S A 100 (12), 7075 (2003).
48. Sellick, C. A. et al. Evaluation of extraction processes for intracellular metabolite profiling of mammalian cells: matching extraction approaches to cell type and metabolite targets. Metabolomics 6 (3), 427 (2010).
49. Mauney, J. R. et al. In vitro and in vivo evaluation of differentially demineralized cancellous bone scaffolds combined with human bone marrow stromal cells for tissue engineering. Biomaterials 26 (16), 3173 (2005).
50. Mauney, J. R. et al. Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials 28 (35), 5280 (2007).
51. Chomczynski, P. & Sacchi, N. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1 (2), 581 (2006).
52. Schroer, K., Zelic, B., Oldiges, M. & Lutz, S. Metabolomics for Biotransformations: Intracellular Redox Cofactor Analysis and Enzyme Kinetics Offer Insight Into Whole Cell Processes. Biotechnology and Bioengineering 104 (2), 251 (2009).