Endogenous Fluorescence Signatures in Living Pluripotent Stem Cells Change with Loss of Potency

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Squirrell, Jayne M ^a   Fong, Jimmy J ^a   Ariza, Carlos A ^b   Mael, Amber ^c   Meyer, Kassondra ^d   Shevde, Nirupama K ^c,e   Roopra, Avtar ^d   Lyons, Gary E ^a,d   Kamp, Timothy J ^a   Eliceiri, Kevin W ^a,b   Ogle, Brenda M ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Madison   (United States)

^c WiCell Research Institute   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e MORGRIDGE INSTITUTE FOR RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL METABOLISM; CELL POPULATION; CELL POTENCY; CELL TRANSFORMATION; CELLULAR PARAMETERS; CONTROLLED STUDY; CYTOLOGY; EMBRYONIC STEM CELL; FLUORESCENCE; HUMAN; HUMAN CELL; LIGHT INTENSITY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; EMBRYOID BODIES; GLUCOSE; HUMANS; MICE; MICROSCOPY; MOLECULAR IMAGING; PLURIPOTENT STEM CELLS; SPECTROMETRY, FLUORESCENCE; TRETINOIN;

MURINAE;

EID: 84865600673     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043708     Document Type: Article

References (71)

1. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG, (2004) Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 167: 723-734.
2. Nelson TJ, Ge Z-D, Van Orman J, Barron M, Rudy-Reil D, et al. (2006) Improved cardiac function in infarcted mice after treatment with pluripotent embryonic stem cells. Anat Rec A Discov Mol Cell Evol Biol 288: 1216-1224.
3. Tang C, Lee AS, Volkmer J-P, Sahoo D, Nag D, et al. (2011) An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat Biotechnol 29: 829-834.
4. Ohgushi M, Matsumura M, Eiraku M, Murakami K, Aramaki T, et al. (2010) Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 7: 225-239.
5. Buschke DG, Squirrell JM, Ansari H, Smith MA, Rueden CT, et al. (2010) Multiphoton Flow Cytometry to Assess Intrinsic and Extrinsic Fluorescence in Cellular Aggregates: Applications to Stem Cells. Microsc Microanal: 1-16.
6. Chen AA, Underhill GH, Bhatia SN, (2010) Multiplexed, high-throughput analysis of 3D microtissue suspensions. Integr Biol (Camb) 2: 517-527.
7. Fernandez LA, Hatch EW, Armann B, Odorico JS, Hullett DA, et al. (2005) Validation of large particle flow cytometry for the analysis and sorting of intact pancreatic islets. Transplantation 80: 729-737.
8. Lakowicz JR, Szmacinski H, Nowaczyk K, Johnson ML, (1992) Fluorescence lifetime imaging of free and protein-bound NADH. Proc Natl Acad Sci USA 89: 1271-1275.
9. Gallas JM, Eisner M, (1987) Fluorescence of melanin-dependance. Photochem and Photobiol 45: 595-600.
10. Georgakoudi I, Jacobson BC, Müller MG, Sheets EE, Badizadegan K, et al. (2002) NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes. Cancer Res 62: 682-687.
11. Menter JM, (2006) Temperature dependence of collagen fluorescence. Photochem Photobiol Sci 5: 403-410.
12. Zipfel WR, Williams RM, Christie R, Nikitin AY, Hyman BT, et al. (2003) Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci USA 100: 7075-7080.
13. Berezin MY, Achilefu S (2010) Fluorescence Lifetime Measurements and Biological Imaging. Chem Rev Chem. Rev: 1-44.
14. Lakowicz JR (1999) Principles of Fluorescence Spectroscopy. New York: Plenum Publishers.
15. Chance B, Baltscheffsky H, (1958) Respiratory enzymes in oxidative phosphorylation. VII. Binding of intramitochondrial reduced pyridine nucleotide. J Biol Chem 233: 736-739.
16. Huang S, Heikal AA, Webb WW, (2002) Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. Biophys J 82: 2811-2825.
17. Gaspers LD, Thomas AP, (2008) Calcium-dependent activation of mitochondrial metabolism in mammalian cells. Methods 46: 224-232.
18. Koretsky AP, Balaban RS, (1987) Changes in pyridine nucleotide levels alter oxygen consumption and extra-mitochondrial phosphates in isolated mitochondria: a 31P-NMR and NAD(P)H fluorescence study. Biochim Biophys Acta 893: 398-408.
19. Skala MC, Riching KM, Bird DK, Gendron-Fitzpatrick A, Eickhoff JC, et al. (2007) In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia. J Biomed Opt 12: 024014.
20. Skala MC, Squirrell JM, Vrotsos KM, Eickhoff JC, Gendron-Fitzpatrick A, et al. (2005) Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues. Cancer Res 65: 1180-1186.
21. Vishwasrao HD, Heikal AA, Kasischke KA, Webb WW, (2005) Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy. J Biol Chem 280: 25119-25126.
22. Zhang JC, Savage HE, Sacks PG, Delohery T, Alfano RR, et al. (1997) Innate cellular fluorescence reflects alterations in cellular proliferation. Lasers Surg Med 20: 319-331.
23. Levitt JM, Baldwin A, Papadakis A, Puri S, Xylas J, et al. (2006) Intrinsic fluorescence and redox changes associated with apoptosis of primary human epithelial cells. J Biomed Opt 11: 064012.
24. Liang J, Wu W-L, Liu Z-H, Mei Y-J, Cai R-X, et al. (2007) Study the oxidative injury of yeast cells by NADH autofluorescence. Spectrochim Acta A Mol Biomol Spectrosc 67: 355-359.
25. Ezashi T, Das P, Roberts RM, (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102: 4783-4788.
26. St John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY, et al. (2005) The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7: 141-153.
27. Choi YM, Kwon S, Pak YK, Seol HW, Park DJ, et al. (2006) Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 348: 1472-1478.
28. Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, et al. (2007) A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9: 293-299.
29. Wang J, Alexander P, Wu L, Hammer R, Cleaver O, et al. (2009) Dependence of Mouse Embryonic Stem Cells on Threonine Catabolism. Science 325: 435-439.
30. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CAt, et al. (2011) Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 6: e20914.
31. Birket MJ, Orr AL, Gerencser AA, Madden DT, Vitelli C, et al. (2011) A reduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. J Cell Sci 124: 348-358.
32. Hattori F, Chen H, Yamashita H, Tohyama S, Satoh YS, et al. (2010) Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 7: 61-66.
33. Bird DK, Yan L, Vrotsos KM, Eliceiri KW, Vaughan EM, et al. (2005) Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH. Cancer Res 65: 8766-8773.
34. Conklin MW, Provenzano PP, Eliceiri KW, Sullivan R, Keely PJ, (2009) Fluorescence lifetime imaging of endogenous fluorophores in histopathology sections reveals differences between normal and tumor epithelium in carcinoma in situ of the breast. Cell Biochem Biophys 53: 145-157.
35. Tadrous PJ, Siegel J, French PMW, Shousha S, Lalani E-N, et al. (2003) Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer. J Pathol 199: 309-317.
36. Stringari C, Cinquin A, Cinquin O, Digman MA, Donovan PJ, et al. (2011) 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: 13582-13587.
37. Rice WL, Kaplan DL, Georgakoudi I, (2007) Quantitative biomarkers of stem cell differentiation based on intrinsic two-photon excited fluorescence. J Biomed Opt 12: 060504.
38. Rice WL, Kaplan DL, Georgakoudi I, (2010) Two-photon microscopy for non-invasive, quantitative monitoring of stem cell differentiation. PLoS ONE 5: e10075.
39. Uchugonova A, König K, (2008) Two-photon autofluorescence and second-harmonic imaging of adult stem cells. J Biomed Opt 13: 054068.
40. König K, Uchugonova A, Gorjup E, (2011) Multiphoton fluorescence lifetime imaging of 3D-stem cell spheroids during differentiation. Microsc Res Tech 74: 9-17.
41. Stringari C, Sierra R, Donovan PJ, Gratton E, (2012) Label-free separation of human embryonic stem cells and their differentiating progenies by phasor fluorescence lifetime microscopy. J Biomed Opt 17: 046012.
42. Centonze VE, White JG, (1998) Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging. Biophys J 75: 2015-2024.
43. Squirrell JM, Wokosin DL, White JG, Bavister B, (1999) Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability. Nat Biotechnol 17: 763-767.
44. Maltsev VA, Rohwedel J, Hescheler J, Wobus AM, (1993) Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44: 41-50.
45. Becker W, Bergmann A, Hink MA, König K, Benndorf K, et al. (2004) Fluorescence lifetime imaging by time-correlated single-photon counting. Microsc Res Tech 63: 58-66.
46. King MA, (2000) Detection of dead cells and measurement of cell killing by flow cytometry. J Immunol Methods 243: 155-166.
47. Lee ER, McCool KW, Murdoch FE, Fritsch MK, (2006) Dynamic changes in histone H3 phosphoacetylation during early embryonic stem cell differentiation are directly mediated by mitogen- and stress-activated protein kinase 1 via activation of MAPK pathways. J Biol Chem 281: 21162-21172.
48. Okada Y, Shimazaki T, Sobue G, Okano H, (2004) Retinoic-acid-concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev Biol 275: 124-142.
49. Pacherník J, Esner M, Bryja V, Dvorák P, Hampl A, (2002) Neural differentiation of mouse embryonic stem cells grown in monolayer. Reprod Nutr Dev 42: 317-326.
50. Ying Q-L, Nichols J, Evans EP, Smith AG, (2002) Changing potency by spontaneous fusion. Nature 416: 545-548.
51. Wu TYH, Ding S, (2006) Applying chemical tools to the dicovery of novel regenerative medicine. Drug Discovery Today: Technologies 3: 255-260.
52. Mohr JC, Zhang J, Azarin SM, Soerens AG, De Pablo JJ, et al. (2010) The microwell control of embryoid body size in order to regulate cardiac differentiation of human embryonic stem cells. Biomaterials 31: 1885-1893.
53. Feraud O, Debili N, Penninger JM, Kroemer G, (2007) Cavitation of embryoid bodies requires optimal oxidative phosphorylation and AIF. Cell Death Differ 14: 385-387.
54. Hernández-García D, Castro-Obregón S, Gómez-López S, Valencia C, Covarrubias L, (2008) Cell death activation during cavitation of embryoid bodies is mediated by hydrogen peroxide. Exp Cell Res 314: 2090-2099.
55. Lim H-J, Han J, Woo D-H, Kim S-E, Kim S-K, et al. (2011) Biochemical and morphological effects of hypoxic environment on human embryonic stem cells in long-term culture and differentiating embryoid bodies. Mol Cells 31: 123-132.
56. Mathur A, Hong Y, Kemp BK, Barrientos AA, Erusalimsky JD, (2000) Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovasc Res 46: 126-138.
57. Bird DK, Eliceiri KW, Fan C-H, White JG, (2004) Simultaneous two-photon spectral and lifetime fluorescence microscopy. Appl Opt 43: 5173-5182.
58. Hronik-Tupaj M, Rice WL, Cronin-Golomb M, Kaplan DL, Georgakoudi I, (2011) Osteoblastic differentiation and stress response of human mesenchymal stem cells exposed to alternating current electric fields. Biomed Eng Online 10: 9.
59. Wang H-W, Wei Y-H, Guo H-W, (2009) Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death. Anticancer Agents Med Chem 9: 1012-1017.
60. Belenky P, Bogan KL, Brenner C, (2007) NAD+ metabolism in health and disease. Trends Biochem Sci 32: 12-19.
61. Pollak N, Dölle C, Ziegler M, (2007) The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem J 402: 205-218.
62. Fjeld CC, Birdsong WT, Goodman RH, (2003) Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc Natl Acad Sci USA 100: 9202-9207.
63. Kumar V, Carlson JE, Ohgi KA, Edwards TA, Rose DW, et al. (2002) Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol Cell 10: 857-869.
64. Zhang Q, Piston DW, Goodman RH, (2002) Regulation of corepressor function by nuclear NADH. Science 295: 1895-1897.
65. Awasthi S, Matthews DL, Li RA, Chiamvimonvat N, Lieu DK, et al. (2012) Label-free identification and characterization of human pluripotent stem cell-derived cardiomyocytes using second harmonic generation (SHG) microscopy. J Biophotonics 5: 57-66.
66. Panopoulos AD, Yanes O, Ruiz S, Kida YS, Diep D, et al. (2012) The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 22: 168-177.
67. Iyer V, Hoogland TM, Saggau P, (2006) Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy. J Neurophysiol 95: 535-545.
68. Lakowicz J, Gryczynski I, Gryczynski Z, (1999) High throughput screening with multiphoton excitation. J Biomol Screen 4: 355-362.
69. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R, (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45.
70. Ying QL, Nichols J, Chambers I, Smith A, (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115: 281-292.
71. Ungrin MD, Joshi C, Nica A, Bauwens C, Zandstra PW, (2008) Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS ONE 3: e1565.